CASE REPORTJ Neurosurg 128:731–734, 2018

The standard treatment for indirect carotid-cavernous fistulas (CCFs) is currently endovascular transve-nous embolization.9 But transarterial ethylene vinyl

alcohol copolymer (Onyx) embolization has been increas-ingly used in the treatment of CCFs, especially in cases with an inaccessible venous route, because of the agent’s nonadhesive nature and penetration propensity over con-ventional liquid embolics.3,5,6 We report a rare complica-tion of Onyx migration into the cerebral artery during Onyx injection via the accessory meningeal artery (AMA) in a patient with indirect CCF and discuss the dangerous collaterals between the external carotid artery (ECA) and internal carotid artery (ICA). This case was briefly cov-ered in a previous report on dural arteriovenous fistulas.4

Case ReportHistory and Examination

A 49-year-old woman presented with a 2-month history of chemosis and proptosis in her right eye. She had no his-tory of head injury. Bruit was audible in her right orbit. Orbital CT demonstrated an enlarged superior ophthalmic

vein (SOV) suggesting spontaneous CCF. Cerebral angio-grams demonstrated a Barrow Type D CCF, which had fistulas between the right cavernous sinus and the dural branches of the ICA and the AMA of the ECA (Fig. 1). Manual carotid compression was performed for 2 months with the hope of spontaneous occlusion, but her chemosis did not resolve.

Therapeutic PlanA transvenous approach is considered to be more reli-

able and safer than a transarterial approach for the treat-ment of indirect CCF. Thus, our treatment plan for the pa-tient consisted of 1) a transvenous coil embolization via the inferior petrosal sinus (IPS), 2) a direct SOV approach, and finally 3) transarterial Onyx embolization. We dis-cussed these 3 treatment options with the patient and her family, but the patient did not agree to the facial scar that could occur after direct exposure of the SOV. Thus, we decided to perform transarterial Onyx embolization after the transvenous IPS access had failed.

Transvenous Approach. With the patient under general

ABBREVIATIONS ACA = anterior cerebral artery; AMA = accessory meningeal artery; CCF = carotid-cavernous fistula; EC = extracranial; ECA = external carotid artery; IC = intracranial; ICA = internal carotid artery; ILT = inferolateral trunk; IPS = inferior petrosal sinus; MCA = middle cerebral artery; MRA = MR angiography; SOV = superior ophthalmic vein.SUBMITTED November 20, 2015. ACCEPTED September 1, 2016.INCLUDE WHEN CITING Published online March 3, 2017; DOI: 10.3171/2016.9.JNS152677.

Surgical removal of embolic material after its unexpected migration through extracranial-intracranial anastomosis in the treatment of Barrow Type D carotid-cavernous fistula: case report Jae-Sang Oh, MD, Dong-Sung Kim, MD, Jai-Joon Shim, MD, PhD, and Seok-Mann Yoon, MD, PhD

Department of Neurosurgery, Soonchunhyang University Cheonan Hospital, Cheonan, Republic of Korea

Endovascular occlusion via the transvenous route is the favored treatment for indirect carotid-cavernous fistulas (CCFs). However, transarterial embolization can be used as an alternative method in patients with an inaccessible venous route. The authors present the case of a 49-year-old woman with a 2-month history of chemosis and proptosis in her right eye. Angiography demonstrated a Barrow Type D CCF. Transarterial Onyx embolization through the accessory meningeal artery was performed after an unsuccessful transvenous approach. Unexpected Onyx migrations to the cerebral arteries were detected while injecting the embolic material. Three hours after failed attempts to retrieve the Onyx cast endovas-cularly, it was microsurgically removed from the right middle cerebral artery. To the authors’ knowledge, this is the first report of the surgical removal of Onyx from a normal cerebral artery.https://thejns.org/doi/abs/10.3171/2016.9.JNS152677KEY WORDS carotid cavernous fistulas; Onyx; migration; transarterial embolization; vascular disorders

J Neurosurg Volume 128 • March 2018 731©AANS 2018, except where prohibited by US copyright law

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anesthesia, both the right femoral artery and right femo-ral vein were accessed with 5-Fr and 6-Fr short sheaths, respectively. A 6-Fr Envoy guiding catheter was placed in the internal jugular vein under venous phase roadmap guidance via right common carotid artery injection. Even though we attempted multiple trials to catheterize the IPS using a microcatheter and microwire, we could not gain access to the cavernous sinus. Thus, we changed the pro-cedure to a transarterial approach.

Onyx Embolization. A transarterial approach through the AMA was performed. The Rebar 10 microcatheter (ev3/Covidien) was located in the AMA. Microcatheter angiography demonstrated the fistula clearly. Under blank roadmap guidance, we injected Onyx 18 in the usual manner (Fig. 2). During the injection, we detected sud-den Onyx cast migration to the ipsilateral anterior ce-rebral artery (ACA) and middle cerebral artery (MCA). Even though Onyx casts were seen in the MCA bifurca-tion and A4 segment, distal MCA flow was maintained on the control angiogram. Thus, endovascular retrieval of the Onyx cast was tried first for the distal ACA emboli using a Solitaire stent (ev3/Covidien). Initially, Onyx cast was captured in the stent retriever, but it was inadvertently re-leased from the stent when it passed the right A1 segment. Repeated trials resulted in anterior communicating artery and A2 occlusion by the mobilized cast. Thus, to minimize the extent of postoperative ACA infarction, we pushed the Onyx cast distally beyond the origin of the callosomar-ginal artery, expecting retrograde collateral flow from the splenial artery (Fig. 3). A final angiogram showed com-plete obliteration of the indirect CCF with preserved MCA flow. Even though Onyx cast in the right MCA bifurcation did not occlude the MCA flow, we decided to remove the cast to prevent delayed occlusion of MCA flow.

Surgical Removal of Embolic Material. Immediately after intervention, the patient complained of severe left-sided paresis, especially in the upper extremity. Diffusion-weighted imaging of the brain showed multiple scattered high signal–intensity lesions in part of the right ACA and MCA territories. Magnetic resonance angiography (MRA) demonstrated suspected occlusion of the distal ACA (A4 segment) and distal MCA (Fig. 4). While the patient was under general anesthesia with propofol, we performed a right pterional approach and removal of the Onyx cast from the right MCA as soon as possible. After dural in-

cision, a lateral to medial sylvian dissection exposed the M2 segment, occluded MCA bifurcation, and M1 segment. Onyx cast could be identified by its dark color in the MCA bifurcation and the proximal part of both M2 segments. After temporary clipping of the M1 segment and both superior and inferior divisions of the M2 segment for 15 minutes, en bloc removal of the Onyx cast was performed following a small arteriotomy on the distal M1 segment just proximal to the bifurcation. The staghorn-shaped Onyx cast measured 9 mm in length. The arteriotomy site was repaired with 6-0 nylon sutures (Fig. 4). Until the mi-grated Onyx cast was removed, we tried to keep systolic blood pressure between 140 and 160 mm Hg by using ino-tropic agents.

Postoperative CoursePostoperatively, the patient’s orbital symptoms com-

pletely disappeared, although her motor weakness re-mained. Postoperative MRA showed complete recanali-zation of MCA flow but occluded distal ACA flow (Fig. 5). The patient’s left-sided paresis was improved to Grade 4+ at the 6-month follow-up, but she complained of left-sided sensory change. She recovered a lot by the 3-year follow-up with a modified Rankin Scale score of 1.

DiscussionIn the literature, most endovascular treatments for indi-

rect CCF are performed transvenously through the petro-sal sinus, facial vein, or ophthalmic veins.1,9 Transarterial

FIG. 1. Preoperative radiological images showing indirect CCF. Enhanced orbital CT scan (A) shows an enlarged SOV on the right side. Right ICA (B) and ECA (C) angiograms, lateral view, demonstrating an enlarged cavernous sinus and SOV. Images in B and C reproduced from Oh et al: J Korean Neurosurg Soc 59:17–25, 2016. Published with permission.

FIG. 2. Microcatheter angiograms, lateral view, through the right AMA showing contrast filling of the cavernous sinus and SOV (left). Onyx cast is visible on the fistulas and cavernous sinus (right).

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Surgical removal of migrated Onyx in Barrow Type D CCF

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Onyx embolization can also be a valuable option in the treatment of a Barrow Type D CCF when venous access is difficult.9 When a transvenous IPS approach has failed, a trans-SOV approach could be a second option for the treatment of indirect CCF. However, this approach raises cosmetic concerns in some women. The patient in our case was afraid of having a scar on the eyelid and strongly re-fused to undergo the direct SOV approach. Thus, we tried a transarterial approach as the next option.

However, because embryologic and phylogenetic devel-opment closely links the ECAs to the intracranial arter-ies, certain common anastomotic routes must be kept in mind while performing embolization procedures in order to avoid potential major complications such as embolic stroke or cranial nerve palsies.2 Although these anasto-motic channels may not be visible on routine catheter angiography, they are always present and thus will open under circumstances such as increased intraarterial pres-sure, in the presence of high-flow shunts as a result of the “sump effect,” or as collateral routes for occlusions of the major intracranial arteries.2

The known major extracranial (EC)–intracranial (IC) anastomotic pathways are the orbital region via the oph-thalmic artery that is the interface between the internal maxillary and internal carotid territories; the petrous-cav-ernous region via the inferolateral trunk (ILT), the petrous

branches of the ICA, and the meningohypophyseal trunk to the carotid artery; and the upper cervical region via the ascending pharyngeal, occipital, and ascending and deep cervical arteries to the vertebral artery.2 Knowledge of these channels may guarantee a more satisfactory out-come and safer procedure.

Several cases of Onyx migration during transarterial Onyx injection have been reported in the literature. Most of these cases involved migration into the adjacent vein, venous sinus, right ventricle distally, and lung through a venous route.3,6,8 These venous migrations were mostly asymptomatic or were minimally symptomatic if the ve-nous outflow obstruction was not severe.8 However, trans-arterial EC-IC Onyx migration can be dangerous or fatal. To our knowledge, only 1 case of EC-IC Onyx migration has been reported.6 Migration into the cavernous ICA occurred during Onyx embolization through the ECA feeding artery in a patient with transverse sinus dural ar-teriovenous fistula. Although the migration did not result in flow obstruction, the patient died of his initial hemor-rhage. In our patient, Onyx migrated into the cavernous ICA and then to the distal MCA and ACA. The probable route of Onyx migration to the IC artery was from the AMA to the posteromedial branch of the ILT through the artery of the foramen ovale.

Theoretically, migrated Onyx cast can be removed sur-

FIG. 3. Radiographic and angiographic images of migrated Onyx cast and retrieval using a Solitaire stent. Initial anteroposterior skull radiograph (A) showed migrated Onyx cast on pathways of ACA and MCA. Unexpected migrated Onyx casts were seen in the distal ACA beyond the origin of the callosomarginal artery and in the MCA bifurcation, as was the disappearance of the fistula on a lateral ICA angiogram (B). Although repeated trials to retrieve the migrated Onyx cast in the distal ACA were attempted using a Solitaire stent, a right ICA angiogram (C) showed an A1 segment occluded by the Onyx cast released from the stent when the right A1 segment was passed. A final angiogram (D) obtained after the Onyx cast had been pushed distally beyond the origin of the callosomarginal artery with the hope of retrograde collateral filling of the distal ACA (A5 segment) from the splenial artery, demonstrating partial recanalization of distal ACA flow. Image in A reproduced from Oh et al: J Korean Neurosurg Soc 59:17–25, 2016. Published with permission.

FIG. 4. Intraoperative photographs obtained during MCA embolectomy. Darkish discoloration of the MCA bifurcation due to the migrated Onyx cast is evident (A). After temporary occlusion of the M1 segment and both superior and inferior divisions of the M2 segment, Onyx cast was removed through a small arteriotomy (B). The arteriotomy site was repaired with 3 stitches (C). The staghorn-shaped Onyx cast molded in MCA bifurcation was easily removed in 1 piece, measuring 9 mm in length (D). Panels A, C, and D reproduced from Oh et al: J Korean Neurosurg Soc 59:17–25, 2016. Published with permission.

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gically or endovascularly. Because endovascular retrieval can be performed without time delay, it should be tried first if it is possible. In our patient we tried endovascu-lar retrieval first, but it was not easy compared with stent thrombectomy. Even though passage of the microcatheter beyond the Onyx emboli and capture of the Onyx cast us-ing a Solitaire stent were possible, the cast was repeatedly inadvertently released from the stent retriever at the A1-A2 junction probably because of the abrupt change in the A1-A2 angle. After endovascular retrieval failed, we did not try suction embolectomy because the Onyx cast was not moldable under negative pressure given its hard, solid consistency, which may preclude effective suction using aspiration thrombectomy. Instead of retrieving the Onyx cast, we pushed it farther distally to minimize postoper-ative infarction.

For the Onyx cast in the MCA bifurcation, endovas-cular retrieval was not attempted because the cast did not occlude MCA flow on the final angiogram. However, post-operative MCA occlusion was strongly suspected since the patient complained of severe left upper-extremity weakness. Thus, we microsurgically removed the Onyx cast, which was easier than expected. The cast could be removed from the occluded vessel in one piece without fragmentation or further vascular injury because it was not adhesive or fragile.

At our institution, neurophysiological monitoring via motor evoked potentials recording, somatosensory evoked potentials recording, and electromyography has been routinely performed in all endovascular or surgical pro-cedures with the patient under general anesthesia. In our patient, however, we did not employ neurophysiological monitoring, as it was not available a few years ago.

Because the intervention was performed under general anesthesia using propofol, we did not administer addition-al neuroprotective agents. But we elevated the blood pres-sure to enhance collateral flow after occlusion of the distal ACA by migrated Onyx.

Microsurgical removal of Onyx material from an aneu-rysm has been reported to alleviate mass effect or edema.7 However, open surgical removal of an Onyx cast in a nor-mal vessel has not yet been reported. Because the proce-dure is not difficult, we suggest prompt surgical removal of an unexpected Onyx emboli in cases of unsuccessful endovascular retrieval.

ConclusionsOnyx cast migration can occur from the ECA to ICA

through the ILT between the AMA and ICA during the treatment of indirect CCF. Prompt surgical removal of em-bolic material can result in a satisfactory outcome when unexpected migration of the embolic material occurs.

AcknowledgmentsThis study research was supported by the Soonchunhyang

University Research Fund.

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3. Lv X, Jiang C, Li Y, Liu L, Liu J, Wu Z: The limitations and risks of transarterial Onyx injections in the treatment of grade I and II DAVFs. Eur J Radiol 80:e385–e388, 2011

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6. Shi ZS, Loh Y, Gonzalez N, Tateshima S, Feng L, Jahan R, et al: Flow control techniques for Onyx embolization of in-tracranial dural arteriovenous fistulae. J Neurointerv Surg 5:311–316, 2013

7. Van Loock K, Menovsky T, Voormolen MH, Plazier M, Parizel P, De Ridder D, et al: Microsurgical removal of Onyx HD-500 from an aneurysm for relief of brainstem compres-sion. Case report. J Neurosurg 113:770–773, 2010

8. Wang H, Lv X, Jiang C, Li Y, Wu Z, Xu K: Onyx migration in the endovascular management of intracranial dural arte-riovenous fistulas. Interv Neuroradiol 15:301–308, 2009

9. Zaidat OO, Lazzaro MA, Niu T, Hong SH, Fitzsimmons BF, Lynch JR, et al: Multimodal endovascular therapy of traumatic and spontaneous carotid cavernous fistula using coils, n-BCA, Onyx and stent graft. J Neurointerv Surg 3:255–262, 2011

DisclosuresThe authors report no conflict of interest concerning the materi-als or methods used in this study or the findings specified in this paper.

Author ContributionsConception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: Oh, Kim. Drafting the article: Oh. Critically revising the article: Yoon, Kim, Shim. Reviewed submitted version of manuscript: Yoon, Oh. Study supervision: Yoon.

CorrespondenceSeok-Mann Yoon, Department of Neurosurgery, Soonchunhyang University Cheonan Hospital, 23-20 Bongmyeong-dong, Cheon-an, Chungcheongnam-do 330-721, Republic of Korea. email: smyoon@sch.ac.kr.

FIG. 5. Postprocedural diffusion-weighted image showing scattered high signal intensity on part of the right ACA and MCA territories (left). Post-operative MR angiogram obtained after removal of the Onyx cast, dem-onstrating complete recanalization of right MCA flow without narrowing of the arteriotomy site (right). Right panel reproduced from Oh et al: J Korean Neurosurg Soc 59:17–25, 2016. Published with permission.

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