Abstract
Purpose
The purpose of this article is to present a case series of transarterial venous sinus occlusion for dural arteriovenous fistulas (DAVFs) of the transverse and sigmoid sinuses.
Materials and methods
From 2006 to 2012, 11 patients with DAVF of the transverse and sigmoid sinuses were treated with transarterial closure of the affected venous sinus using ethylene vinyl alcohol copolymer (ONYX). The consecutive retrospective cohort included six female and five male patients with an age range of 30–79. Patients presented with stroke, intracranial hemorrhage, seizure, headache, focal neurologic deficit or cognitive change. Lesions were categorized as Cognard II a + b (n = 5) or Cognard II b (n = 6). Four of this latter group consisted of isolated sinus segments. Selection criteria for dural sinus occlusion included direct multi-hole fistulas involving a broad surface in length or circumference of the sinus wall. External carotid artery (ECA) branches were directly embolized when considered safe. High-risk arterial supply from ICA, PICA, AICA or ECA cranial nerve branches were closed via retrograde approach during sinus occlusion.
Results
DAVF closure was accomplished in all 11 patients with a total of 17 embolization procedures using ONYX. High-risk arterial collaterals were closed via artery-artery or artery-sinus-artery embolization. The vein of Labbe was spared in the four cases with initial antegrade flow. No neurologic complications occurred, and DAVF closures were durable on three-month angiography.
Conclusion
Transarterial closure of the transverse and sigmoid sinuses.
Keywords: Dural arteriovenous fistula, embolization, ONYX
Introduction
It is estimated that 5% of cranial arteriovenous shunts are based in the dural coverings. Venous sinus thrombosis, smoking history, oral contraception, radical neck dissection or radiation treatment for cancer treatment of the head and neck are the major etiologies. Sixty-two percent of these dural arteriovenous fistulas (DAVFs) are located in the transverse and sigmoid sinuses. Venous hypertension is the key physiologic mechanism in the development of clinical symptoms. Patients may present with tinnitus, headaches, focal neurologic deficits or global cognitive decline. When cortical venous reflux is present, patients have a 10%–65% risk of intracranial hemorrhage depending on classification type.1 In patients presenting with hemorrhage there is at least a 7.4% annual risk of re-bleed compared to 1.5% annual risk in the non-hemorrhagic cohort.2,3
Given the high morbidity associated with cortical venous reflux, contemporary management calls for treatment when this threshold is reached. Typically, embolization is performed to eliminate the arteriovenous shunt and improve circulation of the brain. Microsurgical disconnection or in some cases radiosurgery can be used as adjunctive treatment.
In 1989 Halbach and colleagues4 described a transvenous approach with venous sinus coil occlusion for transverse and sigmoid sinus DAVFs. In 2010 Nogueira et al.5 and Cognard et al.6 described ethylene vinyl alcohol co-polymer (ONYX) for treatment of DAVFs. While treatment with n-butyl cyanoacrylate (n-BCA) has been used,7,8 a 2012 retrospective, single-center series9 demonstrated that transarterial embolization using ONYX had greater efficacy than n-BCA in the treatment of DAVFs. Durability of this embolization technique has been well documented with delayed angiographic follow-up at one year.10 There is one case report in the literature of closure of an isolated sinus using ONYX.11
We present a consecutive retrospective cohort of patients in whom the arteriovenous shunt affected a large segment of the sigmoid and transverse sinuses resulting in cortical venous reflux. The treatment method we describe here is transarterial venous sinus occlusion with ONYX.
Materials and methods
ONYX is an ethylene vinyl alcohol copolymer dissolved in dimethyl sulfoxide (DMSO) (Medtronic, Dublin, Ireland). It comes in 6% (ONYX 18) and 8% (ONYX 34) concentrations and contains tantalum powder in suspension for fluoroscopic visualization.
We searched our institutional database of DAVF cases from 2006 to 2012. There were 11 patients with cranial DAVFs involving extensive surface area in length and/or circumference of the transverse and sigmoid sinuses. These patients were treated with transarterial venous sinus occlusion. Lesions that involved a focal site, an isolated leaflet or an adjacent cortical vein as the primary site of fistula were excluded as they were closed selectively without the need for sinus occlusion. Approval for medical chart evaluation for this retrospective case series was obtained from the institutional review board at our hospital.
Patients were specifically consented for off-label use of ONYX and informed pre-procedure of the therapeutic intent to occlude the affected dural sinus. For embolization we selectively catheterized an appropriate arterial pedicle with a DMSO-compatible microcatheter such as Marathon, Echelon 10, Echelon 14 or Apollo (Medtronic, Dublin, Ireland). The microcatheter was cleared with 6–10 cc of saline and the dead space was filled with DMSO. ONYX was then delivered with a standard plug-and-push method used for arteriovenous malformation (AVM) treatment. A DMSO-compatible Scepter C balloon catheter (Medtronic, Dublin, Ireland) was considered for use in large external carotid branches.
Multistage embolization was performed when it was deemed necessary for radiation dose concerns or to decrease flow incrementally to avoid cortical vein thrombosis. All patients were treated under general anesthesia and observed in a neurointensive care unit for at least 24 hours post-procedure. Neither anticoagulation nor antiplatelet medications were administered in systemic doses during or after the procedures with one exception, which is described below.
Results
Eleven patients with extensive DAVFs of the transverse and sigmoid sinuses were identified including five male and six female patients with an age range 30–79 years. Initial symptoms included headaches (n = 7), tinnitus (n = 7), papilledema (n = 1), or other neurologic changes including seizure (n = 2), aphasia (n = 1), hemianopsia (n = 1), gait instability (n = 1) or ischemic stroke (n = 1), subarachnoid hemorrhage (n = 1) or chronic hemorrhage (n = 2).
Angiographic categorization included five patients with Cognard II a + b and six Cognard II b lesions (Table 1). The latter group included four cases of isolated sinus segments (Figure 1(a)–(d)). The other two patients in this cohort had single, focal occlusions of the affected dural sinus. All patients demonstrated venous sinus irregularity suggestive of previous sinus thrombosis and partial recanalization. The vein of Labbe had antegrade flow and was separate from the DAVF in four cases. It had retrograde flow in two cases, and it was not visualized in three cases.
Table 1.
Transverse and sigmoid sinus DAVF closure cases.
| Patient | Age/ Gender | Cognard | Sinus | Isolated/ Focal Occ/ Sinus Irr | ICA/PICA/ Asc Ph/ CN VII Arcade | Labbe | #Tx | Neurologic Complication | Three-month Angio |
|---|---|---|---|---|---|---|---|---|---|
| 1 | 76/F | II a + b | R Sig | –/–/+ | +/–/+/+ | Ante | 1 | – | – |
| 2 | 66/M | II a + b | L Trans | –/–/+ | –/–/+/+ | Retro | 3 | – | – |
| 3 | 50/F | II a + b | R Trans | –/+/+ | +/–/+/+ | Retro | 1 | – | – |
| 4 | 61/M | II a + b | L Trans | –/+/+ | +/–/+/+ | Retro | 1 | – | – |
| 5 | 54/F | II a + b | R Trans | –/–/+ | +/–/+/+ | Ante | 1 | – | – |
| 6 | 63/M | II b | R T + S | +/–/+ | –/–/+/+ | Ante | 1 | – | – |
| 7 | 51/F | II b | L T + S | +/–/+ | –/–/+/+ | Retro | 3 | – | – |
| 8 | 30/M | II a + b | R Sig | –/–/+ | +/+/+/+ | Ante | 2 | – | – |
| 9 | 30/F | II a + b | L Sig | –/–/+ | +/+/+/+ | Retro | 1 | – | – |
| 10 | 54/M | II b | L T + S | +/–/+ | –/–/+/– | Retro | 1 | – | – |
| 11 | 79/F | II b | L Trans | +/–/+ | –/–/+/+ | Retro | 1 | – | – |
Angio: angiography; Ante: antegrade; Asc Ph: ascending pharyngeal artery; CN: cranial nerve; DAVF: dural arteriovenous fistula; F: female; ICA: internal carotid artery; L: left; M: male; PICA: posterior inferior cerebellar artery; R: right; Retro: retrograde; Sig: sigmoid; Trans: transverse; Tx: treatments.
Figure 1.
Arterial anteroposterior (AP) (a) and lateral (b) phase angiographic images of patient 7 demonstrate a Cognard II b dural arteriovenous fistula with an isolated segment of left sigmoid sinus (black outline arrow). Low-risk arterial supply is identified from the left occipital artery (small white arrow) and squamosal branch of the middle meningeal artery (MMA) (large white arrow). High-risk supply from petrous branches of the MMA caudally as well as the neuromeningeal trunk (white line arrow) is present. Venous-phase angiographic images AP (c) and lateral (d) show venous congestion and hypertension that had resulted in intracranial hemorrhage and stroke.
All 11 DAVFs were occluded through embolization using ONYX (total 17, average 1.5 procedure per patient, maximum three procedures). Seven cases were treated successfully with single-stage embolization. All 11 lesions had supply from high-risk arterial branches including the internal carotid artery; (ICA), posterior inferior cerebellar artery (PICA) or anterior-inferior cerebellar artery (AICA), ascending pharyngeal artery, and facial arcade (Table 1). Embolizations were accomplished from access to low-risk external carotid artery (ECA) branches including the occipital artery and/or squamosal branches of the middle meningeal artery (MMA). The vein of Labbe was spared in the four cases in which it had initial antegrade flow. No neurologic or other complications were incurred. Three-month angiograms demonstrated no recurrence in any of the 11 patients. One-year follow-up was performed in seven of the patients, and treatment was found to be durable (Figure 2(a)–(d)).
Figure 2.
One-year follow-up digital subtraction angiography anteroposterior (AP) (a) and lateral (b) demonstrate stable closure of the dural arteriovenous fistula. There is closure of the petrous middle meningeal artery (MMA) and neuromeningeal trunk supply from artery-to-sinus-to-artery approach (white line arrow). Unsubtracted radiographs in AP (c) and lateral (d) demonstrate ONYX cast of the sigmoid sinus and the squamosal branch of the MMA used for embolization.
Complications were minimal. One patient developed thrombus in a left external carotid artery branch treated with 1500 units intra-arterial (IA) heparin and then aspirin 325 mg for one month before stage 3 embolization. One microcatheter rupture occurred at the end of a procedure during occipital artery embolization. No neurologic complications occurred. Radiation dose per procedure ranged from 3.5 Gy to 9.3 Gy. (Procedures were all accomplished before dose reduction strategies were widely used.) Patients with >5 Gy dose were reported through standard radiation safety reporting at our institution and followed in clinic. Two patients had mild, transient epilation.
Discussion
This retrospective cohort of 11 consecutive patients with transverse and sigmoid sinus DAVFs with cortical venous outflow was treated to completion safely by the technique of transarterial venous sinus occlusion. Stable closure of all lesions was documented by angiography at three months.
DAVFs occur at the interface of arteries and veins within the dura mater. Endovascular closure of a lesion can be considered from either direction depending on access to the lesion, risks and possibility of success. Decision to occlude the transverse or sigmoid sinus in a patient is multifactorial. Native venous anatomy and physiology are important in decision analysis. Firstly, this technique was considered when a lesion was determined to have extensive involvement in circumference or length of the sinus wall and had cortical venous reflux. DAVFs that involve a focal segment of sinus, a specific leaflet or cortical vein adjacent to a sinus can usually be embolized without sinus closure.12 Secondly, one must consider whether the sinus provides significant venous outflow of the brain. All of the cases in this series involved co-dominant or non-dominant transverse and/or sigmoid sinus. Thirdly, cranial venous sinuses can be isolated or compartmentalized because of previous thrombosis, which occurs in 39% of cases in the transverse and sigmoid sinus region.13 We found that all 11 patients had irregularity of the affected sinus with four cases of isolated sinus and two cases of focal occlusion. These findings suggest previous sinus thrombosis and recanalization processes are likely etiologies in this cohort. Considering these latter two points, it is likely that the affected sinus can be permanently occluded without neurologic sequelae.
There is a spectrum of venous sinus involvement, and it is often during embolization that a final strategy is chosen. Most patients with Cognard I or II a lesions were followed clinically during this interval as their natural history is generally benign. Selected patients with such lesions may be treated with embolization as a strategy to reduce symptoms such as tinnitus or headache. Cognard III and IV lesions that involve direct flow into cortical veins immediately adjacent to a sinus can generally be closed by embolization and/or surgery without affecting the sinus.
Isolated sinus segments categorized as Cognard II b lesions can be treated in a similar way as Cognard III lesions. Because all of the cortical veins are retrograde, one can fill the venous sinus segment and seal the origins of the cortical veins. We considered but did not treat such patients with heparin post-embolization. Isolated sinuses can be treated by direct access embolization through a burr hole or focal craniotomy or by recanalization of the sinus as one might attempt for carotid cavernous fistula via recanalization of an inferior petrosal sinus. However, coils may not reach or pack densely in a sinus, which is compartmentalized from previous thrombosis. A combined method of placing a cage of platinum coils which is then filled in with ONYX could be considered.14 However, it is a more-invasive yet less-certain method of occluding the arterial inflow of the shunt, which could result in incomplete treatment or recurrence.
Cognard II a + b lesions must be evaluated by angiography to determine whether antegrade cortical veins also utilize the affected sinus segment. In this series the vein of Labbe was identified as antegrade in four cases. In each case it was immediately adjacent to the fistula segment, and it was preserved. One can consider adjunctive venous sinus balloon placement (Copernic balloon, Balt Extrusion) during embolization to increase the likelihood of retaining patency of a sinus as the affected dural leaflets are embolized. This can be especially helpful at the torcular herophili or adjacent to the vein of Labbe. It is important to choose DMSO-compatible devices. Transvenous sinus occlusion is an option, but it risks venous closure of normal antegrade parenchymal veins into the affected segment.
Using this transarterial approach, ONYX can safely close high-risk arterial supply to a lesion and avoid embolization of the carotid or vertebral arteries through normal collateral branches at the skull base. All 11 lesions had supply from high-risk arterial branches including the ICA (lateral tentorial branches), PICA or AICA (dural branches), ascending pharyngeal artery (neuromeningeal trunk) and facial arcade (petrous branch of MMA or posterior auricular artery).15 All 11 cases in this series were embolized via low-risk ECA branches (occipital artery or MMA-squamosal branch) to close the venous lesion and the high-risk arterial supply (Figures 1 and 2). This was accomplished via artery-to-sinus-to-artery vascular network or via artery to artery anastomoses around the affected sinus.
Properties of ONYX facilitate selective sinus treatment. A standard plug-and-push technique was used in these cases. One could also use a detachable-tip microcatheter or two-microcatheter technique in the occipital artery or DMSO-compatible balloon catheter for delivery.16,17 There are advantages of the properties of ONYX over n-BCA in overall closure rates of DAVFs as a result of better penetration throughout these lesions.9 ONYX may close affected dural leaflets without closing the entire sinus. Its dense and cohesive liquid form is modeled by flowing blood. It tends to laminate on the periphery of a sinus in the initial stages of embolization.18,19 It is pushed away from the origin of normal cortical veins flowing into the sinus and toward retrograde cortical veins. Angiography can be performed during the 30- to 120-second pauses to assess progress and closure.
DAVF closure can be more difficult to accomplish using other embolization methods. N-BCA, one alternative liquid embolic agent, has a rapid polymerization and is prone to fragmentation. Its thrombogenic property may hypothetically work in a positive way for initial closure but may allow for recanalization as the clot resolves. Nelson and colleagues20 had success in closing a high percentage of selected DAVFs using a wedged catheter technique. However, venous sinus coil occlusion was chosen for 11 cases similar in physiology to those presented here. Guedin et al.7 reported an arterial embolization closure rate of 76% using n-BCA with only three additional patients triaged to transvenous closure strategies. The comprehensive reports by Cognard et al.6 and Rabinov et al.9 show closure rates of 80% and 85% using ONYX in their consecutive case series. Cognard stated that four cases in their series had failed transvenous catheterization for coil embolization.
It is important the keep in mind the value of focal surgery of a focal-specific part of a lesion following embolization. However, surgical skeletonization of an extensive and diffuse lesion is a difficult process with the skull base surrounding the venous sinuses.21 In addition, the lower cranial nerves may be placed at risk at the jugular fossa. The role of radiosurgery can also be considered for focal areas of a DAVF left as residual or recurrent but the time needed for efficacy of treatment must be understood.22
Conclusion
Transarterial venous sinus occlusion using ONYX is safe, effective and durable in the treatment of extensive DAVFs of the transverse and sigmoid sinuses.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
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