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Neurointervention > Epub ahead of print
Mahmoud, Koc, and Mahmoud: Hemodynamic Instability during Squid Embolization of Dural Arteriovenous Fistula: A Case Report

Abstract

There are few documented cases of bradycardia or asystole occurring during Onyx embolization of intracranial dural arteriovenous fistulas (DAVFs), although these events are more commonly observed in open neurosurgical procedures, particularly those involving the skull base. We present a case treated for a ruptured paramedian occipital DAVF. During the administration of Squid into the middle meningeal artery, while balloons were inflated in the large occipital arteries bilaterally to control the flow during embolization of the DAVF, the patient experienced an abrupt episode of sinus bradycardia, which recurred after a second injection of Squid. After temporarily halting the injections and deflating the balloons, a third injection was successfully administered without complications, allowing total exclusion of the fistula.

INTRODUCTION

Hemodynamic instability during endovascular procedures has been documented, but there are few published case reports of bradycardia or asystole occurring during Onyx embolization of dural arteriovenous fistula (DAVF) [1-7]. To our knowledge, there have been no reports of bradycardia associated with Squid injection in the context of DAVF. Furthermore, there is a lack of literature addressing hemodynamic instability during balloon inflation in the dural arteries.
We recently encountered a case in which the patient experienced sinus bradycardia, and it remains unclear whether this was related to the use of Squid or the inflation of balloons in the occipital arteries. We believe this case carries important teaching points for all neurovascular team members involved in the care of these patients.

CASE REPORT

A patient presented with headache. Computed tomography (CT) scan of the brain revealed diffuse intraventricular hemorrhage and a right occipital intracerebral hemorrhage (Fig. 1A). A CT angiography suggested the presence of an arteriovenous malformation. The patient then experienced a sudden decrease in the level of consciousness, resulting in a Glasgow Coma Scale score of 6. He was intubated immediately and taken to the operating room for the insertion of an external ventricular drain.
Subsequently, a digital subtraction angiography was performed, which revealed a Cognard class IV DAVF with significant irregularity and aneurysmal dilatation in the draining cortical vein. The fistula was in the right occipital paramedian region adjacent to the right transverse sinus, with feeders arising from the occipital arteries bilaterally and the middle meningeal artery (MMA) on the right side. After discussing treatment options with the neurosurgical team, it was decided to proceed with endovascular treatment of the fistula. The patient had no significant cardiac history. The procedure was performed under general anesthesia and systemic heparinization. Following the initial diagnostic angiography (Fig. 1B, C), a 6F Guider Soft Tip XF guide catheter (Boston Scientific) was placed in the left occipital artery. An 80 cm Neuron Max guide catheter (Penumbra, Inc.) was then positioned in the proximal right external carotid artery. Using a “Traxcess 0.014” hydrophilic microwire (MicroVention, Inc.), an Eclipse balloon microcatheter 6×12 (Balt) was advanced and positioned in the occipital arteries bilaterally to achieve effective flow control during the embolization and enhance the penetration of the embolic material into the fistula network. The balloon was positioned distally on the left occipital artery, near the fistula network, and at the origin of the first branch supplying the fistula from the right occipital artery (Fig. 1D). With the aid of the “Traxcess 0.014” microwire, an Apollo 2.7 French microcatheter (Covidien, EV3) was advanced to the right MMA and placed distally; however, it was not possible to reach the fistula point. A microcatheter injection was performed to confirm both the flow and the wedge-shaped position of the Apollo microcatheter. Once all catheters were in stable positions, embolization of the fistula commenced while inflating the balloons in both occipital arteries.
The embolization procedure was conducted using Squid 18 (Emboflu). Dimethyl sulfoxide (DMSO) was injected without incident; however, after the initial 0.3 cc of Squid was administered, the patient experienced sinus bradycardia with the heart rate dropping to 36 beats per minute. The injection was immediately paused, and both balloons were deflated. Following the return of normal cardiac rhythm and after consulting the anesthetist, a second injection of Squid was performed while inflating the balloons, resulting in a similar hemodynamic response. Once again, the cardiac rhythm returned to normal after pausing the injection of Squid and deflating the balloons.
After further discussion with the anesthetist, a third injection of Squid was successfully administered without inflating the balloons, and no further cardiac episodes were observed. Angiographic results demonstrated effective occlusion of the fistula, with the embolizing cast extending to the foot of the draining vein (Fig. 1E, F). Traces of the embolic cast were observed within the aneurysmal dilatation of the draining vein (Fig. 1G). Final angiography revealed no thromboembolic complications resulting from the procedure.
The patient was subsequently transferred intubated to the intensive care unit due to a low Glasgow Coma Scale prior to the procedure. During this time, he experienced no additional hemodynamic instability. The cardiac workup following the procedure revealed no abnormalities. Over the next few days, he experienced some improvement in his initial neurological symptoms. Over the following 4 weeks, the patient showed progressive improvement and was discharged with a Glasgow Coma Scale score of 15 and no neurological deficits. A follow-up CT scan 2 weeks post-embolization revealed no evidence of venous infarction and significant resolution of both the intraventricular hemorrhage and the right occipital intracerebral hemorrhage (Fig. 1H).

DISCUSSION

Asystole or sinus bradycardia during Onyx (ethylene-vinyl alcohol copolymer) embolization of a DAVF was observed, likely due to the trigemino-cardiac reflex (TCR), a physiological reflex that occurs in response to trigeminal nerve stimulation, which was first described in endovascular Onyx embolization by Lv et al. [6]. TCR has been documented during the injection of both DMSO and Onyx. Literature predominantly associates this reflex with transarterial injections into the MMA or transvenous injections into the cavernous and inferior petrosal sinuses. However, whether this phenomenon is attributable to the neurotoxic effects of DMSO or to direct compression of the trigeminal nerve innervating the dura mater by formation of the Onyx plug remains uncertain (Table 1) [1-6]. Wang et al. [3] proposed that injection pressure in the MMA during Onyx embolization triggers neuronal signals transmitted via the Gasserian ganglion to the sensory nucleus of the trigeminal nerve, leading to the TCR. Similarly, Lv et al. [4] hypothesized that the neurotoxic effects of DMSO on cranial nerves within the cavernous sinus or on the trigeminal nerve innervating the dura mater could contribute to TCR during transvenous Onyx embolization for carotid-cavernous fistulas.
To our knowledge, no cases of TCR have been reported in association with Squid injection. In our case, we first occluded the large bilateral occipital artery feeders and proceeded to inject Squid into the smaller MMA. This approach was employed to control flow during embolization and achieve better penetration into the fistula network. A similar technique, involving the use of two microcatheters, has been previously described. In this method, the feeder is proximally occluded with coils, while a distally placed catheter is used for the injection of embolic material, facilitating improved penetration [8]. In our case, the TCR occurred a few minutes after initiating the Squid injection while the balloon was inflated. We believe the TCR was triggered by injection pressure within the MMA. The absence of sinus bradycardia after balloon deflation during the third injection suggests that the TCR may have been triggered by mechanical stimulation of dural nerves due to balloon inflation in the occipital arteries. Given the unpredictable nature of this response, we recommend that neurointerventionists should be aware of TCR, which may occur not only with the use of Onyx but also with Squid or any mechanical intervention, such as balloon inflation, within dural branches.
Neurointerventionists should be aware of the potential risk for hemodynamic instability during endovascular treatment of DAVFs. This risk is not limited to the use of Onyx but may also arise with Squid or during balloon inflation within dural branches. It is essential to inform the entire team of this potential risk before the injection of embolic materials or balloon inflation.

Notes

Fund

None.

Ethics Statement

We confirm that the study was conducted in accordance with the Helsinki Declaration as revised in 2013. This study has been approved by the Ethics board committee at Hamad Medical Corporation and the requirement for informed consent was waived. Patient information such as sex and age were anonymized.

Conflicts of Interest

The authors have no conflicts to disclose.

Author Contributions

Concept and design: EM. Analysis and interpretation: EM. Data collection: EM. Writing the article: EM. Critical revision of the article: EM, MM, and OK. Final approval of the article: EM, MM, and OK. Overall responsibility: EM.

Fig. 1.
(A) Pre-embolization computed tomography (CT) shows intraventricular hemorrhage and right occipital intracerebral hemorrhage. (B) Anteroposterior digital subtraction angiography view show supply to the right paramedian dural arteriovenous fistula primarily from the right occipital artery and, to a lesser extent, from the right middle meningeal artery. Note the aneurysmal dilatation in the draining vein (white arrow). (C) Additional supply is seen from the left occipital artery. (D) Balloons are inflated and positioned in the occipital artery bilaterally (white arrows). The tip of the microcatheter is placed in the right middle meningeal artery (black arrow). (E, F) Injections in the right and left external carotid arteries confirm complete exclusion of the fistula. (G) Anteroposterior, non-subtracted image showing the Squid cast within the fistula network, extending to occlude the vein’s origin (white arrow). Note the embolic material traces in the aneurysmal dilatation (black arrow). (H) Post embolization CT follow up shows a significant resolution of the hematoma and no evidence of venous infarction. Note the Squid traces in the draining vein (white arrow).
neuroint-2024-00521f1.jpg
Table 1.
Summarization of previously reported cases with hemodynamic instability during Onyx embolization
Author Case Embolized vessel Embolized material Interpretation
Song et al. [1] 1 TA, MMA Onyx TCR occurred due to backflow of Onyx into the petrous branch, leading to increased pressure of the MMA.
Nicholson et al. [2] 1 TA, PMA Onyx The fistula was located adjacent to the transverse sinus, and the dura mater of the posterior fossa is partially innervated by branches of the trigeminal nerve while receiving vascular supply from branches of the PMA. Consequently, embolization of these vessels can stimulate the trigeminal nerve and trigger a TCR.
Wang et al. [3] 2 Case 1: TA, MMA Onyx They thought that direct distraction by the dilated MMA due to formation of Onyx plug produces an injection pressure.
Case 2: TV (CS) Coils+Onyx They suggested that TCR may also occur due to the chemical stimulus of DMSO during transvenous Onyx embolization of dural CS fistulas.
Lv et al. [4] 5 3 Cases TA, MMA Onyx They suggested that TCR occurs due to the neurotoxicity of DMSO on the cranial nerves within the CS or from direct compression of the trigeminal nerve innervating the dura mater by the formation of an Onyx plug.
2 Cases TV, IPS Coils+Onyx
Amiridze and Darwish [5] 9 4 Cases TA, MMA Onyx They proposed that TCR could result from the direct effect of DMSO on the trigeminal nerve and its branches, particularly the ophthalmic division.
2 Cases TA, VA, and APA branches
1 Case TA, ethmoidal artery
2 Cases TV (CS) Coils+Onyx
Lv et al. [6] 1 TA, MMA Onyx Compression of the nervus spinosus by the dilated MMA due to formation of Onyx plug.

TA, transarterial; MMA, middle meningeal artery; TCR, trigemino-cardiac reflex; PMA, posterior meningeal artery; CS, cavernous sinus; DMSO, dimethyl sulfoxide; IPS, inferior petrosal sinus; VA, vertebral artery; APA, ascending pharyngeal artery.

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