26 Radiosurgery for Dural Arteriovenous Fistulas: Indications and Outcomes
Stereotactic radiosurgery using the Gamma Knife or other radiosurgical devices is a safe and effective alternative treatment for dural arteriovenous fistulas (DAVFs). This method provides a minimally invasive therapeutic modality for patients who harbor less aggressive DAVFs, but who suffer from intolerable headache, pulsatile tinnitus, or ocular symptoms. For aggressive DAVFs with extensive cortical venous drainage, immediate risks of hemorrhage, progressive neurological deficits, or severe venous hypertension, initial treatment with endovascular procedure, including embolization and angioplasty, or surgery is suggested. In such cases, radiosurgery may serve as a secondary treatment for further management of the residual fistulas. The latent period for the effects of radiation to occur and the longer time for cure compared to surgery and endovascular therapy remains a major drawback for radiosurgery. However, the gradual obliteration of a DAVF after radiosurgery can avoid immediate risk of aggravated venous hypertension or infarction, which sometimes complicates endovascular embolization and surgery. It is believed that using a multidisciplinary approach to DAVF management yields better results.
Keywords: dural arteriovenous fistula, Gamma Knife, stereotactic, radiosurgery
- For Borden type I (Cognard type I, IIa) dural arteriovenous fistulas (DAVFs) with persistent benign symptoms (pulsatile tinnitus or ocular symptoms), radiosurgery may be indicated as an initial treatment.
- For Borden type II/III (Cognard type IIa + b, IIb, III) DAVFs with asymptomatic cortical venous drainage (CVD; headache, pulsatile tinnitus, or ocular symptoms), endovascular procedure may be the first-line management. Radiosurgery can be considered an initial treatment alternatively for patients who are elderly, medically frail, or harboring complicated angioarchitecture.
- For Borden type II/III (Cognard type IIa + b, IIb, III) DAVFs with severe symptomatic CVD (hemorrhage or progressive neurological deficits), surgery or endovascular procedures are indicated for the initial treatment.
- An obliteration rate of 70% is expected for the cavernous sinus DAVFs, and 60% for the noncavernous sinus DAVFs. Few complications are reported.
Intracranial dural arteriovenous fistulas (DAVFs) are abnormal arteriovenous communications within the dura, in which meningeal arteries shunt blood directly into the dural sinus or leptomeningeal veins.1,2 DAVF is considered an acquired disease, although the exact pathophysiology was not well established. DAVFs with anterograde cortical venous drainage (CVD) have been clinically regarded as benign, whereas DAVFs with retrograde CVD are considered aggressive in behavior. For DAVFs without CVD or DAVFs with asymptomatic CVD, radiosurgery may be indicated as an initial treatment. An obliteration rate of 70% is expected for the cavernous sinus (CS) DAVFs, and 60% for the noncavernous sinus (NCS) DAVFs. For aggressive DAVFs with extensive CVD, harboring severe venous hypertension, progressive neurological deficits, or immediate risks of hemorrhage, initial treatment with endovascular intervention, including embolization and angioplasty, or surgery is suggested.
The incidence of DAVFs has been estimated at 5 to 20% of all intracranial vascular malformations.1,3,4,5 DAVFs comprise only 6% of supratentorial vascular malformations, whereas they are 35% of infratentorial malformations.6 The median age of presentation for a DAVF is 50 to 60 years of age with no sex preference, though there is a wide range seen.7,8 Unlike the more common intracerebral or parenchymal arteriovenous malformations (AVMs), DAVFs most commonly occur in the regions of the CS, transverse/sigmoid sinuses, tentorium/torcula, or cerebral convexities with drainage to superior sagittal sinus (► Fig. 26.1, ► Table 26.1)1,9,10
Fig. 26.1 The common locations and symptoms/signs of intracranial dural arteriovenous fistulas.
The underlying etiology and natural course of DAVF are not yet very well understood, and the magnitude of the risk varies considerably between studies.11,12,13,14 Söderman et al reported an 85-patient series with 25-year follow-up that demonstrated approximately 1.5% annual hemorrhage rate among the patients without previous hemorrhage and 7.4% among those with previous hemorrhage.13
26.1.2 Clinical Manifestations
The clinical presentation of a DAVF is dependent on its location and pattern of the venous drainage (► Fig. 26.1). The most common locations are the CS, followed by transverse-sigmoid sinus, which together account for about 80% of the cases.4 Patients with CS DAVFs often have ocular manifestations (exophthalmos, chemosis, visual impairment, and diplopia). In the transverse-sigmoid sinus (TSS) DAVFs, pulsatile tinnitus and throbbing headache were the most common symptoms.4
Similar to other cerebral AVMs, DAVFs can hemorrhage, with an estimated annual risk of approximately 1.5 to 1.8%.13 van Dijk et al in 2002 reported that persistence of the cortical venous reflux in DAVFs yields an annual hemorrhage rate of 8.1% and a mortality rate of 10.4%.14 Duffau et al reported a high risk of early rebleeding (35% within 2 weeks) after the first episode of hemorrhage, with graver consequence from the second bleed.12 Söderman et al in 2008 evaluated hemorrhage rate in their 85 cases of DAVFs with retrograde CVD. They found a lower hemorrhage rate compared to those of the other previous reports. In their patients already presenting with an intracranial hemorrhage, the annual risk for the recurrent hemorrhage was 7.4%, while in those patients not presenting with a hemorrhage, the bleeding rate was approximately 1.5% per year.13 Pan et al in 20134 reported a Gamma Knife radiosurgery (GKRS) series of 321 DAVF patients; 7 of the 206 CS DAVF patients (3.4%) experienced a hemorrhage and 16 of the 115 NCS DAVF patients (13.9%) had a hemorrhagic event prior to diagnosis. The report also demonstrated that arteriovenous shunts involving the anterior skull base, tentorium, or sphenoparietal sinus harbored a higher risk of hemorrhage4 (► Table 26.1).
Table 26.1 Incidence of intracerebral hemorrhage (ICH) and nonhemorrhagic neurological deficit (NHND) before GKRS in 321 patients with DAVFs
Beyond hemorrhagic episodes, some patients suffered persistent or slowly progressive neurological deficits, including symptoms of hemiparesis, hemiparesthesia, cerebellar sign, dementia, and mental confusion. From the authors’ experience in analysis of 321 DAVF patients, the incidence of nonhemorrhagic neurological deficits (NHND) is 4.4% (9 of 206 cases) in CS DAVFs and 37.4% (43 of 115 cases) in NCS DAVFs (► Table 26.1).
DAVFs are thought to be acquired due to inflammation, thrombosis, or trauma of the dural sinus. However, the exact etiology and underlying disease are difficult to trace in many cases and the DAVFs are considered idiopathic.15,16 A thorough understanding of a DVAF morphology requires a detailed cerebral angiographic investigation. Drainage of the venous flow from DAVF can be antegrade or retrograde through a dural sinus, through a cortical vein, or both. The pattern of the venous drainage is not necessary static though. Gradual alternation in the venous flow from antegrade to retrograde and delayed recruitment of arterial feeders into the nidus (sump effect) have been observed in some patients.8,17,18 This is hypothesized to occur as a result of progressive sinus hypertension with redirection of the blood flow into cortical veins.2,9,19 The gradual venous hypertension and reflux of the cortical veins may eventually predispose to the risks of cerebral hemorrhage and/or other neurological deficits.1
Not all DAVFs demonstrate such a progressive clinical course though. Although not frequently seen, some DAVFs can regress and thrombose gradually, resulting in a spontaneous cure.20,21 The factors predisposing to DAVF progression or involution have not been clearly clarified.
26.1.4 Angioarchitecture and Classifications of DAVF
There are at least three classifications for intracranial DAVFs (► Table 26.2, ► Table 26.3, ► Table 26.4). The most popularly used classifications in DAVFs are Cognard classification and Borden–Shucart system.9,19 Both systems classify the DAVFs based on their angiographic venous drainage pattern However, owing to the unique clinical characteristics of DAVFs involving the CS, Barrow’s classification, which describes the feeding arteries to the CS DAVFs, is also commonly used to classify this particular type of DAVFs.22
Table 26.2 Cognard classification for dural arteriovenous fistulas
Confined to sinus wall with normal anterograde flow
Confined to sinus with cortical veins reflux
Retrograde drains into sinus with cortical veins reflux
IIa + b
Retrograde drains into sinus + cortical veins
Drains direct into cortical veins (not to sinus) drainage
Drains direct into cortical veins (not to sinus) drainage with venous ectasia
Spinal perimedullary venous drainage, associated with progressive myelopathy
Table 26.3 Borden classification for dural arteriovenous fistulas
Drains anterograde into venous sinus
Drains retrograde into venous sinus + cortical vein
Drains retrograde into cortical vein only
Table 26.4 Barrow classification for the CS DAVFs
Direct high-flow shunts between ICA and CS
Indirect low-flow shunts meningeal branches of ICA and CS
Indirect low-flow shunts meningeal branches of ECA and CS
Indirect low-flow shunts meningeal branches of both ICA and ECA and CS
Abbreviations: CS, cavernous sinus; DAVFs, dural arteriovenous fistulas; ECA, external carotid artery; ICA, internal carotid artery.
The system of Cognard similarly separates DAVFs depending on the site of drainage and the presence of CVD, and also considers the direction of flow through the draining vein as well as the presence of cortical venous ectasia9 (► Table 26.2). Cognard type I DAVFs have solely antegrade sinus drainage, similar to the Borden–Shucart system. Cognard type II DAVFs demonstrate retrograde drainage and are subdivided depending on whether drainage is through the sinus (IIa), cortical vein (IIb), or both (IIa + b). Cognard type III DAVFs drain directly into cortical veins similar to the Borden–Shucart system, but Cognard gives lesions with venous ectasia a separate designation of type IV. DAVFs that drain into spinal perimedullary veins are designated type V by Cognard. Cognard et al present their series of 258 patients and demonstrate a strong correlation between DAVF type and rate of aggressive clinical symptoms and risk of hemorrhage.
The Borden–Shucart system distinguishes DAVFs depending on the site of drainage and the presence of CVD19 (► Table 26.3). Tape I DAVFs drain directly into the sinus or meningeal veins with antegrade flow, whereas type II DAVFs have retrograde flow through the sinus into the subarachnoid veins. Type III DAVFs directly drain into the subarachnoid veins in a retrograde fashion.
According to Barrow’s classification,22 CS DAVFs are classified into direct (type A) and indirect (types B–D) types (► Table 26.4). Direct CS DAVFs are high-flow shunts between the cavernous portion of the internal carotid artery and the CS, usually caused by a traumatic laceration of the internal carotid artery or rupture of an intracavernous carotid aneurysm. Indirect CS DAVFs are dural fistulas between the CS and meningeal branches of the internal carotid artery (type B), the external carotid artery (type C), or both (type D).
26.1.5 Treatment Options
The recommended therapeutic intervention for a DAVF is dependent on the anticipated natural history and hemodynamic change of the lesion. For lesions with antegrade sinus drainage (Borden type I or Cognard type I) and benign clinical manifestations, intervention is usually palliative or observational unless the patient’s symptoms are intolerable.5,8 For patients with throbbing headache, pulsatile tinnitus, ophthalmological deterioration, progressive neurological deficits, increased intracranial pressure, or elevated risk of hemorrhage, therapeutic intervention is recommended.9,19,23,24
Advances in the field of interventional neuroradiology have increased treatment options for patients with DAVFs. Obliteration of the fistula can be attempted through a transarterial or transvenous route. Transarterial embolization alone rarely leads to a complete obliteration of the DAVF, because there are usually numerous arterial feeders to the nidus. The purpose of a transarterial approach is mainly for reduction of arterial feeders and the palliative symptomatic relief.23 For curative treatment, additional treatment through a retrograde transvenous approach may be necessary. In transvenous embolization, superselective disconnection of the refluxing vein is preferred over sacrifice of the dural sinus, although this sometimes becomes necessary to achieve a cure.23 Endovascular therapy can also be combined with surgery or radiosurgery when it is not feasible to completely obliterate a DAVF alone.
An open surgical approach is indicated for DAVFs with aggressive features that are not amenable to comprehensive endovascular treatment. Typically, lesions involving the anterior cranial fossa or tentorial incisura are often associated with hemorrhage; thus, surgical intervention is indicated. Surgical strategies include ligation of the fistula at the junction with the drainage vein, interruption of arterial feeders, coagulation and/ or excision of the fistula in the dura, and resection of the involved sinus.25,26,27 Recent studies have suggested that disconnection of the draining vein alone without resection of the sinus is equally efficacious as resection of the fistula. The former can avoid risks of venous hypertension associated with the sinus removal, particularly where the sinus is patent.28,29,30,31 Reported morbidity and mortality of surgical intervention has ranged from 0 to 13%.31
Stereotactic radiosurgery (SRS) has long been used for treatment of intraparenchymal AVMs, and treatment of DAVFs would be a natural extension of this. In 1993, Chandler and Friedman first reported a case in which a DAVF located in the anterior fossa was successfully treated with radiosurgery.32 Since then, radiosurgical treatment has been delivered for DAVFs in various locations including CS, transverse-sigmoid sinus, superior sagittal sinus, tentorium, and other locations.33,34,35,36,37,38,39,40,41 Radiosurgery is often combined with endovascular therapy to provide immediate relief of symptoms and possibly reduction of the hemorrhage risk.10,33,35,36,42,43,44 In some reports, DAVF obliteration rates using radiosurgery alone are comparable to those using the combined method, as the rates of symptomatic improvement.34,36,38 Complications directly related to the radiosurgical procedure are only uncommonly found.
26.1.6 Treatment Strategy for a Dural Arteriovenous Fistula
The management for a DAVF should be individualized, taking into consideration the clinical presentation of the patient, the anticipated natural history of the lesion based on location and angioarchitecture of the DAVFs, and the benefit and inherent risk of the treatment modality. It is generally agreed that DAVFs presenting with hemorrhage, progressive neurological deficits, or increased intracranial pressure require prompt treatment by endovascular embolization, surgery, or a combination of these procedures, to provide immediate relief of the venous congestion.
For Borden type II–III (or Cognard type IIb, IIa + b, III, IV, and V) lesions with a single or few CVDs, or DAVFs with an isolated dural sinus and CVDs, complete obliteration of the lesion may be achieved effectively by surgery or endovascular intervention.45,46,47 However, when DAVFs involve dural sinuses with multiple complex feeders and CVDs, surgical and endovascular treatment can be technically challenging. Lucas et al in 1997 reported a meta-analysis and concluded that even with combined therapy of surgery and embolization, over 30% of DAVFs involving transverse-sigmoid sinus will demonstrate residual filling or persistent symptoms.48 The current application of SRS can provide an additional therapeutic method to improve the treatment result.
When a treatment is indicated for Borden type I DAVF (or Cognard type I and IIa), the therapeutic benefit should outweigh the risks of the treatment. Evidence had shown that injury or increased pressure in the dural sinus could trigger the development of DAVFs or cause neurologic deficits secondary to venous hypertension.2 Thus, sacrificing a functioning dural sinus in Borden type I DAVFs by transvenous intervention or surgery may not be justified. Furthermore, it is difficult to achieve a complete obliteration of Borden type I DAVF by transarterial embolization alone due to the frequently complex and torturous course of the arterial supply.23 Studies had shown that local ischemia caused by incomplete closure of the DAVFs after endovascular and/or surgical intervention can increase expression of various vascular growth factors, which can recruit new collaterals resulting in recanalization of the DAVFs.49,50,51,52 Thus, the use of endovascular intervention or surgery as a first-line treatment for Borden type I DAVFs with the intention of palliation rather than cure should carefully balance the risks and benefits of the procedure. Our study and others’ have shown that DAVFs with benign venous drainage can be safely treated using radiosurgery with a high angiographic complete obliteration rate with preservation of functioning dural sinuses.5,34,38,41
- For Borden type I (Cognard type I, IIa) DAVFs with persistent benign symptoms (headache, pulsatile tinnitus, or eye symptoms), radiosurgery may be indicated as an initial treatment.
- For Borden type II/III (Cognard type IIa + b, IIb, III) DAVFs with retrograde CVD the following strategy is adopted:
- For symptomatic CVD24 (with hemorrhage, increased intracranial pressure, or progressive neurological deficits), surgery or endovascular procedures are indicated for the initial treatment.
- For symptomatic CVD24 (with only headache, pulsatile tinnitus, or eye symptoms, but without hemorrhage or increased intracranial pressure), endovascular procedure may be the first-line management. Alternatively, radiosurgery can be considered as an initial treatment for patients who are elderly, medically frail, or harboring complex DAVFs.
- For symptomatic CVD24 (with hemorrhage, increased intracranial pressure, or progressive neurological deficits), surgery or endovascular procedures are indicated for the initial treatment.
26.1.7 Principle and Dosage of Stereotactic Radiosurgery
SRS is characterized by a steep dose fall-off of radiation to the target margin, thereby relatively sparing the radiation exposure to surrounding normal tissues. Its application has been improved by many neurosurgeons, neuroradiologists, radiation oncologists, and physicists to advance the treatment for intracranial vascular or neoplastic lesions. Although SRS facilities change over the ensuing decades, the basic concepts have not changed: the radiobiological effects of radiosurgery on vascular lesions is due to an endothelial damage, undulation of internal elastic membrane, proliferative vasculopathy with narrowing the lumen, subendothelial cell proliferation, and, finally, complete lumen obliteration.53
Target localization of the DAVF is performed by integrating imaging data from a stereotactic noncontrast magnetic resonance imaging (MRI), a thin-cut axial view time-of-flight magnetic resonance angiography (MRA), and a cerebral X-ray angiogram. Our goal of the treatment is to occlude the fistulous shunts completely. Proper delineation of the treatment target to include all abnormal arteriovenous shunts on the dural sinus wall is crucial for a successful treatment (► Fig. 26.2, ► Fig. 26.3) The target volume is defined along the involved dural sinus wall where the true arteriovenous fistula occurs.2,17,38,54,55 The remote arterial feeders and drainage veins distal to the sinus are excluded from the treatment volume, as they are not considered a part of the true nidus.
Fig. 26.2 Dosing plan for a cavernous sinus dural arteriovenous fistula. Red: optic apparatus. Green: the oculomotor nerve. Yellow: the radiation volume.