INTRODUCTION
Intracranial dural arteriovenous fistulas (dAVFs) are abnormal connections between meningeal arteries and venous structures such as dural venous sinuses, meningeal veins, or cortical veins. Endovascular techniques using transvenous (TVE) or transarterial embolization (TAE) are the main treatment for dAVFs. Among the materials used in TAE, Onyx plays a crucial role, enhancing the safety and efficacy of this therapeutic intervention for dAVFs.
When performing TAE, selecting an appropriate arterial route is crucial. Factors such as accessibility to the shunt point, the size of the feeder, the potential risk of ischemic injury to the cranial nerves, and the possibility of anastomosis with the internal carotid or vertebral artery will influence the decision.
The ascending pharyngeal artery (APA) often serves as the supplying artery for dAVF in various regions, including the cavernous sinus, transverse-sigmoid sinus, and foramen of the skull base including the hypoglossal canal and foramen magnum. However, due to its small caliber, potential risk of anastomosis with the internal carotid artery, and its role in supplying the vasa nervorum to the lower cranial nerves, the APA is not typically the preferred route for embolization [3,4]. Generally, TAE through more capacious and safer pedicles, such as the middle meningeal artery (MMA) or occipital artery (OA), is preferred. However, there are certain situations where selecting TAE through the APA is necessary to achieve successful treatment and favorable outcomes in the management of dAVF. In this study, we retrospectively analyzed the outcomes of cases in which the APA serves as a pedicle for embolization.
MATERIALS AND METHODS
The Institutional Review Board of Samsung Medical Center approved this retrospective study (IRB No. 2021-10-144). We conducted a retrospective analysis of medical records from January 2009 to April 2021, identifying 305 patients with cranial dAVF who underwent endovascular treatment at our center. Among them, 11 patients treated for dAVF through the APA with Onyx (Medtronic, Minneapolis, MN, USA) were included in this case series.
Embolization through the APA
The primary therapeutic strategy for cavernous sinus dAVFs in our practice involves a transvenous approach, entailing TVE with packing of the cavernous sinus using coils and Onyx Liquid Embolic System (eV3 Neurovascular, Irvine, CA, USA). However, in cases where TVE is unfeasible or when cortical venous reflux (CVR) persists post-transvenous intervention, TAE is carefully implemented. For non-cavernous dAVFs, TAE was the first choice of treatment. In situations where the involved venous sinus was non-functioning, TVE was also utilized when deemed necessary. The choice of route for TAE was based on each lesion’s angioarchitecture. Typically, the MMA or OA branches were the preferred routes. However, when embolization through the APA is considered essential due to the absence of suitable alternatives, the APA is cautiously employed. Endovascular procedures were performed under general anesthesia for all patients. For TAE, a 5 F or 6 F guiding catheter was inserted into the external carotid artery (ECA), and a microcatheter was advanced into the APA using a microguidewire. Prior to embolization, superselective angiography using a microcatheter was conducted to evaluate the angioarchitecture of the fistula point, the location of the neuromeningeal trunk (NMT), and the presence of potential anastomoses. In most instances, embolization was executed using a microcatheter, specifically the Excelsior SL-10 or XT-17 (Stryker, Kalamazoo, MI, USA), Headway 17 (Terumo Corporation, Tokyo, Japan), or Echelon 10 (Medtronic). However, in one case, a Scepter balloon (Microvention, Aliso Viejo, CA, USA) was utilized to mitigate the excessive reflux of embolic agents and to manage the extended distance to the fistulous point.
Follow-up and outcomes
Immediate angiographic outcomes were categorized as follows : 1) complete occlusion, 2) residual shunt without CVR, and 3) residual shunt with CVR. Postprocedural magnetic resonance angiography (MRA) was conducted within 7 days of the embolization procedure. Patients underwent regular outpatient clinical and radiological follow-ups, including MRA at 6 or 12 months, followed by an annual evaluation thereafter. Follow- up assessments were performed or omitted at the discretion of the attending physician.
Results
Among the 305 cranial dAVFs that underwent endovascular treatment at our center, onyx embolization was carried out through APA in 11 cases (3.6%). Clinicoradiological findings and detailed treatment information for the patients included in the study are provided in Tables 1 and 2. Table 2 offers a detailed summary of the cases treated by TAE through the APA, highlighting the procedural specifics and individual case outcomes. Dural AVFs were most frequently located in the transverse-sigmoid sinus (n=4), followed by the cavernous sinus (n=2), tentorium (n=2), hypoglossal canal (n=1), falx cerebri (n=1), and craniocervical junction (n=1). All 11 lesions showed CVR. Pretreatment magnetic resonance imaging (MRI) showed venous infarction (n=2), and intracerebral hemorrhage (n=2), and venous hypertension related parenchymal edema without stroke (n=1).
Of the 11 dAVF cases in which TAE was performed with APA, two (18.0%) were performed with APA alone and nine (82.0%) were performed with APA and other pedicles. In two patients, TAE with the APA was the only available option : one was for transverse-sigmoid sinus dAVF and another for tentorial dAVF. Three cases (27.0%) were concurrently treated with transvenous embolization. In eight cases, MMA supply was seen as well.
More specifically, TAE with the APA was performed through the pharyngeal trunk in two cases (18.0%), jugular branch in three cases (27.0%), clival branch in one case (9.0%), hypoglossal branch in one case (9.0%), and posterior meningeal artery from jugular branch in four cases (36.0%) (Fig. 1).
In one of two cases in which the APA was used as the only transarterial route, complete occlusion was achieved through the single APA pedicle. In the one case where partial occlusion was achieved (Fig. 2, case 4), the patient exhibited symptoms of facial nerve palsy following the procedure. In one case where APA was the first access route and MMA was also used as an access route of the TAE, complete occlusion was confirmed. In eight other cases of various types of dAVFs, the APA was used as a salvage arterial pedicle after multiple attempts through MMA or OA or PMA routes.
Of the 11 dAVFs, five (45.0%) were completely occluded, three (27.0%) showed residual shunt but disappeared CVR, and three (27.0%) showed decreased shunt flow but persistent CVR.
One facial nerve palsy developed after TAE using jugular branch of the APA (Fig. 2, case 4), and one hypoglossal nerve palsy developed after TAE using hypoglossal branch of the APA (Fig. 3, case 8). Cranial nerve palsies ccurred immediately after the procedure; both the hypoglossal and facial nerve palsies showed partial improvement over a 4-6 months period but did not fully resolve.
Postprocedural MRA revealed no newly developed infarction or hemorrhage. Cranial nerve palsy was developed in two patients (18.0%) after the procedure. There was no cranial nerve palsy after TAE using pharyngeal trunk or posterior meningeal artery from jugular branch.
DISCUSSION
The APA serves as a crucial conduit for supplying the neural structures in the posterior fossa. Understanding its anatomy, variations, and anastomotic pathways is vital for treating lesions serviced by its branches and for preventing complications from unintended damage to the artery.
Before branching into the pharyngeal trunk anteriorly and the NMT posteriorly, the APA provides a musculospinal branch. The pharyngeal trunk subsequently divides into superior, middle, and inferior pharyngeal branches. The NMT passes through the foramen magnum, supplying the dura of both the foramen magnum and varying portions of the clivus and posterior fossa dura. Infrequently, the NMT can originate from the posterior auricular or OA. Once it has passed through the foramen magnum, the NMT initially gives off a hypoglossal branch to the hypoglossal canal and cranial nerve XII, followed by a jugular branch to the jugular foramen and cranial nerves IX to XI. Additional higher distal branches may occasionally extend to the internal auditory canal and include another branch oriented superiorly towards the clivus [3].
Endovascular treatment is most often used to treat cranial dAVFs, with meta-analysis findings indicating an overall initial completion rate of 82% (47-100%) and a recurrence rate of 2% [11]. Due to the complexity and heterogeneity of dAVFs, difficulty regarding lesion access is variable. Vollherbst et al. [13] recently reported angiographic features that influence treatment success. According to the study, a large number of feeding arteries and involvement of the APA negatively affected outcomes. Supply through the APA may increase angioarchitecture complexity, thereby reducing the rate of treatment success.
In the study by Gross et al. [3], out of 267 dAVFs treated endovascularly, 68 were supplied by the APA (25%). Of these, embolization was performed through APA in eight cases (12%), and seven resulted in complete occlusion. The APA was chosen as the primary pedicle for embolization in five dAVF cases, two marginal sinus, one distal sigmoid, one cavernous, and one tentorial dAVF case. The perception of the APA as a relatively ineffective salvage pedicle may be due to selection bias. In instances where it was chosen as the primary pedicle, there were cases of high success rates. In specific cases, the APA serves as an excellent pathway for TAE of cranial dAVFs. Gross et al. [3] presented specific examples demonstrating the APA as a useful pedicle, while explaining its relative ineffectiveness for dAVFs of the transverse sinus and proximal sigmoid sinus.
In our retrospective evaluation of the APA’s role in the embolization of cranial dAVFs using Onyx, we explored its application across 11 of 305 cases treated at our institution. The APA’s utilization highlights its importance as an alternative approach when preferred embolization routes are unsuitable or unsuccessful. Although there are inherent risks, such as potential cranial nerve palsy, our findings suggest that precise angiographic planning and technique adjustment can significantly mitigate these risks, leading to reasonably safe dAVF management. To the best of our knowledge, this is the largest assessment of dAVF patients treated through the APA to date.
Our intention in this study is not to assert that the APA is a safe and effective branch for embolization. We aimed to determine the actual clinical risk of cranial nerve palsy associated with APA embolization and identify specific situations where selecting the APA carries a higher risk. We carefully explored whether embolizing dural AVFs through the APA, even when used as a last resort, could be a justifiable option under certain circumstances. Our results indicate that embolizing through the jugular and hypoglossal branches of the APA NMT demands greater caution. Comparatively, selecting the posterior meningeal artery or pharyngeal trunk was associated with a lower risk.
Cranial nerve complications following transarterial onyx embolization for dAVFs
Multiple reports indicate that cranial nerve palsy can present after transarterial Onyx embolization in the treatment of dAVF [2,6-8,10,14]. Among these, Lee et al. [6] reported one case of facial nerve palsy after APA embolization using Onyx, and Pei et al. [10] described a case of hypoglossal nerve palsy after Onyx embolization. The mechanism of cranial nerve injury is unclear; however, it may be mediated by the penetration of Onyx into the vasa nervorum. Direct effects of dimethyl sulfoxide (DMSO) toxicity may explain cranial nerve palsy. DMSO concentrations are likely greatest at the microcatheter tip, which is often located at the site of cranial nerve injury [6,8]. Nyberg et al. [8] argued that traction nerve injury may occur when the microcatheter is removed from the Onyx cast.
Of the cases in this study, a patient with dAVF of the transverse-sigmoid sinus developed facial palsy after embolization through the jugular branch of the APA NMT (Fig. 2, case 4). The patient’s facial nerve palsy symptoms of grade 4 developed immediately after the procedure and had almost recovered after 4 months.
There was another case of hypoglossal nerve palsy with hypoglossal canal dAVF after transarterial Onyx embolization through the posterior meningeal artery and hypoglossal branch of the APA NMT (Fig. 3, case 8). As previously stated, the posterior meningeal artery may supply the hypoglossal nerve; therefore, we cannot be sure that the pedicle caused nerve injury. This patient recovered from tongue deviation after a few months but complained of tongue discomfort, a finding that is consistent with prior reports.
However, the rest of the cases in our center did not develop cranial nerve palsy. Cranial nerve palsy occurred in cases in which TAE was performed with the jugular and hypoglossal branches of the NMT, but not in cases in which embolization was performed with lateral access to the pharyngeal trunk or posterior meningeal artery (Fig. 1). The jugular and hypoglossal branches, among the other branches of the APA, are located relatively medially and are associated with cranial nerve supply. It was observed that selecting these branches as a treatment route carries a higher risk of cranial nerve palsy. In one case, a transverse-sigmoid sinus dAVF was supplied by MMA, APA and OA (Fig. 4, case 2). TAE with MMA was performed, but lateral view of a ECA angiography showed residual dAVF in the jugular bulb area supplied by the APA. The lesion was accessed through jugular branch of the APA NMT and further embolization was performed, but reflux through the petrosal vein remained.
Another case without accompanying cranial nerve palsy is a patient with craniocervical junction dAVF supplied by APA (Fig. 5, case 7). TAE was performed through MMA, OA and jugular branch of the APA NMT. ECA angiography showed complete occlusion of the dAVF and no neurological deficit occurred.
According to a meta-analysis of previous reports of transarterial Onyx embolization of intracranial dAVFs, the rate of postoperative cranial nerve palsy is 2% [11]. Lesions close to the skull base are associated with a particularly high risk of ischemic nerve injury [11]. To minimize the occurrence of cranial nerve injury, Onyx reflux should not be tolerated and an adequate safety margin should be considered to avoid Onyx migration. Lv et al. [7] suggested that when TAE is performed through the MMA, Onyx reflux to the foramen spinosum level should be avoided because it may result in trigeminal and facial nerve deficit. Watanabe et al. [14] reported a case in which vagal nerve palsy developed after embolization through the occipital and middle meningeal arteries. This might be explained by the fact that the MMA acts as a channel to the lateral fossula, which supplies the vagus nerve.
Approach through APA and balloon catheter use in embolization of dAVFs
In cases of cavernous sinus (CS) dAVF and tentorial dAVF, a pharyngeal trunk approach has been occasionally selected. CS dAVF is most often treated using TVE; however, in cases of residual fistula after TVE or when route loss occurs due to inferior petrosal sinus occlusion, TAE was used. The pharyngeal trunk, which is divided into several branches, supplies extracranial lesions. Occasionally, the pharyngeal trunk may anastomose with the internal carotid artery (ICA) through the carotid ramus. Additionally, the NMT may anastomose with the ICA through the meningohypophyseal trunk [1]. Due to anastomoses between the ECA and the ICA, Onyx migration may occur. Two recently published reports revealed the occurrence of Onyx migration from the ECA to the ICA [9,12].
In case 5 of our series, Onyx migration to the ICA occurred during embolization through the pharyngeal branch of the APA in a patient with tentorial dAVF. After we knew that an Onyx column had reached the ICA wall, a balloon guiding catheter was used instead of a 5 Fr guiding catheter to compromise ICA flow. Deployment of an expandable stent (Enterprise stent) stabilized the Onyx column. Thereafter, no abnormal findings on postoperative angiography or MRI were observed.
In case 11 of our series, we used a balloon catheter for embolization through the APA in one patient with tentorial dAVF due to difficulty establishing a sufficient safety margin as a result of a long distance between the microcatheter tip and fistulous point. An immediate angiographic cure was achieved in the patient.
Jang et al. [5] reported that use of a dual-lumen balloon catheter for Onyx embolization of dAVFs is safe and effective. According to the authors, no differences were observed regarding complete occlusion rates through the MMA versus other arteries including OA, superficial temporal artery, and APA (94.4% vs. 94.1%, respectively).
Techniques for performing dural AVF embolization through the APA
One of the precautions when using the APA as a route to access the fistula, as mentioned in previous studies, is that most marginal sinus dural AVFs are supplied by branches of the NMT [3]. Therefore, before attempting TAE, it must be ensured that the microcatheter's position does not involve potential vascular supply to the lower CNs’ vasa nervorum. If a sufficiently capacious NMT supplying branch is inevitably confirmed, using a balloon microcatheter to inflate and reduce the risk of reflux into critical pedicles supplying the lower CNs can be an option. Alternatively, using a wedged microcatheter for NBCA embolization can make the procedure safer.
It is crucial to position the microcatheter as close to the fistula point as possible. To achieve this, careful pre-procedural angiography should be conducted to thoroughly understand the Angioarchitecture. Onyx must not migrate to the cranial nerve vicinity or reflux into the NMT; typically, Angioarchitecture is complex enough that distinguishing between cranial nerve and vasa nervorum locations is challenging. Therefore, avoiding branches leading to the cranial nerve during angiography is challenging. The key point for avoiding cranial nerve damage during the procedure is to perform the onyx embolization from as close to the fistula point as possible, thus staying away from the cranial nerve. Even if entering through the NMT, achieving maximum proximity to the fistula point during embolization can help maintain distance from anatomically dangerous structures. The APA’s jugular branch, hypoglossal branch, internal auditory canal, CNs 7 and 8, lower cranial nerves, and related foramina are mostly located medially. Most dural AVFs undergoing Onyx embolization, including TSS dAVFs, typically have the shunt point located laterally. Even when accessing the TSS through the NMT, the route is extensively lateral and transverse.
CONCLUSION
Transarterial Onyx embolization through the APA could be selectively used when alternative routes are not feasible and the risk of incomplete treatment is high. A thorough understanding of angiography is essential to identify cases where this approach can be performed relatively safely and those where complications are more likely to occur.
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