DURAL FISTULAS DURAL FISTULAS
TOPIC
Endovascular Treatment of Intracranial Dural Arteriovenous Fistulas Matthew VanLandingham, MD Benjamin Fox, MD Daniel Hoit, MD, MPH Lucas Elijovich, MD Adam S. Arthur, MD, MPH Semmes-Murphey Clinic, Department of Neurosurgery, University of Tennessee, Memphis, Tennessee Correspondence: Adam S. Arthur, MD, MPH, FAANS, FACS, Semmes-Murphey Clinic, 6325 Humphreys Blvd, Memphis, TN 38120. E-mail: [email protected] Received, June 18, 2013. Accepted, September 17, 2013. Copyright © 2014 by the Congress of Neurological Surgeons
Endovascular treatment options for dural arteriovenous fistulas (DAVFs) have vastly expanded and become progressively safer in the last several years. Angiographic imaging systems have improved, catheter technology has advanced, and liquid embolic and coil options have increased. As a likely result, an increasing proportion of DAVFs are treated via an endovascular approach. In addition to allowing physicians to appreciate and treat lesions better, varied approaches have been developed. The “plug and push” technique and the new availability of dimethyl sulfoxide–compatible dual lumen balloons have allowed safer and more thorough transarterial treatments. Transvenous treatment has proved to be a valuable technique for some lesions. Hybrid approaches with surgical assisted access to vascular structures have been successfully used to treat more challenging fistulas. KEY WORDS: Dural arteriovenous fistula, Endovascular techniques, Therapeutic embolization Neurosurgery 74:S42–S49, 2014
DOI: 10.1227/NEU.0000000000000180
D
ural arteriovenous fistulas (DAVFs) are pathological shunts between meningeal or extracranial arteries and the dural venous sinuses, dural veins, or cortical veins. They are classified by the Borden-Shucart or Cognard schemes (Table), which describe the patterns of cerebral venous drainage and the patency of the dural venous system.1,2 Highergrade lesions (Borden-Shucart 2-3; Cognard IIb, IIa1b, and III-V) are more likely to become symptomatic with cranial neuropathies, visual loss, retro-orbital pain, and chemosis/proptosis with cavernous/paracavernous and tentorial DAVFs, and pulsatile tinnitus, encephalopathy, parkinsonism, and cerebellar dysfunction with transverse sigmoid sinus DAVFs.3-7 Additionally, higher-grade and symptomatic fistulas are more likely to present with intracranial hemorrhage. The Borden-Shucart classification scheme also takes into account the number of arterial connections in the fistula (single vs multiple). ABBREVIATIONS: DAVF, dural arteriovenous fistula; NBCA, n-butyl cyanoacrylate; TAE, transarterial embolization; TVE, transvenous embolization Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).
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The decision to treat a DAVF is based on an analysis of the patient’s symptoms, medical comorbidities, and risk of intracranial hemorrhage. Asymptomatic, low-grade DAVFs pose minimal risk of hemorrhage and generally warrant only close observation.8-11 High-grade DAVFs with cortical venous reflux or intolerably symptomatic DAVF may be considered candidates for treatment.5,12 The goal of any DAVF treatment is obliteration of the fistulous connection between the arterial and venous systems. The endovascular correlate to surgical disconnection of an artery and vein is the presence of embolic material on both the arterial and venous side in close proximity to the fistulous connection. Complete endovascular obliteration typically results in a lasting cure. Incomplete treatment of a fistula can allow recruitment of new arterial blood supply to the lesion and may not improve symptoms or lower the risk of intracranial hemorrhage. If endovascular treatment is excluded because of the anatomy of the DAVF or fails to produce complete obliteration, hybrid open/endovascular, open surgical intervention, or stereotactic radiosurgery may be considered.13 Endovascular approaches to treatment of DAVFs have evolved with our understanding of the pathogenesis and angioarchitecture of these lesions. Advancements in catheter and embolic technology have also made endovascular therapy more effective. Disconnection of the arteriovenous
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ENDOVASCULAR TREATMENT OF INTRACRANIAL DAVFs
TABLE. Borden-Shucart and Cognard Classifications Borden-Shucart classification 1 2 3 Cognard classification I IIa IIb IIa1b III IV V
Venous drainage directly into dural venous sinus or meningeal vein Venous drainage into dural venous sinus with cortical venous reflux Venous drainage directly into subarachnoid veins (cortical venous reflux only) Venous drainage into dural venous sinus with antegrade flow Venous drainage into dural venous sinus with retrograde flow Venous drainage into dural venous sinus with antegrade flow and cortical venous reflux Venous drainage into dural venous sinus with retrograde flow and cortical venous reflux Venous drainage directly into subarachnoid veins (cortical venous reflux only) Type III with venous ectasias of the draining subarachnoid veins Direct drainage into spinal perimedullary veins
shunt may be complicated by the presence of multiple arterial feeders (Borden-Shucart), long segments of affected venous sinus, or isolation of a venous sinus segment owing to occlusive venopathy. Endovascular approaches allow continuous evaluation of the arteriovenous shunt over the course of the procedure and have become the primary modality for treatment. Transvenous, transarterial, direct access, or a combination of these approaches is often necessary for complete cure of a fistula. Liquid embolics, including nbutyl cyanoacrylate (NBCA, Cordis, Miami Lakes, Florida), ethylene vinyl alcohol copolymer (Onyx, ev3, Irvine, California), and coil occlusion, all have a role in complete closure of the arteriovenous shunt. The purpose of this review is to describe the major current strategies for the endovascular treatment of DAVFs that have evolved with improvements in endovascular technology.
APPROACHES TO DAVF EMBOLIZATION Improvements in microcatheters and wires, biplane angiographic image resolution, 3-dimensional rotational imaging with software-enhanced postprocessing, coil technology, and liquid embolic agents (NBCA and Onyx) have made transarterial embolization (TAE) and transvenous embolization (TVE) of DAVFs possible. TAE requires selective catheterization of a distal arterial feeding pedicle and placement of the microcatheter tip as close to the fistulous connection as possible.14-16 The advantages of transfemoral transarterial treatment are the familiarity and ease of endovascular navigation compared with transvenous access. Complete treatment requires penetration of the embolic agent through the arterial feeding vessel into the venous outflow pouch to ensure obliteration of the fistulous connection. Distal placement of the microcatheter can be limited by tortuosity of the feeding artery and distance to the site of the fistula. The transarterial approach is usually effective in small DAVFs and those that have associated venous occlusions or significant venous stenosis, which may limit a transvenous approach. The treatment of large, complex DAVFs is also possible via the transarterial route but may require access of multiple arterial pedicles to completely occlude the fistula and may need to be
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staged over multiple procedures to limit contrast and radiation exposure. Coils are generally not useful as a primary embolic agent in the transarterial approach because the coils stay on the arterial side, whereas liquid embolic agents have the ability to pass through small tortuous end arteries into the venous side. In complex DAVFs that require multiple pedicle catheterization, we have found that saving the most direct, closest access for last improves the chance of success. Unfortunately, incompletely treated DAVFs often recanalize. There are many cases in which a patient has been told that the fistula has been “80%” or “90%” treated, leaving an intact shunt that can recruit additional arterial supply. We prefer to “prune” off the smaller arterial supply first, which causes the DAVF to rely on the last, largest pedicle. This improves the flow through this route, creating a sump that facilitates penetration into the vein when the large pedicle is injected. Better results are also seen when the fistula can be treated through the meningeal arterial supply rather than the extracranial arterial system. Nonmeningeal external carotid arterial supply to DAVFs (from the superficial temporal or occipital arteries) must penetrate the skull via transosseous branches. These vessels can have submillimeter calibers and be extremely tortuous, making penetration with even dilute liquid embolics problematic.17 This follows from observations that closure of a fistula is more likely if the microcatheter can be positioned immediately adjacent to the fistula, which by definition is on the inner side of the calvarium. High-flow fistulas present a challenge to TAE because of the rapid transition from arterial to venous flow across the fistulous point. Even relatively concentrated or high-density liquid embolics may be sucked into the venous circulation without occlusion of the connection. Strategies including balloon occlusion of the feeding artery,18 coil embolization of the feeding artery, or balloon and coil embolization of the venous outflow before liquid embolic embolizations have been used and described. Complications in TAE include catheter retention, embolization to normal vascular structures, reflux, and incomplete embolization, which may limit access in future procedures. A careful understanding of the fistula, its venous outflow, and the unaffected normal venous drainage is necessary before TVE is attempted. TVE requires selective retrograde catheterization of the
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proximal venous side of the fistula. With the distal microcatheter tip in the venous outflow pouch, embolic agents are placed to occlude and disconnect the fistulous venous outflow from the normal venous drainage of the brain. This is a distinctly different strategy from treating arteriovenous malformations for which the goal is not to occlude venous outflow because this could result in arteriovenous malformation rupture. Care must be taken to avoid occlusion of the normal (not associated with the fistula) venous outflow or cortical veins. The transvenous approach is useful in large, complex DAVFs when a portion of the normal draining dural sinus has become diseased and isolated from the normal venous anatomy, as may happen in a sinus or internal jugular venous occlusion. In these cases, the affected portion of the sinus drains only the fistula with the remaining normal venous outflow of the brain occurring through other venous routes. In these cases, the pathological portion of the sinus can usually be safely occluded without affecting the normal venous outflow of the brain.19,20 Venous occlusive disease may completely isolate the pathological sinus segment from the normal venous sinuses. It is sometimes possible to pass a microcatheter through these occlusions.21 We not infrequently find transvenous approaches necessary and effective in cases when fistulas have been previously incompletely treated through transarterial routes, leaving multiple small, difficult-toaccess arteries feeding the fistula.
Some patients lack adequate femoral transarterial or transvenous approaches because of proximal vessel tortuosity, previous unsuccessful embolization attempts, or venous occlusive disease. Alternative percutaneous arterial approaches include transradial,22 transcarotid, or direct puncture of a cavernous or ophthalmic fistula through the orbit. Venous access alternatives include the facial vein, angular vein, or superior ophthalmic vein via the femoral vein; direct transorbital or transforamen ovale puncture of the cavernous sinus presents another option.23,24 Minimally invasive surgical procedures can also allow more direct access to a DAVF. A stereotactically placed burr hole can allow direct puncture of a cortical draining vein or the fistula itself.25,26 Another option requires direct surgical cut-down to expose a vessel for more proximal access to a fistula. Cut-down to the superior division of the ophthalmic vein via a small incision on the eyelid can be performed safely in the angiography suite by an ophthalmologist.27 When any percutaneous transorbital approach is considered, it is advisable to keep an ophthalmologist immediately available to perform a lateral canthotomy (and possible inferior/superior cantholysis) should the patient develop a retro-orbital hematoma. These multidisciplinary, hybrid procedures are individualized to the patient’s fistula anatomy and offer nontraditional solutions for difficult and complex DAVFs that are not accessible via isolated traditional surgical or endovascular access (Figure 1).
FIGURE 1. A, an indirect cavernous carotid fistula in a patient with visual loss, proptosis, chemosis, and cranial neuropathy draining via the superior ophthalmic vein. The arterial supply to the fistula is via multiple branches of the external carotid artery: artery of foramen rotundum (black arrow) and accessory meningeal (yellow arrow), as well as the inferior lateral trunk (blue arrow) from the internal carotid artery. B, microcatheter injection from the accessory meningeal artery demonstrates connection to the cavernous sinus with drainage to the ophthalmic vein. C, a balloon is inflated to prevent reflux into the internal carotid artery before n-butyl cyanoacrylate (NBCA) injection (D, white arrows). E, despite penetration of the fistula with NBCA, persistent filling from an inferior lateral trunk is observed. It was not possible to catheterize this branch. F, direct cut-down on the superior ophthalmic vein through the eyelid allows catheterization with a microcatheter. G, venous injection shows intraluminal catheter placement before coil embolization of the vein (H and I). J, complete closure of the fistula.
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ENDOVASCULAR TREATMENT OF INTRACRANIAL DAVFs
Once the DAVF is successfully accessed, treatment can proceed with liquid embolics alone or in combination with adjuncts such as coils or balloons. Although coils can be used as the sole embolic device via a traditional transvenous approach, more recent techniques use their ability to improve the successful application of liquid embolics. By decreasing the blood flow through a DAVF, coils facilitate the controlled delivery of liquid embolics into the fistula. Coils also serve as a foundation or nest to capture and limit the distal flow of the polymerizing liquid embolic agent, thereby protecting the origin of vessels with known collaterals to vital structures (retina, cranial nerves, etc). A more direct method for protecting vessels from undesired embolization involves deployment of an endovascular balloon.28 Balloons can be deployed in venous structures when patency outside the fistulous connection must be maintained. In such cases, the balloon is advanced through a transvenous approach and inflated in the sinus, occluding the fistulous connection. The liquid embolic is then applied into the fistula from a transarterial approach. Once polymerization of the embolic is complete, the balloon can be taken down, preserving the sinus. Alternatively, a balloon can be temporarily deployed distal to the site of transarterial liquid embolic application, providing additional protection of normal vascular anatomy from incidental iatrogenic occlusion. Recent advances in occlusive balloons, in particular dual-lumen balloons (Sceptor, Terumo-Microvention, Inc, Tustin, California), allow the endovascular specialist to use a single catheter to inflate an occlusive balloon while at the same time delivering an embolic agent through the distal tip of the microcatheter.29 NBCA Treatment The liquid embolic agent NBCA (Trufill, Codman & Shurtleff, Raynham, Massachusetts) is delivered via manual injection through a specially purposed microcatheter designed to be compatible with the compound. Commonly referred to as glue, NBCA has adhesive properties, and the liquid form rapidly polymerizes after interaction with the ionic components of blood. Polymerization results in thrombosis and vessel occlusion, which can result in fistula cure if NBCA penetrates the fistula into the venous side from a transarterial approach or completely occludes the venous outflow from a transvenous approach. NBCA received US Food and Drug Administration approval in 2000, and its approved indication is for the preoperative treatment of brain arteriovenous malformations. The use of NBCA in the treatment of DAVF is off-label. The Trufill NBCA package is supplied with containers of NBCA, ethiodized oil, and tantalum powder. NBCA is not injected as a pure solution but is typically mixed with ethiodized oil, which is a radiopaque substance that dilutes the glue and aids in visualization during the embolization procedure. The amount of ethiodized oil added to the mixture has direct effects on the rate of NBCA polymerization (dilute NBCA polymerizes slowly; less dilute NBCA polymerizes more quickly). The endovascular operator varies the ratio of ethiodized oil to NBCA, depending
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on the rate of flow through a fistula and the distance the compound must travel (from the microcatheter tip to the fistulous connection). There are no published guidelines that standardize these ratios, so the determination of the appropriate concentration required to obtain penetration through the fistula before polymerization is usually based on operator experience. In high-flow fistulas, little ethiodized oil is added (a ratio of # 1:1), and in slowflow fistulas or when the NBCA needs to travel farther to reach the fistula, more ethiodized oil is added (ie, ratio of 8:1). In very-high-flow fistulas that require rapid polymerization and little ethiodized oil is added, tantalum powder can be added to the mixture to improve radiopaque visualization during embolization. Dextrose 5% solutions (which minimize the ionic interaction) are used to flush the catheter before NBCA injections and can be infused before or concurrently with NBCA through a guide catheter to increase NBCA penetration distance.30 Multiple case series and individual reports have documented the safe, durable, and effective use of NBCA in the treatment of DAVFs.31-33 Because DAVFs are a relatively rare entity, these case series are small, ranging from 2 to 42 patients. Cure rates of 63% (7 of 11 patients) were seen in anterior cranial fossa lesions,13 in 81% (34 of 42 patients) of all lesions treated at a single institution (with elimination of cortical venous reflux in the remaining 12 patients),31 and in 100% (5 of 5 patients) in a case series using only glue as the primary embolic agent.34 Delayed closure of fistula after incomplete treatment with NBCA has also been described.35 In one of the largest series of patients with DAVF using NBCA in combination with other adjunctive techniques, Kirsch et al36 described 150 patients managed with endovascular intervention alone. TAE achieved an initial angiographic cure in 30% and TVE an initial cure in 81%. In cases when TAE and TVE were combined, 54% of patients showed no residual shunting at the conclusion of the procedure; however, in those patients with a follow-up angiogram, 88% of fistulas with residual flow were found to be completely occluded. Onyx Onyx (ev3 Neurovascular) received Food and Drug Administration approval in 2005 for the preoperative treatment of brain arteriovenous malformations. Similar to the use of NBCA, the use of Onyx in the treatment of DAVFs is off-label but has also been established as safe and effective and is considered a standard of care. The transarterial application of Onyx follows the same technical principles as for NBCA. Onyx is available in 3 different viscosities, 2 of which are used in the treatment of fistulas: Onyx 18 (6% ethylene vinyl alcohol) and Onyx 34 (8% ethylene vinyl alcohol). Vessel occlusion into the early venous phase serves as the end point of embolic injection. The wedged or occlusive catheter technique, as described for NBCA,14 provides the ideal flow-arrest state for controlled embolization. In contrast to the adhesive properties of NBCA, Onyx has cohesive properties that allow slow, controlled application, without fragmentation in normal or arrested hemodynamic states. Theoretically, the cohesive properties of
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Onyx should offer a benefit over NBCA, but only noninferiority in the treatment of brain arteriovenous malformations (not DAVFs) has been statistically demonstrated.37 Patient selection for TAE with Onyx is critical: DAVFs with cortical venous reflux but without drainage into a patent sinus maximize clinical benefit while minimizing the risk of embolic complications.
With these selection criteria, the first prospective report using TAE with Onyx achieved complete cure in 23 of 25 DAVFs.38 Subsequent studies with less selective criteria for treatment support a cure rate between 63% and 100% with TAE alone.39-41 Cure was achieved most frequently without adjunctive measures when the middle meningeal artery was the primary feeding vessel to the DAVF. Early results for DAVF treated with Onyx show
FIGURE 2. A and B, anteroposterior and lateral views of a right-sided injection of a dural arteriovenous fistula in a patient with progressive encephalopathy. C, contribution is also observed from the left external carotid artery via the meningeal and transosseous branches. D, microcatheter injection of the fistula after cannulation of the right occipital artery. E and F, anteroposterior and lateral views of the Onyx cast after multiple pedicle embolizations. G and H, no further filling is observed after injection of either the right or left external carotid artery.
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potential for higher cure rates than have previously been achieved. A single-center study evaluating DAVF occlusion rates before and after the advent of Onyx demonstrated an increase in cure from 27% to 65% (Figure 2).42 Retrograde embolization with Onyx from an involved sinus to the arterial pedicles has been described.43 The advantage of this technique is the ability to potentially embolize multiple arterial feeders through a single point of venous access with the desired result of closing all of the fistulous connections. Injecting Onyx against the flow of the fistula is technically challenging, and the tendency of the compound to follow the direction of flow is one of the limitations for its use in the transvenous approach. Deploying coils into the sinus before injecting Onyx serves the purpose of slowing blood flow through the fistula and providing a framework onto which Onyx can precipitate in a large venous channel. Complete cure with a combination of coils and Onyx can usually be achieved.44,45 TVE without the use of coils has been accomplished in select cases. Zenteno et al46 report a series of 5 carotid-cavernous fistula cases treated via an endovascular approach, one of which was successfully treated with TVE using Onyx while using a transarterial balloon to occlude the internal carotid artery. Arat et al47 report successful embolization of a carotid-cavernous fistula with Onyx alone using real-time angiography rather than balloon protection of the internal carotid artery. When contending with complex DAVFs fed by multiple arterial pedicles, complete obliteration of all pedicles via a transarterial application of Onyx may not be technically feasible. In such cases, TVE provides an additional route to the remaining feeders and can result in higher overall occlusion rates. Abud et al39 report a 79.5% cure rate with TAE alone, but by following with TVE using coils plus Onyx, they achieved a cure in 90.9% of patients, and the further addition of open surgery boosted the cure rate to 100%. Similarly, Hu et al48 used TAE with Onyx in 50 of 76 consecutive embolization procedures but required application of NBCA, coils, stents, or a transvenous approach in the remaining procedures. Other groups have also used combined techniques with similar results.49 Transarterial or transvenous balloon occlusion serves as a useful adjunct in technically challenging DAVFs.28 Endovascular treatment of DAVF with Onyx carries a complication rate of 8% to 15% with a permanent morbidity of 2% and a mortality of 0%,41,48 comparable to pre-Onyx endovascular complication rates.36,50 This complication rate reflects treatment of all DAVF subtypes with all available endovascular techniques. Not all complications result in clinically appreciable deficits but also include technical failures during the procedure itself. The most frequent clinically significant complication is unique to the treatment of cavernous DAVFs: cranial nerve palsy. Fortunately, such palsies typically improve with time and are rare causes of permanent morbidity. Thromboembolic complications cause most lasting symptomatic deficits. Both arterial and venous strokes have been reported, often without a causative technical failure. A recent case report describes massive postprocedural venous thrombosis thought to be secondary to venous stasis in particularly large venous varices.51 Although it
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is feasible that postprocedural heparinization may lower the risk of infarct from venous thrombosis, the risks of systemic anticoagulation in a dramatically altered hemodynamic state after occlusion of a DAVF must be weighed carefully. Technical failures associated with endovascular treatment of DAVFs include migration of Onyx, migration of adjunctive coils, and microcatheter fracture. As with most novel technical approaches, the application of Onyx has a learning curve. When the microcatheter is removed at the end of Onyx application, it is critical to apply only delicate tension. If a tip fractures or the embolic migrates, both securing the fragment to the vessel wall with a stent48 and endovascular retrieval of the fragment have been successful.52 The middle meningeal artery may provide a safer route for Onyx embolization as a result of both ease of access and the ability of the artery to resist tension during withdrawal of the microcatheter because the artery is anchored in bone and dura.
CONCLUSION Endovascular treatment represents the primary therapy for treatment of DAVF, regardless of anatomic subtype. The advancement of endovascular techniques has enabled successful treatment of these lesions via transarterial or transvenous routes. When both approaches are combined or they are modified with minor surgical access or direct puncture procedures, most complex DAVF can be treated safely via endovascular procedures, and few require large open surgical treatment or radiosurgery. The liquid embolics NBCA and Onyx are useful for off-label treatment of DAVFs, and cure rates using different approaches with these devices appear to be improving with operator familiarity with them. DAVF is a catch-all term for a diverse array of vascular malformations with different clinical, anatomic, and radiographic presentations. Standardization of approaches to these lesions is problematic, and pooled institutional studies are necessary to move the quality of treatment and outcome data beyond case series. Successful endovascular treatment will continue to rely on operator experience and familiarity with embolic devices, as well as tailoring the approach to each individual patient’s lesion. A podcast associated with this article can be accessed online (http://links.lww.com/NEU/A589). Disclosure Dr Arthur has served as a consultant for Codman, Covidien, Microvention, and Stryker. Dr Elijovich has served as a consultant for Microvention. Dr Hoit has served as a proctor for Covidien. The other authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
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3. Cognard C, Casasco A, Toevi M, Houdart E, Chiras J, Merland JJ. Dural arteriovenous fistulas as a cause of intracranial hypertension due to impairment of cranial venous outflow. J Neurol Neurosurg Psychiatry. 1998;65(3):308-316. 4. Hurst RW, Bagley LJ, Galetta S, et al. Dementia resulting from dural arteriovenous fistulas: the pathologic findings of venous hypertensive encephalopathy. AJNR Am J Neuroradiol. 1998;19(7):1267-1273. 5. Kakarla UK, Deshmukh VR, Zabramski JM, Albuquerque FC, McDougall CG, Spetzler RF. Surgical treatment of high-risk intracranial dural arteriovenous fistulae: clinical outcomes and avoidance of complications. Neurosurgery. 2007;61 (3):447-457; discussion 457-459. 6. Nogueira RG, Baccin CE, Rabinov JD, Pryor JC, Buonanno FS, Hirsch JA. Reversible parkinsonism after treatment of dural arteriovenous fistula. J Neuroimaging. 2009;19(2):183-184. 7. Benndorf G, Schmidt S, Sollmann WP, Kroppenstedt SN. Tentorial dural arteriovenous fistula presenting with various visual symptoms related to anterior and posterior visual pathway dysfunction: case report. Neurosurgery. 2003;53(1): 222-226; discussion 226-227. 8. Davies MA, Ter Brugge K, Willinsky R, Wallace MC. The natural history and management of intracranial dural arteriovenous fistulae, part 2: aggressive lesions. Interv Neuroradiol. 1997;3(4):303-311. 9. Zipfel GJ, Shah MN, Refai D, Dacey RG Jr, Derdeyn CP. Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus. 2009;26(5):E14. 10. Satomi J, van Dijk JM, Terbrugge KG, Willinsky RA, Wallace MC. Benign cranial dural arteriovenous fistulas: outcome of conservative management based on the natural history of the lesion. J Neurosurg. 2002;97(4):767-770. 11. Shah MN, Botros JA, Pilgram TK, et al. Borden-Shucart type I dural arteriovenous fistulas: clinical course including risk of conversion to higher-grade fistulas. J Neurosurg. 2012;117(3):539-545. 12. Jung KH, Kwon BJ, Chu K, et al. Clinical and angiographic factors related to the prognosis of cavernous sinus dural arteriovenous fistula. Neuroradiology. 2011;53 (12):983-992. 13. Agid R, Terbrugge K, Rodesch G, Andersson T, Söderman M. Management strategies for anterior cranial fossa (ethmoidal) dural arteriovenous fistulas with an emphasis on endovascular treatment. J Neurosurg. 2009;110(1):79-84. 14. Nelson PK, 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. J Neurosurg. 2003;98(3):498-506. 15. Iizuka Y, Maehara T, Hishii M, Miyajima M, Arai H. Successful transarterial glue embolisation by wedged technique for a tentorial dural arteriovenous fistula presenting with a conjunctival injection. Neuroradiology. 2001;43(8):677-679. 16. Russell SM, Woo HH, Nelson PK. Transarterial wedged-catheter, flow-arrest, n-butyl cyanoacrylate embolization of three dural arteriovenous fistulae in a single patient. Interv Neuroradiol. 2003;9(3):283-290. 17. Jung C, Kwon BJ, Kwon OK, et al. Intraosseous cranial dural arteriovenous fistula treated with transvenous embolization. AJNR Am J Neuroradiol. 2009; 30(6):1173-1177. 18. Andreou A, Ioannidis I, Nasis N. Transarterial balloon-assisted glue embolization of high-flow arteriovenous fistulas. Neuroradiology. 2008;50(3):267-272. 19. Mironov A. Selective transvenous embolization of dural fistulas without occlusion of the dural sinus. AJNR Am J Neuroradiol. 1998;19(2):389-391. 20. Agid R, Willinsky RA, Haw C, Souza MP, Vanek IJ, terBrugge KG. Targeted compartmental embolization of cavernous sinus dural arteriovenous fistulae using transfemoral medial and lateral facial vein approaches. Neuroradiology. 2004;46(2): 156-160. 21. Naito I, Iwai T, Shimaguchi H, et al. Percutaneous transvenous embolisation through the occluded sinus for transverse-sigmoid dural arteriovenous fistulas with sinus occlusion. Neuroradiology. 2001;43(8):672-676. 22. Eskioglu E, Burry MV, Mericle RA. Transradial approach for neuroendovascular surgery of intracranial vascular lesions. J Neurosurg. 2004;101(5):767-769. 23. Benndorf G, Campi A, Hell B, Hölzle F, Lund J, Bier J. Endovascular management of a bleeding mandibular arteriovenous malformation by transfemoral venous embolization with NBCA. AJNR Am J Neuroradiol. 2001;22(2): 359-362. 24. Kim MJ, Shin YS, Ihn YK, et al. Transvenous embolization of cavernous and paracavernous dural arteriovenous fistula through the facial vein: report of 12 cases. Neurointervention. 2013;8(1):15-22.
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25. Chaudhary N, Lownie SP, Bussière M, Pelz DM, Nicolle D. Transcortical venous approach for direct embolization of a cavernous sinus dural arteriovenous fistula: technical case report. Neurosurgery. 2012;70(2 suppl operative):343-348. 26. Houdart E, Saint-Maurice JP, Chapot R, et al. Transcranial approach for venous embolization of dural arteriovenous fistulas. J Neurosurg. 2002;97(2): 280-286. 27. Miller NR, Monsein LH, Debrun GM, Tamargo RJ, Nauta HJ. Treatment of carotid-cavernous sinus fistulas using a superior ophthalmic vein approach. J Neurosurg. 1995;83(5):838-842. 28. Shi ZS, Loh Y, Duckwiler GR, Jahan R, Viñuela F. Balloon-assisted transarterial embolization of intracranial dural arteriovenous fistulas. J Neurosurg. 2009;110(5): 921-928. 29. Jagadeesan BD, Grigoryan M, Hassan AE, Grande AW, Tummala RP. Endovascular balloon-assisted embolization of intracranial and cervical arteriovenous malformations using dual lumen co-axial balloon microcatheters and Onyx: initial experience [published online ahead of print February 25, 2013]. Neurosurgery. doi:10.1227/NEU.0b013e31828d602b. 30. Moore C, Murphy K, Gailloud P. Improved distal distribution of n-butyl cyanoacrylate glue by simultaneous injection of dextrose 5% through the guiding catheter: technical note. Neuroradiology. 2006;48(5):327-332. 31. Guedin P, Gaillard S, Boulin A, et al. Therapeutic management of intracranial dural arteriovenous shunts with leptomeningeal venous drainage: report of 53 consecutive patients with emphasis on transarterial embolization with acrylic glue. J Neurosurg. 2010;112(3):603-610. 32. Kiyosue H, Hori Y, Okahara M, et al. Treatment of intracranial dural arteriovenous fistulas: current strategies based on location and hemodynamics, and alternative techniques of transcatheter embolization. Radiographics. 2004;24 (6):1637-1653. 33. Tomak PR, Cloft HJ, Kaga A, Cawley CM, Dion J, Barrow DL. Evolution of the management of tentorial dural arteriovenous malformations. Neurosurgery. 2003; 52(4):750-760; discussion 760-762. 34. Liu HM, Huang YC, Wang YH, Tu YK. Transarterial embolisation of complex cavernous sinus dural arteriovenous fistulae with low-concentration cyanoacrylate. Neuroradiology. 2000;42(10):766-770. 35. Fok KF, Agid R, Souza MP, terBrugge KG. Thrombosis of aggressive dural arteriovenous fistula after incomplete embolization. Neuroradiology. 2004;46(12): 1016-1021. 36. Kirsch M, Liebig T, Kühne D, Henkes H. Endovascular management of dural arteriovenous fistulas of the transverse and sigmoid sinus in 150 patients. Neuroradiology. 2009;51(7):477-483. 37. Loh Y, Duckwiler GR. A prospective, multicenter, randomized trial of the Onyx liquid embolic system and N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations: clinical article. J Neurosurg. 2010;113(4):733-741. 38. Cognard C, Januel AC, Silva NA Jr, Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol. 2008;29(2):235-241. 39. Abud TG, Nguyen A, Saint-Maurice JP, et al. The use of Onyx in different types of intracranial dural arteriovenous fistula. AJNR Am J Neuroradiol. 2011;32(11): 2185-2191. 40. van Rooij WJ, Sluzewski M. Curative embolization with Onyx of dural arteriovenous fistulas with cortical venous drainage. AJNR Am J Neuroradiol. 2010;31(8):1516-1520. 41. Stiefel MF, Albuquerque FC, Park MS, Dashti SR, McDougall CG. Endovascular treatment of intracranial dural arteriovenous fistulae using Onyx: a case series. Neurosurgery. 2009;65(6 suppl):132-139; discussion 139-140. 42. Macdonald JH, Millar JS, Barker CS. Endovascular treatment of cranial dural arteriovenous fistulae: a single-centre, 14-year experience and the impact of Onyx on local practise. Neuroradiology. 2010;52(5):387-395. 43. Albuquerque FC, Ducruet AF, Crowley RW, Bristol RE, Ahmed A, McDougall CG. Transvenous to arterial Onyx embolization [published online ahead of print March 6, 2013]. J Neurointerv Surg. doi:10.1136/neurintsurg-2012010628. 44. Bhatia KD, Wang L, Parkinson RJ, Wenderoth JD. Successful treatment of six cases of indirect carotid-cavernous fistula with ethylene vinyl alcohol copolymer (Onyx) transvenous embolization. J Neuroophthalmol. 2009;29(1):3-8. 45. Suzuki S, Lee DW, Jahan R, Duckwiler GR, Viñuela F. Transvenous treatment of spontaneous dural carotid-cavernous fistulas using a combination of detachable coils and Onyx. AJNR Am J Neuroradiol. 2006;27(6):1346-1349.
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46. Zenteno M, Santos-Franco J, Rodríguez-Parra V, et al. Management of direct carotid-cavernous sinus fistulas with the use of ethylene-vinyl alcohol (Onyx) only: preliminary results. J Neurosurg. 2010;112(3):595-602. 47. Arat A, Cekirge S, Saatci I, Ozgen B. Transvenous injection of Onyx for casting of the cavernous sinus for the treatment of a carotid-cavernous fistula. Neuroradiology. 2004;46(12):1012-1015. 48. Hu YC, Newman CB, Dashti SR, Albuquerque FC, McDougall CG. Cranial dural arteriovenous fistula: transarterial Onyx embolization experience and technical nuances. J Neurointerv Surg. 2011;3(1):5-13. 49. Natarajan SK, Ghodke B, Kim LJ, Hallam DK, Britz GW, Sekhar LN. Multimodality treatment of intracranial dural arteriovenous fistulas in the Onyx era: a single center experience. World Neurosurg. 2010;73(4):365-379. 50. Tsumoto T, Terada T, Tsuura M, et al. Analysis of complications related to endovascular therapy for dural arteriovenous fistulae. Interv Neuroradiol. 2004;10(suppl 1):121-125.
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51. Gonzalez LF, Chalouhi N, Jabbour P, Teufack S, Albuquerque FC, Spetzler RF. Rapid and progressive venous thrombosis after occlusion of high-flow arteriovenous fistula [published online ahead of print October 24, 2012]. World Neurosurg. doi:10.1016/j.wneu.2012.10.043. 52. Alamri A, Hyodo A, Suzuki K, et al. Retrieving microcatheters from Onyx casts in a series of brain arteriovenous malformations: a technical report. Neuroradiology. 2012;54(11):1237-1240.
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TOPIC
Endovascular Treatment of Intracranial Dural Arteriovenous Fistulas Matthew VanLandingham, MD Benjamin Fox, MD Daniel Hoit, MD, MPH Lucas Elijovich, MD Adam S. Arthur, MD, MPH Semmes-Murphey Clinic, Department of Neurosurgery, University of Tennessee, Memphis, Tennessee Correspondence: Adam S. Arthur, MD, MPH, FAANS, FACS, Semmes-Murphey Clinic, 6325 Humphreys Blvd, Memphis, TN 38120. E-mail: [email protected] Received, June 18, 2013. Accepted, September 17, 2013. Copyright © 2014 by the Congress of Neurological Surgeons
Endovascular treatment options for dural arteriovenous fistulas (DAVFs) have vastly expanded and become progressively safer in the last several years. Angiographic imaging systems have improved, catheter technology has advanced, and liquid embolic and coil options have increased. As a likely result, an increasing proportion of DAVFs are treated via an endovascular approach. In addition to allowing physicians to appreciate and treat lesions better, varied approaches have been developed. The “plug and push” technique and the new availability of dimethyl sulfoxide–compatible dual lumen balloons have allowed safer and more thorough transarterial treatments. Transvenous treatment has proved to be a valuable technique for some lesions. Hybrid approaches with surgical assisted access to vascular structures have been successfully used to treat more challenging fistulas. KEY WORDS: Dural arteriovenous fistula, Endovascular techniques, Therapeutic embolization Neurosurgery 74:S42–S49, 2014
DOI: 10.1227/NEU.0000000000000180
D
ural arteriovenous fistulas (DAVFs) are pathological shunts between meningeal or extracranial arteries and the dural venous sinuses, dural veins, or cortical veins. They are classified by the Borden-Shucart or Cognard schemes (Table), which describe the patterns of cerebral venous drainage and the patency of the dural venous system.1,2 Highergrade lesions (Borden-Shucart 2-3; Cognard IIb, IIa1b, and III-V) are more likely to become symptomatic with cranial neuropathies, visual loss, retro-orbital pain, and chemosis/proptosis with cavernous/paracavernous and tentorial DAVFs, and pulsatile tinnitus, encephalopathy, parkinsonism, and cerebellar dysfunction with transverse sigmoid sinus DAVFs.3-7 Additionally, higher-grade and symptomatic fistulas are more likely to present with intracranial hemorrhage. The Borden-Shucart classification scheme also takes into account the number of arterial connections in the fistula (single vs multiple). ABBREVIATIONS: DAVF, dural arteriovenous fistula; NBCA, n-butyl cyanoacrylate; TAE, transarterial embolization; TVE, transvenous embolization Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.neurosurgery-online.com).
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The decision to treat a DAVF is based on an analysis of the patient’s symptoms, medical comorbidities, and risk of intracranial hemorrhage. Asymptomatic, low-grade DAVFs pose minimal risk of hemorrhage and generally warrant only close observation.8-11 High-grade DAVFs with cortical venous reflux or intolerably symptomatic DAVF may be considered candidates for treatment.5,12 The goal of any DAVF treatment is obliteration of the fistulous connection between the arterial and venous systems. The endovascular correlate to surgical disconnection of an artery and vein is the presence of embolic material on both the arterial and venous side in close proximity to the fistulous connection. Complete endovascular obliteration typically results in a lasting cure. Incomplete treatment of a fistula can allow recruitment of new arterial blood supply to the lesion and may not improve symptoms or lower the risk of intracranial hemorrhage. If endovascular treatment is excluded because of the anatomy of the DAVF or fails to produce complete obliteration, hybrid open/endovascular, open surgical intervention, or stereotactic radiosurgery may be considered.13 Endovascular approaches to treatment of DAVFs have evolved with our understanding of the pathogenesis and angioarchitecture of these lesions. Advancements in catheter and embolic technology have also made endovascular therapy more effective. Disconnection of the arteriovenous
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ENDOVASCULAR TREATMENT OF INTRACRANIAL DAVFs
TABLE. Borden-Shucart and Cognard Classifications Borden-Shucart classification 1 2 3 Cognard classification I IIa IIb IIa1b III IV V
Venous drainage directly into dural venous sinus or meningeal vein Venous drainage into dural venous sinus with cortical venous reflux Venous drainage directly into subarachnoid veins (cortical venous reflux only) Venous drainage into dural venous sinus with antegrade flow Venous drainage into dural venous sinus with retrograde flow Venous drainage into dural venous sinus with antegrade flow and cortical venous reflux Venous drainage into dural venous sinus with retrograde flow and cortical venous reflux Venous drainage directly into subarachnoid veins (cortical venous reflux only) Type III with venous ectasias of the draining subarachnoid veins Direct drainage into spinal perimedullary veins
shunt may be complicated by the presence of multiple arterial feeders (Borden-Shucart), long segments of affected venous sinus, or isolation of a venous sinus segment owing to occlusive venopathy. Endovascular approaches allow continuous evaluation of the arteriovenous shunt over the course of the procedure and have become the primary modality for treatment. Transvenous, transarterial, direct access, or a combination of these approaches is often necessary for complete cure of a fistula. Liquid embolics, including nbutyl cyanoacrylate (NBCA, Cordis, Miami Lakes, Florida), ethylene vinyl alcohol copolymer (Onyx, ev3, Irvine, California), and coil occlusion, all have a role in complete closure of the arteriovenous shunt. The purpose of this review is to describe the major current strategies for the endovascular treatment of DAVFs that have evolved with improvements in endovascular technology.
APPROACHES TO DAVF EMBOLIZATION Improvements in microcatheters and wires, biplane angiographic image resolution, 3-dimensional rotational imaging with software-enhanced postprocessing, coil technology, and liquid embolic agents (NBCA and Onyx) have made transarterial embolization (TAE) and transvenous embolization (TVE) of DAVFs possible. TAE requires selective catheterization of a distal arterial feeding pedicle and placement of the microcatheter tip as close to the fistulous connection as possible.14-16 The advantages of transfemoral transarterial treatment are the familiarity and ease of endovascular navigation compared with transvenous access. Complete treatment requires penetration of the embolic agent through the arterial feeding vessel into the venous outflow pouch to ensure obliteration of the fistulous connection. Distal placement of the microcatheter can be limited by tortuosity of the feeding artery and distance to the site of the fistula. The transarterial approach is usually effective in small DAVFs and those that have associated venous occlusions or significant venous stenosis, which may limit a transvenous approach. The treatment of large, complex DAVFs is also possible via the transarterial route but may require access of multiple arterial pedicles to completely occlude the fistula and may need to be
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staged over multiple procedures to limit contrast and radiation exposure. Coils are generally not useful as a primary embolic agent in the transarterial approach because the coils stay on the arterial side, whereas liquid embolic agents have the ability to pass through small tortuous end arteries into the venous side. In complex DAVFs that require multiple pedicle catheterization, we have found that saving the most direct, closest access for last improves the chance of success. Unfortunately, incompletely treated DAVFs often recanalize. There are many cases in which a patient has been told that the fistula has been “80%” or “90%” treated, leaving an intact shunt that can recruit additional arterial supply. We prefer to “prune” off the smaller arterial supply first, which causes the DAVF to rely on the last, largest pedicle. This improves the flow through this route, creating a sump that facilitates penetration into the vein when the large pedicle is injected. Better results are also seen when the fistula can be treated through the meningeal arterial supply rather than the extracranial arterial system. Nonmeningeal external carotid arterial supply to DAVFs (from the superficial temporal or occipital arteries) must penetrate the skull via transosseous branches. These vessels can have submillimeter calibers and be extremely tortuous, making penetration with even dilute liquid embolics problematic.17 This follows from observations that closure of a fistula is more likely if the microcatheter can be positioned immediately adjacent to the fistula, which by definition is on the inner side of the calvarium. High-flow fistulas present a challenge to TAE because of the rapid transition from arterial to venous flow across the fistulous point. Even relatively concentrated or high-density liquid embolics may be sucked into the venous circulation without occlusion of the connection. Strategies including balloon occlusion of the feeding artery,18 coil embolization of the feeding artery, or balloon and coil embolization of the venous outflow before liquid embolic embolizations have been used and described. Complications in TAE include catheter retention, embolization to normal vascular structures, reflux, and incomplete embolization, which may limit access in future procedures. A careful understanding of the fistula, its venous outflow, and the unaffected normal venous drainage is necessary before TVE is attempted. TVE requires selective retrograde catheterization of the
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proximal venous side of the fistula. With the distal microcatheter tip in the venous outflow pouch, embolic agents are placed to occlude and disconnect the fistulous venous outflow from the normal venous drainage of the brain. This is a distinctly different strategy from treating arteriovenous malformations for which the goal is not to occlude venous outflow because this could result in arteriovenous malformation rupture. Care must be taken to avoid occlusion of the normal (not associated with the fistula) venous outflow or cortical veins. The transvenous approach is useful in large, complex DAVFs when a portion of the normal draining dural sinus has become diseased and isolated from the normal venous anatomy, as may happen in a sinus or internal jugular venous occlusion. In these cases, the affected portion of the sinus drains only the fistula with the remaining normal venous outflow of the brain occurring through other venous routes. In these cases, the pathological portion of the sinus can usually be safely occluded without affecting the normal venous outflow of the brain.19,20 Venous occlusive disease may completely isolate the pathological sinus segment from the normal venous sinuses. It is sometimes possible to pass a microcatheter through these occlusions.21 We not infrequently find transvenous approaches necessary and effective in cases when fistulas have been previously incompletely treated through transarterial routes, leaving multiple small, difficult-toaccess arteries feeding the fistula.
Some patients lack adequate femoral transarterial or transvenous approaches because of proximal vessel tortuosity, previous unsuccessful embolization attempts, or venous occlusive disease. Alternative percutaneous arterial approaches include transradial,22 transcarotid, or direct puncture of a cavernous or ophthalmic fistula through the orbit. Venous access alternatives include the facial vein, angular vein, or superior ophthalmic vein via the femoral vein; direct transorbital or transforamen ovale puncture of the cavernous sinus presents another option.23,24 Minimally invasive surgical procedures can also allow more direct access to a DAVF. A stereotactically placed burr hole can allow direct puncture of a cortical draining vein or the fistula itself.25,26 Another option requires direct surgical cut-down to expose a vessel for more proximal access to a fistula. Cut-down to the superior division of the ophthalmic vein via a small incision on the eyelid can be performed safely in the angiography suite by an ophthalmologist.27 When any percutaneous transorbital approach is considered, it is advisable to keep an ophthalmologist immediately available to perform a lateral canthotomy (and possible inferior/superior cantholysis) should the patient develop a retro-orbital hematoma. These multidisciplinary, hybrid procedures are individualized to the patient’s fistula anatomy and offer nontraditional solutions for difficult and complex DAVFs that are not accessible via isolated traditional surgical or endovascular access (Figure 1).
FIGURE 1. A, an indirect cavernous carotid fistula in a patient with visual loss, proptosis, chemosis, and cranial neuropathy draining via the superior ophthalmic vein. The arterial supply to the fistula is via multiple branches of the external carotid artery: artery of foramen rotundum (black arrow) and accessory meningeal (yellow arrow), as well as the inferior lateral trunk (blue arrow) from the internal carotid artery. B, microcatheter injection from the accessory meningeal artery demonstrates connection to the cavernous sinus with drainage to the ophthalmic vein. C, a balloon is inflated to prevent reflux into the internal carotid artery before n-butyl cyanoacrylate (NBCA) injection (D, white arrows). E, despite penetration of the fistula with NBCA, persistent filling from an inferior lateral trunk is observed. It was not possible to catheterize this branch. F, direct cut-down on the superior ophthalmic vein through the eyelid allows catheterization with a microcatheter. G, venous injection shows intraluminal catheter placement before coil embolization of the vein (H and I). J, complete closure of the fistula.
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ENDOVASCULAR TREATMENT OF INTRACRANIAL DAVFs
Once the DAVF is successfully accessed, treatment can proceed with liquid embolics alone or in combination with adjuncts such as coils or balloons. Although coils can be used as the sole embolic device via a traditional transvenous approach, more recent techniques use their ability to improve the successful application of liquid embolics. By decreasing the blood flow through a DAVF, coils facilitate the controlled delivery of liquid embolics into the fistula. Coils also serve as a foundation or nest to capture and limit the distal flow of the polymerizing liquid embolic agent, thereby protecting the origin of vessels with known collaterals to vital structures (retina, cranial nerves, etc). A more direct method for protecting vessels from undesired embolization involves deployment of an endovascular balloon.28 Balloons can be deployed in venous structures when patency outside the fistulous connection must be maintained. In such cases, the balloon is advanced through a transvenous approach and inflated in the sinus, occluding the fistulous connection. The liquid embolic is then applied into the fistula from a transarterial approach. Once polymerization of the embolic is complete, the balloon can be taken down, preserving the sinus. Alternatively, a balloon can be temporarily deployed distal to the site of transarterial liquid embolic application, providing additional protection of normal vascular anatomy from incidental iatrogenic occlusion. Recent advances in occlusive balloons, in particular dual-lumen balloons (Sceptor, Terumo-Microvention, Inc, Tustin, California), allow the endovascular specialist to use a single catheter to inflate an occlusive balloon while at the same time delivering an embolic agent through the distal tip of the microcatheter.29 NBCA Treatment The liquid embolic agent NBCA (Trufill, Codman & Shurtleff, Raynham, Massachusetts) is delivered via manual injection through a specially purposed microcatheter designed to be compatible with the compound. Commonly referred to as glue, NBCA has adhesive properties, and the liquid form rapidly polymerizes after interaction with the ionic components of blood. Polymerization results in thrombosis and vessel occlusion, which can result in fistula cure if NBCA penetrates the fistula into the venous side from a transarterial approach or completely occludes the venous outflow from a transvenous approach. NBCA received US Food and Drug Administration approval in 2000, and its approved indication is for the preoperative treatment of brain arteriovenous malformations. The use of NBCA in the treatment of DAVF is off-label. The Trufill NBCA package is supplied with containers of NBCA, ethiodized oil, and tantalum powder. NBCA is not injected as a pure solution but is typically mixed with ethiodized oil, which is a radiopaque substance that dilutes the glue and aids in visualization during the embolization procedure. The amount of ethiodized oil added to the mixture has direct effects on the rate of NBCA polymerization (dilute NBCA polymerizes slowly; less dilute NBCA polymerizes more quickly). The endovascular operator varies the ratio of ethiodized oil to NBCA, depending
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on the rate of flow through a fistula and the distance the compound must travel (from the microcatheter tip to the fistulous connection). There are no published guidelines that standardize these ratios, so the determination of the appropriate concentration required to obtain penetration through the fistula before polymerization is usually based on operator experience. In high-flow fistulas, little ethiodized oil is added (a ratio of # 1:1), and in slowflow fistulas or when the NBCA needs to travel farther to reach the fistula, more ethiodized oil is added (ie, ratio of 8:1). In very-high-flow fistulas that require rapid polymerization and little ethiodized oil is added, tantalum powder can be added to the mixture to improve radiopaque visualization during embolization. Dextrose 5% solutions (which minimize the ionic interaction) are used to flush the catheter before NBCA injections and can be infused before or concurrently with NBCA through a guide catheter to increase NBCA penetration distance.30 Multiple case series and individual reports have documented the safe, durable, and effective use of NBCA in the treatment of DAVFs.31-33 Because DAVFs are a relatively rare entity, these case series are small, ranging from 2 to 42 patients. Cure rates of 63% (7 of 11 patients) were seen in anterior cranial fossa lesions,13 in 81% (34 of 42 patients) of all lesions treated at a single institution (with elimination of cortical venous reflux in the remaining 12 patients),31 and in 100% (5 of 5 patients) in a case series using only glue as the primary embolic agent.34 Delayed closure of fistula after incomplete treatment with NBCA has also been described.35 In one of the largest series of patients with DAVF using NBCA in combination with other adjunctive techniques, Kirsch et al36 described 150 patients managed with endovascular intervention alone. TAE achieved an initial angiographic cure in 30% and TVE an initial cure in 81%. In cases when TAE and TVE were combined, 54% of patients showed no residual shunting at the conclusion of the procedure; however, in those patients with a follow-up angiogram, 88% of fistulas with residual flow were found to be completely occluded. Onyx Onyx (ev3 Neurovascular) received Food and Drug Administration approval in 2005 for the preoperative treatment of brain arteriovenous malformations. Similar to the use of NBCA, the use of Onyx in the treatment of DAVFs is off-label but has also been established as safe and effective and is considered a standard of care. The transarterial application of Onyx follows the same technical principles as for NBCA. Onyx is available in 3 different viscosities, 2 of which are used in the treatment of fistulas: Onyx 18 (6% ethylene vinyl alcohol) and Onyx 34 (8% ethylene vinyl alcohol). Vessel occlusion into the early venous phase serves as the end point of embolic injection. The wedged or occlusive catheter technique, as described for NBCA,14 provides the ideal flow-arrest state for controlled embolization. In contrast to the adhesive properties of NBCA, Onyx has cohesive properties that allow slow, controlled application, without fragmentation in normal or arrested hemodynamic states. Theoretically, the cohesive properties of
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Onyx should offer a benefit over NBCA, but only noninferiority in the treatment of brain arteriovenous malformations (not DAVFs) has been statistically demonstrated.37 Patient selection for TAE with Onyx is critical: DAVFs with cortical venous reflux but without drainage into a patent sinus maximize clinical benefit while minimizing the risk of embolic complications.
With these selection criteria, the first prospective report using TAE with Onyx achieved complete cure in 23 of 25 DAVFs.38 Subsequent studies with less selective criteria for treatment support a cure rate between 63% and 100% with TAE alone.39-41 Cure was achieved most frequently without adjunctive measures when the middle meningeal artery was the primary feeding vessel to the DAVF. Early results for DAVF treated with Onyx show
FIGURE 2. A and B, anteroposterior and lateral views of a right-sided injection of a dural arteriovenous fistula in a patient with progressive encephalopathy. C, contribution is also observed from the left external carotid artery via the meningeal and transosseous branches. D, microcatheter injection of the fistula after cannulation of the right occipital artery. E and F, anteroposterior and lateral views of the Onyx cast after multiple pedicle embolizations. G and H, no further filling is observed after injection of either the right or left external carotid artery.
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potential for higher cure rates than have previously been achieved. A single-center study evaluating DAVF occlusion rates before and after the advent of Onyx demonstrated an increase in cure from 27% to 65% (Figure 2).42 Retrograde embolization with Onyx from an involved sinus to the arterial pedicles has been described.43 The advantage of this technique is the ability to potentially embolize multiple arterial feeders through a single point of venous access with the desired result of closing all of the fistulous connections. Injecting Onyx against the flow of the fistula is technically challenging, and the tendency of the compound to follow the direction of flow is one of the limitations for its use in the transvenous approach. Deploying coils into the sinus before injecting Onyx serves the purpose of slowing blood flow through the fistula and providing a framework onto which Onyx can precipitate in a large venous channel. Complete cure with a combination of coils and Onyx can usually be achieved.44,45 TVE without the use of coils has been accomplished in select cases. Zenteno et al46 report a series of 5 carotid-cavernous fistula cases treated via an endovascular approach, one of which was successfully treated with TVE using Onyx while using a transarterial balloon to occlude the internal carotid artery. Arat et al47 report successful embolization of a carotid-cavernous fistula with Onyx alone using real-time angiography rather than balloon protection of the internal carotid artery. When contending with complex DAVFs fed by multiple arterial pedicles, complete obliteration of all pedicles via a transarterial application of Onyx may not be technically feasible. In such cases, TVE provides an additional route to the remaining feeders and can result in higher overall occlusion rates. Abud et al39 report a 79.5% cure rate with TAE alone, but by following with TVE using coils plus Onyx, they achieved a cure in 90.9% of patients, and the further addition of open surgery boosted the cure rate to 100%. Similarly, Hu et al48 used TAE with Onyx in 50 of 76 consecutive embolization procedures but required application of NBCA, coils, stents, or a transvenous approach in the remaining procedures. Other groups have also used combined techniques with similar results.49 Transarterial or transvenous balloon occlusion serves as a useful adjunct in technically challenging DAVFs.28 Endovascular treatment of DAVF with Onyx carries a complication rate of 8% to 15% with a permanent morbidity of 2% and a mortality of 0%,41,48 comparable to pre-Onyx endovascular complication rates.36,50 This complication rate reflects treatment of all DAVF subtypes with all available endovascular techniques. Not all complications result in clinically appreciable deficits but also include technical failures during the procedure itself. The most frequent clinically significant complication is unique to the treatment of cavernous DAVFs: cranial nerve palsy. Fortunately, such palsies typically improve with time and are rare causes of permanent morbidity. Thromboembolic complications cause most lasting symptomatic deficits. Both arterial and venous strokes have been reported, often without a causative technical failure. A recent case report describes massive postprocedural venous thrombosis thought to be secondary to venous stasis in particularly large venous varices.51 Although it
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is feasible that postprocedural heparinization may lower the risk of infarct from venous thrombosis, the risks of systemic anticoagulation in a dramatically altered hemodynamic state after occlusion of a DAVF must be weighed carefully. Technical failures associated with endovascular treatment of DAVFs include migration of Onyx, migration of adjunctive coils, and microcatheter fracture. As with most novel technical approaches, the application of Onyx has a learning curve. When the microcatheter is removed at the end of Onyx application, it is critical to apply only delicate tension. If a tip fractures or the embolic migrates, both securing the fragment to the vessel wall with a stent48 and endovascular retrieval of the fragment have been successful.52 The middle meningeal artery may provide a safer route for Onyx embolization as a result of both ease of access and the ability of the artery to resist tension during withdrawal of the microcatheter because the artery is anchored in bone and dura.
CONCLUSION Endovascular treatment represents the primary therapy for treatment of DAVF, regardless of anatomic subtype. The advancement of endovascular techniques has enabled successful treatment of these lesions via transarterial or transvenous routes. When both approaches are combined or they are modified with minor surgical access or direct puncture procedures, most complex DAVF can be treated safely via endovascular procedures, and few require large open surgical treatment or radiosurgery. The liquid embolics NBCA and Onyx are useful for off-label treatment of DAVFs, and cure rates using different approaches with these devices appear to be improving with operator familiarity with them. DAVF is a catch-all term for a diverse array of vascular malformations with different clinical, anatomic, and radiographic presentations. Standardization of approaches to these lesions is problematic, and pooled institutional studies are necessary to move the quality of treatment and outcome data beyond case series. Successful endovascular treatment will continue to rely on operator experience and familiarity with embolic devices, as well as tailoring the approach to each individual patient’s lesion. A podcast associated with this article can be accessed online (http://links.lww.com/NEU/A589). Disclosure Dr Arthur has served as a consultant for Codman, Covidien, Microvention, and Stryker. Dr Elijovich has served as a consultant for Microvention. Dr Hoit has served as a proctor for Covidien. The other authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
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