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Show ORIGINAL CONTRIBUTION Successful Transarterial Embolization of a Barrow Type D Dural Carotid-Cavernous Fistula with Ethylene Vinyl Alcohol Copolymer (Onyx) Dheeraj Gandhi, MD, Sameer A. Ansari, MD, PhD, and Wayne T. Cornblath, MD Abstract: Endovascular occlusion via the trans-venous route is the favored treatment method for dural carotid-cavernous fistulas (CCFs). Ethylene vinyl alcohol copolymer (Onyx), recently approved for treatment of arteriovenous malformations, has advantages over conventional liquid embolic agents in its nonadhesive nature, which allows for longer injections with decreased risk of catheter retention. We report the use of Onyx in the successful transarterial embolization of a dural CCF fed by arterial branches of the internal and external carotid arteries (Barrow type D) after multiple failed attempts to access the cavernous sinus transvenously. Trans-arterial Onyx embolization could be a valuable option in transarterial treatment of CCFs when venous access is difficult. (J Neuro-Ophthalmol 2009;29:9-12) Dural-based carotid-cavernous fistulas (CCFs) are believed to result from dural sinus thrombosis (1). Also called indirect CCFs, they are distinct from direct CCFs (Barrow type A) that result from trauma or aneurysm rupture within the cavernous sinus (2). Dural CCFs are classified as type B, C, and D, depending on whether arterial feeders arise exclusively from the internal carotid artery (ICA) (type B), from the external carotid artery (ECA) (type C), or from both the ICA and ECA (type D) (3). Endovascular occlusion, usually via a transvenous approach to the cavernous sinus, is the standard of care for Department of Radiology, Division of Interventional Neuroradiology (DG), Johns Hopkins University, Baltimore, Maryland; Department of Radiology (Interventional Neuroradiology) (SAA), University of Chicago, Chicago, Illinois; and Kellogg Eye Center, Department of Ophthalmology and Visual Sciences (WTC) and Department of Neurology (WTC), University of Michigan, Ann Arbor, Michigan. Address correspondence to Dheeraj Gandhi, MD, Assistant Professor of Radiology, Division of Interventional Neuroradiology, Johns Hopkins University, 600 N. Wolfe St., Radiology B-100, Baltimore, MD 21287; E-mail: dgandhi2@jhmi.edu symptomatic dural fistulas. A variety of embolic agents have been used, including detachable platinum coils, high-grade alcohol, and n-butyl cyanoacrylate (nBCA) (4). Recently, ethylene vinyl alcohol copolymer (Onyx; ev3 Neurovascular, Irvine, CA) has been successfully used in combination with detachable coils via the transvenous approach (4,5) and after covered stent placement in treat-ment of a recurrent dural CCF via the transarterial approach (6). We describe a case of a complex type D dural CCF that was successfully treated with transarterial embolization with Onyx after multiple failed attempts to catheterize the cavernous sinus. CASE REPORT A 70-year-old woman presented with sudden pain in the right eye, together with redness and proptosis of that eye. She had undergone a liver transplant and suffered chronic renal insufficiency, brittle diabetes mellitus, congestive heart failure, and severe iodine allergy. Ophthalmologic assessment revealed best-corrected visual acuities of 20/70 in the right eye and 20/25 in the left eye. There was no afferent pupillary defect. Extraocular movements were full. Slit lamp examination showed modest chemosis and dilated, tortuous conjunctival vessels. Applanation intraocular pressures were 20 mmHg in the right eye and 15 mmHg in the left eye. Ophthal-moscopy disclosed retinal vein tortuosity and dot-blot hemorrhages in the right eye and no abnormalities in the left eye. Given her complicated medical history, an angio-graphic evaluation was considered risky and a trial of obser-vation and close follow-up was recommended. However, she experienced worsening visual acuity and orbital soft tissue swelling. After receiving sodium bicarbonate infusion and oral n-acetylcysteine for prevention of contrast agent-induced nephropathy, she underwent a cerebral angiogram that demonstrated a Barrow type D CCF with multiple tiny arterial feeders from the ICA and ECA bilaterally (Figs. 1 and 2). Multiple dural arterial branches opacified a septated J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 9 J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 Gandhi et al FIG. 1. Anteroposterior view of a left common carotid angiogram shows that tiny branches of the left internal carotid artery and left external carotid artery (arrows) fill the right cavernous sinus (arrowhead). right cavernous sinus (Fig. 3). The ipsilateral inferior petrosal sinus (IPS) was occluded, and there was no filling of the left cavernous sinus. Venous drainage was via an enlarged right superior ophthalmic vein (SOV), which demonstrated two areas of stenosis, one involving the junction of the cavernous sinus and SOV and the other involving the junction of the SOV and the angular vein (Fig. 3). FIG. 2. Anteroposterior view of the right external carotid artery shows multiple small arterial feeders from the internal maxillary artery (arrows) opacifying the right cavernous sinus (arrowhead). FIG. 3. Lateral view of the right external carotid artery shows a small septated cavernous sinus. Two areas of venous stenosis are marked with arrows, one at the junction of the right cavernous sinus and superior ophthalmic vein (SOV) and the other at the junction of the right SOV and angular veins (arrows). Under general anesthesia, a standard transfemoral 5-F diagnostic catheter was placed in the right ECA for arterial contrast agent injections. A 6-F guide catheter was navigated via transfemoral venous access over a 0.035-inch glide wire into the origin of the ipsilateral jugular vein. Using an Echelon 10 (ev3 Neurovascular) microcatheter and Synchro 14 microwire (Boston Scientific), access could be obtained into the IPS, but it did not opacify the right cavernous sinus. We were equally unsuccessful in gaining access to the right cavernous sinus via the contralateral IPS. We then punctured the right facial vein, but could not advance the microcatheter beyond the junction of the angular and superior ophthalmic veins. Next we exchanged the right ECA diagnostic catheter for a 5-F guide catheter (Envoy, Cordis, Miami) and superselectively catheterized the distal internal maxillary artery with an Echelon 10 microcatheter. The microcatheter was flushed with normal saline, and the catheter dead space was filled with dimethyl sulfoxide (DMSO). Onyx-18 was slowly injected into the microcatheter dead space over 1 minute. Using constant fluoroscopy and intermittent control angiography, the small branches of the terminal internal maxillary artery supplying the fistula were embolized. The Onyx cast finally penetrated and filled the septated portion of the cavernous sinus that harbored the fistula (Fig. 4). A total of 1.4 mL of Onyx-18 was injected over approx-imately 20 minutes. The microcatheter could be withdrawn easily after termination of Onyx injection. Postprocedure angiograms confirmed complete occlusion of the fistula (Fig. 5). 10 q 2009 Lippincott Williams & Wilkins Onyx Transarterial Embolization of an Indirect Fistula J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 FIG. 4. Magnified anteroposterior view shows the Onyx cast of the arterial feeders and the right cavernous sinus. There were no immediate complications. The patient had a significantly improved appearance of her right eye on the day after the procedure. Visual acuity and ophthalmic congestive features improved over the next few days. At a 3-week follow-up visit, a left abduction defect was noted, consistent with a partial sixth cranial nerve palsy. At the 12-week follow-up visit, the abduction deficit had mostly resolved, and visual acuity was back to baseline. The orbital soft tissue edema had completely resolved. FIG. 5. Post-embolization lateral angiogram shows com-plete occlusion of the fistula by Onyx (arrows). DISCUSSION We have demonstrated successful occlusion of a complex Barrow type D CCF with Onyx embolization via the transarterial route. A nonadhesive liquid embolic agent, Onyx received Food and Drug Administration (FDA) approval for embolization of intracranial arteriovenous malformations (AVMs) in July 2005, but it has recently also been used in the treatment of dural arteriovenous fistulas (7-9). One of its major advantages over nBCA is its nonadhesive nature, allowing for longer injections with decreased risk of catheter retention (8). Therefore, even fairly extensive and complex fistulas can be treated in one or two sessions (8,9). In our early experience (unpublished material), catheterization of a single large pedicle can allow Onyx penetration into the fistula and the draining vein, as well as retrogradely into the branches of other arterial feeders. This feature decreases the frequent need for super-selective catheterization and embolization of different arte-rial feeders with the use of nBCA. Nogueira et al (9) found Onyx to be more predictable and controllable than cyanoacrylates. Dural (indirect) CCFs are often supplied by tiny meningeal branches of the ICA and ECA that are difficult to catheterize superselectively. Therefore, transvenous occlu-sion of the cavernous sinus has been advocated as the mainstay of endovascular treatment because of its safety and high rate of permanent success (2,10,11). The goal of treatment is obliteration of the sinus and disconnection of the arteriovenous (AV) shunt, which can be accomplished with a variety of embolic agents. Detachable platinum coils are the most commonly used agents, but sometimes these fail to completely occlude the sinus (12). Coil placement can also be limited by the complex architecture, septation, or small size of the affected cavernous sinus. This limitation has prompted several inves-tigators to use nBCA as an embolic agent via the trans-venous approach to the cavernous sinus (2,11). In our patient, however, it was impossible to navigate the micro-catheter into the diseased cavernous sinus because of an occluded ipsilateral IPS, circular sinus, and high-grade stenosis at the junction of the SOV and angular vein. Although surgical exposure of the SOV was an option, this would have entailed significant prolongation of the procedure. We were encouraged to use Onyx via the transarterial approach on the basis of our recent success with this agent in treating dural AV fistulas (unpublished data). A unique feature of Onyx is its ability to penetrate and travel along tiny arterial branches, ultimately allowing casting of rather remote venous pouches and occluding the fistula. This property is very helpful when the vascular tortuosity or small size of feeders prevents distal navigation of the microcatheter. 11 J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 Gandhi et al Arat et al (4) first described intracavernous injection of Onyx, in combination with coils, via an IPS approach. Subsequently, Suzuki et al (5) described the combined use of coils and Onyx in 3 patients. Lv et al (6) recently demonstrated transarterial Onyx treatment of a recurrent CCF that developed a dural supply; no complications were reported. In our patient, a temporary contralateral abduction defect was noted at the 3-week follow-up. The cause of this complication is unclear, especially as there was no pene-tration of Onyx into the left cavernous sinus, but it could have been an inflammatory response generated by Onyx. Delayed cranial nerve palsy has been reported with the use of nBCA (2) and coils (13). Given that the existing clinical experience of treating CCFs with liquid embolic agents is relatively limited, continued caution and close follow-up are necessary. One limitation of our report is the lack of angiographic follow-up. The complex medical history of our patient was a caution to follow-up angiography. However, previous animal studies have shown that the results obtained with Onyx are durable. No histologic evidence of recanalization was noted in a rete swine AVM model 6 months after Onyx embolization (14). Cognard et al (8) reported that among 23 of the 24 patients with dural fistulas treated with Onyx who underwent follow-up angiography at 3 months, none demonstrated recurrent fistulas. A note of caution is necessary with the use of Onyx in the treatment of dural fistulas. Onyx has a propensity to retrogradely fill other arterial feeders to the fistula (9,15) either via their common connection to the vein or via preexisting collateral anastomoses. Therefore, thorough understanding of the morphology of the potential arterial feeders and the fistula is necessary before Onyx emboli-zation is undertaken. The possibility of dangerous ICA-ECA anastomoses must always be kept in mind. REFERENCES 1. Nukui H, Shibasaki T, Kaneko M, et al. Long-term observations in cases with spontaneous carotid-cavernous fistulas. Surg Neurol 1984; 21:543-52. 2. Wakhloo AK, Perlow A, Linfante I, et al. Transvenous n-butyl-cyanoacrylate infusion for complex dural carotid cavernous fistulas: technical considerations and clinical outcome. AJNR Am J Neuro-radiol. 2005;26:1888-97. 3. Barrow DL, Spector RH, Braun IF, et al. Classification and treatment of spontaneous carotid-cavernous fistulas. J Neurosurg 1985;62:248-56. 4. Arat A, Cekirge S, Saatci I, et al. Transvenous injection of Onyx for casting of the cavernous sinus for the treatment of carotid-cavernous fistula. Neuroradiology 2004;46:1012-5. 5. Suzuki S, Lee DW, Jahan R, et al. Transvenous treatment of spontaneous dural carotid-cavernous fistulas using a combination of detachable coils and Onyx. AJNR Am J Neuroradiol 2006;27:1346-9. 6. Lv XL, Li YX, Liu AH, et al. A complex cavernous sinus dural arteriovenous fistula secondary to covered stent placement for a traumatic carotid artery-cavernous sinus fistula: case report. J Neurosurg 2008;108:588-90. 7. Carlson AP, Taylor CL, Yonas H. Treatment of dural arteriovenous fistula using ethylene vinyl alcohol (onyx) arterial embolization as the primary modality: short-term results. J Neurosurg 2007;107:1120-5. 8. Cognard C, Januel AC, Silva NA Jr, et al. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol 2008;29:235-41. 9. Nogueira RG, Dabus G, Rabinov JD, et al. Preliminary experience with Onyx embolization for the treatment of intracranial dural arteriovenous fistulas. AJNR Am J Neuroradiol 2008;29:91-7. 10. 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