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Original Article

Neuromeningeal access for transarterial intravenous carotid-cavernous fistula embolization

Interventional Neuroradiology 2015, Vol. 21(2) 234–239 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1591019915581968 ine.sagepub.com

Ramsey Ashour and Ram Chavali

Abstract While numerous endovascular access routes have been described for carotid-cavernous fistula (CCF) treatment, transarterial embolization via the neuromeningeal trunk of the ascending pharyngeal artery is typically avoided due to the risk of cranial nerve palsy or non-target embolization via external-to-internal carotid anastamoses. We present the case of a dural CCF in which access to the venous side of the fistula was achieved via the neuromeningeal trunk and allowed for curative transarterial intravenous coil/liquid embolic embolization of the lesion. The utility of a transarterial intravenous approach in the face of venous sinus occlusion is highlighted. The neuromeningeal trunk should not be overlooked as a potential access route for transarterial intravenous CCF embolization in cases where traditional endovascular access is limited; this approach does not carry the same risks that are generally associated with pure transarterial embolization along this pathway.

Keywords Neuromeningeal trunk, ascending pharyngeal artery, carotid-cavernous fistula, endovascular treatment, Onyx, embolization

Introduction A carotid-cavernous fistula (CCF) is an abnormal arteriovenous shunt connecting the internal carotid artery (ICA) and/or the external carotid artery (ECA) to the cavernous sinus. Endovascular approaches have emerged as the primary method of treating most CCFs, although the techniques and agents used continue to evolve.1 In this report, we present the case of a dural CCF treated by transarterial intravenous coil/Onyx embolization via the neuromeningeal trunk of the ascending pharyngeal artery (APA). The utility of a transarterial intravenous approach in the face of venous sinus occlusion is highlighted, and the potential for achieving endovascular access using the neuromeningeal trunk for CCF embolization is emphasized.

Case report A middle-aged patient presented with a 10-day history of persistent double vision. Physical examination revealed right conjunctival injection, right periorbital edema, and the right eye appeared deviated downward and slightly inward. Brain computed tomography angiography (CTA) demonstrated bilateral cavernous sinus fullness, right superior ophthalmic vein dilation, and multiple prominent posterior fossa veins (Figure 1). These findings were not present on brain magnetic

resonance imaging (MRI) with contrast performed for headaches 16 months prior. Cerebral angiography demonstrated a left CCF with ECA supply arising from bilateral APA, bilateral middle meningeal (MMA), and bilateral distal internal maxillary (IMAX) branches and ICA supply arising from bilateral petrocavernous branches (Figure 2). Venous drainage of the lesion proceeded from the left cavernous sinus across the intercavernous sinus to the right cavernous sinus and subsequently into the right superior ophthalmic vein (SOV) anteriorly and through the right superior petrosal sinus posteriorly into multiple posterior fossa leptomeningeal veins. The inferior petrosal sinuses were not visualized bilaterally due to chronic occlusion. Given the presence of leptomeningeal venous drainage, orbital venous congestive signs, and persistent diplopia, urgent endovascular intervention was recommended. Under general anesthesia, the left external carotid supply to the lesion was first reduced by

Departments of Neurosurgery and Radiology, Harvard Medical School/ Brigham and Women’s Hospital, Boston, MA, USA Corresponding author: Ram Chavali, Departments of Neurosurgery and Radiology, Harvard Medical School/Brigham and Women’s Hospital, Boston, MA, USA. Email: [email protected]

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Figure 1. CT angiographic images demonstrating (a) enlargement of the right SOV (white arrow) (b) bilateral cavernous sinus fullness/ contrast uptake (white arrows) and (c) multiple prominent tortuous posterior fossa veins (white arrow).

Figure 2. Pre-treatment angiographic images. (a) Lateral right ICA (b) Anteroposterior right ECA (c) Lateral right ECA (d) Lateral left ICA (e) Anteroposterior left ECA (f) Lateral left ECA.

performing distal MMA, APA, and IMAX branch transarterial embolization using a combination of polyvinyl alcohol particles, gelfoam particles, and Onyx (Covidien). An Echelon 10 (Covidien) microcatheter was then navigated into the right APA. We were able to navigate from the posterior division of the right APA via the neuromeningeal trunk across the fistula and into

the left cavernous sinus venous pouch (Figure 3). Rather than embolize from this position, we decided to navigate intravenously from the left cavernous sinus across the intercavernous sinus to the right cavernous sinus venous pouch, anticipating that we may lose access to the right cavernous sinus if we embolized the left side first. Beginning at its connection to the

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Figure 3. Transarterial intravenous access – Right APA (a) anteroposterior and (b) lateral microangiographic pre-treatment images. Roadmap (c) anteroposterior and (d) lateral angiograms demonstrate the microcatheter being navigated over a microwire from the right APA into the left cavernous sinus across the fistula and subsequently across the intercavernous sinus to the right cavernous sinus at its connection to the right superior petrosal sinus.

‘‘high-risk’’ superior petrosal sinus outflow, coil embolization of the right cavernous sinus pouch was performed (Figure 4). The microcatheter was withdrawn slightly, and coil embolization of the left cavernous sinus pouch was performed. The microcatheter was again withdrawn into the distal arterial feeding pedicle of the clival branch supplying the fistulous pouch. From this position, 0.4 ml of Onyx 34 was injected to occlude the remaining clival arterial branch supply to the lesion. The microcatheter was removed. Final post-procedure bilateral ECA and ICA angiography demonstrated complete obliteration of the fistula. The patient’s diplopia and orbital congestive signs resolved after embolization. Follow-up angiography performed 14 months after embolization demonstrated no recurrence of the fistula (Figure 5).

Discussion Dural CCFs are among the most complex lesions treated by neuroendovascular specialists and mandate a

careful analysis and thorough understanding of the normal and pathologic arterial and venous anatomy prior to treatment. Curative embolization of a dural CCF fed by multiple ECA and ICA branches is difficult to achieve by a pure transarterial route. The numerous small distal arterial feeders are challenging to catheterize and may be dangerous to embolize, particularly if liquid embolic agents are utilized, because unrecognized ECA-to-ICA anastomoses may be inadvertently embolized. Furthermore, unless the venous outflow is occluded at the site of pathologic arteriovenous fistulization, further arterial recruitment by the lesion and/or re-routing of venous drainage encourage persistence of the fistula.1 As such, the transvenous approach, initially pioneered by Debrun2 via the inferior petrosal sinus, is an ideal option for CCF embolization, allowing for embolization of the cavernous sinus itself. However, a pure transvenous approach may not be feasible in the face of venous outflow occlusion. In a recent literature review evaluating all previously reported dural arteriovenous fistula cases in which

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Figure 4. (a) Roadmap right APA anteroposterior angiogram during coil embolization of the right cavernous sinus. (b) Roadmap lateral angiogram during coil embolization of the right cavernous sinus. The microcatheter has been navigated along the posterior division (black arrow) of the APA via the neuromeningeal trunk. The tip of the coil is demonstrated emanating posteriorly from the right cavernous sinus into the right superior petrosal sinus (white arrow). (c) Roadmap view during embolization of the distal clival arterial supply to the fistula with Onyx (white arrow) (d) Native skull X-ray demonstrating coil masses within the cavernous sinuses bilaterally (white arrows) and Onyx casts (black arrows) within the embolized APAs bilaterally.

Figure 5. Angiographic images 14 months post-treatment. (a) Lateral right ECA (b) Lateral right ICA (c) Anteroposterior left common carotid artery.

transarterial intravenous coil embolization was performed, Baik et al.3 found no cases in which the neuromeningeal trunk was utilized to achieve endovascular access for treatment. Pero et al.4 reported three CCF

cases in which pure transarterial Onyx embolization was performed via the pharyngeal (anterior) division of the APA, resulting in two cures and one nearcomplete fistula occlusion. They stressed the danger

238 of performing pure transarterial embolization using the neuromeningeal (posterior) division of the APA, due to the risk of cranial nerve palsy or inadvertent non-target embolization through ECA-to-ICA anastomoses.5,6 In the current case, access to the left cavernous sinus was achieved from the right APA via the neuromeningeal trunk, and the intercavernous connection was then exploited to access the right cavernous sinus, allowing for definitive sequential embolization of the pathologic venous outflow of the fistula. In order to ensure complete obliteration of the fistula, we took the extra step of performing Onyx embolization to occlude the remaining clival arterial branch supply to the lesion; however, it must be recognized that this maneuver introduces the additional risk of the liquid embolic agent penetrating small but important anastamotic channels that may not be visible prior to injection. An awareness of the anatomy, embryology, and clinical significance of the APA is of paramount importance during the planning and execution of neuroendovascular procedures. Although a comprehensive description of these concepts can be found elsewhere,7,8 the following discussion briefly highlights the relevant anatomy of the neuromeningeal trunk: The APA divides into two major trunks: the ‘‘extracranial’’ pharyngeal trunk and the ‘‘intracranial’’ neuromeningeal trunk. The neuromeningeal trunk subsequently divides into two major divisions: 1. The hypoglossal branch enters the hypoglossal canal and supplies the vasa nervorum of cranial nerve XII. 2. The jugular branch enters the jugular foramen and supplies the vasa nervorum of cranial nerves IX, X, and XI. 3. Three small branches leave the jugular foramen: 4. A superior branch supplies the meninges of the internal auditory canal. 5. A medial ‘‘clival’’ branch supplies the dura of the inferior petrosal sinus and possibly the vasa nervorum of cranial nerve VI proximal to Dorello’s canal. This branch may also anastomose with the ICA via the meningohypophyseal trunk. 6. A lateral branch supplies the dura of the sigmoid sinus. The inferior tympanic branch may rise from the proximal aspect of the neuromeningeal trunk or as a separate branch between the pharyngeal and neuromeningeal trunks. It may anastamose with caroticotympanic branches of the ICA, the vasa nervorum of cranial nerve IX, or the vasa nervorum of cranial nerve VII via the stylomastoid artery or the petrosquamosal branch of the middle meningeal artery. Thus, it is readily apparent from the above summary that multiple cranial nerves (VI–XII) may be placed at risk during embolization of the neuromeningeal trunk. Alternative transvenous access routes to the cavernous sinus in the face of inferior petrosal sinus occlusion include transfemoral facial-to-SOV, direct SOV, direct

Interventional Neuroradiology 21(2) transorbital cavernous sinus puncture, and surgicallyassisted cavernous sinus exposure, among others.1 In our case, the traditional transvenous access was limited by bilateral inferior petrosal sinus occlusion. Even in the face of a non-opacified or occluded inferior petrosal sinus, cavernous sinus access can be achieved through the thrombosed segment in up to 80% of cases with a low reported complication rate.9 Nevertheless, even in experienced hands,10 this approach introduces a risk of sinus perforation, particularly during advancement of the wire tip, which may be stiffened by the catheter, into a narrow/occluded venous structure. A transfemoral facial-to-SOV approach could have been attempted; however, this would have resulted in a more complicated procedure, requiring a second groin puncture, a second set of catheters to be advanced through the venous system, and navigation into a narrow facial vein, which was noted to harbor an area of focal stenosis. A direct SOV approach would have required operative exposure of the vein, similarly increasing the complexity of the procedure. Importantly, either of these approaches would have entailed the undesirable risk of SOV occlusion, potentially worsening the degree of cortical venous outflow during the procedure or even permanently if the fistula was not completely obliterated. A transarterial intravenous approach via the neuromeningeal trunk, in which the intercavernous connection was utilized to access both cavernous sinuses through the same catheterization, proved to be an effective curative solution for this complex lesion, and should not be overlooked as a treatment option in selected CCFs, as detailed in our report. Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest None declared.

References 1. Ashour R, Elhammady M and Aziz-Sultan MA. Carotidcavernous fistulas. In: Jabbour P (ed) Neurovascular Surgical Techniques. New Delhi: Jaypee Brothers Medical Publishers, 2013, pp. 296–308. 2. Debrun G, Lacour P, Vin˜uela F, et al. Treatment of 54 traumatic carotid-cavernous fistulas. J Neurosurg 1981; 55: 678–692. 3. Baik SK, Kim YW, Lee SW, et al. A treatment option for nontraumatic adult-type dural arteriovenous fistulas: Transarterial venous coil embolization. World Neurosurg 2014; 82: 417–422. 4. Pero G, Quilici L, Piano M, et al. Onyx embolization of dural arteriovenous fistulas of the cavernous sinus through the superior pharyngeal branch of the ascending pharyngeal artery. J Neurointerv Surg 2015; 7: e16. 5. Byun JS, Hwang SN, Park SW, et al. Dural arteriovenous fistula of jugular foramen with subarachnoid hemorrhage: Selective transarterial embolization. J Korean Neurosurg Soc 2009; 45: 199–202.

Ashour and Chavali 6. Geibprasert S, Pongpech S, Armstrong D, et al. Dangerous extracranial-intracranial anastomoses and supply to the cranial nerves: Vessels the neurointerventionalist needs to know. Am J Neuroradiol 2009; 30: 1459–1468. 7. Hacein-Bey L, Daniels DL, Ulmer JL, et al. The ascending pharyngeal artery: Branches, anastomoses, and clinical significance. Am J Neuroradiol 2002; 23: 1246–1256. 8. Cavalcanti DD, Reis CV, Hanel R, et al. The ascending pharyngeal artery and its relevance for neurosurgical and

239 endovascular procedures. Neurosurgery 2009; 65(6 Suppl): 114–120; discussion 120. 9. Lekkhong E, Pongpech S, Ter Brugge K, et al. Transvenous embolization of intracranial dural arteriovenous shunts through occluded venous segments: Experience in 51 patients. Am J Neuroradiol 2011; 32: 1738–1744. 10. Halbach VV, Higashida RT, Dowd CF, et al. Management of vascular perforations that occur during neurointerventional procedures. Am J Neuroradiol 1991; 12: 319–327.

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Neuromeningeal access for transarterial intravenous carotid-cavernous fistula embolization.

While numerous endovascular access routes have been described for carotid-cavernous fistula (CCF) treatment, transarterial embolization via the neurom...
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