Fistula Carotido Cavernosa

Seminars in Cerebrovascular Diseases and Stroke Vol. 1 No. 1 2001

Carotid Cavernous Fistula

TIMOTHY LAWRENCE TYTLE and PAVAN KUMAR PUNUKOLLU

Oklahoma City, Oklahoma

ABSTRACT

Carotid cavernous fistulae are an uncommon disorder, actually consisting of 2 disease

processes. One category is a direct internal carotid artery to cavernous sinus fistula. A second category is the indirect or dural type carotid cavernous fistula. It is the purpose of this article to provide an overview of the anatomy of the cavernous sinus and to discuss the classification, clinical findings, diagnostic imaging evaluation, reasons for misdiagnosis, and treatment

options. Key words: carotid artery fistula, carotid cavernous fistula.

Carotid cavernous fistulae are an uncommon disorder, actually consisting of 2 disease processes. One has a rapid onset, precipitated by a traumatically induced tear or, less commonly, a ruptured aneurysm of the cavernous segment of the internal carotid artery (ICA). A second category is a more insidious, less direct, and often less dramatic process that perhaps is described best as dural arteriovenous fistula involving the cavernous sinus (CS). Although the diagnosis was long based on clinical findings, in more recent years, a variety of radiographic modalities have been used to assist in this diagnosis and treatment. Treatment also has undergone considerable evolution from a predominately surgical solution to an almost exclusively intravascular remedy. In this article, we provide an overview of the anatomy of the cavernous sinus and discuss the classification, clinical findings, reasons for misdiagnosis, and treatment options for carotid cavernous fistulae.

CS Anatomy

The normal CS (Fig 1) in adults is 2 cm long by 1 cm wide and extends from the orbit to the petrous apex.t It

From the Department of Radiology, Oklahoma University Health Sciences Center, Oklahoma City, OK.

Address reprint requests to Timothy Lawrence Tytle, MD, Depart- ment of Radiology, Oklahoma University Health Sciences Center, 800 NE 13th St, 1NP606, Oklahoma City, OK 73104.

Copyright �9 2001 by W.B. Saunders Company 1528-9931/01/0101-0008535.00/0 doi: 10.1053/scds.2001.24080

lies in the middle cranial fossa in a parasellar location lateral to the sphenoid sinus. Surrounding osseous structures that contribute to the borders of the cavernous sinus boundaries include the sphenoid body, greater and lesser wings of the sphenoid, tuberculum sellae, carotid groove, and dorsum sellae, as well as clinoid processes. Osseous variants include a large middle clinoid process, carotico- clinoid foramen and interclinoid osseous bridge (osseous continuity between anterior and posterior clinoids). Based on the numerous contents of the cavernous sinus, such as nerves, fat, meninges, arteries, and veins, as well as the lack of a true dural venous sinus, some believe it would be more accurate to refer to the cavernous sinus region as the lateral sellar compartment as a whole and to the veins within this compartment as the lateral sellar venous plexus. 2

Dura mater covers the superior, lateral, and medial surfaces of the cavernous sinus, whereas the inferior surface is formed by the middle cranial fossa. Umansky 3 divides the roof of the cavernous sinus into 3 regions: the oculomotor trigone, the carotid trigone, and the clinoid space. The oculomotor trigone is formed laterally by the anterior petroclinoid ligament, medially by a line overlying the interclinoid ligament and posteriorly by the posterior petroclinoid ligament. The oculomotor nerve enters the oculomotor trigone, which forms the posterior two thirds of the roof of the cavernous sinus, whereas the anterior third is formed by the osseous anterior clinoids. The carotid trigone is limited laterally by a line overlying the interclinoid ligament, medially by the dura of the diaphragm sellae, and anteriorly by the endosteal dura.

84 Seminars in Cerebrovascular Diseases and Stroke Vol. 1 No. 1 March 2001

Fig 1. Anatomy of the cavernous sinus region. 1, pituitary gland; 2, infundibular stalk; 3, CN III; 4, CN IV; 5, CN V1; 6, CN VI; 7, sphenoid sinus; 8, internal carotid artery; 9, anterior clinoid process; 10, third ventricle; 11, optic chiasm; 12, suprasellar cis- tern. 13, venous spaces of cavernous sinus; 14, temporal lobe; 15, hypothalamus; 16, CN V2; 17, diaphragma s ellae; 18, Meck- el's cave. (Reprinted with permission from Anne Osborn in Diagnostic Neuroradiology, 1994 Mosby-Year Book, Inc)

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The anterior portion of the carotid trigone provides the opening for the ICA at the proximal portion of its supraclinoid segment. There is an area here known as the carotid cave in which the distal dural ring is not as tightly adherent to the ICA as it is along the remainder of the ICA dorsolateral circumference.

The anterior clinoid fold dura has superficial and deep layers as it extends to the anterior clinoid process. The deeper layer surrounds the ICA proximal to the ophthalmic artery origin and forms the distal dural ring, which is tightly adherent to the ICA adventitia. The proximal dural ring is formed by the periosteal layer around the ICA as it exits the CS. Between the 2 rings is the clinoid segment of the ICA. The distal dural ring is difficult to localize clinically, but plays an important role in planning treatment. Unfortunately, there is no reliable radiographic technique to identify this structure preop- eratively, although proposed landmarks have included the base of the anterior clinoid process, the origin of the ophthalmic artery, and the tuberculum sellae. 4

The CS lateral wall is formed by a combination of dura superficially and a deeper inner membranous layer formed by the sheaths of cranial nerves (CN) III, IV, V1, and sometimes V2. Parkinson's triangle, which is used

for exposure during some surgical approaches to carotid cavernous fistula (CCF) treatment, is formed superiorly by the lower margin of the trochlear nerve (CN IV), inferiorly by the upper rim of V1 and the trigeminal ganglion and posteriorly by the dorsum sellae and clivus. Anteriorly, the inner membrane of the lateral wall (but not the superficial dura) covers the superior orbital fissure. The CS medial wall is formed by the dura propria superiorly and the sella periosteum inferiorly. 5

Although there are many classifications, a recent description by Bouthillier 6 of pertinent ICA nomenclature includes the following 7 segments numbered in the direction of blood flow (Fig 2):

C1, cervical segment C2, petrous segment C3, laceral segment C4, cavernous segment C5, clinoid segment C6, ophthalmic segment C7, communicating segment

The laceral segment might have small, usually angiographically invisible branches that can communicate

Carotid Cavernous Fistula �9 Tytle and Punukollu 85

Ophthalmic a. ,C7

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Petrolingual lig.

C3

~ C 6 5

4

C2

~. .Carot id Canal

Fig 2. Segmental nomenclature of the internal carotid artery. (Reprinted with permission from Anne Osborn in Cerebral Angiography, Second Edition. Lippincott Williams and Wilkins, 1999)

with the ascending pharyngeal artery (recurrent artery of the foramen lacerum). Branches of the cavernous ICA include the meningohypophyseal trunk (whose branches include the inferior hypophyseal, the marginal and basal tentorial arteries, and the dorsal meningeal/lateral clival branches) and the posteroinferior hypophyseal artery (which has clival branches that can anastomose with the ascending clival branches from the hypoglossal artery). There are also medially directed capsular arteries from the cavernous ICA. The lateral malnstem artery (also known as the inferolateral trunk) arises on the lateral aspect of the cavernous ICA and is directed inferiorly. It has several branches, the most important of which is the artery of the foramen rotundum, that can anastomose with branches of the internal maxillary artery. In some individuals, there can also be a recurrent (deep) meningeal artery that is a remnant of the dorsal ophthalmic artery. This can anastomose with the superior ophthalmic artery after passing through the superior orbital fissure. The marginal tentorial artery can arise off

the inferolateral trunk, the middle meningeal artery or sometimes the ophthalmic artery. 7-9

The venous anatomy of the CS is still controversial. At one time, many believed this was a single trabeculated space. Now, many believe the venous portion of the CS is actually an extradural plexus of veins. According to Keller, 1 embryologically, the venous channels begin as a plexus of thin veins surrounded by adipose tissue with the channels enlarging and adipose tissue decreasing in adults. Tributaries of the CS include the superior and inferior ophthalmic veins (SOV and IOV), which can drain separately or confluently into the anterior CS (Fig 3). The IOV also connects with the facial vein and can drain into the pterygoid plexus through the inferior orbital fissure. The superficial middle cerebral vein, inferior cerebral veins (including uncal from the temporal lobe), sphenoparietal vein or sinus (drains superficial middle cerebral vein with variable contributions from the meningeal, orbital, medial anterior temporal and inferior frontal veins) as well as hypophyseal veins can drain towards the CS. a

Drainage from the CS is usually mainly through the superior petrosal sinus (SPS), which drains into the junction of the transverse and sigmoid sinuses, and the inferior petrosal sinus (IPS), located in the petroclival fissure and draining into the jugular bulb in the pars nervosa of the jugular foramen. The basilar venous plexus connects the CS to the vertebral epidural venous plexus (Batson's venous plexus). Multiple emissary veins connect the CS to the pterygoid plexus by the foramen ovale or an emissary sphenoidal foramen medial to the foramen ovale.

Harris and Rhoton separate the CS into 4 venous spaces based on their relation to the ICA including medial, lateral, anteroinferior, and posterosuperior. 1~ Mullan described the CS as being composed of 2 main larger anterior inferior and smaller posterior superior cavities divided by the cavernous ICA. 11 The CSs are connected across midline by the anterior and posterior inter-CSs (circular sinus), basilar plexus and intercavern- ous plexuses in the floor of the sella, and on the diaphragma sellae. These interconnections might be of variable size and are found throughout the sells from its anterior to posterior extent. The SPS and IOVs can have afferent or efferent drainage relative to the CS. Occasion- ally, the sphenoparietal sinus will not drain into the CS and will instead form the sphenopetrosal sinus, which courses along the middle cranial fossa floor and into the SPS or into the pterygoid plexus.

Cranial nerves III, IV, VI, V 1, and sympathetic/parasympathetic connections are present in the CS. CN III (oculomotor) courses in the CS lateral wall along the inferolateral surface of the anterior clinoid process and enters the superior orbital fissure through the annulus of Zinn. CN IV (trochlear) enters the CS lateral


foramen ovate). Sympathetic fibers ascend with the ICA in 1 to 3 bundles as the internal carotid nerve, including extending along the intradural ICA to supply the cerebral arteries, as well as coursing along cranial nerves IV, V, and VI and giving rise to the deep petrosal nerve. Parasympathetic fibers and ganglion cells also are associated with the cavernous ICA. 1

Fig 3. Venous anatomy and cavernous sinus drainage pathways.

wall posterolateral to CN III and crosses CN III proximal to entering the superior orbital fissure (and enters the orbit outside the annulus of Zinn). V1 runs from the Gassserian ganglion (Meckel's cave) into the inferior lateral wall of the CS (below IV and VI) and then into the superior orbital fissure. A small portion of V2 also can pass along the inferior aspect of the CS before entering the foramen rotundum. CN VI (abducens) penetrates the clival dura and ascends towards Dorello's canal (a passage beneath the petroclinoid ligament from the petrous apex to the posterior clinoid process, which also contains the IPS and dorsal meningeal artery as well as CN VI). CN VI exits Dorello's canal to enter the interdural CS and passes along the lateral aspect of the cavernous ICA, sometimes with very little space between the nerve and the lateral wall of the CS. 1 Harris 1~ reported most individuals have a single abducens trunk in the CS but noted up to 5 rootlets in some patients.

Blood supply to the cavernous cranial nerves is important when endovascular treatment is considered. As described by Keller, the cavernous portions of the cranial nerves are mainly supplied by the inferolateral trunk of the ICA (including a superior or tentorial branch supplying CN III and IV, an anteromedial branch supplying CN III, IV, V 1, and VI, a lateral branch supplying V2, and a posterior branch supplying V3). In some, supply to the CS cranial nerves comes principally from the accessory meningeal artery (internal maxillary branch that enters through the foramen of vesalius or

Carotid Cavernous Fistula Classification and Etiology

CCFs are arteriovenous communications between the carotid (internal and/or external) artery and the CS. There are similar clinical manifestations regardless of the type of communication. Accurate CCF classification with strict angiographic protocols is key to the diagnosis and management of CCFs. There have been several classification schemes principally used to guide therapy. The Barrow classification is most commonly used and consists of direct (Type A, shunt from the ICA to the CS) or indirect (Types B, C, and D; communications between dural meningeal branches of the ICA and/or external carotid artery [ECA] and the CS) fistulae (Fig 4). 12 These latter are referred to also as dural arteriovenous fistulae or low-flow fistulae.

Type A fistulae: direct communications between the ICA and CS (high-flow and the most common type seen after trauma)

Type B fistulae: rare, only supplied by ICA dural branches

Type C fistulae: exclusively supplied by ECA dural branches

Type D fistulae: most common dural type, supplied by dural branches of both ICA and ECA (might have unilateral or bilateral ICA and ECA supply)

Ernst and Tomsick 13 proposed a subclassification of Type D fistulae into D1 (unilateral ICA and ECA supply) and D2 (bilateral ICA and ECA supply) to further guide therapy when a transarterial route is considered. The classification schemes do not take into account Type A CCFs caused by a cavernous carotid artery aneurysm rupture that can alter the therapeutic approach.

Debrun separated direct CCFs based on the location of the fistula site after the ICA from the anterior clinoid process to the petrous canal in his original report of 54 traumatic CCFs. 14 This included locations (1) on the anterior ascending intracavernous segment of the carotid (least common location, 1 case); (2) at the junction of the anterior ascending and horizontal segment of the ICA (5 cases); (3) on the horizontal intracavernous ICA (most common, 22 cases); (4) at the junction of the horizontal


Fig 4. Barrow classification of CCFs. Type A fistulae are direct shunts between the internal carotid artery and the cavernous sinus; type B, C, and D fistulae are dural shunts. Type B are those between meningeal branches of the internal carotid artery and the cavernous sinus; type C are those between meningeal branches of the ECA and the cavernous sinus; type D are those between meningeal branches of both the internal and external carotid arteries and the cavernous sinus. (Reprinted with permission from Barrow DL, Spector RH, Braun IF: Classifi- cation and treatment of spontaneous carotid-cavernous sinus fistulae. J Neurosurg 62:248-256, 1985)

Type A Type C

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and intracavernous segment of the ascending ICA (second most common, 15 cases); and (5) on the posterior ascending intracavernous segment of the ICA (11 cases).

Direct (type A) fistulae are usually high-flow fistulae. These are most commonly posttraumatic (up to 80% according to some series), with the remainder being spontaneous, as Traumatic CCFs are most common in young men. Motor vehicle accidents are the most common cause, but CCFs are seen also with penetrating injuries or might result from iatrogenic causes. Accord- ing to Gobin, 16 CCFs are rare after indirect trauma, making up only 3 of 60 ICA injuries. Postulated etiologies of traumatic CCF with indirect trauma have included injury by a fracture related bone fragment, tears of the ICA intracavernous branches at their origins, or a sudden increase in ICA intraluminal pressure resulting in rupture of its most distensible segment into the CS. Tomsick ~5 also speculates that traumatic CCFs might he caused by stretching and shearing of the more mobile portion of the ICA relative to the fixed petrous and clinoidal segments accounting for the large majority of CCFs that involve the horizontal cavernous ICA and the vertical postlaceral segment of the posterior genu of the ICA siphon. Iatrogenic causes of Type A CCFs are numerous and include guidewire perforation, intracranial endarterectomy by a Fogarty-type balloon with ICA rupture, septoplasty, transsphenoidal surgery, LeFort I maxillary osteotomy, and microcompression of the Gas- serian ganglion for trigeminal neuralgia. 17-2s

Direct CCFs might be symptomatic acutely, or it might take days to months before being manifested clinically. Possibilities for late manifestations include a

small fistula that enlarges over time or development of a traumatic ICA pseudoaneurysm that is initially intact and later ruptures into the CS. Most direct CCFs do not resolve spontaneously, although Tomsick 15 reports this occasionally occurs.

Spontaneous Type A CCFs can be caused by rupture of a cavernous ICA aneurysm as well as occurring in fibromuscular dysplasia (FMD) and Ehlers-Danlos caused by a weakened arterial wall. Bilateral traumatic CCFs account for 1% to 2% of all cases. In Tomsick's series, spontaneous Type A CCFs were most common in women and most commonly caused by rupture of a cavernous ICA aneurysm, whereas others were caused by a congenitally weak (Ehlers-Danlos, FMD, pseudoxan- thoma elasticum, osteogenesis imperfecta) or atherosclerotic artery. 15 A few cases of CCF have been identified as being congenital as well as occurring in association with a persistent trigeminal artery ICA variant. 3~

Newton and Hoyt 32 suggested dural CCFs are caused by straining, predisposing vascular disease, or trauma. Predisposing conditions included postmenopausal, preg- nant, or recent postpartum females as well as males over 50 years age. Tomsick reports that arteriovenous shunts are known normally to be present in the dura of the superior sagittal and transverse sinuses and that thrombosis of the sinus might cause the potential shunts to open in an attempt to revascularize the sinus. 33 Preg- nancy and delivery associated dural CCFs might be related to straining at stool or work, during vomiting, or caused by small vessel rupture during delivery. Tomsick also postulates that diminished estrogen levels might play a role in postmenopausal women developing


CCFs. 33 Estrogen, which inhibits progression of atherosclerosis, might play a role in the regulation of potential dural arteriovenous shunts and also has thrombogenic effects. Trauma accounted for only a small number of the dural CCFs in Tomsick's literature review (only 3% of 299 indirect CCFs were related to trauma). Tomsick 33 reports that most traumatic dural CCFs have been type C, often caued by supply by an enlarged middle or accessory meningeal artery, but has also seen Type D fistulae (including a case after percutaneous retrogasserian rhizo- tomy). Congenital dural CCFs were reported as being Type C with single branch communications between the middle meningeal artery and CS.

In Tomsick's 33 review, spontaneous indirect CCFs were 5 times more common then spontaneous direct CCFs. Tomsick also emphasized that bilateral dural arterial supply or bilateral drainage does not necessarily mean there are bilateral dural CCFs. He reported up to 35% of dural CCFs underwent spontaneous resolution in a literature review of 260 cases (individual studies in the review had closure rates as high as 90%) with clinical improvement noted over periods of 6 months to 6.8 years. 33 In Tomsick's experience, up to 16% of his patients with dural CCF had some pial venous drainage, but none of these had hemorrhages before or after treatment. He believes that unlike direct CCFs, the presence of pial drainage does not by itself require urgent treatment. However, we have had a patient with a Type D CCF with known pial venous drainage develop a venous infarction before successful endovascular treatment. Tomsick also reported changes in a patient's symptoms, including worsening, might be caused by thrombosis of the CS and/or draining veins (including SOV) (which

would contraindicate further thrombosis by intervention), as well as caused by changes in venous drainage patterns. 33 Potential pathways of venous drainage with indirect CCFs are similar to direct CCFs. In Debrun's series, Type B CCFs were the rarest dural CCFs, whereas Type D was the most common, with the majority of Type D CCFs having arterial feeders off bilateral ECA and ICA branches. 34 In the same series, he reported the majority of spontaneous CCFs were of the dural type.

Clinical Manifestations

In direct (high-flow, Barrow Type A) CCFs, the onset of clinical manifestations is usually both acute and profound. Here, the classic triad of pulsatile exophthalmos, episcleral venous engorgement, and cranial bruit should rapidly lead to the correct diagnosis (Fig 5). By contrast, the indirect (low-flow, dural Barrow type B, C, and D) CCFs are most often characterized by their insidious onset and generally their similar, but less dramatic findings.

Although the cranial bruit is often unmistakable to both patients and clinicians with direct CCFs, it is invariably less dramatic or even absent with the indirect forms. Here, if noted at all, it is usually in a quiet setting such as at bedtime. In fact, there are several reports in the literature that have described the spontaneous closure of dural CCFs. 35-40

Should the major decompressive route of vascular drainage of the CS be posteriorly through the petrosal sinuses, then the ocular signs and symptoms might be minimal or absent. Far more commonly, a major decompres-

Fig. 5. (A, B) Posttraumatic direct CCF showing third nerve palsy with proptosis and conjunctival chemosis of the right eye.


Fig. 6. Patient with an indirect CCE (A) Example of episcleral venous engorgement of the left eye. (B) Close-up photograph of the eye revealing the characteristic corkscrew appearance of engorged episcleral veins. (C) Image showing conjunctival chemosis with episcleral venous engorgement.

C C F s . 42 Acute diminished visual acuity is believed by some to be a cause for urgent transvascular intervention. 43

Whereas pulsating exophthalmos classically presents with direct CCFs, proptosis might be minimal in the indirect forms. In fact, it might be overshadowed by the more prominent findings, such as chemosis, arterialization of the conjunctival vessels, increased intraocular pressure, and cranial nerve palsies.

sive route is through retrograde flow into the ophthalmic veins, resulting in ocular manifestations. This often leads to the hallmarks of CCFs, such as arterialization of conjunctival vessels and conjunctival chemosis (Fig 6). 41

The increased intraorbital pressure often leads to ipsilateral enlargement of the extraocular muscles and to ophthatmoplegia from CS involvement of the affected nerves. The abducens nerve is most frequently involved, occurring in up to 85% of direct C C F s . 42 Compromise of the involved cranial nerves also frequently leads to diplopia. (Fig 7)

The increased orbital pressure heralds the fundoscopic findings of optic disk swelling, engorgement of the retinal veins and retinal hemorrhage (Fig 8). These findings are caused by venous stasis and impaired retinal blood flow. 41 Increased intraocular pressure caused by the same venous stasis results in glaucoma.

The visual loss sometimes seen in direct CCFs might be from optic nerve damage, or, when delayed, from exposure keratopathy, increased intraocular pressure, vitre- ous hemorrhage, retinal venous stasis, central retinal vein occlusion, or choroidal detachment. Anterior or posterior visual loss occurs in up to 90% of patients with direct

Imaging Evaluation

Angiography Angiography is key to the evaluation of CCFs. Today,

diagnostic angiography is often performed in the same session as treatment. Angiography is often the only diagnostic imaging test that shows the CCF, particularly in low-flow lesions, and is critical to planning treatment and prognosis. With Type A lesions (Fig 9), angiography is used to define the site and size of the direct fistula, identify all venous drainage pathways define the Circle of Willis, as well as any concomitant and/or preexisting vascular abnormalities that would alter the approach to treatment. Carotid artery dissection was seen in up to 5% of traumatic CCFs in Tomsick's series, including some extending intracranially to the site of the fistula] 3 In the older patients with nontraumatic CCFs, angiography also is useful to identify any atherosclerotic irregularity or narrowing involving the cervical carotid arteries to more safely pursue endovascular treatment. Additionally, the flow patterns on arteriography in acute traumatic CCFs can identify patients who are at risk for steal and cerebral ischemia, when most of the flow is seen entering the fistula with only minimal distal flow and poor collaterals.


Fig. 7. Angiographically proven Barrow type B carotid cavernous fistula. This patient's only complaint was of double vision. Note involvement of the inferior rectus muscle producing paresis of downward gaze of the right eye (indicating partial third cranial nerve involvement).

Diagnostic angiography is most often performed through a transfemoral arterial approach. Single- or double-wall needle entry might be performed with single- wall preferred for patients who might undergo anticoagulation for the procedure. There are a variety of preshaped catheters that allow selection of the cervical carotid arteries. In the elderly, in whom selective catheterization is difficult, an arch aortogram might be performed with a pigtail catheter to better identify the carotid origins and the best approach before selective catheterization. Prin- cipal complications of cerebral angiography include infarction (0.1% to 0.5% incidence, including a 0.1% incidence of death), hemorrhage at the puncture site, and possible adverse effects of contrast on renal function, s

Fig. 8. Classic funduscopic findings of carotid cavernous fistula showing an early central retinal vein occlusion.

Angiographic protocols for the evaluation of a direct CCF include bilateral common carotid artery (CCA) injections to evaluate the cervical portions of the carotid arteries for stenosis, including dissection, as well as possible contralateral vascular abnormality. Ipsilateral selective ICA, ECA, and, sometimes, vertebral artery injections might improve evaluation of the fistula. Be- cause the CS might opacify rapidly, particularly in high-flow fistulae, it is important to use high-quality imaging, high frame rates of image acquisition (above 5 frames/sec), and higher-than-usual rates of selective ICA contrast injection (up to 10 mL/sec in some cases). Identification of the fistula site is key, and this can be aided by several different maneuvers, including ipsilateral ICA-selective catheterization and injection while compressing the ipsilateral ICA (the Mehringer- Hieshima maneuver) to show the flow and better show the fistula. Endovascular ICA occlusion by a balloon catheter while slowly injecting the more distal ICA through the end hole lumen of a double lumen balloon catheter also might prove effective in showing the fistula (Fig 10). 13"44 The Huber maneuver consists of vertebral artery injection while compressing the ICA of interest (allows slow opacification of the fistula by flow through a patent ipsilateral or contralateral posterior communicating artery) (Fig 11). Filming is in the lateral projection. These maneuvers are particularly important in identification of the rare double fistulae or complete ICA transection, where the ICA is not seen to opacify beyond the fistula. 44

During the arterial phase, it is important to identify the site of the fistula as well as its size. The size of the fistula, usually 2 to 6 mm diameter, will aid in determining the size of balloons or coils that might be needed during treatment] 4 If the fistula ostium is too large, carotid artery sacrifice or surgery rather than endovascular balloon occlusion of the fistula might be indicated. The arterial phase might also show aneurysms or pseudoaneurysms that might have to be addressed during treatment and possible additional sources of fistulous supply other than the ICA (ie, indirect dural supply with a non-type A CCF). It is also important to document how much of the carotid artery flow is being diverted through the fistula and how well developed collaterals such as the circle of Willis are. This will help predict tolerance of the balloon occlusion test (BOT) and later carotid artery sacrifice, if needed. Angiographic location of the fistula is also important in the occasional surgical patient to guide more exact dural entry into the CS. Additionally, the cervical portion of the arteriogram will determine if the ICA is large enough to allow transarterial catheter navigation for a fistula occlusion procedure.

The venous phase is also important in the evaluation of type A CCFs. The CS might not appear significantly enlarged or might be markedly enlarged with the sug-


Fig. 9. (A) Lateral arteriogram of a selective internal carotid arteriogram in a posttraumatic patient with a type A fistula. (B) Diagram illustrating a type A fistula. Cavernous sinus (open arrows), approximate site of fistula (white arrow), SOV(black arrow), and inferior petrosal sinus (black arrowhead).

gestion of extension into the adjacent subarachnoid space. The CS has to be evaluated for early opacification, possible venous pseudoaneurysm, or varix (which would be an indication for urgent CCF treatment because of the propensity for subarachnoid hemorrhage in such cases). It is valuable also in the identification of outflow pathways from the CS. Venous outflow pathways are important to note because they have a direct bearing on the clinical presentation and treatment approach. In their series of patients, Tomsick et a113 reported 89% of Type A CCFs had drainage into the SOV, 83% into the IPS, and 49% into the sphenoparietal sinus as well as pial drainage into the posterior fossa (27%) and middle cerebral veins (32%). Pial cortical venous drainage is important to note, because this is considered an indication for urgent therapy by some. 45 Sometimes, there might only be a single drainage pathway from the CS.

Fig. 10. An example of the Mehringer-Hieshima maneuver. The ipsilateral ICA was compressed while injecting the contralateral ICA in this patient with a right type A carotid cavernous fistula. Cavernous sinus (open arrows).

Venous outflow stenoses and thromboses must also be noted, because they will impact on access routes for a transvenous approach to the fistula and affect the final treatment approach (for example, stenosis involving a low-flow fistula draining vein might allow one to accept subtotal fistula closure in the hope that it will spontaneously thrombose over time).

Angiographic protocol for Types B, C, and D fistulae (indirect), when possible, includes bilateral selective ICA and ECA and vertebral artery injections (Figs 12, 13, 14). Some also prefer to perform selective injections of ECA branches, such as the internal maxillary and ascending pharyngeal arteries, for better delineation of the arterial supply to the fistula. Debrun 46 recommends selective angiography of both ascending pharyngeal arteries and internal maxillary arteries in the workup of indirect CCFs. It is important to perform a complete angiographic assessment of the contralateral side because there is often contralateral dural supply in indirect CCFs. 4v If a transarterial embolization procedure is being considered, it is important to recognize anglo- graphic variants and dangerous anastomoses. These include the ophthalmic artery (OA) arising from the middle meningeal artery (MMA) or the MMA off the OA, branches of the internal maxillary and ascending pharyngeal arteries supplying flow to the ICA, and any enlarged dural branches arising from the ICA. The venous phase of the study is important, because the primary mode of therapy is transvenous for indirect CCFs. Tomsick ~3 reported pathways of drainage in indirect CCFs as ipsilateral SOV (62%), ipsilateral IPS (20%), ipsilateral SPS (7%), pial (16%), and contralateral drainage only (6%). Pial drainage should be recognized because of the potential for venous hypertension.


Fig. 11. Lateral arteriogram of vertebral artery contrast injection with ICA compression (Huber maneuver). Note the location of the Type A fistula (arrow).

Computed Tomography (CT) and Magnetic Resonance Imaging (MRI)

Cross-sectional imaging is often the initial method of imaging evaluation. Usually, MR/ and magnetic resonance angiography (MRA) are preferred over CT. A normal CT or MRI does not exclude the diagnosis of CCF, and, if there is a high clinical suspicion, an arteriogram should follow (Fig 15). Scanning protocols include axial and coronal imaging with and without contrast in CT and MRI, including high-resolution images of the orbits and CSs. Additional techniques include dedicated orbital imaging with fat saturation and various MRA and CT angiography (CTA) techniques.

Imaging findings involving the CS can be subtle and only show asymmetric widening or lateral bulging of a CS on one side (Fig 16). In cases of bilateral CCFs or inter-CS communication, bilaterally enlarged CSs might be seen, although similar findings might be seen with the carotid artery ectasia associated with atherosclerosis. One might also note enlarged pseudoaneurysms or varices arising from the CS and extending into the adjacent subarachnoid space or even sphenoid sinus. These channels ahow enhancement on CT but have variable signal on MRI, depending on the flow, and can be of low signal intensity (SI) because of flow voids with rapid flow. They can also have high signal caused by flow-related enhancement and on post-gadolinium studies. If there is thrombosis of a CS or a draining vein, this can be seen as a high-attenuation structure on noncontrast CT and mistaken for hemorrhage if its vascular nature is not recognized. This can present as a filling defect on contrast-enhanced CT(CECT) within the CS or a draining vein. Clot has variable signal on MRI, depending on its age, and can be low-SI on T1- and

T2-weighted images early and high-SI later. Venous thrombosis should be carefully evaluated because it might be the cause of a sudden neurologic change.

Dural CCFs might show enhancement of the lateral CS wall, caused by enlarged feeding dural arteries. CS widening and enhancement has multiple nonvascular etiologies on cross-sectional imaging, including secondary tumor invasion from pituitary adenomas and adjacent skull base and head and neck primaries, schwannoma, meningioma, CS thrombosis, pachymeningitis, CS hemangioma, granulomatous disease (infectious and non- infectious), lymphoma, and pseudotumor. Elster 48 reported dilated inter-CSs visible on high-resolution MRI as an additional sign of CCFs.

The ICA also should be evaluated carefully. On neck CT, an acute carotid artery dissection can show a crescentic rim of high attenuation (with or without an adjacent pseudoaneurysm or pericarotid hematoma), with a narrowed enhancing lumen on the CECT.

A more chronic dissection can have a low-attenuation rim caused by evolution of the hemorrhage in the wall of the carotid artery. On MR/, carotid artery dissections show variable signal and can be isointense or low-SI early on T1 and T2 and tend to be high on Tt and T2 in the later subacute stage. The normal flow void of the cervical ICA might be much smaller than usual (and as compared with the other side) or completely absent in cases of carotid artery occlusion. The carotid artery distal to the occluded segment can show higher than usual T1 and T2 signal because of slow flow or thrombosis.

Intracranial carotid artery aneurysms might sometimes be visible on CT or MRI but are often obscured by the adjacent CSs. Neck CT or MRI can sometimes show asymmetrically enlarged ECA branches in cases of indirect CCFs as small flow voids or enhancing vessels in the infratemporal region with enlarged branches of the ascending pharyngeal and internal maxillary arteries. If there is drainage of the CS into the pterygoid plexus, this might be seen as asymmetrical enlargement and enhancement in the upper neck.

Cranial findings separate from the CS are variable. In a traumatic setting, one might see fractures involving the cranium, including the skull base in particular and the other intracranial sequela of trauma. Fractures crossing the carotid canal, foramen lacerum, and sphenoid body are particularly worrisome for possible carotid artery injury and CCE According to Helmke, 49 the large majority of CCFs in their study did not have an identifiable fracture on CT. One might also see hemorrhage in the sphenoid sinus as an indirect sign of carotid artery injury. Sec- ondary cranial findings associated with CCFs include enlarged draining veins such as the sphenoparietal sinus, middle cerebral veins, or other pial draining veins. These will enhance on CT and have variable MR signal based on flow rate and patency. They can appear as large hyper-

dense tubular structures at the surface of the brain on noncontrast-enhanced CT. These draining veins have been noted to extend into the supratentorial space and the posterior fossa, with the effects of venous hypertension seen on imaging involving the cerebral hemispheres, brainstem, and cerebellum. Imaging findings of venous hypertension have included areas of low attenuation or high T2 signal involving mainly the cerebral white matter (Fig 17), mimicking a vasogenic edema pattern and causing brainstem and cerebellar edema (including death attributed to the brainstem edema). 5~ Simple edema usually resolves on imaging after appropriate treatment. 51 A re- versible pattern of edema with high T2 SI also has been noted in the medulla and upper cervical cord. 52 Hemor- rhage is a known complication of venous hypertension with intra-axial bleeding seen in some cases, often with enlarged serpiginous enhancing structures (CT/MRI) or flow voids in the vicinity representing arterialized veins.


i i! !i iiiiiii ii ! i ii i i

Fig. 12. Patient with a Type D CCF. (A) Selective left internal carotid artery injection showing early cavernous sinus opacification with drainage into the SOV and inferior petrosal sinus. (B, C) Selective right ECA injection in the lateral (B) and an- teroposterior (C) projections. There is supply of the left carotid cavernous fistula from branches of the right ECA. Cavernous sinus (open arrows), SOV (small straight black arrow), inferior petrosal sinus (arrowheads), branches of ECA decompressing into cavernous sinus (large curved arrows).

Venous infarcts with or without hemorrhage might be a permanent cause of high T2 SI on MRI or low density on CT and might or might not enhance.

Orbital findings depend on the CCF drainage pattern. Normally, the SOV is formed by the junction of the frontal and angular veins at the anterior orbit and is later joined by the IOV before passing through the superior orbital fissure to enter the CS. Usually, the SOV is 2 to 3.5 mm in diameter and changes size with changes in head position or valsalva. 53 It can normally be asymmetric. If there is anterior drainage into the SOV or IOV, one might see proptosis, extraocular muscle enlargement, and increased density of the orbital fat (Fig 18). Enlargement of the SOVs (in 75% to 100%) and IOVs might be the only intraorbital sign of a CCF and is often but not always asymmetric (Fig 19). 54-57 One might see bilateral enlargement or even contralateral-only enlargement of the SOV, depending on the venous drainage pathways or an unusual bilateral CCF. One might also note a completely normal-appearing orbit on imaging when there is little anterior drainage, although the patient might have oculomotor nerve palsy caused by the CS abnormality. These have been referred to clinically as white-eyed cavernous shunts. 58 SOV thrombosis should be noted on imaging, because this might be a cause for clinical worsening of symptoms, as reported by Sergott. 59 In


Fig. 13. Another example of a Type D CCF showing internal and ECA supply. (A) External carotid arteriogram in the lateral projection with early cavernous sinus opacification (open arrows) noted. There is drainage into the superior and IOVs (black arrows). (B) Internal carotid arteriogram in the lateral projection showing early opacification of the posterior cavernous sinus (open arrow) and inferior petrosal sinus (arrowhead).

Sergott's study, there was later spontaneous improvement in the clinical picture in all 4 patients involved. This may be seen on MRI as high T1 SI in the SOV, but this can be obscured by adjacent high SI fi'om the orbital fat, although chemical shift artifact and, particularly, fat saturation orbital imaging would allow the diagnosis. Sometimes slow flow in the SOV might have high T1 SI even without thrombosis, and differentiation would be

Fig. 14. An example of a Type B CCF. Internal carotid arteriogram in the lateral projection shows early opacification of the posterior cavernous sinus (open arrow).

difficult (Fig 20). In this situation, phase contrast (PC) MRA with a low velocity encoding gradient might help. On non-contrast-enhanced CT, an acutely thrombosed SOV would be seen as a hyperdense structure with attenuation greater than the normal arteries and veins. On CECT, a thrombosed SOV may not opacify or present as a filling defect. A recently described finding was that of choroidal effusion as a CT sign of a C C E 6~

With newer CT scanners, dynamic CT imaging has been reported in which serial CECT images are obtained at the level of the CS and show early opacification as a sign of CCF. 61 Dynamic MR imaging allowing very rapid image acquisition also can show early CS opacification after intravenous injection of gadolinium before the expected venous phase.

MR angiography and CT angiography also can play a role in the initial workup of CCFs. MRA techniques include time of flight (TOF) and phase-contrast M R A . 62 On MRA/magnetic resonance venography (MRV), high-flow lesions will exhibit high SI in the the CS and arterialized veins (which would normally have less flow SI). PC MRA/ MRV can determine direction of flow and quantitate flow velocities and identify slow flow in venous structures that might not be visible on a TOF study. MRA/MRV also can identify associated findings such as carotid artery stenosis or venous stenosis/occlusion. Primary findings reported to be characteristic of CCFs on MRA have been flow signal on TOF studies in the CS and IPS/SOV as well as widening of the CS or SOV, with Hirai et al63 reporting a sensi-


Fig. 15. Cross sectional imaging in a patient with a CCE (A) Contrast enhanced coronal CT. (B) Proton density weighted axial MRI image. This patient is the same as in Figure 14. There is only a slight asymmetry with right cavernous sinus (open white arrow) appearing slightly larger than the left on the CT. This shows how carotid cavernous fistulas might be subtle or inapparent on cross-sectional imaging.

Fig. 16. Post-gadolinium-enhanced coronal Tl-weighted MRI of the brain in a patient with a low-flow CCF on the right. The fight cavernous sinus (open arrow) appears slightly wider with greater enhancement of the wall in this dural fistula.

tivity of 83% and a specificity of 100% with a FISP (fast imaging with steady state free precession) technique. Hi- rai reported that in comparing CECT, spin echo-MRI (SE), post-gadolinium MRA, and 3-dimensional (3D) MRA, the 3D MRA technique was the most useful. Hirai also reported that dural arteriovenous fistulas (AVFs) show cur- vilinear or spotlike areas of increased SI on 3D FISP adjacent to or within a CS and increased SI within the CS, whereas direct CCFs showed only increased SI within the CS. Whereas CCFs show increased flow signal in the CS and draining veins such as the IPS, one must be careful in interpreting this finding on MRA, especially in asymptomatic patients; Ouanounou 64 reported up to 17% of asymptomatic patients without a history of CCF showed some flow signal in the posterior CS and IPS on 3D-TOF MRA. These findings were scanner- and technique-boses depen- dent. Another pitfall of TOF MRA is that throm(either in the CS or a draining vein/varix) can mimic flow signal and patency attributable to T1 shortening. However, if the question arises, attention to the SE sequences and an additional PC-MRV will resolve this uncertainty. Coskun 65 used spiral CTA (injection of intravenous contrast and rapid image acquisition) to identify 4 out of 4 CCFs and major drainage pathways, with findings including early venous opacification and venous enlargement (including


Fig. 17. Example of venous infarction associated with a CCE This is the same patient as in Figure 28. (A) Tl-weighted axial MRI showing low signal in the left perisylvian region (arrows). (B) T2-weighted axial MRI showing high signal in the same distribution (arrows).

of the CS, SOV, IPS, and basilar venous plexus). Limits of MRA/CTA include the inability to clearly identify the fistula location in direct CCFs, identification of small feeding arteries seen on conventional angiography, and not de- tecting some low-flow fistulae. Xenon CT has been used to evaluate brain perfusion and steal associated with acute traumatic CCFs. 66

Other Imaging Modalities Plain films have little role in the evaluation of CCFs,

but can be useful for baseline and follow-up purposes to determine balloon status for possible interval migration or deflation. Nuclear medicine has played a l imited role in CCF evaluation. Brain perfusion studies, such as with TcHMPAO and PET (positron emission tomography)

Fig. 18. Orbital CT findings in carotid cavernous fistula patients showing extraocular muscle enlargement. (A) Noncontrast-enhanced coronal CT showing subtle asymmetric extraocular muscle enlargement (arrowheads) on the fight, (B) Contrast-enhanced axial CT in a second patient showing more obvious extraocular muscle enlargement (arrowheads) on the left.


have been used to evaluate perfusion before and after treatment. These have been used also with BOT to more quantitatively assess tolerance of carotid artery sacrifice.

Ultrasound findings of CCF in t5 patients were reported by Chen, 67 including findings on carotid duplex sonography and trancranial color-coded duplex sonography (TCCD) through transorbital, transtemporal and transforaminal windows. Carotid duplex sonography revealed decreased resistive indices and increased flow in the ICA in most direct CCFs, whereas indirect CCFs showed increased flow in the ECA in some patients. They also reported seeing a mosaic flash of color doppler signal on TCCD in the expected region of the CS in direct CCFs but not with indirect CCFs. Turbulent flow in the CS was observed, whereas increased flow with reversed direction was noted in the SOV. The study also reported identification of some patients in whom an ICA aneurysm led to the CCE The aneurysm had a bidirectional, more laminar flow signal on color doppler unlike the adjacent turbulent flow in the CS. The authors concluded that ultrasound might be useful in identification of direct versus indirect CCFs and noninvasive follow-up of treated and conservatively managed patients. Kotva168 reported periorbital sonographic evaluation of CCFs with indirect findings including etevated ipsilateral flow volume and decreased

Fig. 19. Contrast-enhanced CT in a patient with a right CCE There is subtle enlargement of the right cavernous sinus (open arrow), but the most obvious finding is the asymmetrically enlarged right SOV(arrowheads).

resistive index in the ICA and retrograde flow in the ophthalmic veins in the ipsilateral orbit with arterialized doppler flow signal. Although similar findings also might be seen in the ICA with intracranial arteriovenous malformations (AVMs), they report the flow increases are greater with CCFs, and there is usually no reversal of flow in the ophthalmic veins with AVMs.

Jugular venous blood oxygen saturation levels have been used to diagnose CCFs because of the higher oxygen content caused by the fistula. 69 Transcranial cerebral oximetry also has been used to monitor therapy. 7~

Misdiagnosis

Whereas posttraumatic exophthalmos is a common presentation of Type A CCFs, this finding is not pathog- nomonic. Orbit roof fractures with retrobutbar brain herniation might precipitate marked exophthalmos. The absence of a bruit should suggest another diagnosis later confirmed by MRI and/or CT (Fig 21).

Direct fistulous connections decompressing into the CS from sources other than the cavernous segment of the ICA have rarely occurred. There have been at least 2 instances in a posttraumatic setting in which a fistula occulted between the posterior communicating artery and the CS (Fig 22). 71'72 A third reported fistula occurred between the supraclinoid segment of the ICA and the CS ]3

Additional clinical and other imaging mimics of Type A CCF that should be differentiated angiographically include indirect (Types B, C, D) CCFs and dural AVFs ouside the CS but with primary drainage into the CS (IPS and tentorial marginal sinus AVFs, for example). 74 Also, there might be a CCF with obstructed ipsilateral outflow pathways leading to enlargement of the contralateral CS and resulting contralateral orbital or cranial nerve symptoms. Also, there might be occasional isolated enlargement of the SOV in which the angiogram shows normal or late opacification rather than early as with CCFs. In trauma patients, rarely, a meningeal artery to meningeal vein fistula with drainage into the CS can mimic a CCE 33 We have seen one patient present with a spontaneous orbital arteriovenous fistula that mimicked a CCF clinically and on cross-sectional imaging.

Because of the insidious presentation and lack of precipitating event, indirect carotid-cavernous fistulae are often misdiagnosed. The chronic red eye and diplopia in these patients often leads to the misdiagnosis of chronic conjunctivitis, orbital pseudotumor, or Graves' disease, resulting in inappropriate treatment. 41

Although extraocular muscle enlargement is a common finding in CCFs, it is an even more common finding in Graves' disease. However, in CCFs the more uniform enlargement of the extraocular muscles best identified by mi- dorbital CT should exclude Graves' disease, in which the inferior rectus, followed by the medial rectus and superior rectus muscles, are most frequently enlarged. On occa-


Fig. 20. Patient with fight orbital signs of CCF showing a markedly enlarged right SOV (white arrow). (A) Gadolinium- enhanced coronal Tl-weighted image of the orbits. (B) Axial proton density-weighted image. (C) Contrast-enhanced axial orbit CT.

sion, thyroid ophthalmopathy might present as an asymmetric predominantly unilateral enlargement of the extraocular muscles with proptosis and increased density of the orbital fat (Fig 23). Anterior displacement of orbital fat precipitated by pressure from enlarging orbital contents also is noted in Graves' disease and might further differ- entiate this disease from carotid-cavernous fistulae. 75

An additional cause of extraocular muscle enlargement is orbital pseudotumor, in which a minority of patients will have an isolated, singly enlarged extraocnlar muscle noted. Finally, orbital trauma also can produce extraocu-

lar muscle enlargement. Most important, of these abnormalities, except for the extremely rare, orbital AVE only CCFs have an enlarged SOV. Conditions resulting in an enlarged SOV in addition to CCF include orbital venous drainage of an intracranial AVM, bilateral sigmoid sinus atresia, isolated varix, non-CCF-related SOV or CS thrombosis, orbital apex mass causing SOV compression, thyroid ophthalmopathy, idiopathic orbital inflammation, capillary hemangioma, and normal variant. 53

Occasionally, despite an in-depth clinical evaluation and noninvasive radiographic assessment, a definitive diagnosis cannot be established. Here, a high-resolution arteriogram with selective injections of both external and internal carotid arteries and occasionally the posterior circulation might be necessary to secure the diagnosis. 4~

CCF Treatment

Surgical Treatment of CCFs

Surgical intervention in direct CCFs was the initial method of treatment. Endovascnlar treatment later be- came the favored primary method because of the devel-


Fig. 21. (A) An example of posttraumatic exophthalmos. In this patient, despite an initial clinical impression of a Type A fistula, no bruit was auscultated. (B) Diagram showing the imaging findings of cribriform plate fracture with brain herniation into the posterior orbit displacing the globe anteriorly.

opment of balloon technology, microcatheters, and coils. Surgery for CCFs is mainly limited to the occasional direct fistulae and only rarely used with indirect CCFs. Initial surgical methods included cutting down to the ICA and either occluding the cavernous segment entirely or packing it with muscle. 76-79 Early surgical methods also included ICA trapping by cervical ICA occlusion and clipping of the supraclinoid ICA. This was successful in two thirds of the patients but was unsuccessful in the other third because collateral flow from the ECA or ophthalmic artery. Later surgical techniques included direct repair of the CCF with preservation of the ICA but were technically extremely difficult. 8~ In 1979, Mullan 11 reported surgical packing of the venous compartment as an alternative to the direct arterial approach by entering through Mullan's triangle (between V1 and V2) or through one of the draining veins (SOV, IPS, SPS, and so on), but this procedure also could have significant morbidity.

Currently, the endovascular approach is the favored approach, with surgery reserved for patients with unfa- vorable vascular anatomy, such as access artery narrowing caused by trauma (iatrogenic or other cause), a wide necked cavernous carotid artery aneurysm, a lack of direct venous access to the CCF, or in patients with intradural dissections with subarachnoid hemorrhage or as a part of a concomitant surgical procedure. Today,

surgery mainly relies on trapping of the cavernous ICA or packing of the CS. The operation is usually preceded by a BOT to determine if the carotid artery can be sacrificed. In those patients who fail the BOT, an extracranial-intracranial bypass procedure might allow occlusion of the affected ICA while allowing sufficient intracranial flow. The BOT might be falsely positive in some patients because of retrograde flow in the intracranial ICA during BOT, which would not be present once distal control is also obtained.

Surgical approach is based on the fistula location in the cavernous ICA. A frontotemporal craniotomy commonly is used. Intraoperative angiography by the femoral approach is helpful and can serve also as an access site for balloon occlusion of the more proximal ICA when proximal control is needed. Usually, control of the proximal ICA is first achieved either by endovascular technique or direct cervical ICA approach. Then, before occluding the proximal ICA, distal control of the ICA at the clinoidal segment proximal to the origin of the ophthalmic artery (to preserve retinal artery flow and minimize the risk of retrograde flow by ECA collaterals) is obtained. Distal control should be obtained before proximal occlusion to ensure that steal phenomenon does not precipitate cerebral ischemia.

After obtaining control of the cavernous ICA, the CS is approached through a dural opening, the location of which


V

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Fig. 22. (A, B) AP and lateral internal carotid arteriogram showing a posterior communicating artery aneurysm (curved arrow) decompressing into the cavernous sinus. There is decompression into the SOV (arrowheads) and posteriorly into the superior (small arrow) and inferior (large arrows) petrosal sinuses. (C) Diagram depicting a posterior communicating artery aneurysm decompressing into the cavernous sinus. (Reproduced with permission of the American Journal of Neuroradiology)

depends on the location of the carotid fistula. Then, thrombogenic material is packed into the CS to precipitate com- pressive carotid artery occlusion, direct intracarotid packing, or packing around the carotid in the region of the fistula (thus allowing preservation of carotid artery patency). Serial intraoperative angiograms can be obtained to evaluate results of the packing to confirm closure of the fistula. The primary complication from this procedure is cranial nerve injury with palsies seen in up to two thirds of patients, including permanent injury in up to one quar- ter of all patients. 81 Successful surgery includes cases in which the fistula is completely obliterated and incom- pletely closed but with enough slowed flow that further treatment is not clinically required. Other methods, such as direct clipping or suturing of the fistula, are much more difficult to perform, sl

Day and Fukushima s2 reported on direct microsurgery in 9 patients with Barrow Type D CCFs after initial failure of endovascular therapy. The operative technique was a combined extradural and intradural approach with blockage of ECA feeders and then sequential dural opening of the cavernous triangles followed by packing

with Surgicel (Johnson and Johnson, New Brunswick, NJ) to obliterate the arteriovenous fistula. They were able to achieve complete resolution of the CCFs in all 9 patients without a reported recurrence and with resolution of the presenting symptoms. Transient diplopia and trigeminal distribution hypesthesia were seen in all patients but resolved by 6 months after surgery. One patient had permanent hemiparesis secondary to carotid artery occlusion that we believed was caused by overpacking. A second patient developed an abducens nerve deficit that was also believed to be caused by overpacking. They reported an understanding of CS anatomy and triangular corridors of entry was key to the surgery. Tu s3 reported on direct surgery of 19 patients with Types A, C, and D fistulae after failure of endovascular therapy in 18 patients and primary surgery in one. Goals of the surgery were fistula obliteration and ICA preservation. Access was obtained by a combined extradural-intradural approach with proximal and distal ICA control. Direct methods of fistula closure used included clipping of the fistula, suture repair of the fistula, or sealing the fistula with fascia and acrylate glue. Indirect methods included

Fig. 23. Patient with Graves' disease. Note the enlargement of the right medial rectus muscle (arrow) with sparing of the lateral rectus muscle (arrowhead).

packing the CS with muscle, Gelfoam (Pharmacia and Upjohn Co, Kalamazoo, MI), Surgicel, and thrombin- fibrinogen sealant. In 3 cases, a high-flow large pseudoaneurysm did not allow resection of the fistula with ICA preservation. In these 3 patients, an intracranial bypass between the petrous segment and supraclinoid segment of the ICA using a saphenous venous graft was performed, followed by permanent occlusion of the cavernous segment of the ICA. Initial attempts at direct fistula closure had mixed results, and their technique shifted to stepwise opening and packing of all the CS compart- ments. Two of 8 patients treated with packing had ICA thrombosis that the authors attributed to overpacking. They were able to achieve ICA patency postoperatively in 73% (14 of 19), although none of the thrombosed ICA patients developed permanent neurologic deficits attributable to ischemia from the thrombosed artery. Eight patients developed transient third nerve palsy, but all recovered within days to 6 weeks after surgery.

Batjer et a184 reported on a combined surgical and angiographic technique of Type A fistula obliteration after failure of endovascular therapy. They reported endovascular balloon fistula occlusion was particularly difficult with fistulae involving the posterior carotid artery wall at the cavernous entry, the anterior inferior carotid wall in the initial horizontal cavernous segment, and small or low-flow fistulae at any location because of difficulty of advancing the flow-directed balloon into the fistula. A subtemporal transdural approach to the CS was used. They precisely mapped the location of the fistula with intraoperative angiography and opened the dura at this location,

Carotid Cavernous Fistula �9 Tytle and Punukollu 1 O1

followed by insertion of an introducer sheath. A latex balloon (or balloons) was then inserted through the sheath and inflated to appropriate levels to ensure fistula closure while maintaining ICA patency with confirmation of the result by intraoperative arteriography.

Endovascular Treatment

Balloons were among the first modern endovascular embolic materials used for the treatment of CCFs and are still considered by many to be the primary method of treating direct CCFs (Fig 24). The technique originated in Russia, and, over the years, various balloon materials (principally silicone and latex) and various delivery and detachment systems have been used. s5 Latex is more compliant than silicone, allowing greater inflation of a similarly sized deflated introduction balloon. The balloons classically are marketed in a variety of sizes. The silicone detachable balloons (DSBs) are marketed by Boston Scientific/Target Therapeutics (Fremont, CA). The balloon valve base is color-coded to identify the specific release range including low-, medium-, and high-release to accommodate different flow situations. Delivery methods have included loading the balloon unsecured onto a microcatheter tip, tying the balloon to the tip of the microcatheter with a ligature, using coaxial catheters (where the outer catheter pushes the balloon off the smaller inner catheter), or even an electrolytically detachable wire-guided balloon. 86 Various materials have been used to inflate the balloon, with Metrizamide and HEMA (hydroxyethyl methacrylate, often mixed with Metrizamide) historically used. More recently, for best long-term results, the isosmolar contrast agent Visipaque (iodixanol, Nycomed Inc, Princeton, N J) has been recommended as a balloon inflation agent. The silicone balloon is semipermeable and produces much less inflammation as compared with the latex balloons, s6 Sili- cone balloons recently have been FDA-approved in the United States for treatment of carotid cavernous fistulae and for carotid artery occlusions.

Technical aspects of balloon deployment include placing a guide catheter in the ICA or CCA, then advancing the balloon in coaxial fashion under fluoroscopic guid- . ance. The balloon may not make all the bends in the ICA and if it fails to advance, gentle inflations and deflations might propel the balloon along. Usually, once the balloon is at the level of the fistula, it is sucked into the fistula by sump effect because of the the high flow rate. The position of the balloon within the fistula rather than the carotid artery lumen has to be confirmed fluoroscopically before inflation. The balloon might then be inflated and a control angiogram performed to determine if the balloon is of the appropriate size and location before deployment. Some fistulae require several balloons for complete closure because of the large size of the CS (Fig 25), but most require only 1 balloon. One might achieve complete clo-


Fig. 24. Patient with posttraumatic type A fistula. (A) Lateral internal carotid arteriogram showing immediate carotid artery decompression into the cavernous sinus (open arrows), ophthalmic veins (black arrow), and inferior petrosal sinus (arrowhead). (B, C) Frontal and lateral angiographic images following endovascular repair with a solitary detachable balloon (arrow).

sure or only partial closure of the fistula with this technique. In cases of partial closure, in which there is enough slowing of flow, there may be adequate clinical improvement such that no further immediate treatment is needed. A follow-up study in a few weeks to months might show the fistula has completely closed. On occasion, it is safer to occlude the ICA proximal and distal to the fistula when the CS cannot be reached adequately endovascularly or the CS is so large that it would require too many balloons, causing pressure on and narrowing of the ICA. If the direct ICA arterial approach is not feasible, alternative routes to CS embolization include venous by either the IPS (femoral approach) or SOV (surgical cutdown as needed or endovascular approach by femoral to facial and angular vein, then to the SOV) and direct surgical exposure of the sphenoparietal sinus or a draining cortical vein. In addition, there are alternative transarteriat routes when the ipsilateral ICA is not approachable, including through the contralateral ICA, patent anterior communicating artery, and the vertebral artery and patent posterior communicating artery.

ICA preservation is a goal of balloon treatment of direct CCFs and can be accomplished in up to 90% of cases (although reported ranges include rates as low as

60% patency), s7 ICA preservation rates improve with greater operator experience. ICA occlusion should be considered in cases in which the balloon partially pro- trudes into the carotid artery lumen with thromboembolic potential or when it is not possible to keep the balloon in the CS because of too large a fistula. If ICA occlusion is necessary, BOT might be needed before the procedure unless angiography suggests all the carotid artery flow is being diverted into the fistula. The BOT is best performed at the level of the fistula neck or below, with BOT above the fistula avoided as it might lead to sudden elevations of pressures in the draining veins and accom- panying orbital and intracranial complications. BOT can be combined with brain perfusion imaging, such as nuclear brain scans (TcHMPAO, PET) or Xenon-CT to quantitate perfusion. Proximal to the level of the fistula, BOT can be falsely positive, because it might allow retrograde flow into the CCF and steal blood flow. Potentially, this can result in cerebral ischemia that would not occur during the course of permanent distal and proximal carotid artery occlusion. Permanent carotid artery occlusion is usually accomplished with balloons proximal and distal to the level of the fistula. If the carotid artery distal to the fistula is not occluded,


A

J

Fig. 25. Patient with a posttraumatic type A fistula. (A) Lateral internal carotid arteriogram after deployment of the second of 3 balloons (open arrows) in the contrast opacified cavernous sinus (arrowheads). (B) Lateral internal carotid arteriogram one week after balloon deployment. The 3 opacified balloons (arrows) can be seen within the cavernous sinus. Note complete fistula closure and cavernous internal carotid artery displacement and narrowing (arrowheads).

retrograde carotid artery flow or collateral flow through the ophthalmic artery can reconstitute the CCF with loss of arterial access for further intervention. The ophthalmic artery origin from the carotid artery can be blocked safely in the majority of patients, with preservation of flow in the retinal artery through ECA collaterals. Cases of subarachnoid hemorrhage associated with CCF (ie, traumatic dissection with intracranial extension) present a management difficulty in that posttraumatic subarachnoid hemorrhage, associated vasospasm can be severe on occassion and the lack of inflow from the occluded carotid artery can make the situation worse. Additionally, carotid artery occlusion in such cases leads to loss of access for possible angioplasty or selective papaverine infusion to treat vasospasm. The carotid artery dissection might make safe carotid artery navigation for balloon occlusion impossible and require a surgical or transvenous approach rather than the preferred arterial approach, s7

Technical success in closing a direct CCF has been reported as being as high as 98% with the balloon technique in some series, but it is more commonly in the 85% to 90% range, with rates improving with modern microcatheters and improved navigation and improve- ments in secondary salvage procedures such as coil embolization, s7 A significant number of CCFs have a smaller residual fistula at the end of the procedure that completely seals later (up to 27% in Tsai's ss series). Clinical improvement can be seen in up to 90% of patients, but some deficits such as cranial nerve palsy and blindness caused by retinal ischemia are permanent. Masaryk et al s9 recently described a technique wherein

direct CCFs that were difficult to enter with the balloon might be entered by using a double-balloon technique. This consists of placing 2 guide catheters in the ICA and putting a minimally inflated DB at the fistula ostium, then positioning a nondetachable balloon (NDB) next to this. Inflating the NDB will direct the DB into the CS. Morris 9~ further noted that in a similar procedure, he introduces both DB and NDB catheters through a single 8-fr guiding catheter. In Lewis '9~ series, no long-term clinical or radiographic evidence of fistula recurrence was noted in 86 direct CCF patients treated with detachable latex and silicone balloons. We have witnessed a case of recurrent, Type A fistula a week after successful DSB closure, a finding noted by others. 87'93

According to Tomsick et al, a7 complications from the balloon occlusion procedure occur in about 6% of cases, including death in 1%. Complications of balloon use include balloon rupture or deflation (with recurrent CCF or pseudoaneurysm formation), premature deployment, cranial nerve palsy caused by mass effect, rupture of the vessel if there is overinflation, and balloon migration or prolapse. As a result, this might lead to embolic infarction, including occuring months after the procedure and causing new ICA occlusion or embolizing to a cerebral artery such as the middle cerebral artery (MCA). Balloon prolapse into the ICA also can result in proximal ICA occlusion with ischemia aided by retrograde flow in the more distal ICA when the fistula recurs. There have been several postulated etiologies of balloon rupture, including impinging on a bony spicule in trauma cases, on sharp atherosclerotic calcification arising from the carotid artery, or even impinging on coils when the 2 are


used simultaneously. 87"92 Balloon deflation can be potentially devastating, allowing not only recurrence of the fistula and its associated symptoms, but also potential balloon migration into the carotid artery and causing cerebral infarction as a result of narrowed lumen or slowed flow and thromboembolic complications (Fig 26). This last complication is most often associated with a wide-necked aneurysm arising from the ICA, where the partially or fully deflated balloon can enter the carotid artery lumen. Some balloon deflation occurs over time with all nonpolymerizing inflatants, but the balloons need to be inflated only 1 to 2 weeks in most cases to allow the fistula to seal, although there have been reports of deflation or change in position months after placement with fistula recurrence. 93 According to Lewis et al, 91 most fistulae do not recur after the first 48 hours after balloon embolization. Thrombus forms around the balloon even when it deflates, preventing fistula recurrence. Balloons have been filled with more permanent solidify- ing agents such as HEMA (hydroxyethyl methacrylate) when deflation is a concern.

Treatment of balloon migration has included percutaneous needle puncture fluoroscopically through the foramen ovale or transorbital route under CT guidance and aspiration of the migrated balloon. 94'95 Tomsick 87 recommends anticoagulation with heparin during the procedure to avoid the thromboembolic complications of having introduced the catheter/balloon into the intracranial circulation. Other complications reported by Tomsick 87 include infarction, possibly from an air bubble during control angiography, and cranial nerve palsies. Debrun TM experi- enced a 20% rate of transient ophthalmoplegia possibly caused by pressure by the inflated balloons with resolu-

tion of the ophthalmoplegia over time. Pseudoaneurysms can occur as the balloon slowly deflates and axe seen as a pouching out of contrast from the ICA fistula site, but without venous drainage. Debrun 14 reported a 44% incidence of pseudoaneurysms in his series, which he attributed to the premature balloon deflation as a result of an imperfect ligature of a latex balloon. Tomsick s7 indicates a much lower incidence of pseudoaneurysms. The pseudoaneurysm can lead to mass effect with new pain or ophthalmoplegia after the initial success. Symptomatic pseudoaneurysms must be treated, most often with ICA occlusion, although Guglielmi Detachable Coil (GDC) (Boston Scientific/Target Fremont, CA) embotization and balloon occlusion with a permanent solidifier such as HEMA or silicone fluid also might be used. If asymptomatic, most pseudoaneurysms are of little clinical signifi- cance and do not by themselves require treatment. 87

Other occasional complications include normal perfusion pressure breakthrough (especially in chronic CCFs with steal) and resulting cerebral edema or hemorrhage, infection and groin hematoma. Deaths have been associated with ICA occlusion intolerance (intentional or caused by post-procedure balloon prolapse) (Fig 26) venous outflow redirection caused by balloon placement, or migration with the development of venous hypertension including a report of a pontine hemorrhage. 96 According to Tomsick, there have been no reports of death caused by CS rupture by a detachable balloon. 87 IPS ruptures during transvenous navigation have been reported and treated by embolization of the IPS. 97

Direct CCFs also can be treated with coil deployment, either as the primary method of treatment or as an adjunct to balloon or surgery. Various coils are available

Fig. 26. Patient with a type A fistula who underwent balloon embolization. (A) Unsubtracted lateral internal carotid arteriogram shows balloon (arrow) in place. (B) Digital subtraction lateral internal carotid arteriogram showing narrowing of the cavernous ICA (arrow). The anterior defect (arrowhead) might be an artifact of subtraction caused by the balloon. The patient had a follow-up arteriogram 1 week later that showed complete occlusion of the ICA. Fortunately, this patient remained asymptomatic.

including GDC (which is retrievable and is electrolytically detached once in position) as well nonretrievable fibered and nonfibered coils. According to Derdeyn and Strothers, 98 the two primary indications for coil treatment of type A CCFs are (1) individual unable to tolerate ICA occlusion and (2) Ehlers-Danlos Type IV patient with a Type A CCF (prone to arterial rupture/dissection such that a venous approach might be favored with a 36% morbidity and 12% mortality rate reported from angiography alone by Schievink et a199).

According to Derdeyn and Strothers, 9s some fistulae are too small or have too low a flow rate to allow the balloon traversal across the fistula ostium. In other patients, there is too much carotid artery atherosclerotic disease or tortuosity to allow safe balloon navigation. In these patients, a wire-directed microcatheter might be able to more easily access the fistula transarterially for coil placement. 98'1~176 The transarterial route is often the sim- plest, most direct approach to the Type A fistula for coil packing. However, if needed (ie, when there is no arterial access because of carotid artery occlusion or trapping, having already placed detachable balloons in the vicinity of the fistula or if arterial puncture is contraindicated as with Ehlers-Danlos patients), a transvenous approach can be used. This includes from the common femoral vein to the IPS to CS route, through the facial angular vein or by surgical cutdown to access the SOV (Fig 27).

Disadvantages of the venous approach include the inability to access the fistula because of difficult CS anatomy. This can result in incomplete CS packing and occasional guidewire perforation of the arterialized veins. Coils have the advantage of being able to conform more closely to the CS shape than balloons while preserving the patency of the carotid artery lumen.

Fig. 27. Lateral control angiogram during transorbital coil embolization of a difficult-to-access indirect CCE Access to the SOV(arrows) was obtained by surgical cutdown. Cavernous sinus (open arrows).


Coil disadvantages include the need to pack numerous coils to slow the fistula adequately to allow thrombosis to occur, unlike the direct and often immediate closure with balloon placement. The coils also might exert mass effect and result in cranial nerve injury. Additionally, the coils may result in a change in the venous drainage pattern, resulting in new symptoms attributable to venous hypertension. Halbach advocates coil embolization of the SOV or sphenoparietal sinus preliminary to CS coil embolization if these represent major drainage pathways (Fig 28). 1~

Complications of coil 3 principally involve coil deployment and migration into an unintended vessel or prolapse back into the carotid artery lumen in cases of wide-necked carotid artery aneurysms. Associated ischemic complications or vascular perforation have also been reported, lm Nonfibered retrievable coils such as the nonfibered GDC have both an advantage and disadvantage of not being particularly thrombogenic, whereas fibered coils are much more thrombogenic. One has to be certain the coils are being deposited on the venous side of the fistula rather than having an arterial component where thrombosis and infarction can occur. Morris m2 described a case in which a nondetachable balloon was inflated across a large Type A fistula in the ICA while a transvenous route was used to pack the CS with coils. The inflated balloon prevented the coils from prolapsing into the ICA during coil deployment. This also ensured ICA patency when it could no longer be seen easily on control angiography becuase of the superimposed coil mass.

Unusual techniques of CS access for CCF endovascular closure in the face of previous carotid artery occlusion have been reported. Teng et al 1~ described percutaneous access to the CS in direct CCFs by transorbital puncture of the CS through the superior orbital fissure. The CS was then filled with coils, gelatin sponge strips, or cyanoacrylate. Barker et al 1~ described surgical exposure of the medial wall of the CS by a transethmoidal transsphenoidal approach followed by direct cannu- lation of the venous outflow and coil embolization. Hatbach et al a~ described direct percutaneous puncture of the carotid artery in 3 patients with traumatic carotid artery occlusions. They described puncture of the carotid artery above the occluded segment followed by access to the fistula and balloon or coil embolization.

Indirect (Types B, C, and D) CCFs might be left untreated, conservatively treated, or, if warranted, closed through a transvenous approach. Transarterial (including combined transvenous and transarterial) and surgical approaches and radiotherapy also have been used. Unlike Type A CCFs, which rarely close spontaneously, indirect CCFs are known to have a significant incidence of spontaneous closure. This can be as high as 10% according to Dandy, 1~ whereas Hamby et a1107 indicated an up to 40% rate of spontaneous resolution after diagnostic

106 Seminars in Cerebrovascutar Diseases and Stroke Vol. t No. 1 March 2001

anglography alone. They often present a low risk and might not warrant the dangers associated with intervention. These might be followed clinically to ensure stabil- ity or resolution.

Manual carotid artery compression is a conservative method described to treat indirect CCFs in patients in whom urgent therapy is not needed and has a success rate as high as 30%. l~ The carotid compression maneuver involves allowing the patient to use the hand opposite the side to be compressed to exert firm pressure on the carotid artery briefly but repeatedly and can be done for weeks before achieving success. The opposite hand is used so that if any significant vascular compromise occurs, the patient might develop weakness in the compressing arm and thereby remove it. This procedure also results in concomitant jugular vein compression at pressures

Fig. 28. Patient with a type D fistula with symptomatic cortical venous infarction, (A) Sphenoparietal sinus angiogram (large arrow) during coil embolization. Note the persistent retrograde flow into the superficial middle cerebral vein (small m-rows) and cortical veins (an'owheads). (B, C) Postcoiling frontal and lateral skull base radiographs showing coils within the sphenoparietal sinus (large arrows), cavernous sinus (curved arrow), and SOV(smatl arrow). This is the same patient as in Figure 17.

needed to compress the carotid artery and thus produces both venous and arterial stasis. Relative or absolute con- traindications include hypersensitive carotid sinus syndrome; atherosclerotic stenosis or ulceration of the carotid artery; or low-flow or borderline cerebral ischemic conditions, vertebral basilar insufficiency, reflux syncope or hypotension, transient ischemic attacks, cardiac arryth- mias, and previous fistula region hemorrhage.t 1 One death from the procedure has been reported, to9

Higher risk fistulae as identified by Phatouros et a144 include those with associated neurologic deficits, intradural hemorrhage, venous thrombosis, altered mental status, progressive ocular symptoms, or retrograde cortical venous drainage. 44 Such CCFs deserve more urgent intervention. The primary treatment of these indirect lesions is by the transvenous route. Access is usually through the femoral vein with navigation through the IPS into the CS, surgical exposure of the SOV (if there is IPS occlusion as is known to occur with CCFs), or by the facial angular veins. A predominantly pial draining dural CCF might be difficult to approach transvenously. Surgical vein exposure and transfemoral navigation into a pial draining vein have been described. A pterygoid plexus venous approach to a dural CCF has been reported. 11~ Halbach et al lm report a greater than 80% success rate using the transvenous route and occluding the SOV and CS with various types of coils. Phatouros 44 reports that patients might have an

initial worsening of symptoms after the procedure because of CS and SOV thrombosis, but this usually resolves over time and can be treated with steroids and/or heparin to decrease the severity of the symptoms.

Monsein, et a lm described a SOV approach whereby a balloon could be introduced into the CS to cure either direct or indirect CCFs. Direct surgical exposure of the SOV requires a surgeon trained in orbit procedures in addition to the endovascular operator. A transfemoral venous approach through the internal jugular vein (IJV), the superior sagittal sinus, and a draining cortical vein to access the cavernous sinus also has been described, t12

If the transvenous route is not possible or not adequate, the transarterial route might be used as either the primary method or as a salvage procedure to further slow flow through the indirect fistula(e). In some cases, if there appears to be only a single feeding artery, a transarterial route with embolization (preferably with coils, glue, or other liquid sclerosant) might be adequate and the preferred initial approach. Arteriovenous communication does not have to be completely obliterated during the procedure as adequate slowing of flow will let many cavernous sinuses eventually thrombose and close the fistula. Superselective embolization of the arteries feeding the fistula is carried out and embolization performed with particles such as polyvinyl alcohol (PVA), various coils, or liquid embolic agents and might close the fistula. Arterial branches that may be embolized include dural ECA feeders, such as branches of the ascending pharyngeal artery and internal maxillary artery (including middle meningeal artery, accessory meningeal artery, artery of the foramen rotundum, and vidian artery). A CCF might be supplied by bilateral ECA branches and requiring bilateral embolization. Rarely, there can even be dural branches from the vertebral artery that contribute to the posterior portion of a CCE Dural branches of the cavernous ICA that can supply the Types B and D CCFs include McConnell's Capsular arteries, inferolateal trunk and meningohypophyseal trunk branches and recurrent meningeal branches from the ophthalmic artery. The external branches may be safely selected and embolized in most patients, although this is not without danger becuase of collaterals with the ICA and vertebral artery. These might not be apparent at initial angiography but might open up over the course of embolization, placing the patient at risk for infarction. Additionally, various cranial nerves are supplied by branches arising from the ECA that can also participate in supplying the fistula. Particles (150- to 250-~m PVA) or coils are often used in the external circulation, but the occluded vessels often recanalize. Liquid embolic agents such as n-BCA (n-butyl cyanoacrylate) offer a permanent occlusion of the embolized vessel, but also penetrate more deeply into the small branches. This carries a greater risk of flow into eloquent collateral channels,


creating cranial nerve injury. Before embolization, pro- vocative testing with amytal and lidocaine can be performed, although this does not guarantee that a neurologic complication will not occur.

Attempted embolization of the ICA dural branches in Types B and D fistulae can be risky. Safe ICA dural branch embotization can be accomplished if the CCF is believed to be of persistently high risk, and other less risky approaches prove inadequate. The dural branches must be large enough to allow safe superselective catheterization. 113 Combination arterial embolization and radiosurgery also have been used to treat some dural type CCFs. 114

Radiosurgery Radiosurgery often has been used in the treatment of

cranial arteriovenous malformations. Over time, radiation therapy results in intraluminal occlusion of vascular channels and therefore is the basis for its use in dural CCFs. Stereotactic radiosurgery might be performed to more accurately focus the radiation. The Leksell gamma knife can be used in association with stereotactic angiography and MR for appropriate targeting. Protocols tested have included radiation therapy alone and transarterial or transvenous embolization before or after radiation therapy. Hirai et al ~15 reported 58% of dural CCF patients treated with radiation alone had improvement at 3 months, whereas estimated cure rates at 1, 2, and 3 years were 50%, 50%, and 80%, respectively. Low-flow and medium-flow dural CCFs responded best to radiation alone, whereas high-flow CCFs were much less likely to improve. Generally, it took months to years to realize results with radiation alone. A combination of embolization followed by radiation resulted in more rapid clinical and angiographic improvement. This also improved out- come in high-flow dural CCFs. Radiation has been advocated for patients with complex fistulae where embolization alone might not provide adequate treatment due to numerous feeders or inadequate venous access.

Additionally, radiation plays a role when there is significant dural ICA branch supply and safe transarterial embolization is not possible. As radiation usually requires considerable time to be effective, immediate treatment is recommended when there is prominent cortical venous drainage, visual acuity is diminishing or a CS varix is seen. Complications of radiosurgery include thromboembolic events related to the gamma knife planning angiography and the effects of radiation on the adjacent brain, cranial nerves, and normal arteries. The optic apparatus is usually spared from the effects of radiation as most dural fistulae are in the posterior inferior CS away from the chiasm.

Pollock et al H4 reported 19 of 20 patients treated with stereotactic radiosurgery and particulate embolization for dural CCFs had improvement of the clinical symptoms,


with 93% showing total or near total CCF resolution on follow-up angiography. Complications were mainly related to the embolization procedure or planning angiog-

raphy rather than the radiosurgery. The median maximal dose was 40 Gy. Embolotherapy was performed after radiosurgery to allow complete incorporation of the abnormal area in the radiation field as some embolized CCFs have been known to recanalize after embolization alone. Median time to clinical improvement was 2 weeks when combined radiosurgery and embolotherapy were used compared with 6 months with radiosurgery alone. Three patients had recurrent symptoms caused by CCF recanalization that responded to repeat embolizaton.

Acknowledgement

The authors extend their gratitude to Dr Bradley Farris of the Dean Magee Eye Institute (Oklahoma City, OK) for his assistance in preparing this manuscript.

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Fistula Carotido Cavernosa