A dural arteriovenous fistula (DAVF), also known as a dural arteriovenous malformation (DAVM), is an abnormal arteriovenous connection that occurs solely within the leaflets of the dura mater, usually within or near the walls of a dural sinus. A truly unique patho-anatomic entity, DAVFs only gained wide recognition and had their pathophysiology and clinical behaviors gradually elucidated in the past two decades. No longer angiographic curiosities, DAVFs can present with a wide spectrum of symptomatology, and their natural history may range from very benign with spontaneous resolution to highly dangerous with frequent life-threatening intracranial hemorrhage.

The past two decades also witnessed important advances in endovascular techniques for treatment of DAVF as safety, technical feasibility, and outcome continue to improve. The effectiveness, risks, and complications of these techniques are undergoing continuous reassessment as experience and technology evolve. Yet, neurosurgical treatment continues to provide safe and effective definitive management for various intracranial DAVFs in different locations. Not infrequently, surgical therapy may be a safer and more efficacious option for a particular lesion. We review the anatomy, indications, general principles, techniques, and outcome of neurosurgical management of selected intracranial DAVFs.

Classification of Intracranial Dural Arteriovenous Fistulas

Dural arteriovenous fistulas have been classified according to location, hemodynamics, associated dural sinus thrombosis, and their venous drainage pattern, which are related to their clinical manifestations^1–4 and responses to treatment modalities. Individual symptomatology is dependent on lesion location, while the clinical behavior (benign vs. aggressive) is dependent upon the pattern of fistulous venous drainage. Borden et al have devised a simple and well-accepted classification scheme.¹ Type I has drainage only into a dural sinus or meningeal veins. Type II has drainage into a dural sinus and leptomeningeal veins. Type III has drainage into leptomeningeal veins only. Those DAVFs with leptomeningeal venous drainage (Borden types II and III) are associated with an aggressive natural history and high incidence of hemorrhagic and progressive neurological complications. Those DAVFs draining exclusively into a dural sinus (Borden type I) are associated with a benign natural history.

In a review of the literature on the distribution and clinical courses of 377 DAVFs, Awad and Little found 62.6% occurring in the transverse-sigmoid sinus area, 11.9% in the cavernous sinus area, 8.4% in the tentorial incisural area, 7.4% in the convexity-sagittal sinus area, 5.8% in the orbital-anterior falx area, and 3.7% in the sylvianmiddle fossa region.⁵ The ratio of aggressive to benign behavior was 1:8.8 for transverse-sigmoid sinus location, 1:6.5 for cavernous sinus location, 31:1 for tentorial-incisural location, 1:1 for convexity-sagittal sinus location, 2.1:1 for orbital-anterior falx location, and 2.5:1 for sylvian-middle fossa location. The presence of aggressive behavior (mostly resulting in stroke, hemorrhage, dementia, and blindness) is usually related to the presence of leptomeningeal venous drainage, echoing the findings of Borden et al^1,6 There are anecdotal reports of DAVFs located in the clivus, in the inferior petrosal sinus, in the deep venous sinuses, and in the torcular areas. Additionally, a small group of patients may harbor and present with multiple DAVFs.

Pathophysiology and Natural History

The vascular tree is a remarkably dynamic system that can adjust to many normal and abnormal factors with remodeling and flow alteration. There are normal dural arteriovenous connections that may adapt with dilation and/or flow reversal secondary to venous hypertension. Frequently, venous abnormalities, congenital or acquired, can be identified accompanying DAVFs. These include aplasia, stenosis, and partial or complete thrombosis. Such flow restriction may be further complicated by other hormonal and metabolic factors that eventually lead to an inappropriate remodeling process of the original normal channels, forming pathological DAVFs.⁷ As the lesions progress, the venous hypertension may congest normal leptomeningeal drainage causing flow reversal and formation of venous varices because the intracranial venous system is valveless and potentially bidirectional. It is noted that such pathological leptomeningeal venous hypertension is the source of significant neurological complications.⁸

Davies et al studied the natural history of benign (Borden type I) and aggressive (Borden types II and III) DAVFs.^9,10 Only 2% of the untreated patients with type I DAVFs presented with hemorrhage or progressive neurological deficits. In contrast, 39% of type II and 79% of type III patients presented with these aggressive symptoms. Without treatment, 81% of the patients with Borden type I DAVFs were improved or cured. However, in the untreated patients with Borden types II and III lesions, there was an intracranial hemorrhage rate of 19.2% per patient year, a nonhemorrhagic neurological deficit rate of 10.2% per patient year, and a mortality rate of 19.3% per patient year. More disturbingly, 18% of patients who were treated with partial embolization and who demonstrated persistent retrograde leptomeningeal venous drainage experienced recurrent intracranial hemorrhage or a new neurological deficit.^9–11 Therefore, the presence of retrograde leptomeningeal venous drainage is an overwhelming prognosticating factor for aggressive intracranial DAVFs and their unfavorable natural courses.

Clinical Features

The symptoms of DAVFs are secondary to the increased blood flow and resultant intracranial venous hypertension. If the fistulous volume is low with good venous outflow, there may be no symptoms other than a bruit in those DAVFs close to the temporal bone. As venous hypertension and congestion develop with progressive shunting from the fistula, additional symptoms and complications emerge. In the region of the cavernous sinus and orbits, local signs and symptoms make up the majority of clinical presentation. In other locations, the symptomatology may be more general. When a high-flow fistula develops, increased intracranial pressure may occur, with associated symptoms of headache and papilledema, simulating pseudotumor cerebri. Moreover, when venous hypertension is borne by a leptomeningeal vein, the risks of intraparenchymal and subarachnoid hemorrhage are extremely high.^2,4,5,8,12 A venous aneurysm in the context of DAVFs may have the highest rupture tendency of all intracranial aneurysmal lesions. Rarely, a dilated venous varix can present as a local mass lesion, especially in crowded locations such as the posterior fossa near the brain stem and cranial nerves.¹³

Another clinical problem seen with high-volume fistulas that drain extensively through the leptomeningeal veins is the ischemic parenchymal changes and resultant gliosis and necrosis secondary to chronic venous hypertension and congestion. Patients with such problems may present with seizures, dementia, or other focal neurological deficits.^14–17 More intriguingly, patients with rare DAVFs in the region of the foramen magnum may have leptomeningeal venous drainage through lower dependent medullary veins. Venous hypertension in these plexuses can cause myelopathy with neurologic deficits many segments below the level of fistula.^18–20

Overview of Dural Arteriovenous Fistulas Treatment Options and Indications

Following the diagnosis of a DAVF, the clinician faces a wide variety of management options. An expectant therapeutic approach is possible in many cases and may be safer than any attempt at lesion obliteration. In other instances, palliative treatment of the lesion aiming at controlling the associated symptoms such as pain, ophthalmoplegia, or pulsatile tinnitus is undertaken. In some lesions, secondary manifestations such as increased intracranial pressure and papilledema may require more urgent intervention than the DAVF itself. Lesion obliteration through a variety of feasible approaches may be entertained as definitive treatment for certain DAVFs when aggressive clinical behaviors are anticipated. In each case, the therapeutic strategy should be highly individualized and guided to improve symptoms or to prevent catastrophic consequences of the lesion natural history.

A given therapeutic attitude can never be generalized to all DAVFs in view of the highly variable clinical manifestations and possibilities of natural course. Treatment options for DAVFs, in general, include expectant observation, carotid compression, endovascular transarterial and/or transvenous embolization, and microsurgical disconnection. Conventional radiotherapy and stereotactic radiosurgery as alternative therapeutic options for some DAVFs have been reported. However, there needs to be better characterization of optimal dosimetry, time response, and effectiveness of lesion obliteration, as well as radiation safety or protection to adjacent eloquent neural structures.

Noninvasive options, including observation and carotid compression, are suitable for lesions without aggressive clinical or angiographic features, i.e., leptomeningeal venous drainage. Close clinical follow-up is important in these management strategies, and patients should be educated to report any significant changes in their symptoms. Some changes in symptoms, including sudden resolution of a usual symptom like bruit, may signify the transformation of a previously benign DAVF to an aggressive lesion with cortical venous drainage replacing dural outflow. Once an aggressive venous drainage pattern develops, endovascular or surgical intervention should be strongly considered.

As experience and technology evolve, endovascular therapy has been used to manage an increasing proportion of intracranial DAVFs safely and with good results. However, transarterial embolization alone has limited effectiveness in treating lesions that have a plethora of arterial feeders with numerous channels from multiple sources, particularly when many of the feeding arteries are very small in diameter and stem directly off pial trunks.^21–23 Such circumstances are usually encountered in lesions located in the tentorial-incisura and anterior fossa-falx.

Many “angiographic cures” by transarterial embolization should be viewed as suspect or temporary, because lesions have been shown to recanalize, or acquire alternate arterial supply. Transvenous embolization, especially in combination with adjuvant transarterial embolization to reduce fistulous inflow, has become the favored approach for endovascular therapy of intracranial DAVFs.^22–25 Percutaneous transvenous therapy of intracranial DAVFs can be performed only when a venous drainage pouch that is separate from veins draining normal brain tissue can be identified and accessed by a microguidewire–microcatheter system. When transvenous embolization is limited to the venous outlet immediately distal to the fistula nidus, and functional drainage can be preserved, embolization with platinum coils can provide safe and effective treatment. However, venous outflow occlusion without obliteration of the arteriovenous shunt itself may result in increased venous hypertension in other channels and in hemorrhage or worsened clinical symptomatology.^24,26,27 Open microsurgical fistula disconnection is indicated in cases of endovascular failure or technical infeasibility. Occasionally, direct surgical exposure of the dural sinus can provide the transvenous entry for endovascular obliteration of certain DAVFs by sinus packing when venous access is complicated by severe stenosis or bifocal occlusion of the sinus.

Surgical Techniques for Managing Intracranial Dural Arteriovenous Fistulas

Simple feeding arterial ligation, like stand-alone transarterial embolization, has a very low clinical and radiographical cure rate.²⁸ The partially treated fistulas usually continue to fill and may recruit new arterial supply and alter venous draining patterns, eventually evolving into more dangerous lesions. Thus, surgical ligation of feeding branches is not advisable in the modern management of DAVFs. Objectives of surgical intervention include complete physical interruption of arterialized leptomeningeal venous connections. Recently, some authors have reported good results with simple microsurgical disconnection of pathological leptomeningeal venous outflow flush with the dural leaflet.^29–33 Such a strategy shares the same philosophy with transvenous embolization technique, which is to occlude the venous outlet at the nidus without an interval venous segment between the occlusion and the nidus. Usually, in DAVFs with retrograde leptomeningeal venous drainage, these veins no longer contribute to the venous drainage from normal brain tissue, and occlusion of the venous side of the fistula can be performed without risk of venous infarction. Surgical excision of the pathological dura may be associated with significant blood loss and neurological complications.^34,35

Debates over the optimal strategy continue, and only long-term follow-up of treated patients will demonstrate the efficacy of each procedure. The safety of open surgical approaches may be enhanced by preoperative adjuvant transarterial embolization so as to decrease flow through the DAVFs and control many of the external carotid supply channels to these lesions.^36–39 Moreover, superselective angiography may provide detailed information about the precise location and angioarchitecture of the lesion. Intraoperative angiography and the occasional open coil-induced thrombosis of arterialized venous aneurysms or the cavernous sinus have further improved the effectiveness of neurosurgical treatment. With meticulous attention to detail, experienced neurosurgeons have achieved good results with limited morbidity.^{21,29–33,36,38,40–42}

Transverse and Sigmoid Sinus Dural Arteriovenous Fistulas

Improvements of endovascular techniques and a better understanding of the pathophysiology of these lesions have increased the number of treatment options. The type of treatment (surgical vs. endovascular) and the route of attack (arterial vs. venous) depend on whether the involved sinuses remain patent or have thrombosed. Once treatment is deemed necessary, occlusion of the sinus by either endovascular or surgical routes, as described by Mullan,⁴³ can safely eliminate the majority of these lesions. When the fistula nidus is located in a segment of isolated sinus from the thromboses, open surgical exposure of the dural sinus can provide venous access for intraoperative endovascular sinus occlusion.^{33,36,37,40,42}

The operative exposure requires the patient to be in a lateral or prone position. A small rectangular skin flap is made over the transverse sinus, with optional intraoperative stereotaxis guidance, and a fringe of the occipital muscles is undermined using electrical cautery. A burrhole or a small rectangular channel of bone is drilled away over the sinus, packing continuously with bone wax to achieve meticulous hemostasis. The exposed sinus wall is covered instantly with prothrombotic materials, like Gelfoam™(Pfizer, Inc., New York, New York) or Surgicel™ (Johnson & Johnson, New Brunswick, New Jersey), and suction pressure is applied through saline-soaked cotton. In this manner, the entire extent of the transverse sinus can be exposed with only minor hemorrhage. Then, sinus occlusion can proceed with endovascular techniques. After the sinus is occluded, intraoperative angiography should confirm the obliteration of all retrograde leptomeningeal venous flow and the fistula itself. If there are cortical veins draining independently from the fistulous wall, these will need to be interrupted flush with the sinus wall after opening the dura.

When success is measured by the extent to which the lesion is eliminated, such combined therapy offers the best results with 68% complete angiographic obliteration, compared with 41% for embolization alone and 33% for surgery alone.²⁸ Long-term clinical and angiographic follow-up is important for patients with residual filling or persistent symptoms.

Tentorial Incisura Dural Arteriovenous Fistulas

Dural arteriovenous malformations of the tentorial incisura demonstrate an unfavorable natural history. These lesions are frequently associated with retrograde leptomeningeal venous drainage through the perimesencephalic system into the vein of Galen and carry a high risk of hemorrhage, almost always in the form of subarachnoid hemorrhage.^12,44,45 Venous hypertension of the brain stem structures, which normally drain through such venous plexuses, can cause other focal neurological deficits. Typically, there is a plethora of arterial feeders from a myriad of meningeal arteries, converging into a pathological region of the tentorial leaflet at the incisura, where there are numerous arteriovenous communications instead of a single shunt. The small caliber of the feeding branches and frequent presence of dural branches arising from the distal posterior cerebral and superior cerebellar arteries make transarterial embolization difficult to perform; the lack of an adjacent large dural sinus makes transvenous access equally difficult. Complete lesion obliteration frequently requires open surgical treatment, usually in combination with preparatory arterial embolization from external carotid branches.

We have adopted a venous disconnection technique, which evolved from earlier dural excision methods.³² The procedure is performed via a subtemporal approach, taking care to preserve any normal bridging veins. Arterialized veins connecting the tentorium to the temporal lobe are coagulated and divided. The portion of tentorium with obvious DAVF involvement is extensively bipolar coagulated. The tentorium is carefully incised to expose the inferior surface, and any arterialized venous connection with the cerebellum and brain stem is carefully coagulated and divided. At the incisural border, meningeal branches of the posterior cerebral and superior cerebellar arteries can be similarly disconnected. Intraoperative angiography is performed to confirm the efficacy of obliteration. Some authors advocate direct puncture and open coil-embolization of any residual giant venous aneurysms.³⁴ The minimum goal of surgical therapy should be to eliminate the leptomeningeal venous drainage, and thus the major risk of hemorrhage. Residual arteriovenous shunting should be closely followed with serial postoperative angiograms. In a meta-analysis of the English literature,²⁸ combined therapy demonstrated the best success rate in lesion obliteration (89%), compared with either surgical treatment alone (78%) or endovascular therapy alone (25%).

Anterior Fossa-Falx Dural Arteriovenous Fistulas

Feeding vessels typically arise from the anterior or posterior ethmoidal arteries and less commonly from the anterior falcine artery in anterior fossa-falx DAVFs. The ethmoidal arteries are usually branches of the ophthalmic artery and cannot be embolized without significant risk of complications involving the visual system. Therefore, surgical obliteration is the preferred method of treatment for anterior fossa DAVFs. These lesions drain overwhelmingly through leptomeningeal venous channels with a very high incidence of venous varices and aneurysms, thus accounting for an aggressive natural course and high risk of intracerebral hemorrhage.^46,47

Surgical obliteration is performed through a low frontal craniotomy with minimal brain retraction. If a large intraparenchymal hematoma is present, it should be evacuated initially to allow brain relaxation and safe mobilization of the frontal pole. In most cases, the lesion consists of simple fistulous connections between the feeding arteries and the pial veins without a significant dural nidus. Microsurgical occlusion of the vascular connection between the dura of the cribriform plate area and the arterialized pial veins is curative without the need for further resection of the dysplastic leptomeningeal veins. Intraoperative angiography is useful to confirm the obliteration of the fistula. Success rates of over 95% for surgical intervention have been reported in the literature.²⁸

Cavernous Sinus Dural Arteriovenous Fistulas

Endovascular methods are the primary means of managing cavernous sinus DAVFs. Dural arteriovenous fistulas in this region present little risk of hemorrhage due to the unusual presence of leptomeningeal venous drainage. Transvenous embolization is the preferred treatment once intervention is indicated, although transarterial embolization is a reasonable alternative if all fistulous feeders are from the external carotid system. There are a variety of transvenous access approaches to the cavernous sinus, including direct percutaneous puncture of the superior ophthalmic vein⁴⁸ and cavernous sinus⁴⁹ through the superior orbital fissure. Endovascular failure is very rare; thus, surgery seldom is required.

Other Rare Dural Arteriovenous Fistulas

Dural arteriovenous fistulas involving the convexitysuperior sagittal sinus and the middle fossa dura (usually the sphenoparietal and superior petrosal sinuses) with variable leptomeningeal venous drainage pattern are rare. Arterial supplies usually arise from the middle meningeal artery and other external carotid branches, thus permitting transarterial embolization to reduce shunt inflow. Combined with arterial embolization, transvenous therapy usually can achieve sinus occlusion to cure the fistula radiographically. When venous access is complicated by sinus thrombosis, surgical exposure of the involved sinus using techniques similar to the above for transverse sinus fistulas can be applied. Microsurgical leptomeningeal venous disconnection can be performed as well.^39,41,42 Intraoperative angiography is valuable to document the resolution of fistula.

Another rare location for DAVFs is in the region of the foramen magnum. These lesions may drain directly into the pontine or spinal medullary venous circulation. Dural arteriovenous fistulas located in the posterior fossa are so unusual that they have not been well characterized in the literature. However, when retrograde leptomeningeal venous drainage develops with ensuing venous hypertension, the natural course of these lesions is expected to be poor. The safety and feasibility of transarterial embolization are limited by the multitude of small arterial feeders arising directly from the vertebral arteries. Transvenous routes of endovascular obliteration are limited by the predominance of leptomeningeal venous drainage as opposed to dural sinus outflow. Open surgical obliteration of such DAVFs is feasible and effective. This is approached via a posterior far-lateral craniocervical exposure with upper cervical laminectomy and suboccipital craniotomy. The pathological dura with fistula is exposed and extensively coagulated, and the vertebral artery is controlled. Once the dura is opened, the leptomeningeal venous connection is identified and may be clip-ligated flush with the dura. Intraoperative evoked potential monitoring for the appropriate spinal cord segments and brain stem may add safety to the venous disconnection. An intraoperative angiogram may be helpful to confirm obliteration of the DAVF; however, injection of all possible feeders may not be technically possible in the operating room, and a postoperative angiogram may be necessary.