Introduction  

   Ethmoidal dural arteriovenous fistula is a rare intracranial lesion associated with a high risk of intracranial hemorrhage.⁸⁾ Only a limited number of cases have described the endovascular and surgical management of these lesions.⁴⁾⁶⁾ Furthermore, bilateral ethmoidal DAVF, which was firstly reported by Deshmukh et al., is extremely rare.²⁾ Although surgery and embolization have both been used to treat this lesion, surgery is the treatment of choice at present. Embolization has not been adopted because of the risk of visual compromise and low cure rates. Endovascular treatment of ethmoidal DAVF with Onyx injection, specifically through the ophthalmic artery, has not been reported in the English literature. 
   We present a patient with bilateral ethmoidal DAVF successfully treated with Onyx embolization and subsequent surgery. 

Case report 

   A 60-year-old man had suffered from sustained headache. He had a history of head trauma 5 years ago. At that time, computerized tomography (not shown) showed left frontal hemorrhage, which was treated medically. However, he did not undergo any further evaluation. He was neurologically intact except for mild cognitive dysfunction on admission. Cerebral angiography showed that the ethmoidal DAVF was supplied by bilateral ophthalmic arteries and the left external carotid artery (ECA) (Fig. 1). In the lateral view of the left internal carotid artery (ICA), angiography disclosed that the left central retinal artery originates from the second segment of the ophthalmic artery, which was markedly dilated. Left middle meningeal arterial route for embolization was not adequate because of its tortuousness and small diameter. 
   Embolization was performed under general anesthesia on a biplane angiographic unit (Neurostar and Axiom Artis, Siemens, Erlangen, Germany). Superselective left ophthalmic artery angiography was carried out with 1.2F Balt sonic microcatheter. For further distal vascular access, we used the Mirage 0.008-inch microwire. After the microcatheter tip was selectively placed into the feeding artery as far as the fistula site, Onyx injection was performed. Penetration and reflux of Onyx was monitored under real-time roadmap technique. When proximal catheter reflux was seen, injection was discontinued for 30 to 90 seconds and then resumed with a new roadmap. We injected approximately 0.85ml of 6% Onyx. Left ICA angiography obtained immediately after embolization shows slight penetration into the fistula site and draining vein, and complete occlusion of vascular supply to the DAVF from the left ophthalmic artery (Fig. 2A and B). However, in the right ICA and left ECA angiography, the fistula site with draining vein still remained. There was no neurological complications secondary to the embolization procedure. This patient subsequently underwent surgery 7 days after embolization, resulting in successful resection of the DAVF. Follow up angiography 2 months after surgery demonstrated no angiographic evidence of arteriovenous shunting, suggesting complete obliteration of the DAVF (Fig. 2C). 

Discussion 

   Most DAVFs except ethmoidal DAVF are treated optimally with endovascular rather than surgical techniques, but endovascular treatment of ethmoidal DAVF has not been widely performed for several reasons as follows; first and most importantly, embolization risk of the central retinal artery; second, technical difficulty of the procedure; third, reflux of embolic agent into the cerebral circulation; fourth, the risk of retrograde thrombosis of the ophthalmic artery branches; fifth, catheter-induced ophthalmic artery vasospasm; and finally, the rare effectivity in curing the fistula.³⁾⁸⁾ Deshmukh et al. reported the first case of a patient with bilateral ethmoidal DAVF in 2005.²⁾ The second case of bilateral ethmoidal DAVF was reported by Komotar et al. in 2007.⁵⁾ They selected an operative approach as the treatment option and experienced the intraoperative rupture of the AVF leading to a life-threatening situation. In the largest series of 16 ethmoidal DAVFs reported by Lawton et al., 15 patients were treated with surgical excision with a good outcome.⁶⁾ They demonstrated that surgical management has low associated risk, presents no risk to vision, is highly effective in obliterating the fistula, and results in good clinical outcomes than endovascular treatment in most patients. 
   Technological advances and a variety of embolic agents have made it possible to selectively catheterize the ophthalmic artery and embolize distal arteries supplying a number of anteriorly located cranial base and extracranial lesions.⁹⁾ In 1990, Alvarez et al. reported an uncomplicated embolization of one patient with an ethmoidal DAVF by using histoacryl.¹⁾ They demonstrated that the central retinal artery originates proximal to arteries that supply ethmoidal DAVFs and that embolization risk could be minimized by catheterization beyond this safety point. In a series of 12 lesions involving the ophthalmic artery including three ethmoidal DAVFs reported by Lefkowitz et al., provocative tests with lidocaine/amytal was performed to assess the risk of embolization during the ophthalmic artery embolization.⁷⁾ Even though all of the three ethmoidal DAVFs was not endovascularly obliterated and required subsequent surgery, embolization was successfully performed without any complications. 
   Common embolization agents include polyvinyl alcohol (PVA) available in 350-um particle diameter ranges, n-butyl cyanoacrylate (NBCA) glue, platinum or stainless steel coils, absolute alcohol, or silk particles. PVA is the easiest material to use, but it is known for its impermanent nature. NBCA is a more permanent agent than PVA, but it is more difficult to administer. Furthermore, its injection time would be limited by the polymerization time. 
   Onyx is a non-adhesive embolic agent, which is supplied in ready-to-use vials. Onyx is mechanically occlusive but non-adherent to the vessel wall, allowing prolonged feeder injections. In the specific situation like ours, n-butyl cyanoacrylate (NBCA) injection was not preferred because the multiplicity of the feeders would lessen the likelihood of a successful embolization. It appears to have an advantage over NBCA in not requiring rapid withdrawal of the catheter immediately after embolization, facilitating greater control. Its lower viscosity theoretically facilitates the venous penetration required for obliteration of the nidus and proximal vein. 
   For the cure of a DAVF, it is essential that the fistulous site and the venous outflow be occluded. Although this was partially successful in our patient, embolization of an ethmoidal DAVF with Onyx through the ophthalmic artery can be performed with a minimum of complications, especially preventing the central retinal artery occlusion and the reflux of embolic agent into the cerebral circulation. It may also facilitate surgery by reducing the vascularity of the lesion. 
   Onyx can be potentially used by itself or as an adjunct to surgery in DAVF with a minimum of morbidity in the selected cases. Embolization through the ophthalmic artery with Onyx provides us with new options in the treatment of complex cerebrovascular disorders supplied by the ophthalmic artery. 

REFERENCES

1. Alvarez H, Rodesch G, Garcia-Monaco R, Lasjaunias P. Embolisation of the ophthalmic artery branches distal to its visual supply. Surg Radiol Anat 12:293-7, 1990 

2. Deshmukh VR, Chang S, Albuquerque FC, McDougall CG, Spetzler RF. Bilateral ethmoidal dural arteriovenous fistulae: a previously unreported entity. Case report. Neurosurgery 57:E809, 2005 

3. Goldberg RA, Garcia GH, Duckwiler GR. Combined embolization and surgical treatment of arteriovenous malformation of the orbit. Am J Ophthalmol 116:17-25, 1993 

4. Halbach VV, Higashida RT, Hieshima GB, Wilson CB, Barnwell SL, Dowd CF. Dural arteriovenous fistulas supplied by ethmoidal arteries. Neurosurgery 26:816-23, 1990 

5. Komotar RJ, Connolly ES Jr, Lignelli AA, Mack WJ, Mocco J, Harbaugh RE. Clinicoradiological review: bilateral ethmoidal artery dural arteriovenous fistulas. Neurosurgery 60:131-5; discussion 135-6, 2007 

6. Lawton MT, Chun J, Wilson CB, Halbach VV. Ethmoidal dural arteriovenous fistulae: an assessment of surgical and endovascular management. Neurosurgery 45:805-10; discussion 810-1, 1990 

7. Lefkowitz M, Giannotta SL, Hieshima G, Higashida R, Halbach V, Dowd C, et al. Embolization of neurosurgical lesions involving the ophthalmic artery. Neurosurgery 43:1298-303, 1998 

8. Martin NA, King WA, Wilson CB, Nutik S, Carter LP, Spetzler RF. Management of dural arteriovenous malformations of the anterior cranial fossa. J Neurosurg 72: 692-7, 1990 

9. Tsai FY, Wadley D, Angle JF, Alfieri K, Byars S. Superselective ophthalmic angiography for diagnostic and therapeutic use. AJNR Am J Neuroradiol 11:1203-4, 1990