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Case report
Transarterial balloon assisted Onyx embolization of pericallosal arteriovenous malformations
  1. Ludwig D Orozco1,
  2. Gustavo D Luzardo1,
  3. Razvan F Buciuc1,2
  1. 1Department of Neurosurgery, University of Mississippi Medical Center, Jackson, Mississippi, USA
  2. 2Department of Radiology, Neurosurgery and Neurology, University of Mississippi Medical Center, Jackson, Mississippi, USA
  1. Correspondence to Dr L D Orozco, Department of Neurosurgery, University of Mississippi Medical Center, 2500 N State Street, Jackson, MS 39216, USA; lorozco-castillo{at}umc.edu

Abstract

Summary Preliminary experience using a balloon assisted technique (BAT) for embolization of arteriovenous malformations (AVM) is reported. Two patients with large pericallosal AVMs were successfully embolized with Onyx under Scepter C balloon catheter flow arrest.

Clinical presentation One patient presented with a large intraventricular hemorrhage and hydrocephalus. The second patient presented with a long history of seizures and a small intracerebral hemorrhage. Both patients demonstrated extensive interhemispheric AVMs with multiple arterial feeders, predominantly from the pericallosal arteries.

Intervention A Marathon microcatheter was navigated into the target arterial feeders and a Scepter C occlusion balloon catheter was inflated immediately proximal. Under flow arrest, Onyx was injected via the microcatheter with excellent nidal penetration. In both cases, there was complete angiographic obliteration of the treated component of the AVM.

Conclusions Onyx embolization under balloon catheter flow arrest allows for greater nidal penetration of embolic material and improved reflux control. The technique is limited by the current deliverability of balloon catheters and the potential risk for earlier embolization of dangerous anastomosis.

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Introduction

The current endovascular treatment of cerebral arteriovenous malformations (AVMs) involves intranidal injection of permanent liquid embolic agents with the intent of cure, or as adjuvant therapy to surgery or radiosurgery.1 Consequently, the angiographic cure rates of cerebral AVMs treated with Onyx (eV3, Irvine, California, USA) are very heterogenous, ranging from 8.3% to 94.1%.1–4

Recent reports have employed a balloon assisted technique (BAT) for embolization of dural and pial arteriovenous fistulas.5–8 In this setting, both transarterial and transvenous balloon induced flow arrest enhance Onyx penetration and provide better control of the reflux. We report the first use of BAT to successfully embolize two different pericallosal AVMs.

Description of the technique

Case No 1

A 61-year-old woman presented in a comatose state (modified Rankin Scale score of 5) and with a dense right hemiparesis secondary to a ruptured pericallosal AVM (figure 1). She received a ventriculostomy catheter for acute hydrocephalus. Cerebral angiography demonstrated a pericallosal AVM primarily supplied by the right anterior cerebral artery (ACA), and to a lesser extent by the right posterior cerebral artery (figure 1). This malformation drained through an enlarged cortical vein into the superior sagittal sinus. She underwent first stage embolization with a combination of coils and Onyx (figure 1). Residual AVM was not embolized secondary to close proximity to the motor cortex, en passant cortical arteries and inability to perform selective electrophysiologic testing.

Figure 1

Case No 1. Axial CT scan shows extensive intraventricular hemorrhage secondary to a ruptured pericallosal arteriovenous malformation (AVM) (A). Cerebral angiography demonstrates a pericallosal AVM primarily supplied by the right anterior cerebral artery (B, lateral right common carotid artery (CCA) injection) and to a lesser extent by the right posterior cerebral artery (C, lateral left vertebral injection). Angiographic images after first stage embolization with Onyx and coils show residual AVM (D, lateral right CCA injection).

Three weeks after the first embolization, access was obtained in the right common femoral artery with a 6 French Shuttle sheath (Cook Medical, Bloomington, Indiana, USA) and advanced to the distal right internal cerebral artery. A Scepter 4×20 mm balloon catheter (MicroVention, Tustin, California, USA) was introduced into the right pericallosal artery, and a Marathon microcatheter (eV3) was navigated distal to the balloon. Selective injection demonstrated residual AVM, arterial feeders and at least one en passant branch. At this point balloon test occlusion with motor evoked potential monitoring was performed at 0, 30 s, 1, 5, 8, 10 and 20 min. As no changes were noted, it was considered safe to proceed with embolization. With the balloon inflated, a total of 1.3 ml of Onyx-18 were delivered with thorough penetration into the malformation (figure 2). Post-embolization arteriography demonstrated minimal residual AVM supplied by the left pericallosal artery (figure 2).

Figure 2

Case No 1. Lateral roadmap angiographic image (A) shows Onyx penetration. Note the inflated balloon in the right pericallosal artery (arrow) and the Marathon microcatheter distal to it (arrowhead). Angiographic images of the right common carotid artery (CCA) (B, anteroposterior; C, lateral) and left vertebral artery (D), post-balloon assisted technique Onyx embolization failed to demonstrate residual arteriovenous malformation (AVM). Arterial feeders from the left pericallosal artery supplied a small residual AVM (E, anteroposterior left CCA injection).

Eleven days after the second embolization, the patient underwent craniotomy and complete resection of the AVM. Forty-seven days after presentation, the patient had improved to a modified Rankin Scale score of 4, had spontaneous movements of her left upper and lower extremity, and remained with a dense right hemiparesis.

Case No 2

A 36-year-old man with a 15 year history of left-sided seizures secondary to a large right pericallosal AVM presented with a small intracranial hemorrhage (figure 3). Cerebral angiography demonstrated a pericallosal AVM supplied by both pericallosal, right middle cerebral, right posterior cerebral artery and left middle meningeal arteries (figure 3). Venous drainage was both superficial and deep. He underwent first stage embolization with Onyx to the left middle meningeal artery and left pericallosal arteries (figure 3).

Figure 3

Case No 2. Axial CT scan shows a small intracranial hemorrhage from a large pericallosal arteriovenous malformation (AVM) (A). Cerebral angiography demonstrates an extensive pericallosal AVM supplied by both pericallosal, right middle cerebral artery (B, lateral right common carotid artery (CCA) and C, lateral left CCA injections), right posterior cerebral artery (D, lateral left vertebral artery (VA) injection) and left middle meningeal arteries (MMA) (E, anteroposterior left external cerebral artery injection). Angiographic images after first stage embolization to the left MMA (F, anteroposterior left external cerebral artery injection) and left pericallosal arteries (G, lateral left internal carotid artery  injection) show residual AVM.

Seven weeks after the first embolization, access was obtained in the right common femoral artery with a 6 French Shuttle sheath and advanced to the distal left internal cerebral artery. A Scepter 4×15 mm balloon catheter was introduced into the left pericallosal artery, and a Marathon microcatheter was navigated into a distal pericallosal arterial feeder. Selective hand injection of this feeder under balloon occlusion demonstrated exclusive supply to the AVM, with no evidence of normal parenchymal branches. With the balloon inflated, a total of 1.25 ml of Onyx-34 were delivered to the malformation with adequate penetration (figure 4). Using the same BAT, a second pericallosal branch was used to deliver 2.4 ml of Onyx-34 with adequate penetration (figure 4). Multiple attempts to remove the Marathon microcatheter failed. At this point, cerebral angiography demonstrated significant vasospasm of the A1 segment of the left ACA. Intra-arterial nicardipine 2 ml was administered through the Shuttle sheath and the Scepter balloon catheter was withdrawn to the spastic segment. Angioplasty was performed at the A1 segment and supraclinoid carotid artery with improvement of the vasospasm. This allowed for removal of the Marathon and Scepter balloon catheters. Post-embolization arteriography demonstrated complete angiographic obliteration of the left ACA component of the AVM (figure 4). Two days after the second embolization, the patient was discharged in a stable neurological condition.

Figure 4

Case No 2. Lateral roadmap angiographic images show the Onyx penetration. Note the inflated balloon in the left pericallosal artery (arrow) and the distal Marathon microcatheter (arrowhead) (A, feeder No 1; B, feeder No 2). Post-balloon assisted technique Onyx embolization images of the left internal carotid artery (C, anteroposterior; D, lateral) show complete angiographic obliteration of the left anterior cerebral artery component of the arteriovenous malformation (AVM). Angiographic images of the right common carotid artery (E, lateral) and left vertebral arteries (F, lateral) demonstrate large residual AVM.

Discussion

Onyx is a permanent, non-adhesive polymer, liquid embolic agent that has shown favorable results compared with N-butyl cyanoacrylate,  allowing more effective filling of the AVM nidus. This is due to its non-adhesive properties and low precipitation rates that provide longer and more controlled injections.1 ,7 ,9 During AVM embolization, the intranidal progression of Onyx relies on a pressure gradient. First, the embolic material reaches the nidus in its liquid state (first entry). Once a small portion of the nidus is occluded and Onyx begins to solidify, it tends to flow back along the afferent artery. As this reflux occurs, the arterial access is occluded by solidification of Onyx enclosing the microcatheter. At that point, the resistance to Onyx flow becomes lower within the nidus, as opposed to the resistance around the solidified plug in the afferent artery, and a larger second entry occurs.1 ,7

The first reported use of an endovascular balloon in the treatment of an arteriovenous malformation was in 1971 by Serbinenko.10 This report and subsequent ones employed balloons as permanent embolic devices.11–15 In 1989, Abe et al reported a type of BAT to decrease blood flow from branches of the middle cerebral artery during embolization of a predominantly ACA AVM.16 There are few recent reports of transarterial and transvenous BAT, to provide flow control/arrest, during Onyx embolization of dural and pial arteriovenous fistulas,5–8 and a mandibular AVM.9 Inflation of a proximal balloon creates a ‘plug’, allowing for immediate forward flow of Onyx. Additionally, the balloon increases the proximal resistance in the feeder, resulting in better control of the reflux and enhanced distal penetration.7 ,9

The Scepter C occlusion balloon catheter is a compliant balloon designed for temporary occlusion and balloon assisted embolization of intracranial pathology. It is comparable with the HyperForm and HyperGlide Balloon Systems (eV3). In both cases presented, balloon assisted flow control/arrest resulted in an earlier and more effective ‘plug’, increased nidal penetration of Onyx and reduced procedure time and radiation exposure.7 Additionally, the use of a compliant balloon allowed us to perform selective electrophysiologic balloon test occlusion, as in case No 1. It also proved useful at treating intraprocedural vasospasm and microcatheter retrieval, as in case No 2.17

The potential concerns of this technique need to be considered. These include the size and navigability of current cerebrovascular balloons, which limit their widespread use.9 ,18 Additionally, despite a recent report of a balloon assisted retrieval of a ‘glued’ microcatheter,17 both instruments could become trapped. More importantly, increased proximal resistance may allow Onyx influx into all artery to artery or artery to vein connections, some of which may be dangerous anastomoses. This could lead to embolic strokes and/or sudden increases in intranidal pressure and bleeding.1 ,7 ,9 Meticulous fluoroscopic monitoring of Onyx deposition and a good understanding of cerebrovascular and the AVM's angioarchitecture are critical to minimize the likelihood of this occurrence.

Conclusion

To our knowledge, this is the first reported use of BAT to induce flow arrest and deliver Onyx to two pericallosal AVMs. Balloon induced flow arrest allowed for excellent nidal penetration of embolic material without reflux. Further experience is needed to confirm the enhanced penetration, safety and time efficiency of this technique. As technology advances, application of the BAT for the treatment of brain AVMs will likely become more feasible.

Acknowledgments

The authors thank Dr Huiling Liu for help in the preparation of the images used in this manuscript.

References

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Footnotes

  • Contributors LDO: design, drafting the article, analysis and final approval. RFB: conception, revising and final approval. GDL: revising and final approval.

  • Competing interests None.

  • Patient consent Obtained.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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