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Table of Contents    
Year : 2022  |  Volume : 70  |  Issue : 4  |  Page : 1443-1447

Proof-of-Principle for AVM Embolization Complications Caused by the Proximal Occlusion Technique Using Onyx: A Theoretical Basis for Ante-Grade Drifting Technique

Department of Neurosurgery, Beijing Tsinghua Changgung Hospital, Tsinghua University, Beijing, China

Date of Submission09-Jun-2018
Date of Decision23-Jul-2022
Date of Acceptance01-Aug-2022
Date of Web Publication30-Aug-2022

Correspondence Address:
Xianli Lv
Department of Neurosurgery, Beijing Tsinghua Changgung Hospital, Tsinghua University, Changping, Litang Road 168, 102218, Beijing
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0028-3886.355140

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 » Abstract 

To analyze the complications of the standard proximal plug technique in arteriovenous malformations (AVMs) embolization by Onyx and promote ante-grade drifting technique for AVM embolization. Seven publications reporting complications of AVM embolization by Onyx were identified and reviewed. Render descriptive statistics regarding causes of ischemic and hemorrhagic complications within 1 month following treatment were provided. A novel Onyx injection technique was proposed to overcome these problems. All reported transarterial Onyx AVM embolizations were conducted by employing the proximal plug technique. Causes of complications elicited by utilizing this strategy may generally be attributed to long-fluoroscopy and long-procedure times, embolisate reflux across a considerable extent of the vessel, catheter entrapment, extravasation of Onyx from the arterial lumen, catheter transgression through the arterial wall, the use of an Onyx volume exceeding, and venous occlusion preceding arterial feeder shutdown. Complications occurring during the course of attempts at embolizing AVMs utilizing Onyx constitute unfortunate causes of patient morbidity resulting from this conventional technique. We suggest that institution of a novel “ante-grade drifting technique” for Onyx injection may avoid these commonly elicited deficits. The proximal plug technique has a series of drawbacks that lead to serious adverse outcomes of AVM embolization. The Onyx embolization technology for AVM could be updated to improve clinical outcomes.

Keywords: Arteriovenous malformation, complication, Onyx, technique
Key Message: The proximal plug technique for AVM embolization causes complications attributed to long-fluoroscopy and long-procedure times, embolisate reflux, catheter entrapment, nidus damage, arterial perforation, over volume of Onyx, and premature venous occlusion. The “ante-grade drifting technique” for Onyx injection may avoid these commonly elicited deficits.

How to cite this article:
Zhang H, Liang S, Lv X. Proof-of-Principle for AVM Embolization Complications Caused by the Proximal Occlusion Technique Using Onyx: A Theoretical Basis for Ante-Grade Drifting Technique. Neurol India 2022;70:1443-7

How to cite this URL:
Zhang H, Liang S, Lv X. Proof-of-Principle for AVM Embolization Complications Caused by the Proximal Occlusion Technique Using Onyx: A Theoretical Basis for Ante-Grade Drifting Technique. Neurol India [serial online] 2022 [cited 2022 Sep 30];70:1443-7. Available from: https://www.neurologyindia.com/text.asp?2022/70/4/1443/355140

The introduction and use of the liquid embolisate Onyx (eV3 Neurovascular; Irvine, California, USA) to obliterate intracranial AVM has enhanced endovascular cure rates.[1] Non-adhesiveness promotes the embolic agent to propagate and permeate intranidally to a greater extent before agent solidification.[2] A set of authors suggests attempting to obliterate AVM with Onyx embolization.[3],[4] In a meta-analysis, Onyx was found to improve embolization cure rates but also resulted in higher AVM embolization-related hemorrhagic complications.[5] In this paper, we analyzed the mechanisms by which the conventional proximal plug technique leads to higher hemorrhagic complications and proposed an “ante-grade drifting technique (ADT)” that avoids these mechanisms.

 » Methods Top

Seven publications describing complications of Onyx embolization of AVMs were identified and evaluated [Table 1].[6],[7],[8],[9],[10],[11],[12] The causes of precipitating ischemic and/or hemorrhagic complications within 1 month following transarterial Onyx embolization of AVMs were analyzed. A novel Onyx injection technique was proposed to overcome these problems.
Table 1: Complications associated with Onyx embolization reported in the literatures.

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 » Results Top

Innovation in endovascular techniques and embolic agents has not reduced rates of complications ensuing from Onyx embolization of AVMs. Across evaluated studies, embolization of AVMs yields rates of periprocedural bleeding risk ranging from 2.1% to 16.7% and the rate of ischemic complications ranging from 0 to 13%. Post-embolization hemorrhagic complications exhibited a much poorer clinical prognosis (58% permanent disability and 10% death). Overall reported mortality rates ranged from 0 to 3.0% (average 1.6%) for AVM embolization, requiring a more rigorous and meticulous evaluation of Onyx embolization techniques.

To the best of our knowledge, all attempts at AVM embolization utilizing Onyx employ a strategy termed the proximal plug technique. The causes of ischemic and/or hemorrhagic complications using conventional proximal plug technique included: long fluoroscopy and procedure times, extensive length of propagation of embolisate reflux, difficulty in microcatheter withdrawal, extravasation of Onyx from AVM nidus, transgression of the catheter through the arterial wall, use of a high volume of Onyx, and occlusion of the venous egress preceding nidal and arterial feeder shutdown.

Risk factors for hemorrhagic complication

The direct mechanistic causes and risk factors of precipitating hemorrhagic complications ensued from AVM embolization. Venous occlusion preceding that of the AVM nidus or feeder arteries may cause proximally related intraluminal hypertension putatively precipitating venous infarcts without or with hemorrhagic transformation. Higher volume of Onyx injected into the AVM in one session or over the volume of Onyx injected into the venous egress, nidus, and/or arterial feeders of the AVM to maximal nidal diameter covaries with risk of hemorrhagic complications.

ADT for Onyx injection

ADT is a no proximal plug formation technique perfusing AVMs with small amounts of Onyx through multiple feeders that constitutes a novel, and potentially preferable, alternative to the currently employed proximal plug technique [Figure 1]. Slow permeation filling the entirety of the AVM through intercompartmental communication constitutes the chief theoretical advantage of the proximal plug technique, though more complex AVMs lacking intraluminal fluency may render the chief advantages of such an approach null. In the presence of arteriovenous shunts within an AVM, Onyx will preferentially and more rapidly penetrate arteriovenous shunts exhibiting less resistance. The ADT strategy overcomes the disadvantages of the reflux technique by permitting finer control of the injection, as detailed in our recent reports.[13] Adjusting our technique according to the factors described above, the instances of microcatheter entrapment within the 6 years preceding the authoring of this work had been completely eliminated. To obtain optimal penetration with Onyx without embolisate reflux, maintaining lower intraluminal pressure during the injection of Onyx avoids baro-vascular injury to the AVM or microcatheter burst. The average injection volume per feeder was typically less than 1 mL and the average injection time was less than 2 min. We currently try to limit the amount of Onyx injected within a single session to 2 to 4 mL and divide treatments into multiple sessions as required. Small amounts of Onyx injected prevent occlusion of the proximal venous outlet [Figure 2] and [Figure 3].
Figure 1: Onyx was injected under an empty roadmap using the antegrade floating technique. The Onyx penetrates antegradely without proximal plug formation and reflux

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Figure 2: (a) CT scanning showing a subarachnoid hemorrhage of the right cerebellopontine angle. (b) right vertebral artery angiogram showing two aneurysms on the posterior inferior cerebellar artery, which supply a small AVM. The AVM was also supplied by the superior cerebellar artery. (c) the superselective contrast injection through a microcatheter showing the two aneurysms and distal AVM, which was embolized with antegrade floating Onyx embolization. (d) the superselective contrast injection through a microcatheter showing the AVM, which was embolized with the same technique. (e) Fluoroscopic image showing the Onyx cast after embolization. (f) vertebral artery angiogram showing the aneurysms were completely occluded

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Figure 3: (a) Vertebral artery angiogram showing a temporal AVM of Spetzler–Martin grade III. (b) the last superselective contrast injection through a Headway17 soft microcatheter (Microvention). (c) Vertebral artery angiogram showing the AVM was completely occluded after two sessions of Onyx embolization using “no plug” technique. (d) Fluoroscopic image showing the Onyx cast

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 » Discussion Top

The development of the non-adhesive liquid embolic agent (Onyx) constitutes an evolution of the embolic material to treat AVMs. Given its non-adhesive properties and low precipitation rates, Onyx permits greater control of the injections and prolonged duration of injections, which enhances the probability of complete obliteration of the AVM. However, Onyx embolization has increased the risks of hemorrhagic complications.[5] All ischemic complications were attributable to Onyx embolisate reflux and occlusion of a branch supplying the normal cerebral parenchyma. Adequate perfusion usually restitutes neurological function through the collateral supply. However, absent or diminutive collateral supply may significantly enhance the risk of permanent deficits.

Vessel perforation

Hemorrhagic rupture of the fine vessels constituting the AVMs may ensue from perforation of proximally related arteries by either the guidewire or microcatheter. Perforation may still occur with newer devices and guidewires. When possible, we have adopted the technique of advancing the guidewire past the tip of the microcatheter to prevent stiffening of the wire by the catheter during the procedure. The microcatheter and guidewire should be coordinately and suavely navigated; when the microcatheter and guidewire approach the nidus, the guidewire tip should not transgress past the microcatheter tip. Given the smaller size and presumably increased fragility, a 0.010-inch microguidewire might preferably more gracefully navigate the fine cerebral vasculature in pediatric patients.

Aneurysmal rupture

Approximately 10 to 20% of intracranial AVMs accompany proximal aneurysms.[14],[15] Proximal aneurysms exhibit a propensity to rupture during embolization of the AVM, suggesting proximally related AVM-associated aneurysms should be preferably treated initially, when present or specifically identified as the culprit source of hemorrhage [Figure 3]. Intranidal or feeding artery-related aneurysms constitute fragile components of brain AVMs. According to our experience, increasing flow and pressure in residual nidus and feeding artery following incomplete embolization enhances the risk of lesion rupture and necessitate initial treatment of AVM-related aneurysms located on feeding arteries and fragile AVM compartments [Figure 4]. In the case of an intranidal aneurysm or flow-related feeder aneurysms in close proximity to the nidus, the aneurysm-harboring vessels are initially selected for embolization, in attempts to include the aneurysms in the Onyx cast. In feeder aneurysm not in close proximity to the nidus or flow-related aneurysm localizing to the circle of Willis, coil occlusion should be undertaken before embolizing the nidus.
Figure 4: A case of aneurysm rupture during AVM Onyx embolization. (a) Carotid artery angiogram lateral view, showing a parietal AVM with a proximal middle cerebral artery bifurcation aneurysm. (b) the superselective contrast injection through a Marathon microcatheter (Medtronic). (c) Carotid artery angiogram, lateral view, showing the arterial aneurysm rupture and the contrast leakage during Onyx injection. (d) Fluoroscopic image showing the Onyx cast, subarachnoid hemorrhage, and the coils. This patient died although the aneurysm was coiled

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Onyx extravasation

Authors have reported Onyx extravasation in a few reports using the proximal plug technique and the proximal balloon-assisted technique, both of which have the effect of increasing injection pressure.[16],[17] Increased resistance to syringe plunger movement indicative of complete embolization of the vascular bed may be ignored by the operator. This may precipitate pressure-related injury to AVMs because the injecting pressure acts directly on the walls of blood vessels in the proximal plug technique.[18] The volume of the space filled with Onyx may be larger than the space previously visualized upon superselective AVM angiography.[18] We experienced two cases of Onyx extravasation during Onyx embolization, no resistance was presented to the plunger of the syringe in these instances [Figure 5]. Immediate contrast injections demonstrated no bleeding, presumably because the material had sealed off the putatively rupture site.
Figure 5: A case of Onyx extravasation during conventional “proximal plug” technique of Onyx embolization. (a) Carotid artery angiogram lateral view, showing a small parietal AVM. (b) Fluoroscopic image showing the Onyx extravasation and venous migration. No resistance on the syringe caused a vessel rupture and extravasation was felt while injecting Onyx. Fortunately, the AVM was completely occluded and showed no bleeding. (c) lateral view of the carotid artery angiogram showing the AVM was completely occluded

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Microcatheter entrapment

Onyx reflux around the microcatheter may form a highly viscous plug, thereby constraining the manipulation of the microcatheter during its retrieval.[19] Thin and tortuous arterial access may easily cause catheter entrapment, even following only a small amount of reflux during brief injections, especially in pediatric patients given soft and pliable blood vessels. Under these conditions, we prefer to leave the microcatheter in place. Arterial stretching may precipitate vascular rupture and generate acute bleeding, a potentially fatal complication that demands immediate treatment, typically via endovascular occlusion of the arterial pedicles or parent arterial occlusion.

Methods of reducing complications

Double arterial catheterization with simultaneous injection of Onyx did not reduce the risk of hemorrhagic complications.[20] The introduction of detachable tip catheters may effectively reduce the effects of trapping microcatheters and prevent hemorrhagic complications.[21],[22] However, preliminarily published results indicate arterial rupture continues to constitute a hazard even using this new technology and higher amounts of Onyx injected per session increase the bleeding risk several fold.[10] The security catheter technique constitutes a strategy whereby a second microcatheter may be placed into arterial feeders before microcatheter retrieval.[23] Co-axially presented auxiliary microcatheters may potentially promptly be used to control inadvertent intracranial hemorrhages complicating the procedure. However, the technique insufficiently prevents post-embolization hemorrhagic complications. Transvenous embolization permits endovascular cure of complex AVMs with high Spetzler–Martin grades and AVMs with deep draining veins and relatively small nidal sizes,[24] though has yet to find commonplace use. The pressure cooker technique, a procedural strategy developed and espoused within the past several years, increases the amount of Onyx that may be safely injected into AVMs during a relatively short duration while coordinately eschewing large-volume embolisate reflux retrogradely through the embolized pedicle into para-pedicular arterial feeders irrigating the normal parenchyma.[25] Ovalle et al.[26] demonstrated among 13 potential factors that the volume of the embolic agent constituted the exclusive predictor of delayed interval hemorrhages. Baharvahdat et al. found that the volume of Onyx injected normalized to the ratio of the maximal nidal diameter constitutes a factor predicting inadvertent venous occlusion occurring in precession to arterio-nidal obliteration.[6] Considerable reductions of AVM volume achieved within one session also appear to enhance the technically precipitated hemorrhage events.[27] The described technique permits embolization of large components of AVMs from one catheter position and achievement of high rates of complete obliteration when embolizing only a few arterial feeders. By adjusting our technique according to the factors described above, we have successfully avoided unfortunate instances of microcatheter entrapment. To obtain optimal penetration with Onyx embolisate reflux, it proves prudent to maintain lower intraluminal arterial pressure during Onyx injection to prevent pressure-related AVM damage and microcatheter transgression through the arterial lumen. Small volumes of Onyx prevent the occlusion of the proximal venous outlet.

 » Conclusion Top

The proximal plug technique has a series of drawbacks that lead to serious adverse outcomes of AVM embolization. The Onyx embolization technology for AVM could be updated to improve clinical outcomes.


This work was supported by the Beijing Municiple Administration of Hospitals Incubating Program (PX2020039), Beijing, China & Tsinghua Precision Medicine Foundation (20219990008), Tsinghua University, Beijing, China.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 » References Top

Lv X. Arteriovenous Malformations of the Brain. New York: Nova Science, NY, USA; 2020.  Back to cited text no. 1
Lv X. Letter to the Editor: Comparison of N-butyl cyanoacrylate and onyx for the embolization of intracranial arteriovenous malformations: Analysis of fluoroscopy and procedure times. Oper Neurosurg (Hagerstown) 2017;13:E37-8.  Back to cited text no. 2
Sahlein DH, Mora P, Becske T, Nelson PK. Nidal embolization of brain arteriovenous malformations: Rates of cure, partial embolization, and clinical outcome. J Neurosurg 2012;117:65-77.  Back to cited text no. 3
Lv X, Hu X, Li W, He H, Jiang C, Li Y. Curative and adjunctive AVM Onyx embolization of AVMs through the choroidal arteries. Interv Neuroradiol 2017;23:392-8.  Back to cited text no. 4
Lv X, Zhang Y, Wang J. Systematic review of transcatheter arterial embolization of AVM: Indications, bleeding complications, cure rate, and long-term bleeding risk. Neurol India 2020;68:1285-92.  Back to cited text no. 5
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Consoli A, Scarpini G, Rosi A, Renieri L, Chiarotti I, Vignoli C, et al. Endovascular treatment of unruptured and ruptured brain arteriovenous malformations with Onyx18: A monocentric series of 84 patients. J Neurointerv Surg 2014;6:600-6.  Back to cited text no. 7
Katsaridis V, Papagiannaki C, Aimar E. Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology 2008;50:589-97.  Back to cited text no. 8
Mounayer C, Hammami N, Piotin M, Spelle L, Benndorf G, Kessler I, et al. Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 2007;28:518-23.  Back to cited text no. 9
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Xu F, Ni W, Liao Y, Gu Y, Xu B, Leng B, et al. Onyx embolization for the treatment of brain arteriovenous malformations. Acta Neurochir (Wien) 2011;153:869-78.  Back to cited text no. 12
Lv X, Liang S. Update Onyx embolization for plexiform arteriovenous malformation: Ante-grade drifting technique. Neuroradiol J 2020;33:386-92.  Back to cited text no. 13
Lv X, Wu Z, Li Y, Yang X, Jiang C, Sun Y, et al. Endovascular treatment of cerebral aneurysms associated with arteriovenous malformations. Eur J Radiol 2012;81:1296-8.  Back to cited text no. 14
Lv X, Wu Z, He H, Ge H, Li Y. Proposal of classification of aneurysms coexisting with AVM and possible treatment strategies. Turk Neurosurg 2016;26:229-33.  Back to cited text no. 15
Ikeda H, Imamura H, Agawa Y, Imai Y, Tani S, Adachi H, et al. Onyx extravasation during embolization of a brain arteriovenous malformation. Interv Neuroradiol 2017;23:200-5.  Back to cited text no. 16
Solli E, Jumah F, Narayan V, Quinoa T, Xiong Z, Gupta G, et al. Resection of a posterior fossa arteriovenous malformation complicated by leaked Onyx: A case report and review of literature. Acta Neurochir (Wien) 2020;162:923-8.  Back to cited text no. 17
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Abud DG, Riva R, Nakiri GS, Padovani F, Khawaldeh M, Mounayer C. Treatment of brain arteriovenous malformations by double arterial catheterization with simultaneous injection of Onyx: Retrospective series of 17 patients. AJNR Am J Neuroradiol 2011;32:152-8.  Back to cited text no. 20
Maimon S, Strauss I, Frolov V, Margalit N, Ram Z. Brain arteriovenous malformation treatment using a combination of Onyx and a new detachable tip microcatheter, SONIC: Short-term results. AJNR Am J Neuroradiol 2010;31:947-54.  Back to cited text no. 21
Altschul D, Paramasivam S, Ortega-Gutierrez S, Fifi JT, Berenstein A. Safety and efficacy using a detachable tip microcatheter in the embolization of pediatric arteriovenous malformations. Childs Nerv Syst 2014;30:1099-107. doi: 10.1007/s00381-014-2404-9.  Back to cited text no. 22
Abud DG, Abud TG, Nakiri GS. Management of brain AVM procedural hemorrhagic complication by the “security” catheter technique. J Neuroradiol 2013;40:45-9.  Back to cited text no. 23
Lv X, Song C, He H, Jiang C, Li Y. Transvenous retrograde AVM embolization: Indications, techniques, complications and outcomes. Interv Neuroradiol 2017;23:504-9.  Back to cited text no. 24
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Ovalle F, Shay SD, Mericle RA. Delayed intracerebral hemorrhage after uneventful embolization of brain arteriovenous malformations is related to volume of embolic agent administered: Multivariate analysis of 13 predictive factors. Neurosurgery 2012;70:313-20.  Back to cited text no. 26
Heidenreich JO, Hartlieb S, Stendel R, Pietilä TA, Schlattmann P, Wolf KJ, et al. Bleeding complications after endovascular therapy of cerebral arteriovenous malformations. AJNR Am J Neuroradiol 2006;27:313-6.  Back to cited text no. 27


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]

  [Table 1]


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