Abstract
Objective
The anterior or posterior choroidal artery is often recruited to supply deep location arteriovenous malformations (AVMs). This study is to report curative and adjunctive AVM Onyx embolization through these arteries.
Methods
This study retrospectively reviewed six patients with cerebral AVMs who underwent endovascular embolization through the choroidal arteries between October 2015 and October 2016. Embolization was performed as a curative procedure in five patients and adjunctive procedure in one patient.
Results
Four patients underwent embolization through the anterior choroidal artery (AchA), and two patients underwent embolization through the lateral posterior choroidal artery (LPchA). One of the four patients in whom embolization was from the AchA (distal to the plexal point) developed transient hemiparesis. Complete obliteration was confirmed by angiography at the last follow-up in five patients.
Conclusions
Onyx embolization of cerebral AVMs through the choroidal arteries is possible as a curative or adjunctive procedure.
Keywords: Arteriovenous malformation, embolization, choroidal artery
Introduction
Endovascular arteriovenous malformation (AVM) embolization can be used as an adjunctive treatment to surgery or radiosurgery or as a curative procedure.1,2 The anterior (AchA) and posterior choroidal arteries (PchA) are often recruited to supply arteriovenous malformations (AVMs) involving important paraventricular structures.3–9 Surgical access to the AchA and lateral PchA (LPchA) can be difficult because of their depth, and AVMs superficial to choroidal feeding arteries that could hinder surgical manipulation.7,9 In this situation, curative and preoperative AchA embolization could be beneficial. In the present study, we reported endovascular AVM embolization through the choroidal arteries as curative or adjunctive procedures.
Methods
Six consecutive patients with cerebral AVMs who were treated by endovascular embolization through the AchA and/or the LPchA at Beijing Tiantan Hospital between October 2015 and October 2016 were retrospectively reviewed. All patients were assessed by computed tomography (CT), magnetic resonance imaging (MRI), and digital subtraction angiography. We retrospectively reviewed the clinical and radiological features, which were obtained both from electronic and paper medical records, of the six patients. The Spetzler-Martin grading system was used to establish the AVM grade.10
Treatment
Five patients underwent a curative embolization and one in preparation for resection. Endovascular embolization through the AchAs or LPchAs was performed when embolization was considered curative or ruptured feeder aneurysm was considered remote from the area of resection. Embolization was performed under general anesthesia. A 5 F sheath was placed into the femoral artery and a 5 guiding catheter (Envoy or Navien) was inserted through the sheath. The guiding catheter was continuously flushed with heparinized saline (3000 U/500 ml). Onyx18 (ev3 Neurovascular) was used as the embolic agent, which was delivered through a Marathon Micro Catheter (ev3 Neurovascular) and navigated to the choroidal arteries by a CHIKAI 10 microguidewire (Asahi Intec Co., Ltd.) through the guiding catheter in the internal carotid or vertebral arteries. The microcatheter tip was advanced distally to select the proper feeders. If the AchA was selected, the microcatheter tip was advanced distally to go beyond the angiographic plexal point of the AchA. Onyx was injected without reflux.
Follow-up
Follow-up digital subtraction angiograms were obtained at six months after treatment. Final functional status was evaluated using the modified Rankin Scale.
Results
The patients’ characteristics are summarized in Table 1. Four were female and two were male, and the mean age was 21 years (range 9–34 years). Hemorrhagic onset was confirmed on CT in all cases. The lesions were located in the temporal lobe in three cases, the thalamus in two cases and the splenium of the corpus callosum in one case. Eloquent brain structures were involved within the nidus in four cases. Spetzler-Martin grades II, III, and IV were diagnosed in two, three, and one patient, respectively.
Table 1.
Summary of AVMs embolized with Onyx18 through choroidal arteries.
| Case no. | Age/sex | Presentation | S-M grade | Indications | Approach | Complications | Adjunctive treatment | Follow-up (mRS) |
|---|---|---|---|---|---|---|---|---|
| 1 | 15/F | Rupture | III | Curative | PchA | No | No | 0 |
| 2 | 24/F | Rupture | II | Curative | PchA | No | No | 0 |
| 3 | 34/M | Rupture | III | Curative | AchA | No | No | 0 |
| 4 | 16/F | Rupture | III | Curative | AchA | Transient mild hemiparesis | No | 0 |
| 5 | 9/M | Rupture | II | Curative | AchA | No | No | 0 |
| 6 | 28/F | Rupture | VI | Adjunctive | AchA | No | Surgery | 0 |
AVMs: arteriovenous malformations; F: female; M: male; S-M: Spetzler Martin; PchA: posterior choroidal artery; AchA: anterior choroidal artery; mRS: modified Rankin Scale.
Of the six patients, two were embolized through the lateral LPchA (Figures 1 and 2) and four through the AchA (Figures 3 to 6). The microcatheter tip could be advanced distally to the plexal point in all cases embolized through the AchA. A feeder aneurysm on the AchA was considered to be the rupture site in one patient and disappeared after embolization. None of the patients developed hemorrhagic complications.
Figure 1.
(a) The left vertebral artery angiogram showing an arteriovenous malformation fed by the lateral posterior choroidal artery. (b) The left vertebral artery angiogram after Onyx injection showing the disappearance of the nidus. FOV: field of view; LAO: left anterior oblique; CAU: caudal; LP: left posterior.
Figure 2.
(a) The left vertebral artery angiogram showing a small arteriovenous malformation (AVM) located in the splenium of the corpus callosum fed by the lateral posterior choroidal artery (LPchA). (b) Super-selective angiogram of the right LPchA showing an AVM draining into the ventricular vein. (c) The left vertebral artery angiogram after Onyx injection showing the disappearance of the nidus.
Figure 3.
(a) The left internal carotid artery (ICA) angiogram showing an arteriovenous malformation (AVM) fed by the left anterior choroidal artery (AchA) with a small venous aneurysm. (b) Super-selective angiogram of the left AchA showing that the microcatheter was placed distally to the plexal point. (c) Un-subtracted lateral view showing the Onyx cast without any reflux. (d) The left ICA angiogram after embolization showing occlusion of the AVM. (e) Six-month follow-up angiogram showing the occlusion of the AVM.
Figure 4.
(a) The right internal carotid artery (ICA) angiogram showing an anterior choroidal artery (AchA) supplying the arteriovenous malformation (AVM) with a large aneurysm. (b) Super-selective angiogram of the right AchA showing that the microcatheter was distal to the plexal point and a small aneurysm and a large aneurysm were demonstrated. (c) Un-subtracted lateral view showing the Onyx cast, which occluded the aneurysms without any reflux. (d) The right ICA angiogram after Onyx injection showing the small residual nidus. (e) Six-month follow-up angiogram showing the small residual AVM; the patient refused radiosurgery.
Figure 5.
(a) The right internal carotid artery (ICA) angiogram showing an arteriovenous malformation (AVM) fed by the right anterior choroidal artery (AchA). (b) The right ICA angiogram after embolization showing disappearance of the AVM.
Figure 6.
(a) Preoperative magnetic resonance image showing an intracerebral hemorrhage and a small aneurysm (arrow). (b) The right internal carotid artery (ICA) angiogram showing a ruptured distal anterior choroidal artery (AchA) aneurysm associated with an arteriovenous malformation (AVM) in the ipsilateral temporal lobe fed by the branches of the middle cerebral artery. The aneurysm was occluded with Onyx embolization and the AVM was completely removed by surgery. The AchA was not reached by surgery. (c) The right ICA angiogram after treatment showing the disappearance of both the AVM and the aneurysm. The patient was discharged without any neurological deficits.
Clinical outcomes
Complete obliteration was confirmed by cerebral angiography at the six-month follow-up in five patients. A remnant of the small nidus was present in one patient after embolization. One patient developed a transient mild left hemiparesis that improved at the six-month follow-up.
Discussion
Although the risks of ischemic complications should be considered,5 embolization of cerebral AVMs through choroidal arteries may be an appropriate treatment. It was possible to perform curative AVM embolization for the patients included in this study, based on their angioarchitecture. Presurgical AVM embolization can be used to eliminate deep arterial pedicles encountered only at the later stages of resection, and to secure AVM-related aneurysms, especially if they are remote from the area of resection. Embolization of the choroidal artery can also complement radiosurgery by diminishing arteriovenous shunting or by providing palliation through the obliteration of the intranidal aneurysm.
To achieve safe embolization, it is important to understand the anatomical and angiographic features of choroidal arteries. Principally, the perforating branches of the AchA arise from the cisternal segment, which is proximal to the plexal point. The plexal point is the point of entry of the AchA into the lateral ventricle at the choroidal fissure, marking the point of entry on frontal or lateral angiograms. Therefore, the catheter tip must be placed beyond the plexal point to avoid serious ischemic complications during AVM embolization through an AchA.
To our knowledge, two previous reports described AVM embolization through choroidal arteries in 1991.3,6 Dowd et al. performed particulate embolization of the AchA in 15 patients: Two hemorrhagic complications due to AchA perforation during the catheterization and two ischemic complications developed, which caused one permanent hemiparesis.6 In six patients with temporal AVMs embolized through the AchA using n-butyl cyanoacrylic acid (NBCA) studied by Hodes et al, one patient developed hemiplegia, homonymous hemianopia, and dysphasia after the embolic agent injection at the ostium of the AchA, which was difficult to catheterize.3 With the advent of modern microcatheters, these catheterization-related complications have decreased.9 In one recent publication,7 among four embolizations from the cisternal segment (proximal to the plexal point) of the AchA, only one patient developed a persistent hemiparesis and hemianopia and no symptomatic infarction developed in four embolizations from the plexal segment (distal to the plexal point) of the AchA. In our series, we were able to advance the microcatheter distally to the plexal point of the AchA in our four patients, and one patient developed a mild hemiparesis.
It might be difficult to control ischemic complications after embolization through the LPchA because no angiographic safety point has been reported thus far.7 No symptomatic infarctions have developed in the six embolizations through the LPchA.7 We also encountered neurologic complications in our two patients embolized through the LPchA. We advanced microcatheter as distally as possible to avoid the risks of irretrievable complications.
Furthermore, choroidal arteries that feed AVMs are usually dilated enough to be deeply catheterized by the latest microcatheter.9 The development of smaller catheters has allowed more selective catheter placement, and has reduced the risk of vessel perforation or ischemic complications.9 We experienced no technical complications during selective microcatheter catheterization of the choroidal arteries in any procedure.
Reflux with Onyx is common, but Onyx could give a distal perfusion before reflux and embolization would be stopped once Onyx reflux was found. We usually choose Onyx as the embolic agent for AVM embolization. In recent studies, there was no statistically significant difference in the complication risk following AVM embolization with Onyx and NBCA.11,12 Although a provocative test may be beneficial in AVM cases to protect against ischemic complications,8 we did not perform this test in our patients because they were treated under general anesthesia.
There are several reports in the literature showing that it is possible to safely microcatheterize pial veins that drain AVMs.13,14 Retrograde injection Onyx via one draining vein would allow retrograde spread of Onyx throughout the nidus. However, in this type of AVM, with regard to tortuosity/angulation/length and presence of stenoses, is important in that not all AVMs might be accessible from a transvenous route, and in certain circumstances (e.g. for “functional” draining veins), it might not be desirable to occlude these veins and/or affect adjacent normal cortical drainage. Although radiosurgery is a low-risk alternative treatment for deep AVMs and should also be considered even after AVM rupture, radiopathy of the brain cannot be neglected.
Conclusions
With the advent of endovascular techniques and microcatheters, AVM Onyx embolization through the choroidal arteries is possible as a curative or adjunctive procedure.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
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