Endovascular Treatment of Dural Arteriovenous Fistulas of the Anterior or Posterior Condylar Vein

The venous portion of the jugular foramen is separated from the sigmoid sinus sulcus by a thin bony ridge called the terminal margin. Ventral to this structure the jugular fossa is located, which is filled by the superior bulb of the internal jugular vein (SJB). The condylar canal (CoC), a small bony canal that passes through the occipital condyle dorsoventrally along its longer axis, terminates cranially or caudally of the terminal margin (Fig. 1).

The posterior condylar vein (PCV), which is an emissary vein connecting the extracranial and intracranial venous system (Figs. 1 and 2a, b), runs through the CoC. Extracranially the PCV originates from the suboccipital cavernous sinus (SOCS), which is located within the condylar fossa. Intracranially the PCV drains into the SJB.

The anterior condylar vein (ACV) is located within the hypoglossal canal (HC) and passes through the occipital condyle mediolaterally, perpendicular to the longer axis of the condyle (Fig. 1). The intracranial end of the ACV is connected to the area of the anterior internal vertebral venous plexus (AIVVP), basilar plexus and the marginal sinus (Fig. 3a). The extracranial ending of the ACV terminates in the anterior condylar confluence (ACC). The ACC is a venous pouch located at the extracranial opening of the hypoglossal canal and drains directly into the SJB. The HC and the CC as well as the ACV and PCV within them are situated nearly perpendicularly to each other (Fig. 3a).

In two of the 40 examined cadaveric samples we could verify a bony communication between the HC and CoC within the occipital condyle with a small venous anastomosis connecting the intracondylar portions of the ACV and PCV (Figs. 2a and 3c). In two other cases the ACV drained directly into the internal jugular vein bypassing the ACC and the SJB (Figs. 2b and 3b).

The arterial supply of this region is provided by the ascending pharyngeal artery (APA). The neuromeningeal branch of the APA runs parallel to the internal jugular vein towards the jugular foramen, where it bifurcates. One of the branches enters the jugular foramen and supplies the dura of the posterior fossa. The other branches enter the HC and supply the neuromeningeal structures located within the canal. The hypoglossal nerve can sometimes enter the HC via two or more dural pores. In such cases the individual trunks have their own dural sheaths along the entire length of the canal. The arterial blood supply of these individual trunks is provided by their own branches from the neuromeningeal trunk of the APA through the hypoglossal canal (Fig. 4a, b). This variation was observed in nearly half of the cadaveric samples (17 out of 40).

The HC is an intraosseous canal on both sides of the foramen magnum cranially to the occipital condyle. It contains the hypoglossal nerve, the neuromeningeal branch of the ascending pharyngeal artery and the anterior condylar vein [3, 5, 10]. The ACV is a venous plexus that surrounds the hypoglossal nerve whilst it traverses the HC [5, 10]. It links the ACC to the anterior internal venous vertebral plexus (AIVVP) (Figs. 1 and 3a). Furthermore, connections to the basilar plexus are infrequently observed. In angiograms, the ACV, and hence DAVFs of the ACV and the ACC are found immediately medially, inferiorly and anteriorly to the jugular bulb (Figs. 3c and 5b).

The CoC is an intraosseous canal that connects the dorsal aspect of the jugular foramen with the condylar fossa and terminates directly dorsal to the occipital condyle [11]. Within the CoC run the PCV and meningeal branches of the occipital artery. The PCV originates from the bulb of the jugular vein, the most medial point of the sigmoid sinus or the ACC (Fig. 4b; [10, 12, 13]). It terminates in the vertebral artery venous plexus (VAVP) or deep cervical veins (DCV). As one of the largest emissary veins the PCV is an important anastomosis between the intracranial and extracranial venous systems. In angiograms, the posterior condylar vein and hence also fistulas of the PCV can be found dorsally and posteriorly to the bulb of the internal jugular vein (Fig. 4a; [10]).

Ota et al. [9] reported a rare variant of a PCV originating directly from the intracondylar portion of the ACV (7.4–7.7% of cases). Matsushima et al. reported the same variant in 0–3% of cases in their series [6]. In addition to this variant we found two cases where the PCV is not a branch of the ACV but where a small anastomotic vein connects the ACV and PCV through its own bony canal. In these cases the venous flow is secured though several channels. To the best of our knowledge, this variation has never been previously described. The ACV drains normally into the internal jugular vein over the extracranially located ACC [5, 14‐16]. In the studied specimens we could verify the existence of a single venous branch originating from the extracranial portion of the ACV connecting directly to the internal jugular vein. This anatomical variation has also not been previously reported.

The arterial supply of the examined region is well-described in literature [17]; however, we found an interesting, previously undescribed anatomical variation of the arteries within the HC: in some cases the hypoglossal nerve is divided by dural sheaths to numerous trunks within the HC and these trunks have each their own arterial supply from the APA (Fig. 4a, b). Although there are reported cases of IX–XII cranial nerve dysfunctions after transarterial embolization of DAVFs in the region of the ACV [18], this anatomical fact is a possible explanation why hypoglossal nerve injury is not a frequently observed therapeutic injury.

The DAVFs involving the condylar veins are rare entities. To date approximately 120 cases of DAVFs of the anterior condylar vein [5] and, to our knowledge, only 3 cases of DAVF involving the posterior condylar vein have been reported [19‐21].

The pathophysiology of DAVFs still remains unknown. There is an increased incidence of DAVFs in patients who previously suffered a sinus thrombosis, especially in patients with a lateral DAVF [1, 2, 22]. Head trauma, prior head surgery, infection or inflammation have been discussed in the literature as other possible causes of DAVFs [1, 2]. An association between DAVFs of the ACV or PCV and sinus thrombosis, however, has not been reported in literature, to the best of our knowledge. There was no clear evidence of sinus thrombosis in any of our cases. This might suggest that condylar DAVFs may be unrelated to a previous sinus thrombosis. A more likely cause for condylar DAVFs might be due to infections or after surgery of the skull base; however further studies might be necessary to determine the underlying etiology of condylar DAVFs.

Typical clinical presentations of DAVFs of the ACV are pulse-synchronous tinnitus [3, 5] and ophthalmological symptoms such as chemosis, proptosis or diplopia due to venous reflux into the inferior petrosal sinus, the cavernous sinus and the superior ophthalmic vein [5, 23, 24], hypoglossal nerve palsies [5] and, in the case of cortical venous drainage, intracranial bleeding.

The arterial blood supply of the DAVFs of the ACV is provided typically by neuromeningeal branches of the APA [5] or in some cases secondary through other arteries such as the internal carotid artery, internal maxillary artery, occipital artery, medial meningeal artery or the vertebral artery [5, 15]. If arterial feeding from the APA is present, this finding makes it highly suspicious of a condylar DAVF. This is easy to detect on angiographic images and in case of doubt selective injections of the APA can be performed.

In patients with DAVFs of the anterior condylar vein it can be difficult to distinguish the exact location of the fistula due to the complex anatomy of the arterial and venous system at the skull base and the possible wide arterial supply of the fistulas [3, 5, 13]. In our experience the injection of the contralateral external carotid artery can be very helpful to get a better understanding and overview of the anatomy and the exact location of the point of the fistula. This was previously also reported by Ernst et al. [3].

The DAVFs of the PCV are a much less frequent entity and there are only 3 case reports in the literature (Table 2; [19‐21]). In two of the three reported cases patients presented with pulse-synchronous tinnitus only [19, 21]. The third case presented with an acute subarachnoid hemorrhage [20]. In all three cases, arterial feeders originated from the neuromeningeal branch of the APA and the vertebral artery. In two of the three cases, additional arterial feeders were observed from the occipital artery. The venous drainage in two cases occurred through the PCV to the sigmoid sinus and paravertebral veins.

An important differential diagnosis for lesions with increased vascularization around the jugular foramen are glomus tumors [25]. The main arterial feeder of these paragangliomas is also the APA [26, 27]. The differentiation between the glomus tumors and condylar DAVFs can be difficult in some cases [25]. Paragangliomas show the pathognomonic “salt and pepper”-pattern on MRI [26]. The typical angiographic finding is a relatively well defined tumor blush of the paraganglioma in contrast to condylar DAVFs [27]; however, it is important to include paragangliomas in the differential diagnosis.

The therapeutic options for DAVFs in general are endovascular treatment, microsurgical resection or stereotactic radiosurgery [2]. Microsurgical treatment of DAVFs has been reported to be safe and effective [2]. The success and risk of surgery depend on the location and the morphological characteristics of the DAVF; however, DAVFs at the skull base have a higher operative risk profile compared to other DAVFs. This is due to the more difficult surgical access course because of the intraosseous location of the arteriovenous shunt, the closeness to important structures such as the cranial nerves and the need to remove the condylar bone leading to possible craniocervical instability [3, 8, 28, 29].

The results of stereotactic radiosurgery of DAVFs involving the skull base were discouraging [1, 30]. Furthermore, this treatment modality carries the risk of radiation-induced damage to the brainstem and the cranial nerves and may therefore not be suitable for the treatment of condylar DAVFs [31]. The relatively long time between radiosurgery and the treatment effect is another disadvantage of radiosurgery, especially in high-grade DAVFs with extensive cortical drainage [31]. Endovascular therapy of DAVFs has become the most widely used treatment modality as it is considered to be a safe and effective method [2, 32]. It can be performed as transvenous embolization, transarterial embolization or as a combination thereof but both have the same aim of occluding the point of the fistula [2, 32].

All four presented cases were treated endovascularly. Of the four patients, three had a complete occlusion of the arteriovenous shunt after one treatment session performed as transvenous coil occlusion. One patient had to undergo a second treatment session to achieve complete occlusion of the fistula as transarterial embolization failed to occlude the DAVF. All patients reported an immediate and complete regression of the pulse-synchronous tinnitus after the occlusion of the arteriovenous shunt.

The three reported cases of DAVFs involving the PCV were treated via an endovascular approach. In one case a transarterial embolization was performed due to the extreme tortuosity of the bridging vein with an associated aneurysm. The other two patients were treated by selective transvenous coil embolization of the DAVFs. In all cases the fistula could be excluded completely [19‐21].

The arterial feeders of DAVFs of the ACV and PCV mainly originate from the APA, the occipital artery and from meningeal branches of the vertebral artery [5]. These arteries have well known, dangerous anastomoses with the brainstem and therefore a primary transarterial embolization may not be suitable [17, 33]. Furthermore, the arterial branches supplying these fistulas can be small and extremely tortuous meaning that a stable distal catheter position may not be possible. For these reasons our preferred approach is transvenous embolization with coils. As these venous pathways are “accessory” pathways and not essential for brain drainage there is no risk to the brain by a transvenous treatment.