Article Text
Abstract
Background With the introduction of Onyx, transarterial embolization has become the most common endovascular approach to treating dural arteriovenous fistulas (dAVFs), often via the middle meningeal or occipital arteries. The ascending pharyngeal artery (APA) is a less frequently explored transarterial route because of its small caliber, potential anastomoses to the internal carotid and vertebral arteries, and vital supply to lower cranial nerves.
Objective To review our institutional experience and highlight the prevalence of APA supply to dAVFs and cases where it is a safe and effective pedicle for embolization.
Methods We reviewed our endovascular database (January 1, 1996 to March 1, 2016) for cranial dAVFs, evaluating dAVF characteristics and embolization results for those treated transarterially via the APA.
Results Of 267 endovascularly treated dAVFs, 68 had APA supply (25%). Of these 68 dAVFs, embolization was carried out via this pedicle in 8 (12%) and 7 were ultimately occluded. No complications, including post-treatment cranial neuropathies or radiographic evidence of non-target embolization, were found. For 5 dAVFs, the APA was selected as the initial pedicle for embolization (two marginal sinus, one distal sigmoid, one cavernous, one tentorial). In four of these five cases, dAVF occlusion was achieved via the initial APA feeding artery pedicle. In one case, near-complete, stagnant occlusion was achieved after APA embolization; complete occlusion was achieved after adjunctive embolization of a single additional middle meningeal artery pedicle. In three other cases of complex transverse/sigmoid dAVFs, the APA was used after multiple attempts via middle meningeal and occipital artery pedicles. Occlusion was not achieved transarterially; two of these three dAVFs were ultimately occluded transvenously.
Conclusions In rare, select cases, the APA is an excellent route for transarterial embolization of cranial dAVFs.
- Arteriovenous Malformation
- Artery
- Fistula
- Vascular Malformation
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Introduction
The ascending pharyngeal artery (APA) is a common transarterial conduit employed for the embolization of a variety of extra-axial neoplasms in the foramen magnum region, particularly paragangliomas.1–4 In contrast, although the APA is prevalent among dural arteriovenous fistulas (dAVFs) in this region, use of the APA as a transarterial pedicle for embolization is relatively infrequent. This probably reflects its relatively small caliber, and more importantly, the risk posed by daunting potential anastomoses to the internal carotid artery and vertebral arteries as well as the APA's vital supply to the vasa nervorum of the lower cranial nerves (CNs).5 ,6 Though we generally advocate transarterial embolization via more capacious, ‘safer’ pedicles, such as the middle meningeal artery (MMA) or occipital artery, we sought to review our institutional experience and highlight the prevalence of APA supply to dAVFs and cases where it can serve as a safe and effective pedicle for embolization.
Methods
We performed a retrospective analysis of a prospectively maintained endovascular patient database from January 1, 1996 to March 1, 2016 to identify all patients with cranial dAVFs initially treated via endovascular approaches. We excluded patients with spinal dAVFs, children with dural sinus malformations or infantile dural arteriovenous shunts, and patients managed with surgery or radiosurgery as the initial treatment approach. Patient demographic information, symptoms, treatment approach and arteries involved, angiographic results, and complications were extracted from the medical records.
All embolization procedures were carried out under general endotracheal anesthesia with neurophysiologic monitoring (somatosensory evoked potentials and electroencephalography). As a general endovascular principle, the simplest, safest path that provides intimate access to the fistula site is selected whether this path is arterial, venous, or by direct puncture. For transarterial approaches, MMA pedicles are generally sought; when these are unavailable, occipital artery, APA, ethmoidal, or rarely posterior meningeal artery approaches are considered. Before embolization, superselective angiography via a microcatheter is performed to evaluate proximity to the fistula point, the presence of potential anastomoses, and the rate of arteriovenous shunting. Specifically for APA embolization, microcatheter position adequately distal to the expected takeoff of supply to the lower CNs is vital; embolisate reflux into this region should not be tolerated. Given the size and tortuosity of the arterial pedicles catheterized in this series, balloon microcatheters were not used.
Since 2006, our preferred general embolisate is Onyx (Covidien, Dublin, Ireland); n-butyl cyanoacrylate (NBCA) is now selectively employed in cases of high-flow arteriovenous shunting. After embolization, control angiographic runs are meticulously reviewed to rule out residual arteriovenous shunting and to confirm embolisate casting of the draining vein—both are requirements for the designation of initial occlusion. Patients are observed overnight in the intensive care unit and discharged home the following day if no complications have occurred.
Results
During the 20-year review period, 267 dAVFs were treated initially with embolization. Of these 267 dAVFs, 68 (25%) were noted to have supply from the APA. By cranial location, this included all marginal sinus dAVFs (11/11), 43% of transverse/sigmoid (37/86), 26% of tentorial/petrosal (12/47), 20% of torcular (3/15), and 8% of cavernous sinus (5/60) dAVFs. As expected, no convexity/superior sagittal sinus-based dAVFs were supplied by APA branches.
Among the 68 dAVFs with APA supply, embolization was carried out via this pedicle in eight (12%) cases, all via the neuromeningeal trunk (NMT) (table 1). Embolization was carried out via other transarterial routes (with or without transvenous approaches) in 66% and via exclusive transvenous approaches in 22% of cases with APA supply. By comparison, of 198 cases with MMA supply, embolization was carried out via the MMA pedicle in 150 cases (76%).
Of eight dAVFs treated transarterially via the APA, seven were ultimately occluded. There were no complications. In five cases, the APA was selected as the initial pedicle for embolization: two were for marginal sinus dAVFs and one each for a distal sigmoid/jugular bulb dAVF, carotid-cavernous dAVF, and tentorial dAVF. In two of five cases, cortical venous drainage was seen. In two cases, MMA supply was seen as well. In four of five cases in which the APA was used as the initial transarterial feeding artery, occlusion was achieved via the single APA pedicle. In the one case where initial occlusion was not achieved, there was stagnant, near-complete occlusion with subsequent thrombosis after adjunctive embolization of a single additional MMA pedicle. Notably, Onyx was used as the embolisate in all but one case.
In three other cases of complex transverse/sigmoid dAVF, the APA was used as a salvage arterial pedicle after multiple attempts via MMA and occipital artery routes. Embolization was carried out in two cases with NBCA (before the introduction of Onyx into the treatment armamentarium); Onyx was used in the other case. In none of these three cases was dAVF occlusion achieved via the APA; in two, occlusion was ultimately achieved via transvenous coiling.
Discussion
The APA, most commonly originating from the medial or posterior wall of the proximal external carotid artery,7 is involved in a variety of pathologies, particularly extra-axial tumors and arteriovenous shunts in the region of the foramen magnum.3 ,5–8 It is notorious for ‘dangerous’ anastomoses to both the internal carotid artery and vertebral arteries as well as its precarious supply to the lower CNs (table 2).5–7
Anatomically, the APA often provides an early musculospinal branch before bifurcating into an extracranial, anteriorly oriented pharyngeal trunk and a posteriorly oriented NMT. The pharyngeal trunk then branches into superior, middle, and inferior pharyngeal branches. The NMT enters through the foramen magnum, supplying the dura of the foramen magnum and a variable portion of the dura of the clivus and posterior fossa. After entering through the foramen magnum, the NMT provides an initial hypoglossal branch to the hypoglossal canal and CN XII and then a jugular branch to the jugular foramen and CN IX–XI. Variably, more superior distal branches may also include a branch to the internal auditory canal and another superiorly oriented clival branch. Rarely, the NMT may arise from the posterior auricular or occipital artery.
APA supply to the dura in the region of the foramen magnum lends itself to involvement in a variety of extra-axial neoplastic pathologies as well as dural arteriovenous shunts, most commonly dAVFs of the marginal sinus.2–4 ,6–9 In our experience, all marginal sinus fistulas had supply from the APA NMT. Marginal sinus fistulas, also referred to as condylar, foramen magnum, and hypoglossal canal fistulas, are a heterogeneous group of lesions; patients with these lesions may present with tinnitus, ocular symptoms in the context of reflux into the cavernous sinus or ophthalmic vein, or even with venous hypertension or hemorrhage if cortical venous drainage is recruited (figure 1A, B).8–10 Traditionally, these fistulae required surgical disconnection11 or were managed via transvenous approaches.8 ,9 In an endovascular series of 14 marginal sinus dAVFs, 11 were noted to drain into a sinus first with or without cortical reflux; all were treated successfully without complication via transvenous approaches.8 In the 11 treated marginal sinus fistulas in our series, none harbored direct cortical venous drainage and thus all had a transvenous route of embolization. Nine were treated successfully via transvenous coiling; two were treated via Onyx embolization of the APA (figure 1). As the supply to these fistulas is invariably via branches of the NMT, before attempted transarterial embolization, microcatheter positioning should be reassuringly clear of potential vascular supply to the vasa nervorum of the lower CNs. In the fortuitous circumstance of an adequately capacious NMT supplying branch, a balloon microcatheter may be employed and inflated to mitigate the risk of reflux into important pedicles supplying the CNs.12 Alternatively, a ‘wedged’ microcatheter position has historically allowed for safe, feasible, and successful embolization with NBCA.13 Although transarterial embolization via the APA NMT may be the only feasible endovascular route for treating high-risk marginal sinus dAVFs with direct cortical venous drainage, it remains a less common approach for low-risk lesions with traditional transvenous coiling options.
Although a considerable proportion of transverse/sigmoid dAVFs harbored APA supply in our series (43%), the APA proved ineffective as a salvage pedicle in three complex transverse/sigmoid dAVFs. Its relative ineffectiveness as a salvage pedicle is, in part, due to selection bias—in cases where it was chosen as the primary pedicle, it was believed to be the best choice, and success was expected to be high. In cases where it was used as a salvage pedicle, it was intuitively not the most appealing choice initially and was thus less likely to occlude the fistula. One distal sigmoid/jugular bulb dAVF was successfully embolized via a single APA pedicle. Tentorial/petrosal and torcular dAVFs may less frequently harbor APA supply; we successfully employed a distal jugular NMT branch as a pedicle for successful NBCA embolization of a tentorial/posterior fossa dAVF (figure 2).
In our series, 8% of indirect carotid-cavernous dAVFs harbored APA supply. Supply and subsequent embolization via clival branches of the NMT14 ,15 and, interestingly, superior pharyngeal branches have been reported.16 Our treated case was performed via a clival branch (figure 3). The superior pharyngeal branch is an intriguing and alluring endovascular conduit, which should not present a risk of lower CN palsy. A recent report of three high-risk (cortical venous drainage) dural carotid-cavernous fistulas treated via transarterial Onyx embolization of superior pharyngeal branches reported successful occlusion in two cases.16
Overall, this series illustrates the relatively preponderant involvement of APA supply to dAVFs of the posterior skull base, particularly marginal sinus fistulas. In contrast to the MMA, however, it remains a relatively rare first-choice transarterial conduit (5 of 267 cases in this series (2%)). In three of the five cases, it served as the only feasible transarterial choice in the absence of other adequately sized pedicles (in one patient with a carotid-cavernous fistula, and in two patients with marginal sinus fistulas), and in two other cases, it served as a serendipitously capacious and straight route to the fistula point (in one patient with a tentorial fistula, and one with a jugular fistula). Despite the rarity of these selected cases, knowledge of APA anatomy and its potential utility as an arterial pedicle for dAVF embolization is a crucial tool in the endovascular treatment armamentarium. Our series illustrates selected cases where it proved to be a useful pedicle and reinforces its relative inefficacy for dAVFs of the transverse and proximal sigmoid sinus.
Conclusion
This series illustrates the APA as an important, but rare, transarterial route for the embolization of well-selected dAVFs. It is not our contention to advocate use of this vessel as a general primary route when it is involved in dAVFs, but rather to illustrate it as a feasible route when other, safer, more capacious conduits, such as the MMA, are not involved or are not feasible targets.
References
Footnotes
Contributors Conception and design: BAG, FCA, KM, CGM. Drafting the article: BAG. Data acquisition: BAG. Interpretation and analysis: BAG, FCA, KM, CGM. Critical revision of the article: BAG, FCA, KM, CGM. Statistical analysis: BAG. Study supervision: FCA, CGM.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.