Chapter 80 Surgical Management of Cranial Dural Arteriovenous Fistulas
DAVFs account for approximately 5% to 20% of all intracranial vascular malformations.1,2 They can occur at any age, but the mean age at presentation in most studies lies between the sixth and seventh decades of life.2,3 The term “dural arteriovenous malformation” has been applied by some authors to all types of DAVFs, both pediatric and adult. However, malformation implies a congenital origin. We prefer to use the term DAVF because, at least in adults, there is good evidence that these lesions are acquired rather than congenital.4–6 The rare exception is in the pediatric age group in whom congenital malformations of dural venous sinuses are associated with high-flow arteriovenous fistulas.7
Pathogenesis
The etiologic factors and mechanisms involved in the pathogenesis of DAVFs are poorly understood. DAVFs are associated with several conditions including head injury, previous craniotomy, and dural venous sinus thrombosis, suggesting that they are acquired rather than congenital lesions.4,7 According to the most popular theory, DAVFs are formed as a consequence of thrombosis and subsequent recanalization of dural venous sinuses.8,9 Venous hypertension is thought to play an important role in this process. Indeed animal studies have shown that venous hypertension, even in the absence of sinus thrombosis, can elicit the formation of DAVFs.6 Whether sinus thrombosis is in fact the initial event in the genesis of DAVFs is controversial.8 Only a small number of patients with sinus thrombosis go on to develop DAVFs, and not all DAVFs are associated with sinus thrombosis.4,10
What follows sinus thrombosis and venous hypertension is also controversial. Two hypotheses have been proposed. The first suggests that DAVFs arise from opening up of preexisting microscopic vascular channels within the dura mater. These preexisting channels are thought to open up or enlarge as a result of venous hypertension secondary to sinus thrombosis.7 The second hypothesis suggests that DAVFs result from the formation of new vascular channels in the dura, a process stimulated and regulated by angiogenic factors. To support this, surgical DAVF specimens have been shown to contain basic fibroblastic growth factor and vascular endothelial growth factor, which were absent in control specimens.11,12 Angiogenic factors may originate either directly as part of the inflammatory process that occurs during organization and recanalization of a thrombosed sinus or indirectly as a result of cerebral ischemia secondary to venous hypertension.13 If the angiogenic theory is true, antiangiogenic agents may provide an adjuvant therapy for patients with untreatable DAVFs.8
Many cranial DAVFs ultimately undergo spontaneous resolution. The exact mechanism for this is unknown, but it is thought to result from progressive thrombosis of the involved dural sinus. This is paradoxical in that the cause of the abnormality is also thought to be the curing process. In some cases, however, spontaneous resolution has occurred despite sinus patency.14
Classification
Ideally, a classification system should predict the clinical behavior of a lesion and aid in therapeutic decision making. Several classification schemes have been devised for DAVFs.15–19 The most commonly used are those of Borden and colleagues16 (Borden classification) and Cognard and colleagues17 (Cognard classification) (Table 80-1 and Fig. 80-1). Both are based on the pattern of venous drainage of the lesion, the factor that best predicts the clinical presentation and natural history of DAVFs. The Cognard classification, which is a modification of the classification of Djindjian and colleagues,18 divides cranial DAVFs into five types, based on the presence or absence of CVR, sinusal drainage, and direction of flow in the involved dural sinus.17
Table 80-1 Venous Drainage Pattern of Dural Arteriovenous Fistulas According to Borden and Cognard Classification Schemes
| Borden Classification | Cognard Classification |
|---|---|
| Type I: Drainage into dural venous sinus or meningeal vein only | Type I: Drainage into dural venous sinus only, with normal antegrade flow Type IIa: Drainage into dural venous sinus only, with retrograde flow |
| Type II: Drainage into dural venous sinus or meningeal vein + CVR | Type IIb: Drainage into dural venous sinus (antegrade flow) + CVR Type IIa + b: Drainage into dural venous sinus (retrograde flow) + CVR |
| Type III: CVR only | Type III: CVR only without venous ectasia Type IV: CVR only with venous ectasia Type V: Drainage into spinal perimedullary veins |
CVR, cortical venous reflux. This has also been referred to as cortical venous drainage,3 retrograde leptomeningeal venous drainage,20 and drainage into subarachnoid veins.16
Data from Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg. 1995;82:166-179; Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194:671-680.
The Borden classification16 is a more simplified scheme with three types based on the presence or absence of CVR and sinusal drainage, without taking into account the direction of flow in the venous sinus. In a study by the University of Toronto Brain Vascular Malformation Study Group, Davies and colleagues19 validated the classification systems of Borden and of Cognard with respect to clinical presentation. Aggressive presentation (i.e., intracranial hemorrhage [ICH], focal neurologic deficit, or death) occurred in 2% of the Borden classification type I, 39% of type II, and 79% of type III cranial DAVFs. Similar correlation was found between the Cognard classification and clinical presentation (Table 80-2).19 Subsequent studies by our group have demonstrated that the pattern of venous drainage and in particular the presence or absence of CVR also correlate with the natural history of DAVFs after the initial presentation.3,20
Table 80-2 Relationship between Aggressive Clinical Presentation and Classification of 102 Cranial DAVFs
| Classification and Type | % of DAVFs with Aggressive Clinical Presentation (i.e., ICH or NHND) |
|---|---|
| Borden type I (n = 55) | 2 |
| Cognard type I (n = 40) | 0 |
| Congard type IIa (n = 15) | 7 |
| Borden type II (n = 18) | 39 |
| Cognard type IIb (n = 8) | 38 |
| Cognard type IIa + b (n = 10) | 40 |
| Borden type III (n = 29) | 79 |
| Cognard type III (n = 13) | 69 |
| Cognard type IV (n = 12) | 83 |
| Cognard type V (n = 4) | 100 |
DAVFs, dural arteriovenous fistulas; ICH, intracranial hemorrhage; NHND, nonhemorrhagic neurologic deficit.
From Davies MA, TerBrugge K, Willinsky R, et al. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg. 1996;85:830-837.
DAVFs were previously classified according to their anatomic location.21 Anterior cranial fossa and tentorial lesions were associated with a higher risk of aggressive clinical behavior than lesions in other locations.1,19 However, it was later shown that the poor prognosis of lesions in these “dangerous” locations was purely a function of their pattern of venous drainage.19,22 It is the presence of CVR, not the anatomic location per se, that leads to aggressive clinical behavior.1,19 Hemodynamically, DAVFs may be classified into high-flow or low-flow fistulas. The classification of Barrow and colleagues23 is described later in the section on carotid cavernous fistulas. The classification of pediatric DAVFs is not discussed in this chapter.
Clinical Presentation
Other than pulsatile tinnitus, the symptoms of DAVFs are related to venous hypertension.7,24 This may lead to venous congestion, cerebral edema, cerebral infarction, and ICH. The clinical features of cranial DAVFs are shown in Table 80-3. ICH, nonhemorrhagic neurologic deficit (NHND), and death are considered aggressive.1,19 The most significant risk factor for aggressive clinical presentation is the presence of CVR.1,17,19 Therefore, type II and III lesions of the Borden classification are frequently associated with aggressive clinical behavior, whereas type I lesions are rarely so (see Table 80-2). ICH associated with DAVFs typically results from rupture of an arterialized cortical vein and is usually intraparenchymal but may also occur into the subarachnoid, subdural, and intraventricular spaces (Fig. 80-2). NHND is caused by cerebral ischemia secondary to venous congestion. This category does not include ophthalmoplegia secondary to cranial nerve dysfunction. The neurologic deficit may be focal or global.
Table 80-3 Clinical Manifestations of Dural Arteriovenous Fistulas
| Intracranial hemorrhage |
| Focal neurologic deficit (e.g., motor weakness, aphasia, cerebellar signs, progressive myelopathy) |
| Global neurologic deficit (e.g., dementia) |
| Pulsatile tinnitus, objective bruit |
| Proptosis, conjunctival injection, chemosis |
| Ophthalmoplegia (secondary to extraoccular muscle swelling, or compression of cranial nerves III, IV, VI) |
| Visual loss (secondary to orbital congestion and increased intraocular pressure, retinal hemorrhages, or optic neuropathy) |
| Glaucoma |
| Papilledema (secondary to hydrocephalus or pseudotumor cerebri caused by impaired venous drainage) |
| Facial pain (secondary to compression of the first and second divisions of trigeminal nerve in lateral wall of cavernous sinus) |
FIGURE 80-2 A, Axial computed tomography scan of a 56-year-old man who presented with sudden headache followed by loss of consciousness shows intracerebral and intraventricular hemorrhage. B, Right common carotid artery angiogram, lateral projection, shows a transverse sinus dural arteriovenous fistula (DAVF), fed by branches of the right middle meningeal artery (arrow) and the right occipital artery (large arrow). Venous drainage was by reflux into a cortical vein (white arrow) leading to an ectasia (arrowheads). There was no sinusal drainage, making this a Borden type III/Cognard type IV DAVF. In this patient, selective angiography was not possible because of severe atherosclerosis and tortuosity of the carotid arteries. C, Postoperative angiogram after right occipital craniotomy exposing the transverse sinus. The dura was opened and reflected inferiorly based on its attachment to the transverse sinus. The DAVF was treated by coagulation and division of this vein close to the transverse sinus, at the site shown by the white arrow in Figure 80-3B.
Benign symptoms include pulsatile tinnitus and orbital symptoms. Pulsatile tinnitus is produced by turbulent flow in the diseased dural sinus.4 Objective bruit is heard in 40% of patients with tinnitus. Ophthalmologic symptoms and signs are most commonly seen with cavernous sinus DAVFs, but they can also occur with lesions in other locations, if the venous drainage involves the cavernous sinus and ophthalmic veins.25 The symptoms are caused by venous congestion.4,26 The ophthalmologic symptoms may be progressive and disabling and may even lead to blindness and therefore may not be considered benign by the patient. In infants, heart failure and craniomegaly may occur.
Radiographic Evaluation
Computed Tomography and Magnetic Resonance
In cases of DAVF without CVR, computed tomography and magnetic resonance imaging (MRI) of the brain parenchyma are typically normal. However, MRI and magnetic resonance angiography may show the stenosis or occlusion of the dural sinuses.7 Hydrocephalus may be seen in any DAVF that causes venous hypertension in the superior sagittal sinus. In cases of DAVF with CVR, computed tomography and MRI of the brain may show ICH, engorged pial vessels, and diffuse white matter edema secondary to venous congestion. The ICH is usually intraparenchymal but may also have subdural, subarachnoid, or intraventricular components (see Fig. 80-2). The pattern of hemorrhage is not specific to DAVFs, and a high index of suspicion is required. Dilated pial vessels and white matter edema are more likely to be seen on MRI than on computed tomography.7 On T2-weighted MRI, dilated pial vessels are seen as flow voids on the surface of the brain, and diffuse white matter edema is seen as hyperintensity in the cerebral or cerebellar hemispheres, brain stem, or spinal cord (Fig. 80-3). Recent reports have demonstrated improvements in the ability of magnetic resonance angiography to diagnose DAVFs and to detect CVR.27 However, these results have been reported in small selected series and require further study. At present, the diagnosis of DAVFs cannot be excluded with negative computed tomography, MRI, or magnetic resonance angiography. If clinically suspected, catheter angiography is required to confirm or exclude the presence of a DAVF.
Intra-arterial Catheter Angiography
This is the gold standard method for diagnosis and evaluation of DAVFs. The characteristic angiographic feature of DAVFs is premature visualization of intracranial veins or venous sinuses during the arterial phase (see Fig. 80-3C; Fig. 80-4A).28 This is caused by shunting of arterial blood into the venous system through the fistula. To obtain the necessary information regarding the arterial supply and venous drainage of the DAVF and the venous drainage of the brain, imaging must start in the ultraearly arterial phase and be carried well into the late venous phase. Selective angiography with magnification and subtraction techniques is essential. The study should include injections of both internal carotid arteries (ICAs), both external carotid arteries (ECAs), and both vertebral arteries. This is because a single DAVF may have multiple feeding arteries (see Figs. 80-3 and 80-4) and also because 8% of patients have multiple DAVFs.29 Detailed knowledge of dural arterial anatomy is essential in angiographic evaluation of DAVFs. Meningeal arteries that are invisible or difficult to see on normal angiograms may be dilated and clearly visible when supplying a DAVF. For example, the tentorial branch of the meningohypophyseal trunk of the ICA (the artery of Bernasconi and Cassinari) or the meningeal branch of the posterior cerebral artery (the artery of Davidoff and Schecter) may be dilated and easily seen on the angiograms (see Fig. 80-3C).
FIGURE 80-4 Angiograms of a 52-year-old woman who presented with pulsatile tinnitus and audible bruit behind the right ear. A, Right external carotid artery angiogram, lateral projection shows premature appearance of the sigmoid sinus (arrowheads) in the ultraearly arterial phase of the angiogram. A transverse sinus dural arteriovenous fistula (DAVF) is shown, fed by the posterior branch of the right middle meningeal artery (arrow) and draining antegradely into the transverse/sigmoid sinus (arrowheads) without any cortical venous reflux (CVR) (Borden type I, Cognard type I). The same DAVF is shown in Figure 80-1A being fed also by the right occipital artery. B, Right internal carotid artery angiogram, lateral projection, revealed a hypertrophied artery of Bernasconi and Cassinari, also supplying the DAVF (arrow). As there was no CVR, the patient was managed with observation alone.
The nidus of a DAVF is the site of arteriovenous shunting and refers to that part of the dura where there is convergence of all feeding arteries and the origin of venous draining channels. The best views of the nidus are often obtained during the ultraearly arterial phase of the angiogram and by injections of distant arterial feeders.28 Images obtained when injecting the main arterial feeders, particularly in the later arterial phase or in the venous phase, are often obscured by engorged feeding arteries and draining veins.
Assessment of the venous drainage pattern of DAVFs is extremely important as this factor determines the natural history of the lesion and aids in selecting the most appropriate management strategy. The presence or absence of CVR, venous sinus occlusion, direction of flow in the venous sinuses, and the venous drainage pattern of the brain must be determined. The exact site of CVR must be determined to allow treatment planning.7 At angiography, a delayed circulation time is compatible with venous congestion.30 Focal areas of delayed venous drainage in the brain correspond to the site of CVR.7 In some cases, tortuous, dilated pial veins may be seen that develop as a result of venous hypertension (see Fig. 80-3F). Willinsky and colleagues30 have described this finding as the pseudophlebitic pattern, which is a sign of venous congestion of the brain and may be associated with an aggressive natural history.7
Natural History
The natural history of a disease refers to the disease course after presentation if left untreated. Knowledge of the natural history is essential in patient management. The results and complications of available treatment strategies must be compared with the outcome of the natural history of the disease. Recently, our group reported the results of the largest prospective natural history studies of patients with cranial DAVFs.3,20 The results, summarized in the following, showed that the presence of CVR is the most significant predictive factor for an aggressive natural history.3,20
Dural Arteriovenous Fistulas with Cortical Venous Reflux
Of 236 cranial DAVFs, 119 had CVR (Borden classification type II or III and Cognard classification type IIb, IIa + b, III, or IV). Of these, 96 patients successfully underwent curative treatment, and three patients were lost to follow-up. Van Dijk and colleagues20 followed the remaining 20 patients with persistent CVR (14 patients who refused treatment and 6 who had partial treatment only) for a mean follow-up period of 4.3 years (86.9 patient-years). In these 20 patients, the annual risks of ICH and NHND (disregarding aggressive events at presentation) were found to be 8.1% and 6.9%, respectively, adding up to an annual event rate (i.e., ICH and NHND) of 15%. The annual mortality rate was 10.4%. These results demonstrate that DAVFs with CVR have an aggressive natural history.
Dural Arteriovenous Fistulas without Cortical Venous Reflux
Of the 236 cranial DAVFs, 117 had no CVR (Borden type I, Cognard type I or IIa). Five patients were lost to follow-up. The remaining 112 patients were followed up clinically for a median of 27.9 months (range, 1 month to 17.5 years), amounting to 348 patient-years. Of these, 68 underwent observation alone, and 44 underwent palliative treatment for symptomatic control (43 endovascular, 1 surgery). Palliative treatment, never aimed at cure, was performed if the patient had intolerable symptoms or if there was persistent high intraocular pressure or decreasing visual acuity. Using this conservative management strategy, 98% of patients had a benign and well-tolerated clinical course, without any ICH or NHND.3 Long-term angiographic follow-up in 50 patients showed that DAVFs without CVR have a 2% to 3% risk of developing CVR.3
Indications for Treatment
Decisions regarding treatment of DAVFs should be guided by their natural history. Therefore, DAVFs with CVR should be treated to eliminate the risk of hemorrhage and neurologic deficit. The aim of treatment in these cases is elimination of CVR or complete cure if possible. Lesions without CVR do not require treatment unless they are associated with intolerable symptoms such as intolerable tinnitus and ophthalmologic symptoms including visual deterioration and pain. For these lesions, the aim of treatment is not cure, but palliative symptom control.
Management Options
Observation
DAVFs without CVR usually behave in a benign manner and are rarely associated with hemorrhage or neurologic deficit. Therefore, observation is the most appropriate management option for these patients if they are asymptomatic or are tolerating their symptoms.4,7 As they have a 2% to 3% chance of developing CVR, all patients should be followed up clinically and radiographically. Any change in symptoms (worsening or improvement) may be a warning signal for development of CVR and should prompt repeat cerebral angiography.3,7 In patients with a stable clinical condition, serial MRI and magnetic resonance angiography and a conventional angiogram after 3 years is advised.7 Observation is not a valid treatment option for DAVFs with CVR.
Compression Therapy
Intermittent manual carotid compression by the patient has been used by Halbach and colleagues,8,31 to treat DAVFs of the cavernous sinus in patients with no evidence of carotid atherosclerosis. The patient is instructed to compress the carotid-jugular area ipsilateral to the DAVF, with the contralateral hand for as long as 30 minutes per session. The compression should be terminated if any weakness develops.8 Halbach and colleagues8,31 reported a cure rate of 27% with this technique after 4 to 6 weeks. However, this treatment has been the subject of debate because the 27% cure rate in the short term may reflect the natural history of the disease.7
Transarterial Embolization
Superselective embolization of the dural feeding vessels to a DAVF can be an effective treatment in some cases.8 The ideal goal is to cure the DAVF by occluding the fistula itself. To achieve this from the arterial side, a microcatheter must be navigated into the distal part of a feeding artery and wedged, so that cyanoacrylate glue can be pushed through the nidus and into the most proximal venous outlet. This is essentially a venous treatment performed through the arterial side. Liquid adhesive agents (e.g., n-butyl cyanoacrylate), the rate of polymerization of which can be controlled, are the best agents to permanently occlude a fistula.7 Successful occlusion of the fistula using this technique has been reported in a small number of patients.7,32
In most cases, transarterial embolization involves occlusion of the feeding arteries without occlusion of the fistula. This may decrease flow through the fistula but is rarely curative because most DAVFs have multiple small feeding arteries that are not amenable to transarterial embolization. Furthermore, in most cases, the lesion will continue to recruit feeding arteries from other sources, leading to recurrence.8,32 Transarterial embolization is commonly used as an adjunct before surgical treatment or transvenous embolization of DAVFs. It is also used as palliative treatment for benign DAVFs with intolerable symptoms. Preoperative embolization of large feeding arteries, particularly in the external carotid territory, carries a relatively low risk and helps to reduce intraoperative blood loss. Particles (e.g., polyvinyl alcohol) may be used for this purpose.7
Endovascular therapy is not without risk. Knowledge of the important anastomoses between the external carotid, internal carotid, and vertebrobasilar systems is crucial for safe embolization.33 Embolic agents can inadvertently travel through these anastomoses and lead to occlusion of important branches. Embolization of feeding arteries that arise directly from the ICA or vertebral artery may lead to reflux of embolic material into the parent artery and result in stroke. In the case of benign DAVFs, it is important to ensure that the embolic material does not flow past the fistula site and obstruct venous outflow. If this occurs, venous drainage may be diverted to cortical veins, thereby converting a benign fistula to an aggressive one.
Transvenous Embolization
Transvenous embolization is increasingly used in the management of cranial DAVFs.34,35 This involves a retrograde approach through the veins with deposition of materials such as coils into the venous compartment at the fistula site. Usually the transfemoral route is employed. In the majority of cases, transvenous embolization involves sacrificing the involved dural venous sinus. This can only be performed if detailed study of the venous phase of the cerebral angiogram has shown that the involved dural sinus is not being used by the brain and that alternate pathways for venous drainage of the brain have developed.7 In some cases it may be possible to use a retrograde transvenous approach to disconnect CVR without sacrificing the dural sinus. However, in most cases this is not possible because of the difficulty in access to the refluxing cortical veins and the tortuosity of these veins.
In some cases of transverse/sigmoid sinus DAVFs, the lesion may be draining into a venous pouch, parallel to and separate from the transverse sinus. The University of California-San Francisco interventional neuroradiology group have reported 10 such cases and named this entity the parallel venous channel. In their series, transvenous embolization was used to occlude the parallel venous channel and cure the fistula in all 10 cases while preserving the transverse/sigmoid sinus.36
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