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Treatment of dural arteriovenous fistula by balloon-assisted transarterial embolization with Onyx
Clinical Neurology and Neurosurgery 115 (2013) 1992–1997
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Treatment of dural arteriovenous fistula by balloon-assisted transarterial embolization with Onyx Jian-Ping Deng, Tao Zhang, Jiang Li, Jia Yu, Zhen-Wei Zhao ∗,1 , Guo-Dong Gao 1 Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province 710038, China
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Article history: Received 25 March 2013 Received in revised form 4 June 2013 Accepted 9 June 2013 Available online 2 July 2013 Keywords: Arteriovenous fistula Embolization Balloon assistance Onyx
a b s t r a c t Objective: This study evaluated the feasibility, safety, and efficacy of embolization of dural arteriovenous fistula via a very small, short feeding artery with the assistance of a balloon placed proximal to the tip of the microcatheter, such that the balloon serves as a plug. Methods: Eight patients who underwent treatment of DAVF by balloon-assisted transarterial embolization with Onyx were retrospectively reviewed. Gender, age, angiography findings, procedure details, clinical and angiographic outcomes, complications, and follow-up were recorded and analyzed. Results: Nine embolization procedures were performed in eight male patients via extracranial arteries. Balloon-assisted embolization was successful in all eight patients. A Hyperglide balloon was used in five patients, and a Hyperform balloon was used in three patients. Angiographic resolution of the fistula was achieved in all patients without complications. All patients recovered uneventfully. During the follow-up period of 7–19 months, all patients were asymptomatic except for one patient who experienced mild headaches. Conclusions: Treatment of DAVF by balloon-assisted embolization with Onyx achieved promising results, even in patients with very small and short feeding arteries. This technique allowed the treatment of DAVF cases where other techniques have failed. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The development of Onyx (ev3 Neurovascular, Irvine, CA, USA) was a milestone in the endovascular treatment of dural arteriovenous fistula (DAVF) [1–10]. The combination of Onyx and new microcatheters has greatly improved the ability to treat DAVF via different approaches [1–11]. The reported outcomes after embolization of DAVF with Onyx are promising [1–16]. The viscosity and permeability of Onyx allow slow and intermittent injection, resulting in good penetration into the drainage veins and the other feeding arteries of the fistula [1–16]. Successful treatment requires optimal positioning of the microcatheter, enough space to form an Onyx plug, and enough forward pressure to allow penetration of Onyx into the vascular network [10–13]. Embolization is usually performed via the middle meningeal artery, even when the artery is elongated and tortuous [1–13,16]. However, it may be difficult to achieve good penetration over long distances via small-diameter or low-flow vessels, as it may not
be possible to form a plug. Transarterial embolization of DAVF via very small, low-flow feeding arteries therefore has variable outcomes. This paper describes a technique of balloon-assisted transarterial embolization of DAVF with Onyx. 2. Materials and methods We searched our prospective database of patients with cerebrovascular diseases treated with endovascular therapy at our hospital from January 1996 to December 2012 and identified 151 patients with dural AVF. Eight patients were found to undergo treatment of DAVF by endovascular balloon-assisted embolization with Onyx from 2010 to 2012. Data describing gender, age, symptoms, treatment details, clinical and angiographic outcomes, complications, and follow-up were collected. Pre-procedure angiography findings were extracted and analyzed. 2.1. Endovascular procedures
∗ Corresponding author at: No. 1 Xinsi Road, Baqiao District, Xi’an City, Shaanxi Province, 710038, China. Tel.: +86 29 84777285; fax: +86 29 84777435. E-mail addresses: [email protected], [email protected] (Z.-W. Zhao). 1 These authors equally contributed to this study. 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.06.007
All procedures were performed under general anesthesia via the femoral artery access. An 8-F guiding catheter (Envoy; Johnson & Johnson, Miami, FL, USA) was introduced through an 8-F sheath and advanced through the external carotid artery (ECA) into the occipital artery or internal maxillary artery, depending on the diameters
J.-P. Deng et al. / Clinical Neurology and Neurosurgery 115 (2013) 1992–1997
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of the arteries. A Marathon microcatheter (ev3, Neurovascular) was used to catheterize the feeding artery as distally as possible. A Hyperglide balloon (ev3 Neurovascular) or Hyperform balloon (ev3 Neurovascular) was then advanced into the feeding artery by the operator’s choice. If the ipsilateral ECA and internal carotid artery (ICA) both fed the fistula, the 8-F guiding catheter was withdrawn to the common carotid artery. If the fistula was fed bilaterally, an angiographic catheter was placed in the contralateral common carotid artery via the contralateral femoral artery. The balloon was inflated, and angiography was performed to confirm that the artery was completely occluded. Onyx was injected after flushing the catheter with dimethyl sulfoxide (ev3 Neurovascular). After angiographic confirmation that the fistula was completely obliterated, the microcatheter was withdrawn, followed by the withdrawal of the balloon.
3.3. Treatment, results, and follow-up
2.2. Notes on embolization techniques
3.4. Representative cases
In most cases, initial injection of Onyx into a DAVF feeding artery causes reflux and forms a plug. In the patients in this series, the feeding arteries were very small, and a balloon was used to form a plug. The embolization procedures were slow, with injection being stopped when Onyx reflux reached the balloon. After a waiting of nearly 60 s the injection was resumed. Sometimes several rounds of “waiting” and “injecting” took place. Patience was often needed for an effective plug to form. Several injections were usually performed to ensure good penetration of the nidus by Onyx.
Case 1 (Fig. 1): A 54-year-old man without history of hypertension presented with an intracranial hemorrhage, and underwent craniectomy at another hospital. Two months later, DSA at our center showed a DAVF of the left transverse-sigmoid sinus, fed by very small branches of the left occipital artery and ascending pharyngeal artery, and draining into the sigmoid sinus with cortical venous reflux. Endovascular treatment was planned. Under general anesthesia with endotracheal intubation, a Marathon microcatheter was introduced through a 6-F guiding catheter, and was advanced into a branch of the occipital artery. However, Onyx did not penetrate across the tiny outlet of the fistula, and only the branch of the occipital artery was embolized. An 8-F guiding catheter was then placed, and another Marathon microcatheter was advanced to a more distal branch. A Hyperglide balloon (4 mm × 20 mm) was placed in the occipital artery, across the origin of the feeding vessel. After inflation of the balloon, Onyx was injected, and penetrated very well into the draining vein and the other small feeding arteries. The DAVF was completely obliterated. There was no deterioration of the patient’s neurological status, and he underwent cranioplasty before leaving hospital. Case 3 (Fig. 2): A 42-year-old alert male was diagnosed with a small subarachnoid hemorrhage, and was suspected to have a cerebral aneurysm. However, DSA showed a tentorial DAVF. The feeding arteries were tentorial dural branches of the ICA, branches of the ascending pharyngeal artery, and transosseous branches of the occipital artery. Venous drainage was directly into the leptomeningeal vein via a tortuous outflow, which harbored a stenosis before emerging into the torcular Herophili. A Marathon microcatheter was advanced into the transosseous branch of the occipital artery and embolization was performed with the assistance of a Hyperform balloon (4 mm × 7 mm). The fistula was successfully embolized without complications. Case 5 (Fig. 3): A 40-year-old male presented with weakness of all four extremities, but brain MRI did not detect any vascular lesion. DSA showed a tentorial DAVF. There were many feeding arteries including dural branches of the right ICA and branches of the middle meningeal artery, ascending pharyngeal artery, and occipital artery, but they were all very small and short. Venous drainage was via an aneurysmal varix to the surface of the medulla oblongata and cervical spinal cord. A Marathon microcatheter was placed in the transosseous branch of the occipital artery, and embolization was performed with the assistance of a Hyperglide balloon (4 mm × 20 mm) which was inflated across the origin of the feeding branch. The fistula was successfully embolized without complications. The Onyx penetrated into the proximal drainage veins and all the feeding arteries. Case 7 (Fig. 4): A 44-year-old male experienced sudden headache and was diagnosed with a small SAH. He was Hunt and
2.3. Follow-up Changes in symptoms and signs after the procedure were recorded. Angiographic follow-up was not performed. All patients were followed up clinically in the outpatient department or by telephone. 3. Results 3.1. Patients and symptoms The characteristics of the eight patients who underwent balloon-assisted transarterial embolization are shown in Table 1. The patients were all male, and were aged from 18 to 62 years with an average age of 44.3 years. One patient presented with weakness of all four extremities (Case 5), and the other patients presented with intracranial hemorrhage. Case 1 underwent urgent craniectomy to treat a large intracerebral hematoma. The other six patients presented with a sudden headache, and computed tomography showed subarachnoid hemorrhage. These six patients were all Hunt and Hess grade I or II, with no neurological deficits on physical examination. 3.2. Angiographic images Digital subtraction angiography (DSA) was performed in all patients before treatment. The DAVF was located in the transversesigmoid sinus in four patients (Cases 1, 2, 6, and 8) and in the tentorium in the other four patients. The DAVF was fed by both ECAs in Case 6, and unilaterally in the other seven patients (by the ECA alone in Cases 1 and 7, and by the ipsilateral ECA and ICA in the other five cases). All the feeding arteries were very small, short branches arising from the occipital artery, ICA, middle meningeal artery, or ascending pharyngeal artery. In nearly all cases, the draining veins were small and tortuous. Drainage to the spine occurred in three cases (Cases 4, 5, and 7) and drainage was directly into the cortical veins in two patients (Case 1 and 2) and indirectly into the cortical veins in three patients.
Nine embolization procedures were performed in eight patients, including eight balloon-assisted procedures. Although five patients had feeding arteries arising from the ICA, embolization was performed via feeding arteries arising from the ECA in all cases. A Hyperglide balloon was used in five patients, and a Hyperform balloon was used in the other three patients. Angiographic cure was achieved in all patients, without complications. All patients recovered uneventfully. An additional small surgical procedure was performed in Case 1. In Case 6, the patient’s quadraparesis improved greatly immediately after the procedure. During the follow-up period of 7–19 months, all patients were asymptomatic, except for Case 1 who experienced mild headaches, especially with changes in the weather.
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Table 1 Informations of eight patients, angiographic images and procedures. No.
Age/gender
Symptom
Location
Feeders
Drainage
Cognard
Balloon
1 2 3 4 5 6 7 8
54/M 44/M 42/M 18/M 40/M 62/M 44/M 50/M
ICH ICH ICH ICH Weak of limb ICH ICH ICH
TS TS TT TT TT TS TT TS
PH, OC OC, MM, BI OC, PH, BI OC, BI, MM OC, BI, MM,PH OC, MM, MM, OC,PH OC,PH,BI
TS, C C C SP SP TS,C SP TS,C
IIa + b III III V V IIa + b V IIa + b
G 4 × 20 G 4 × 20 F 4×7 F 4×7 G 4 × 20 F 4×7 G 4 × 20 G 4 × 20
ICH = intracranial hemorrhage; TS = transverse sigmoid sinus; TT = tentorium; OC = occipital artery; PH = pharyngeal artery; MM = middle meningeal artery; BI = dural branch of internal carotid artery; C = cortical vein; SP = spinal vein; G = Hyperglide; F = Hyperform.
Hess grade I at the time of presentation. DSA showed a DAVF. The feeding arteries were branches of the right middle meningeal artery and the ICA, and a very small branch of the occipital artery. Drainage was via a long, tortuous leptomeningeal vein to the surface of the medulla oblongata and the spine. A Marathon microcatheter was advanced into the short branch of the middle meningeal artery originating at the foramen spinosum, although later images indicated that the posterior branch might have been a better choice. A Hyperglide balloon was advanced into the middle meningeal artery and inflated across the origin of the feeding branch. The Onyx penetrated into the vascular network around the fistula, occluding the feeding arteries and the drainage veins. The DAVF was successfully obliterated without complications. 4. Discussion Intracranial DAVF with retrograde flow or direct drainage into a cortical vein carries a high risk of hemorrhage and requires active
treatment to disconnect the cortical vein, with or without obliteration of the fistula [3,6,17–21]. This can be achieved by surgery or by embolization with n-butyl cyanoacrylate or coils, but these procedures may be difficult or dangerous [22–25]. Embolization with Onyx is easier because of its non-adherence to the microcatheter tip, appropriate viscosity, and superior permeability, allowing slow and intermittent injection to achieve occlusion of the whole vascular network including all feeding arteries, the fistula, and the drainage veins [1–16]. The use of Onyx has increased the reported success rates of treatment to 60–100% [10–13]. After injection, Onyx flows down the pressure gradient [10–12]. After filling of the drainage veins, further injection can backfill the feeding arteries. Formation of an Onyx plug proximal to the tip of the injection catheter encourages forward flow of Onyx [12]. Formation of such a plug after a small amount of initial reflux requires sufficient space in the artery. Using routine techniques, embolization with Onyx does not work well in patients with very small, short feeding arteries, as in the cases in this series. The transvenous approach could not
Fig. 1. Angiographic images in Case 1. Anteroposterior view of the right external carotid artery (ECA) (A), anteroposterior view of the left ECA (B), and lateral view of the left ECA (C), showing that the fistula of the transverse-sigmoid sinus did not have a large feeding artery. (D) Onyx cast after the first embolization, showing that only the arterial branch was occluded. (E) Onyx cast after the second embolization with balloon assistance, showing good penetration throughout the vascular network. (F) The fistula was occluded at the end of the procedure.
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Fig. 2. Angiographic images in Case 3. Views of the left internal carotid artery (ICA) (A) and the left ECA (B, C), showing the fistula, feeding arteries, and venous drainage. Fluoroscopic images showing the tip of the microcatheter in the transosseous branch of the occipital artery and the inflated Hyperform balloon before injection (D), and the Onyx cast after injection (E). Anteroposterior views of the left ECA (F) and the left ICA (G), showing that there is no abnormal shunting after treatment.
be used in these patients because of the tortuosity of the draining veins. However, it was important to treat these patients, because of the high risk of bleeding [3,6,17–21]. We therefore developed a balloon-assisted technique for embolization with Onyx.
Hyperglide and Hyperform balloons were designed to assist with coil embolization of intracranial aneurysms with wide necks [26,27]. They have been used for embolization of intracranial DAVF in four situations [9,10,12–15,28,29]. First, they can be used to
Fig. 3. Angiographic images in Case 5. Anteroposterior and lateral views of the right ICA (A, B) and the right ECA (C, D), showing the location, feeding arteries, and drainage of the fistula. Fluoroscopic images showing the tip of the microcatheter in the transosseous branch of the occipital artery and the inflated Hyperglide balloon before injection (E), and the Onyx cast after injection (E). Anteroposterior views of the right ICA (F) and the right ECA (G) after the procedure, showing no abnormal flow (G, H).
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Fig. 4. Angiographic images in Case 7. Anteroposterior views of the right ECA (A) and the right ICA (B), showing the location, feeding arteries, and drainage of the fistula. (C) Fluoroscopy image showing the tip of the microcatheter in the branch of the middle meningeal artery and the inflated Hyperglide balloon. (D, E) Fluoroscopy images showing the Onyx cast, the arterial network, and the proximal vein. After the procedure, no abnormal opacification was observed in the anteroposterior views of the right ICA (F) or the right ECA (G).
reduce the flow in cases of high-flow DAVF, to avoid rapid flow of Onyx into the drainage vein [28,29]. This technique is frequently used for embolization of intracranial high-flow arteriovenous fistulas [28,30], and has only been reported for the treatment of two patients with intracranial DAVF [28,29]. Second, they can be used to change the direction of blood flow. If there is a small arterial branch arising from a main artery at an acute angle, microcatheterization of the small artery is difficult because the catheter tip may become dislodged into the main artery distal to the small branch. Placement of a balloon in the main artery distal to the small branch can increase the ease of microcatheterization. This was described by Zhao et al. [13] for the treatment of patients with DAVF of the anterior cranial fossa. Third, they can be used to protect normal vessels or sinus from unwanted embolization. When a fistula has both extracranial and intracranial feeding arteries, and embolization is performed via an extracranial feeding artery, a balloon can be placed in the main intracranial artery at the origins of the feeding arteries to avoid inadvertent reflux. This technique is usually used for the treatment of cavernous DAVF or DAVF that is fed by a vertebral artery. Such use of a Hyperglide balloon was reported in the internal carotid artery by Rezende et al. [15] and in the vertebral artery by Jiang at al [10] and Saraf et al. [9]. Shi et al. reported use of a balloon in the superior sagittal sinus or transverse sinus to maintain the patency of the sinus or the cortical vein when they embolized DAVF of these sinuses through arterial feeders [12]. Fourth, they can be used as a plug to encourage forward flow. When the feeding artery is short, there may not be enough space to form an Onyx plug. When the feeding artery has a wide proximal segment and a narrow distal segment, a balloon can be used to form a plug proximal
to the tip of the microcatheter. Spiotta et al. [14] used a Hyperform balloon to protect the important proximal branches of the ascending pharyngeal artery, and the balloon also functioned as a plug. Shi et al. [12] also described the use of a balloon for this purpose. They reported four patients with feeding arteries similar to those in our patients. The occipital artery was temporarily occluded with the balloon placed proximal to the microcatheter tip and complete disappear of fistulas was achieved. Our series highlighted this technique. In our experience of patients with such feeding arteries, Onyx reflux occurred much more readily than in other patients, even when there was a long distance to the parent artery, resulting in failure of embolization. Balloon assistance therefore not only increased the ease of embolization, but also enabled curative treatment in some cases that routine embolization could not achieve. This technique worked very well in the patients in this series, who all underwent curative embolization without complications. The use of this technique also protected against unwanted occlusion of the intracranial arteries via anastomoses. All embolization procedures in this series were performed via the extracranial feeding arteries, as also reported by Shi et al. [12]. We chose this route for two reasons. First, it reduced the risk of uncontrollable reflux. Even with balloon assistance, Onyx may leak backwards into the main artery. A small-volume reflux may be inconsequential in an extracranial artery, as in Case 7 in this series, but may cause disastrous complications in an intracranial artery. Of course, excessive reflux should be avoided in cases with anastomoses between the extra- and intracranial arteries. Operators should be aware of the vascular anatomy and the resulting potential risks. Second, it is easier to remove the microcatheter at
J.-P. Deng et al. / Clinical Neurology and Neurosurgery 115 (2013) 1992–1997
the end of the procedure when using this route. A strong plug is needed to achieve curative embolization, which risks vessel rupture when removing the microcatheter from an intracranial artery. Huang et al. [5] reported retention of the microcatheter in one case. This is not a problem when using an extracranial artery. There were no problems with microcatheter removal in this series. 5. Conclusions Balloon-assisted embolization of intracranial DAVF with Onyx is a promising technique. In our case series, curative embolization was performed in all patients without complications. Use of a balloon to form a plug inside a very small, short feeding artery can provide enough encouragement to forward flow to achieve good penetration of Onyx throughout the vascular network of the fistula. This technique enables curative embolization in cases that could otherwise not be treated. With further development of this technique, the rate of curative embolization of intracranial DAVF may be improved even further. A large case series is needed to definitively determine the safety and effectiveness of this technique. Acknowledgement We are grateful and like to acknowledge the language editing provided by Dr. Lei Feng from Diagnostic Radiology, Kaiser Permanente-Los Angeles Medical Center, Los Angeles, California, USA. References [1] Carlson AP, Taylor CL, Yonas H. Treatment of dural arteriovenous fistula using ethylene vinyl alcohol (Onyx) arterial embolization as the primary modality: short-term results. Journal of Neurosurgery 2007;107:1120–5. [2] Nogueira RG, Dabus G, Rabinov JD, Eskey CJ, Ogilvy CS, Hirsch JA, et al. Preliminary experience with Onyx embolizaiton for the treatment of intracranial dural arteriovenous fistulas. American Journal of Neuroradiology 2008;29: 91–7. [3] Cognard C, Januel AC, Silva Jr NA, Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. American Journal of Neuroradiology 2008;29:235–41. [4] Lv XL, Jiang C, Li Y, Wu Z. Results and complication of transarterial embolization of intracranial dural arteriovenous fistulas using Onyx-18. Journal of Neurosurgery 2008;109:1083–90. [5] Huang Q, Xu Y, Hong Bo, Li Q, Zhao W, Liu J. Use of Onyx in the management of tentorial dural arteriovenous fistulae. Neurosurgery 2009;65:287–93. [6] Trivelato FP, Abud DG, Ulhôa AC, MenezesTde J, Abud TG, Nakiri GS, et al. Dural arteriovenous fistulas with direct cortical venous drainage treated with Onyx: a case series. Arquivos de Neuropsiquiatria 2010;68:613–8. [7] Theaudin M, Chapot R, Vahedi K, Bousser MG. Dural carotid–cavernous fistula: relationship between evolution of clinical symptoms and venous drainage changes. Cerebrovascular Disease 2008;25:382–4. [8] Rabinov JD, Yoo AJ, Ogilvy CS, Carter BS, Hirsch JA. ONYX versus n-BCA for embolization of cranial dural arteriovenous fistulas. Journal of Neurointerventional Surgery 2013;5:306–10. [9] Saraf R, Shrivastava M, Kumar N, Limaye U. Embolization of cranial dural arteriovenous fistulae with Onyx: indications, techniques, and outcomes. Indian Journal of Radiology and Imaging 2010;20(232):26–33.
1997
[10] Jiang C, Lv X, Li Y, Zhang J, Wu Z. Endovascular treatment of high-risk tentorial dural arteriovenous fistulas: clinical outcomes. Neuroradiology 2009;51:103–11. [11] Arat A, Inci S. Treatment of a superior sagittal sinus dural arteriovenous fistula with Onyx: technical case report. Neurosurgery 2006;59:169–70. [12] Shi ZS, Loh Y, Duckwiler GR, Tateshima S, Feng L, Jahan R, et al. Balloon-assisted transarterial embolization of intracranial dural arteriovenous fistulas. Journal of Neurosurgery 2009;110:921–8. [13] Zhao WY, Krings T, Yang PF, Liu JM, Xu Y, Li Q, et al. Balloon-assisted superselective microcatheterization for transarterial treatment of cranial dural arteriovenous fistulas: technique and results. Neurosurgery 2012;71:269–73. [14] Spiotta AM, Hughes G, Masaryk TJ, Hui FK. Balloon-augmented Onyx embolization of a dural arteriovenous fistula arising from the neuromeningeal trunk of the ascending pharyngeal artery: technical report. Journal of Neurointerventional Surgery 2011;3:300–3. [15] Rezende MT, Piotin M, Mounayer C, Spelle L, Abud DG, Moret J. Dural arteriovenous fistula of the lesser sphenoid wing region treated with Onyx: technical note. Neuroradiology 2006;48:130–4. [16] Tahon F, Salkine F, Amsalem Y, Aguettaz P, Lamy B, Turjman F. Dural arteriovenous fistula of the anterior treated with the Onyx liquid embolic system and the Sonic microcatheter. Neuroradiology 2008;50:429–32. [17] Ghobrial GM, Marchan E, Nair AK, Dumont AS, Tjoumakaris SI, Gonzalez LF, et al. Dural arteriovenous fistulas: a review of the literature and a presentation of a single institution’s experience. World Neurosurgery 2012, http://dx.doi.org/10.1016/j.wneu.2012.01.053. [18] Hoh BL, Choudhri TF, Connolly Jr ES, Solomon RA. Surgical management of high-grade intracranial dural arteriovenous fistulas: leptomeningeal venous disruption without nidus excision. Neurosurgery 1998;42:796–804. [19] Oh JT, Chung SY, Lanzino G, Park KS, Kim SM, Park MS, et al. Intracranial dural arteriovenous fistulas: clinical characteristics and management based on location and hemodynamics. Journal of Cerebrovascular and Endovascular Neurosurgery 2012;12:192–202. [20] Willinsky R, Goyal M, terBrugge K, Montanera W. Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with presentation, location, and MR findings in 122 patients. American Journal of Neuroradiology 1999;20:1031–6. [21] vanDijk JMC, terBrugge KG, Willinsky RA, Wallace MC. Selective disconnection of cortical venous reflux as treatment for cranial dural arteriovenous fistulas. Journal of Neurosurgery 2004;101:31–5. [22] Westermaier T, Bendszus M, Solymosi L, Roosen K, Ernestus RI. Surgical treatment of dural arteriovenous fistulas of the petrous apex. World Neurosurgery 2012;77:1878–87. [23] Hwang G, Kang HS, Oh CW, Kwon OK. Surgical obliteration in superior petrosal sinus dural arteriovenous fistula. Journal of Korean Neurosurgical Society 2011;49:222–5. [24] Klurfan P, Gunnarsson T, Shelef I, Terbrugge KG, Willinsky RA. Transvenous treatment of cranial dural arteriovenous fistulas with Hydrogel coated coils. Interventional Neuroradiology 2006;12:319–26. [25] Nelson PKN, Russell SM, Woo HH, Alastra AJ, Vidovich DV. Use of a wedged microcatheter for curative transarterial embolization of complex intracranial dural arteriovenous fistulas: indications, endovascular technique, and outcome in 21 patients. Journal of Neurosurgery 2003;98:498–506. [26] Spiotta AM, Bhalla T, Hussain MS, Sivapatham T, Batra A, Hui F, et al. An analysis of inflation times during balloon-assisted aneurysm coil embolization and ischemic complications. Stroke 2011;42:1051–5. [27] Cekirge HS, Yavuz K, Geyik S, Saatci I. Hyperform balloon remodeling in the endovascular treatment of anterior cerebral, middle cerebral, and anterior communicating artery aneurysms: clinical and angiographic follow-up results in 800 consecutive patients. Journal of Neurosurgery 2011;114:944–53. [28] Andreou A, Ioannidis I, Nasis N. Transarterial balloon-assisted glue embolization of high-flow arteriovenous fistulas. Neuroradiology 2008;50:267–72. [29] Arat A, Cil BE, Vargel I, Turkbey B, Canyigit M, Peynircioglu B, et al. Embolization of high-flow craniofacial vascular malformations with onyx. American Journal of Neuroradiology 2007;28:1409–14. [30] Newman CB, Hu YC, McDougall CG, Albuquerque FC. Balloon-assisted Onyx embolization of cerebral single-channel pial arteriovenous fistulas. Journal of Neurosurgery: Pediatrics 2011;7:637–42.
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Treatment of dural arteriovenous fistula by balloon-assisted transarterial embolization with Onyx Jian-Ping Deng, Tao Zhang, Jiang Li, Jia Yu, Zhen-Wei Zhao ∗,1 , Guo-Dong Gao 1 Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province 710038, China
a r t i c l e
i n f o
Article history: Received 25 March 2013 Received in revised form 4 June 2013 Accepted 9 June 2013 Available online 2 July 2013 Keywords: Arteriovenous fistula Embolization Balloon assistance Onyx
a b s t r a c t Objective: This study evaluated the feasibility, safety, and efficacy of embolization of dural arteriovenous fistula via a very small, short feeding artery with the assistance of a balloon placed proximal to the tip of the microcatheter, such that the balloon serves as a plug. Methods: Eight patients who underwent treatment of DAVF by balloon-assisted transarterial embolization with Onyx were retrospectively reviewed. Gender, age, angiography findings, procedure details, clinical and angiographic outcomes, complications, and follow-up were recorded and analyzed. Results: Nine embolization procedures were performed in eight male patients via extracranial arteries. Balloon-assisted embolization was successful in all eight patients. A Hyperglide balloon was used in five patients, and a Hyperform balloon was used in three patients. Angiographic resolution of the fistula was achieved in all patients without complications. All patients recovered uneventfully. During the follow-up period of 7–19 months, all patients were asymptomatic except for one patient who experienced mild headaches. Conclusions: Treatment of DAVF by balloon-assisted embolization with Onyx achieved promising results, even in patients with very small and short feeding arteries. This technique allowed the treatment of DAVF cases where other techniques have failed. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The development of Onyx (ev3 Neurovascular, Irvine, CA, USA) was a milestone in the endovascular treatment of dural arteriovenous fistula (DAVF) [1–10]. The combination of Onyx and new microcatheters has greatly improved the ability to treat DAVF via different approaches [1–11]. The reported outcomes after embolization of DAVF with Onyx are promising [1–16]. The viscosity and permeability of Onyx allow slow and intermittent injection, resulting in good penetration into the drainage veins and the other feeding arteries of the fistula [1–16]. Successful treatment requires optimal positioning of the microcatheter, enough space to form an Onyx plug, and enough forward pressure to allow penetration of Onyx into the vascular network [10–13]. Embolization is usually performed via the middle meningeal artery, even when the artery is elongated and tortuous [1–13,16]. However, it may be difficult to achieve good penetration over long distances via small-diameter or low-flow vessels, as it may not
be possible to form a plug. Transarterial embolization of DAVF via very small, low-flow feeding arteries therefore has variable outcomes. This paper describes a technique of balloon-assisted transarterial embolization of DAVF with Onyx. 2. Materials and methods We searched our prospective database of patients with cerebrovascular diseases treated with endovascular therapy at our hospital from January 1996 to December 2012 and identified 151 patients with dural AVF. Eight patients were found to undergo treatment of DAVF by endovascular balloon-assisted embolization with Onyx from 2010 to 2012. Data describing gender, age, symptoms, treatment details, clinical and angiographic outcomes, complications, and follow-up were collected. Pre-procedure angiography findings were extracted and analyzed. 2.1. Endovascular procedures
∗ Corresponding author at: No. 1 Xinsi Road, Baqiao District, Xi’an City, Shaanxi Province, 710038, China. Tel.: +86 29 84777285; fax: +86 29 84777435. E-mail addresses: [email protected], [email protected] (Z.-W. Zhao). 1 These authors equally contributed to this study. 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.06.007
All procedures were performed under general anesthesia via the femoral artery access. An 8-F guiding catheter (Envoy; Johnson & Johnson, Miami, FL, USA) was introduced through an 8-F sheath and advanced through the external carotid artery (ECA) into the occipital artery or internal maxillary artery, depending on the diameters
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of the arteries. A Marathon microcatheter (ev3, Neurovascular) was used to catheterize the feeding artery as distally as possible. A Hyperglide balloon (ev3 Neurovascular) or Hyperform balloon (ev3 Neurovascular) was then advanced into the feeding artery by the operator’s choice. If the ipsilateral ECA and internal carotid artery (ICA) both fed the fistula, the 8-F guiding catheter was withdrawn to the common carotid artery. If the fistula was fed bilaterally, an angiographic catheter was placed in the contralateral common carotid artery via the contralateral femoral artery. The balloon was inflated, and angiography was performed to confirm that the artery was completely occluded. Onyx was injected after flushing the catheter with dimethyl sulfoxide (ev3 Neurovascular). After angiographic confirmation that the fistula was completely obliterated, the microcatheter was withdrawn, followed by the withdrawal of the balloon.
3.3. Treatment, results, and follow-up
2.2. Notes on embolization techniques
3.4. Representative cases
In most cases, initial injection of Onyx into a DAVF feeding artery causes reflux and forms a plug. In the patients in this series, the feeding arteries were very small, and a balloon was used to form a plug. The embolization procedures were slow, with injection being stopped when Onyx reflux reached the balloon. After a waiting of nearly 60 s the injection was resumed. Sometimes several rounds of “waiting” and “injecting” took place. Patience was often needed for an effective plug to form. Several injections were usually performed to ensure good penetration of the nidus by Onyx.
Case 1 (Fig. 1): A 54-year-old man without history of hypertension presented with an intracranial hemorrhage, and underwent craniectomy at another hospital. Two months later, DSA at our center showed a DAVF of the left transverse-sigmoid sinus, fed by very small branches of the left occipital artery and ascending pharyngeal artery, and draining into the sigmoid sinus with cortical venous reflux. Endovascular treatment was planned. Under general anesthesia with endotracheal intubation, a Marathon microcatheter was introduced through a 6-F guiding catheter, and was advanced into a branch of the occipital artery. However, Onyx did not penetrate across the tiny outlet of the fistula, and only the branch of the occipital artery was embolized. An 8-F guiding catheter was then placed, and another Marathon microcatheter was advanced to a more distal branch. A Hyperglide balloon (4 mm × 20 mm) was placed in the occipital artery, across the origin of the feeding vessel. After inflation of the balloon, Onyx was injected, and penetrated very well into the draining vein and the other small feeding arteries. The DAVF was completely obliterated. There was no deterioration of the patient’s neurological status, and he underwent cranioplasty before leaving hospital. Case 3 (Fig. 2): A 42-year-old alert male was diagnosed with a small subarachnoid hemorrhage, and was suspected to have a cerebral aneurysm. However, DSA showed a tentorial DAVF. The feeding arteries were tentorial dural branches of the ICA, branches of the ascending pharyngeal artery, and transosseous branches of the occipital artery. Venous drainage was directly into the leptomeningeal vein via a tortuous outflow, which harbored a stenosis before emerging into the torcular Herophili. A Marathon microcatheter was advanced into the transosseous branch of the occipital artery and embolization was performed with the assistance of a Hyperform balloon (4 mm × 7 mm). The fistula was successfully embolized without complications. Case 5 (Fig. 3): A 40-year-old male presented with weakness of all four extremities, but brain MRI did not detect any vascular lesion. DSA showed a tentorial DAVF. There were many feeding arteries including dural branches of the right ICA and branches of the middle meningeal artery, ascending pharyngeal artery, and occipital artery, but they were all very small and short. Venous drainage was via an aneurysmal varix to the surface of the medulla oblongata and cervical spinal cord. A Marathon microcatheter was placed in the transosseous branch of the occipital artery, and embolization was performed with the assistance of a Hyperglide balloon (4 mm × 20 mm) which was inflated across the origin of the feeding branch. The fistula was successfully embolized without complications. The Onyx penetrated into the proximal drainage veins and all the feeding arteries. Case 7 (Fig. 4): A 44-year-old male experienced sudden headache and was diagnosed with a small SAH. He was Hunt and
2.3. Follow-up Changes in symptoms and signs after the procedure were recorded. Angiographic follow-up was not performed. All patients were followed up clinically in the outpatient department or by telephone. 3. Results 3.1. Patients and symptoms The characteristics of the eight patients who underwent balloon-assisted transarterial embolization are shown in Table 1. The patients were all male, and were aged from 18 to 62 years with an average age of 44.3 years. One patient presented with weakness of all four extremities (Case 5), and the other patients presented with intracranial hemorrhage. Case 1 underwent urgent craniectomy to treat a large intracerebral hematoma. The other six patients presented with a sudden headache, and computed tomography showed subarachnoid hemorrhage. These six patients were all Hunt and Hess grade I or II, with no neurological deficits on physical examination. 3.2. Angiographic images Digital subtraction angiography (DSA) was performed in all patients before treatment. The DAVF was located in the transversesigmoid sinus in four patients (Cases 1, 2, 6, and 8) and in the tentorium in the other four patients. The DAVF was fed by both ECAs in Case 6, and unilaterally in the other seven patients (by the ECA alone in Cases 1 and 7, and by the ipsilateral ECA and ICA in the other five cases). All the feeding arteries were very small, short branches arising from the occipital artery, ICA, middle meningeal artery, or ascending pharyngeal artery. In nearly all cases, the draining veins were small and tortuous. Drainage to the spine occurred in three cases (Cases 4, 5, and 7) and drainage was directly into the cortical veins in two patients (Case 1 and 2) and indirectly into the cortical veins in three patients.
Nine embolization procedures were performed in eight patients, including eight balloon-assisted procedures. Although five patients had feeding arteries arising from the ICA, embolization was performed via feeding arteries arising from the ECA in all cases. A Hyperglide balloon was used in five patients, and a Hyperform balloon was used in the other three patients. Angiographic cure was achieved in all patients, without complications. All patients recovered uneventfully. An additional small surgical procedure was performed in Case 1. In Case 6, the patient’s quadraparesis improved greatly immediately after the procedure. During the follow-up period of 7–19 months, all patients were asymptomatic, except for Case 1 who experienced mild headaches, especially with changes in the weather.
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Table 1 Informations of eight patients, angiographic images and procedures. No.
Age/gender
Symptom
Location
Feeders
Drainage
Cognard
Balloon
1 2 3 4 5 6 7 8
54/M 44/M 42/M 18/M 40/M 62/M 44/M 50/M
ICH ICH ICH ICH Weak of limb ICH ICH ICH
TS TS TT TT TT TS TT TS
PH, OC OC, MM, BI OC, PH, BI OC, BI, MM OC, BI, MM,PH OC, MM, MM, OC,PH OC,PH,BI
TS, C C C SP SP TS,C SP TS,C
IIa + b III III V V IIa + b V IIa + b
G 4 × 20 G 4 × 20 F 4×7 F 4×7 G 4 × 20 F 4×7 G 4 × 20 G 4 × 20
ICH = intracranial hemorrhage; TS = transverse sigmoid sinus; TT = tentorium; OC = occipital artery; PH = pharyngeal artery; MM = middle meningeal artery; BI = dural branch of internal carotid artery; C = cortical vein; SP = spinal vein; G = Hyperglide; F = Hyperform.
Hess grade I at the time of presentation. DSA showed a DAVF. The feeding arteries were branches of the right middle meningeal artery and the ICA, and a very small branch of the occipital artery. Drainage was via a long, tortuous leptomeningeal vein to the surface of the medulla oblongata and the spine. A Marathon microcatheter was advanced into the short branch of the middle meningeal artery originating at the foramen spinosum, although later images indicated that the posterior branch might have been a better choice. A Hyperglide balloon was advanced into the middle meningeal artery and inflated across the origin of the feeding branch. The Onyx penetrated into the vascular network around the fistula, occluding the feeding arteries and the drainage veins. The DAVF was successfully obliterated without complications. 4. Discussion Intracranial DAVF with retrograde flow or direct drainage into a cortical vein carries a high risk of hemorrhage and requires active
treatment to disconnect the cortical vein, with or without obliteration of the fistula [3,6,17–21]. This can be achieved by surgery or by embolization with n-butyl cyanoacrylate or coils, but these procedures may be difficult or dangerous [22–25]. Embolization with Onyx is easier because of its non-adherence to the microcatheter tip, appropriate viscosity, and superior permeability, allowing slow and intermittent injection to achieve occlusion of the whole vascular network including all feeding arteries, the fistula, and the drainage veins [1–16]. The use of Onyx has increased the reported success rates of treatment to 60–100% [10–13]. After injection, Onyx flows down the pressure gradient [10–12]. After filling of the drainage veins, further injection can backfill the feeding arteries. Formation of an Onyx plug proximal to the tip of the injection catheter encourages forward flow of Onyx [12]. Formation of such a plug after a small amount of initial reflux requires sufficient space in the artery. Using routine techniques, embolization with Onyx does not work well in patients with very small, short feeding arteries, as in the cases in this series. The transvenous approach could not
Fig. 1. Angiographic images in Case 1. Anteroposterior view of the right external carotid artery (ECA) (A), anteroposterior view of the left ECA (B), and lateral view of the left ECA (C), showing that the fistula of the transverse-sigmoid sinus did not have a large feeding artery. (D) Onyx cast after the first embolization, showing that only the arterial branch was occluded. (E) Onyx cast after the second embolization with balloon assistance, showing good penetration throughout the vascular network. (F) The fistula was occluded at the end of the procedure.
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Fig. 2. Angiographic images in Case 3. Views of the left internal carotid artery (ICA) (A) and the left ECA (B, C), showing the fistula, feeding arteries, and venous drainage. Fluoroscopic images showing the tip of the microcatheter in the transosseous branch of the occipital artery and the inflated Hyperform balloon before injection (D), and the Onyx cast after injection (E). Anteroposterior views of the left ECA (F) and the left ICA (G), showing that there is no abnormal shunting after treatment.
be used in these patients because of the tortuosity of the draining veins. However, it was important to treat these patients, because of the high risk of bleeding [3,6,17–21]. We therefore developed a balloon-assisted technique for embolization with Onyx.
Hyperglide and Hyperform balloons were designed to assist with coil embolization of intracranial aneurysms with wide necks [26,27]. They have been used for embolization of intracranial DAVF in four situations [9,10,12–15,28,29]. First, they can be used to
Fig. 3. Angiographic images in Case 5. Anteroposterior and lateral views of the right ICA (A, B) and the right ECA (C, D), showing the location, feeding arteries, and drainage of the fistula. Fluoroscopic images showing the tip of the microcatheter in the transosseous branch of the occipital artery and the inflated Hyperglide balloon before injection (E), and the Onyx cast after injection (E). Anteroposterior views of the right ICA (F) and the right ECA (G) after the procedure, showing no abnormal flow (G, H).
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Fig. 4. Angiographic images in Case 7. Anteroposterior views of the right ECA (A) and the right ICA (B), showing the location, feeding arteries, and drainage of the fistula. (C) Fluoroscopy image showing the tip of the microcatheter in the branch of the middle meningeal artery and the inflated Hyperglide balloon. (D, E) Fluoroscopy images showing the Onyx cast, the arterial network, and the proximal vein. After the procedure, no abnormal opacification was observed in the anteroposterior views of the right ICA (F) or the right ECA (G).
reduce the flow in cases of high-flow DAVF, to avoid rapid flow of Onyx into the drainage vein [28,29]. This technique is frequently used for embolization of intracranial high-flow arteriovenous fistulas [28,30], and has only been reported for the treatment of two patients with intracranial DAVF [28,29]. Second, they can be used to change the direction of blood flow. If there is a small arterial branch arising from a main artery at an acute angle, microcatheterization of the small artery is difficult because the catheter tip may become dislodged into the main artery distal to the small branch. Placement of a balloon in the main artery distal to the small branch can increase the ease of microcatheterization. This was described by Zhao et al. [13] for the treatment of patients with DAVF of the anterior cranial fossa. Third, they can be used to protect normal vessels or sinus from unwanted embolization. When a fistula has both extracranial and intracranial feeding arteries, and embolization is performed via an extracranial feeding artery, a balloon can be placed in the main intracranial artery at the origins of the feeding arteries to avoid inadvertent reflux. This technique is usually used for the treatment of cavernous DAVF or DAVF that is fed by a vertebral artery. Such use of a Hyperglide balloon was reported in the internal carotid artery by Rezende et al. [15] and in the vertebral artery by Jiang at al [10] and Saraf et al. [9]. Shi et al. reported use of a balloon in the superior sagittal sinus or transverse sinus to maintain the patency of the sinus or the cortical vein when they embolized DAVF of these sinuses through arterial feeders [12]. Fourth, they can be used as a plug to encourage forward flow. When the feeding artery is short, there may not be enough space to form an Onyx plug. When the feeding artery has a wide proximal segment and a narrow distal segment, a balloon can be used to form a plug proximal
to the tip of the microcatheter. Spiotta et al. [14] used a Hyperform balloon to protect the important proximal branches of the ascending pharyngeal artery, and the balloon also functioned as a plug. Shi et al. [12] also described the use of a balloon for this purpose. They reported four patients with feeding arteries similar to those in our patients. The occipital artery was temporarily occluded with the balloon placed proximal to the microcatheter tip and complete disappear of fistulas was achieved. Our series highlighted this technique. In our experience of patients with such feeding arteries, Onyx reflux occurred much more readily than in other patients, even when there was a long distance to the parent artery, resulting in failure of embolization. Balloon assistance therefore not only increased the ease of embolization, but also enabled curative treatment in some cases that routine embolization could not achieve. This technique worked very well in the patients in this series, who all underwent curative embolization without complications. The use of this technique also protected against unwanted occlusion of the intracranial arteries via anastomoses. All embolization procedures in this series were performed via the extracranial feeding arteries, as also reported by Shi et al. [12]. We chose this route for two reasons. First, it reduced the risk of uncontrollable reflux. Even with balloon assistance, Onyx may leak backwards into the main artery. A small-volume reflux may be inconsequential in an extracranial artery, as in Case 7 in this series, but may cause disastrous complications in an intracranial artery. Of course, excessive reflux should be avoided in cases with anastomoses between the extra- and intracranial arteries. Operators should be aware of the vascular anatomy and the resulting potential risks. Second, it is easier to remove the microcatheter at
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the end of the procedure when using this route. A strong plug is needed to achieve curative embolization, which risks vessel rupture when removing the microcatheter from an intracranial artery. Huang et al. [5] reported retention of the microcatheter in one case. This is not a problem when using an extracranial artery. There were no problems with microcatheter removal in this series. 5. Conclusions Balloon-assisted embolization of intracranial DAVF with Onyx is a promising technique. In our case series, curative embolization was performed in all patients without complications. Use of a balloon to form a plug inside a very small, short feeding artery can provide enough encouragement to forward flow to achieve good penetration of Onyx throughout the vascular network of the fistula. This technique enables curative embolization in cases that could otherwise not be treated. With further development of this technique, the rate of curative embolization of intracranial DAVF may be improved even further. A large case series is needed to definitively determine the safety and effectiveness of this technique. Acknowledgement We are grateful and like to acknowledge the language editing provided by Dr. Lei Feng from Diagnostic Radiology, Kaiser Permanente-Los Angeles Medical Center, Los Angeles, California, USA. References [1] Carlson AP, Taylor CL, Yonas H. Treatment of dural arteriovenous fistula using ethylene vinyl alcohol (Onyx) arterial embolization as the primary modality: short-term results. Journal of Neurosurgery 2007;107:1120–5. [2] Nogueira RG, Dabus G, Rabinov JD, Eskey CJ, Ogilvy CS, Hirsch JA, et al. Preliminary experience with Onyx embolizaiton for the treatment of intracranial dural arteriovenous fistulas. American Journal of Neuroradiology 2008;29: 91–7. [3] Cognard C, Januel AC, Silva Jr NA, Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. American Journal of Neuroradiology 2008;29:235–41. [4] Lv XL, Jiang C, Li Y, Wu Z. Results and complication of transarterial embolization of intracranial dural arteriovenous fistulas using Onyx-18. Journal of Neurosurgery 2008;109:1083–90. [5] Huang Q, Xu Y, Hong Bo, Li Q, Zhao W, Liu J. Use of Onyx in the management of tentorial dural arteriovenous fistulae. Neurosurgery 2009;65:287–93. [6] Trivelato FP, Abud DG, Ulhôa AC, MenezesTde J, Abud TG, Nakiri GS, et al. Dural arteriovenous fistulas with direct cortical venous drainage treated with Onyx: a case series. Arquivos de Neuropsiquiatria 2010;68:613–8. [7] Theaudin M, Chapot R, Vahedi K, Bousser MG. Dural carotid–cavernous fistula: relationship between evolution of clinical symptoms and venous drainage changes. Cerebrovascular Disease 2008;25:382–4. [8] Rabinov JD, Yoo AJ, Ogilvy CS, Carter BS, Hirsch JA. ONYX versus n-BCA for embolization of cranial dural arteriovenous fistulas. Journal of Neurointerventional Surgery 2013;5:306–10. [9] Saraf R, Shrivastava M, Kumar N, Limaye U. Embolization of cranial dural arteriovenous fistulae with Onyx: indications, techniques, and outcomes. Indian Journal of Radiology and Imaging 2010;20(232):26–33.
1997
[10] Jiang C, Lv X, Li Y, Zhang J, Wu Z. Endovascular treatment of high-risk tentorial dural arteriovenous fistulas: clinical outcomes. Neuroradiology 2009;51:103–11. [11] Arat A, Inci S. Treatment of a superior sagittal sinus dural arteriovenous fistula with Onyx: technical case report. Neurosurgery 2006;59:169–70. [12] Shi ZS, Loh Y, Duckwiler GR, Tateshima S, Feng L, Jahan R, et al. Balloon-assisted transarterial embolization of intracranial dural arteriovenous fistulas. Journal of Neurosurgery 2009;110:921–8. [13] Zhao WY, Krings T, Yang PF, Liu JM, Xu Y, Li Q, et al. Balloon-assisted superselective microcatheterization for transarterial treatment of cranial dural arteriovenous fistulas: technique and results. Neurosurgery 2012;71:269–73. [14] Spiotta AM, Hughes G, Masaryk TJ, Hui FK. Balloon-augmented Onyx embolization of a dural arteriovenous fistula arising from the neuromeningeal trunk of the ascending pharyngeal artery: technical report. Journal of Neurointerventional Surgery 2011;3:300–3. [15] Rezende MT, Piotin M, Mounayer C, Spelle L, Abud DG, Moret J. Dural arteriovenous fistula of the lesser sphenoid wing region treated with Onyx: technical note. Neuroradiology 2006;48:130–4. [16] Tahon F, Salkine F, Amsalem Y, Aguettaz P, Lamy B, Turjman F. Dural arteriovenous fistula of the anterior treated with the Onyx liquid embolic system and the Sonic microcatheter. Neuroradiology 2008;50:429–32. [17] Ghobrial GM, Marchan E, Nair AK, Dumont AS, Tjoumakaris SI, Gonzalez LF, et al. Dural arteriovenous fistulas: a review of the literature and a presentation of a single institution’s experience. World Neurosurgery 2012, http://dx.doi.org/10.1016/j.wneu.2012.01.053. [18] Hoh BL, Choudhri TF, Connolly Jr ES, Solomon RA. Surgical management of high-grade intracranial dural arteriovenous fistulas: leptomeningeal venous disruption without nidus excision. Neurosurgery 1998;42:796–804. [19] Oh JT, Chung SY, Lanzino G, Park KS, Kim SM, Park MS, et al. Intracranial dural arteriovenous fistulas: clinical characteristics and management based on location and hemodynamics. Journal of Cerebrovascular and Endovascular Neurosurgery 2012;12:192–202. [20] Willinsky R, Goyal M, terBrugge K, Montanera W. Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with presentation, location, and MR findings in 122 patients. American Journal of Neuroradiology 1999;20:1031–6. [21] vanDijk JMC, terBrugge KG, Willinsky RA, Wallace MC. Selective disconnection of cortical venous reflux as treatment for cranial dural arteriovenous fistulas. Journal of Neurosurgery 2004;101:31–5. [22] Westermaier T, Bendszus M, Solymosi L, Roosen K, Ernestus RI. Surgical treatment of dural arteriovenous fistulas of the petrous apex. World Neurosurgery 2012;77:1878–87. [23] Hwang G, Kang HS, Oh CW, Kwon OK. Surgical obliteration in superior petrosal sinus dural arteriovenous fistula. Journal of Korean Neurosurgical Society 2011;49:222–5. [24] Klurfan P, Gunnarsson T, Shelef I, Terbrugge KG, Willinsky RA. Transvenous treatment of cranial dural arteriovenous fistulas with Hydrogel coated coils. Interventional Neuroradiology 2006;12:319–26. [25] Nelson PKN, Russell SM, Woo HH, Alastra AJ, Vidovich DV. Use of a wedged microcatheter for curative transarterial embolization of complex intracranial dural arteriovenous fistulas: indications, endovascular technique, and outcome in 21 patients. Journal of Neurosurgery 2003;98:498–506. [26] Spiotta AM, Bhalla T, Hussain MS, Sivapatham T, Batra A, Hui F, et al. An analysis of inflation times during balloon-assisted aneurysm coil embolization and ischemic complications. Stroke 2011;42:1051–5. [27] Cekirge HS, Yavuz K, Geyik S, Saatci I. Hyperform balloon remodeling in the endovascular treatment of anterior cerebral, middle cerebral, and anterior communicating artery aneurysms: clinical and angiographic follow-up results in 800 consecutive patients. Journal of Neurosurgery 2011;114:944–53. [28] Andreou A, Ioannidis I, Nasis N. Transarterial balloon-assisted glue embolization of high-flow arteriovenous fistulas. Neuroradiology 2008;50:267–72. [29] Arat A, Cil BE, Vargel I, Turkbey B, Canyigit M, Peynircioglu B, et al. Embolization of high-flow craniofacial vascular malformations with onyx. American Journal of Neuroradiology 2007;28:1409–14. [30] Newman CB, Hu YC, McDougall CG, Albuquerque FC. Balloon-assisted Onyx embolization of cerebral single-channel pial arteriovenous fistulas. Journal of Neurosurgery: Pediatrics 2011;7:637–42.