Dural arteriovenous fistulas (dAVFs) are acquired arteriovenous shunts confined to the dura and are supplied by branches of the extracranial carotid artery, tentorial branches of the internal carotid artery, meningeal branches of the vertebral artery, and pial branches of cerebral arteries4). Persistence of cortical venous reflux in intracranial dAVFs has a high annual risk of hemorrhage and nonhemorrhagic neurologic deficits. Cognard et al.4) noted intracranial hemorrhage in 40% of patients with type III, and in 65% with type IV dAVFs. Rebleeding rates may be as high as 35% during the first 2 weeks after initial hemorrhage. As neuroendovascular technique has developed considerably, open surgery for dAVFs has become a secondary treatment option. Transvenous coil embolization and transarterial n-butyl-2-cyanoacrylate (n-BCA) injection were strong treatment methods of dAVFs. Even though transvenous access was not always possible and transarterial nBCA injection frequently resulted in partial embolization of feeding arteries. Recently, Onyx (Covidien, Irvine, CA, USA) has become the safe and feasible embolic material with higher obliteration rates than n-BCA7). Some dAVFs have an inaccessible lesion with only 1 route, so the combination of transarterial and transvenous embolization results in higher obliteration rates. Even if endovascular embolization has developed remarkably, surgery or radiosurgery are still required in certain patients for complex lesion, failure of both transvenous and transarterial embolization, or palliation9).

In this study, we reviewed our experience with a consecutive series of 13 patients subjected to the multimodal endovascular approach for intracranial dAVFs treatment. On the basis of our initial experience with multimodal management of complex dAVFs, we proposed our current treatment algorism and detailed consideration of the endovascular, combined surgical or surgical treatment options for dAVFs in the current Onyx era.

This retrospective study was approved by institutional review board (IRB) at our center. All symptomatic intracranial dAVFs were diagnosed and treated by the neurovascular team. In our institution, endovascular intervention was selected as a primary treatment options in all patients except for anterior cranial fossa dAVF, which was treated surgically. After the introduction of Onyx and detachable microcatheter, transarterial embolization was preferred in most dAVF, since dAVF could be successfully obliterated by the arterial injection for a long time.

We determined which patients were candidates for embolization. If dAVFs was not amendable to endovascular treatment because of a lack of appropriate arterial or transvenous access, the patient was treated by combined surgical endovascular embolization. Type I fistulas (4 patients) were treated only if the patient had intractable symptoms that did not respond to conservative treatment.

A review of the records of cerebrovascular center at our hospital identified 13 patients with dAVFs treated by endovascular embolization (transarterial, transvenous embolization, or both) or combined surgery between December 2009 and May 2014. The clinical and angiographic features were retrospectively reviewed from prospectively collected endovascular records. Data collected included age, sex, presenting symptoms, location, type of fistula by Cognard et al.4), feeders, approaches, embolization materials, onyx amount, injected artery, angiographic result and prognosis (Table 1).

The average age at presentation was 72 years (range, 28–78 years). Six patients were men (46%) and 7 were women (54%). All 13 patients had symptomatic lesions. Pulsatile tinnitus was most common followed by seizure, and transient ischemic attack. Other symptoms were headache, intracerebral hemorrhage, exophthalmos, personality change, and syncope (Table 2). The locations of fistulas were TSS in 6 (48%), middle fossa dura in 4 (31%), CS in 2 (15%), and SSS in 1 (8%) patient (Table 3). Cognard types were as follows : I in 4 (31%), IIa in 2 (15%), IIa+IIb in 5 (39%), and IV in 2 (15%) (Table 4). Embolization procedures were performed more than 2 times in 3 patients. Transvenous approach was tried in 4 patients with or without the transarterial approach (1 surgical sinus puncture, 2 transvenous followed by transarterial, 1 transarterial followed by transvenous). Nine (62%) patients were treated with transarterial Onyx embolization alone (Table 5). One of these required direct surgical exposure and puncture of MMA. Complete obliteration of fistulas was achieved in 11/13 (85%) patients after multimodal treatment. Onyx migration into cerebral artery was observed in 1 patient with indirect CCF, who was treated with transarterial Onyx injection after failed transvenous approach (Fig 4). Open surgical removal of migrated Onyx cast after unsuccessful endovascular retrieval resulted in a good clinical outcome. There were no other complications, such as cranial nerve palsy or cerebral infarction. Modified Rankin score (mRS) was acquired at post-operative 3 months. Eleven patients had mRS 0, 2 patients had mRS 3 (1 patient was admitted on Hunt and Hess grade V with subarachnoid hemorrhage, and the other patient had Parkinson disease).

The pathogenesis of dAVFs is controversial. There are two known pathogenic mechanisms based on sinus thrombosis. The first is that arteriovenous shunts between meningeal arteries and dural venous sinuses enlarge in response to elevated local venous pressure, resulting in a pathologic shunt3812). The second is that venous hypertension due to outflow obstruction causes decreased cerebral perfusion and promotes neoangiogenesis310). Predisposing risk factors for venous thrombosis such as antithrombin, protein C and S deficiencies, and trauma are associated with dAVFs development56). In pediatrics, the result of birth trauma, infection, in utero venous thrombosis, or maternal hormones are regarded as the etiology of dAVFs. In our series, sinus occlusion was observed in 2 patients who were treated by the combined surgical approach. Another 2 patients had trauma history. While the dAVFs are more commonly diagnosed in perimenopausal women with underlying hormonal influence, the ratio of male to female was similar and mean age was 58 years old in our series.

The incidence of DAVFs by location is as follows : TS, 50%; CS, 16%; tentorium, 12%; SSS, 8%; and anterior fossa, 2%19). The symptoms could arise from these locations. Borden and Cognard classification systems associate cortical venous reflux with high risk of intracranial hemorrhage and nonhemorrhagic neurologic deficits24). In our series, the most common initial symptom was intractable tinnitus, location was TS sinuses, and they were mostly Cognard I and IIa+IIb.

Management of dAVF is controversial. DAVF is a spectrum of disease that has different severity and various locations. Traditionally anterior fossa dAVF has been treated with surgical disconnection of AVF. However, most dAVF can be treated with endovascular technique with various success rates. Transvenous coil embolization of fistula has been considered gold standard for the treatment of dAVF. Transarterial feeder embolization with nBCA usually resulted in partial embolization because it is very difficult to penetrate multiple feeders with nBCA completely. However, after introduction of Onyx in the treatment of dAVF, single feeder injection could result in complete obliteration of fistula because of good penetration capability of Onyx. Onyx can penetrate the single feeder and fistula and then retrograde obliteration of multiple feeders from different arteries. Slow steady injection using reflux hold reinjection technique is very important to penetrate multiple feeders and fistulas completely from single feeder injection. Even though transarterial approach is preferred option in post-Onyx era, transvenous approach is still primary option in dAVF on the specific location such as cavernous sinus or anterior condylar confluence because there are so many dangerous anastomoses between ECA and ICA. In our complication case, Onyx cast migrated from ECA to ICA through dangerous collaterals. If we tried transarterial approach in this specific location, we'd better to occlude the cavernous ICA with balloon temporarily during transarterial Onyx injection to prevent Onyx migration to cavernous ICA through dangerous anastomosis between accessory meningeal artery and inferolateral trunk of cavernous ICA.

In the technical point of view, location of microcatheter tip is also important to achieve complete obliteration of dAVF with single feeder injection. The tip of microcatheter is placed as close as possible to fistula point. The disadvantage of Onyx injection was long injection time and subsequent radiation exposure. To reduce the injection time, balloon microcatheter can be very useful. When we use balloon microcatheter, we don't need to make Onyx plug around the microcatheter tip because Onyx injection under balloon inflation in the feeder makes onyx go forward instead of going backward. Onyx could not reflux proximally beyond the balloon. Therefore, faster injection of Onyx is possible without the risk of microcatheter gluing.

A review of literature on multimodal treatment results of dAVFs indicated that they were different before and after Onyx1415). Mean obliteration rate of dAVFs was 70% (37.5–75%) in the pre-Onyx Era, and 81% in the post-Onyx Era13). In our series, complete obliteration rate was 85% in overall, and 80% in high grade (III and IV) dAVFs. The reason of high complete obliteration rate at our center was that endovascular embolization with combined surgical approach could overcome the inaccessible route of transarterial or transvenous approach. In our center, 8 patients were successfully treated by the transarterial approach alone and 2 patients by the combined surgical approach. All patients were successfully treated.

MMA was used as a main access route of transarterial Onyx embolization because the MMA was anchored on the dura, and superselection of MMA with microcatheter was not difficult in most of the cases. In addition, MMA diameter was usually smaller than other more dilated feeders such as OA.

Literature review indicated that the common complication during endovascular Onyx embolization was cranial nerve palsy, and sometimes trigeminocardiac reflex. The petrous branch of MMA is often the main supply for dAVFs in the petrotentorial region. It also supplies the cranial nerve at the middle cranial fossa, and permanent cranial nerve palsy can occur. Therefore, we always tried to locate the microcatheter tip into petrous MMA far distally to avoid complications11). There was no complication of cranial nerve palsy.

Onyx migration into cerebral circulation may cause disturbed cerebral blood flow and subsequent cerebral infarction, as well as partial obliteration of dAVF. In our complication case of indirect CCF, Onyx migration occurred from accessary meningeal artery to internal carotid artery beyond the fistula through probably, infero-lateral trunk. In this situation endovascular retrieval using microsnare, or retrieval stent should be tried first. Unfortunately, if this retrieval procedure was not successful, prompt surgical retrieval of Onyx cast may result in favorable outcome in a selected patient. Recently, balloon assistance has been used to prevent Onyx migration to the cerebral arterial system16). However, the neurosurgeon should consider the risk of Onyx migration when it was injected transarterially in patient with indirect CCF, and that the primary treatment route of indirect CCF is the transvenous route.

Transarterial Onyx embolization is a potential first line therapeutic option in patient with dAVFs. However, the transvenous approach should be tried first in cavernous sinus dAVF because of the risk of intracranial migration of liquid embolic materials. Furthermore, combined surgical endovascular approach can be considered as a useful option in case of inaccessible endovascular route.