Intracranial Dural Arteriovenous Fistulas
Pearls
A dural arteriovenous fistula (DAVF) is an abnormal connection between an artery or arteries that supply the dura mater and a vein or venous sinus contained within the leaflets of dura, not in the brain parenchyma, with similar hemodynamics to a brain arteriovenous malformation (AVM): low resistance, high flow arteriovenous shunting, and a susceptibility to hemorrhage that is three to five times greater than brain AVMs.
Dural arteriovenous fistulas are acquired lesions that develop in response to venous pathology: venous hypertension, caused by any venous outflow occlusion, impairs cerebral perfusion and produces venous ischemia; angiogenesis factors such as hypoxiainducible factor-1 (HIF-1) and vascular endothelial growth factor (VEGF) are released as a compensatory response; and aberrant angiogenesis leads to DAVF formation, arteriovenous shunting, and exacerbation of underlying venous hypertension (angiogenesis hypothesis).
Borden type I DAVFs drain anterograde into the associated dural venous sinus or meningeal veins; type II DAVFs drain into dural venous sinuses or meningeal veins, but also have retrograde drainage into cortical veins; and type III DAVFs drain exclusively into cortical veins, without venous sinus or meningeal venous drainage. Borden types II and III are associated with increased hemorrhage risk, and treatment is indicated for these patients.
Dural arteriovenous fistulas are categorized as supratentorial, tentorial, and infratentorial. Supratentorial lesions include superior sagittal sinus and sphenoparietal sinus DAVFs, ethmoidal DAVFs, and carotid-cavernous fistulas; tentorial lesions include galenic, straight sinus, torcular, tentorial sinus, superior petrosal sinus, and incisural DAVFs; and infratentorial DAVFs include transverse-sigmoid sinus, marginal sinus, and inferior petrosal sinus DAVFs.
Surgical treatment of DAVFs consists of following the arterialized cortical draining vein retrograde to the DAVF, and then interrupting the fistulous connection between the arteries in the dura and the draining vein or veins, typically with a clip or cautery on the venous side of the fistula.
Dural arteriovenous fistulas (DAVF) are fascinating lesions. Very simply, a DAVF is an abnormal connection between an artery or arteries that supply the dura mater and a vein or venous sinus contained within the leaflets of dura. DAVFs have similar hemodynamics to brain arteriovenous malformations (AVMs), with low-resistance, high-flow arteriovenous shunting. These dangerous hemodynamics make DAVFs susceptible to hemorrhage similar to brain AVMs, often with an annual rupture risk that is three to five times greater than that of brain AVMs. The fistula resides in the dura and not in the brain parenchyma, distinguishing it from a brain AVM. Intracranial DAVFs are not nearly as common as brain AVMs, with an incidence that is one-tenth that of AVMs. DAVFs have been observed repeatedly to form in patients and can be induced experimentally with venous hypertension in animals, lending themselves to laboratory investigation. Similarities between DAVFs and brain AVMs have led to misnomers for this lesion, such as dural AVM, but it is now clear that this lesion is not a congenital malformation resulting from an embryologic mishap but an acquired lesion with a pathogenesis that is increasingly understood. Similarities between the clinical presentation of and angiographic findings in patients with DAVFs and brain AVMs can also lead to misdiagnosis of DAVFs and mistakes in management. This chapter reviews the pathogenesis, natural history, management options, and surgical techniques associated with DAVFs. These lesions can be treated safely and effectively with endovascular, microsurgical, and combined techniques, but they require a sharp diagnostic eye to plan interventions appropriately.
♦ Pathogenesis
Several hypotheses for DAVF pathogenesis have been proposed, the most common one being that of intrinsic arteriovenous channels in dura mater opening up in response to an inciting event such as venous sinus thrombosis. Pathologic and radiologic studies have identified arteriovenous communications normally present in dura mater.1 Meningeal arteries give rise to a rich anastomotic network of vessels on the outer or periosteal surface of the dura, with arterial branches to the skull, arterioles to the dura, secondary anastomotic arteries, and arteriovenous (AV) shunts. These intrinsic AV shunts are susceptible to changes in venous pressure, and increases in pressure in the venous sinuses can open these shunts to initiate arteriovenous flow. Growth of dural arteries, for example during organization of the thrombus causing a venous sinus occlusion, enlarges these arteriovenous shunts and stimulates DAVF formation.
Another hypothesis suggests that DAVFs develop from dysautoregulation of the dural arterioles.2 In the setting of chronic venous hypertension, dural arterioles vasodilate in response to elevated back pressures on the venous side. Over time, maximally dilated sphincters in arterioles lose auto-regulatory control, turning normal capillary connections into AV shunts and a DAVF. This hypothesis also implicates intrinsic dural channels that become dysfunctional in response to venous hypertension. The initiation of AV shunt flow generates positive feedback for DAVF enlargement.
Inflammation caused by venous sinus thrombosis was one of the earliest explanations of DAVF pathogenesis. Angiographically, patients presenting with an acute sinus thrombosis and no angiographic evidence of DAVF were observed on follow-up studies to have recanalized their sinus and developed a new DAVF. Pathologic studies of resected DAVF specimens demonstrated inflammatory activity, organization of thrombus, and recanalization of venous sinus, to varying degrees. Although it is easy to assume that inflammation triggered DAVF formation in these cases, venous sinus thrombosis is not an infrequent problem and the incidence of DAVF formation is low in these patients. In addition, animal models have demonstrated that sinus thrombosis alone is not sufficient for DAVF formation; venous hypertension is also required with sinus thrombosis.3
Angiogenesis was implicated in the pathogenesis of DAVFs when surgical specimens were observed to have neovascular activity in the overall inflammatory reaction to venous sinus thrombosis.4 An angiogenesis hypothesis proposes that DAVF formation results from newly formed connections between dural arteries and venous sinuses, rather than from preexisting connections opening or becoming dysfunctional. Originally, angiogenesis was considered a by-product of inflammation, but inflammatory angiogenesis at the site of sinus thrombosis fails to explain the not infrequent formation of a DAVF remote from the site of venous sinus thrombosis.
An alternative angiogenesis hypothesis proposes that DAVF formation is a response to abnormal cerebral circulation. Angiogenesis activity in dural specimens was shown to be related to elevated venous sinus pressure and angiographic DAVF formation in a rat model, establishing for the first time a causal link between noninflammatory angiogenesis and venous hypertension.5 This study by Lawton et al also demonstrated regression of DAVFs with elimination of venous hypertension. This angiogenesis hypothesis suggests that venous hypertension, which might be caused by any venous outflow occlusion, impairs cerebral perfusion and produces venous ischemia. Angiogenesis is triggered as a compensatory response, but aberrant angiogenesis may lead to DAVF formation. In this hypothesis, AV shunting exacerbates underlying venous hypertension and initiates a vicious cycle.
Subsequent investigation found increased expression of known angiogenesis factors such as vascular endothelial growth factor (VEGF) in astrocytes using similar animal models6 – 8 and in surgically resected DAVFs.9 Recently, expression of the upstream regulator of angiogenesis, hypoxiainducible factor-1 (HIF-1), demonstrated a rapid increase in response to venous hypertension, located in endothelial cells in parasagittal venules adjacent to the hypertensive sinus.8 These studies confirm the link between venous hypertension and angiogenesis, but suggest a hemodynamic mechanism rather than an ischemic mechanism ( Fig. 25.1 ). DAVF pathogenesis is far from solved, but existing evidence clarifies that this is an acquired lesion with a dynamic clinical course.
♦ Risk Factors for Dural Arteriovenous Fistula Formation
Based on this understanding of DAVF pathogenesis, cerebral venous thrombosis and conditions contributing to it are risk factors for DAVF formation. Inherited predispositions to thrombosis include factor V Leiden mutation,10 , 11 MTHFR C677T mutation,12 and prothrombin gene 20210 mutation.13 Patients who have both factor V Leiden and prothrombin gene 20210 mutations are at a higher risk of developing venous thrombosis than those with either one alone.14 – 16 These mutations have been reported in patients with DAVFs,17 – 20 and a study found a higher frequency of prothrombin gene 20210A mutation in patients with DAVF compared with controls.20 In our experience, approximately one third of patients with DAVF test positively for thrombophilia (factor V Leiden, MTHFR, and/or prothrombin gene mutations).21 In addition, these patients are more likely to present with venous sinus thrombosis or occlusion and with focal neurologic deficits. Based on these findings, we routinely test for factor V Leiden and prothrombin gene mutation in DAVF patients to help manage possible thrombotic complications. Some authors have suggested following blood levels of D-dimer as an indication of acute venous thrombosis in DAVF patients.22 Although we are particularly interested in cerebral venous thrombosis and its role in the pathogenesis of DAVFs, it should be noted that angiographic venous occlusion is present in only approximately 20% of all DAVF patients.
Head trauma is the most obvious cause of DAVF formation, with development of symptoms such as a loud cranial bruit23 at the time of injury and confirmed angiographically. The most common traumatic fistula is a direct communication between the internal carotid artery (ICA) and the cavernous sinus (carotid-cavernous fistula [CCF]), resulting from basilar skull fractures, dissections that ruptures into the cavernous sinus, direct penetrating trauma, or iatrogenic causes (e.g., transsphenoidal surgery, percutaneous trigeminal rhizotomy, or catheter angioplasty). Trauma may also involve the cranial convexity and injure superior sagittal and transverse sinuses. Posttraumatic DAVFs may present with clinical symptoms weeks to years after the head trauma.
Cranial surgery has been associated with DAVF formation, especially meningioma resection.24 – 26 We have observed small DAVFs after ventriculostomy and after craniotomy for routine vascular cases, when postoperative angiography is performed to assess complete aneurysm clipping or AVM resection. These DAVFs are probably due to local trauma, but DAVFs have been reported remote from the surgical site.
Dural arteriovenous fistulas are more common in women than men. In our experience with 400 patients, 57% were women and 43% were men. CCFs were even more likely in women (7:1 female predominance), suggesting a hormonal risk. However, this predominance is modest (2:1) in other locations such as the transverse-sigmoid sinus,27 , 28 and ethmoidal DAVFs have a male predominance. An increased frequency of DAVF diagnosis has been noted during pregnancy,29 suggesting pregnancy may predispose women to DAVF development. Most women with DAVFs develop their first symptoms later in pregnancy or in the peripartum period. Estrogen may play a role in DAVF formation, based on reports of worsened symptoms in premenstrual women with DAVFs,30 a higher prevalence of DAVF in postmenopausal women,31 and regression of DAVF with oral estrogen.32 The risk of estrogen in DAVF formation remains unproven.
Other rare causes of DAVF formation are chronic otitis media, hypertension, and arterial dysplasias such as EhlersDanlos syndrome (type IV), neurofibromatosis, and Rendu-Osler-Weber disease. Some DAVFs have no identifiable cause, and these lesions are considered spontaneous in origin.
♦ Dural Arteriovenous Fistula Classification and Natural History
Numerous classifications have been reported to help understand the varied anatomy and behavior of these diverse lesions. Djindjian and Merland were the first to propose a classification system for intracranial DAVFs, analyzing the number of fistulas, the direction of blood flow, and the venous drainage pattern. Cognard later proposed a system of five types based on drainage or reflux: anterograde venous sinus drainage (type I), reflux into cortical veins (type II), retrograde cortical venous drainage (type III), retrograde cortical venous drainage with venous ectasia (type IV), and spinal venous drainage (type V). The University of California at San Francisco (UCSF) grading system divides DAVFs into four grades: DAVFs with normal anterograde venous sinus drainage without venous restriction or cortical venous drainage (grade 1); DAVFs with both anterograde and retrograde venous sinus drainage with or without cortical venous drainage (grade 2); DAVFs with retrograde venous sinus drainage and cortical venous drainage (grade 3); and DAVFs with only retrograde cortical venous drainage (grade 4).
The number and subtleties of these classifications tends to confuse rather than simplify the angiographic interpretation of these lesions. The Borden classification unifies and simplifies these other classification and has become the more accepted system.33 Type I DAVFs drain anterograde into the associated dural venous sinus or meningeal veins. Type II DAVFs drain into dural venous sinuses or meningeal veins, but also have retrograde drainage into cortical veins. Type III DAVFs drain exclusively into cortical veins, without venous sinus or meningeal venous drainage.
The purpose of this classification is to identify DAVFs with increased risk of hemorrhage, thereby identifying those patients in need of treatment. Borden types II and III are associated with increased hemorrhage risk, and treatment is indicated in these patients. In addition to helping select patients for treatment, the Borden classification provides general guidelines for treatment. Type 1 DAVFs are treated with transarterial embolization or surgical skeletonization of the venous sinuses if venous drainage needs to be preserved. Type II DAVFs are treated by interruption of the arterialized draining cortical vein and occlusion or excision of the venous sinus. Type III DAVFs are treated by interruption of the arterialized draining cortical vein. Unlike with brain AVMs, DAVFs do not require resection, and the draining vein can be safely occluded without excising the dura containing the lesion.
♦ Clinical Presentation
Pathologic consequences of DAVF include arterialization of the venous system at the site of fistula, which can lead to venous hypertension and congestion, and can induce cerebral ischemia and hemorrhage. Some DAVFs can be benign, presenting as an incidental angiographic finding or minor symptoms like headache or pulsatile tinnitus from turbulent blood flow through the shunt. Some DAVFs can be malignant, presenting with progressive neurologic deterioration from venous ischemia or acute deterioration from intracranial hemorrhage. The variety of symptoms is wide and also includes double vision, visual obscuration, focal neurologic deficits, seizures, and progressive dementia.34 – 39 Pulsatile tinnitus, headache, and visual disturbances were the three most common presenting symptoms in our cohort of DAVF patients.21
Type of presentation and severity of symptoms are determined by the location of the fistula, the anatomy of venous drainage, and resultant alterations in cerebral hemodynamics. Alterations in hemodynamics depend on the volume of shunt flow and the degree of compromise of venous outflow. The exact mechanism has not been fully investigated and the relation to patient’s symptoms is not always clear.40 – 42 The annual risk of hemorrhage from a DAVF with cortical venous drainage is as high as 19% annually. Mortality and neurologic morbidity associated with hemorrhagic presentation has been estimated to be 20 to 30%. Cortical venous drainage and posterior fossa location of the DAVF were independent predictors of a hemorrhagic presentation.21
Dural arteriovenous fistula patients present at a mean age of 50 to 60 years. No sex predilection has been established, although men appear more likely than women to present with hemorrhage. An underlying DAVF should be suspected in patients with nontraumatic intracerebral hemorrhage (ICH) with a subarachnoid component.21 Women with DAVF more commonly present with pulsatile tinnitus than do men, whereas men usually present with nontraumatic intraparenchymal and subarachnoid hemorrhage.21
♦ Types of Dural Arteriovenous Fistulas
Our surgical experience with DAVFs consists of 81 patients, and half of these patients had DAVFs located in the tentorium ( Table 25.1 ). We categorized the tentorial DAVFs into six types: galenic, straight sinus, torcular, tentorial sinus, superior petrosal sinus, and incisural DAVFs. Therefore, DAVFs do not differentiate neatly into the usual supra- and infratentorial categories like many other intracranial lesions, and instead we consider DAVFs as supratentorial, tentorial, and infratentorial.
Supratentorial DAVFs include superior sagittal sinus and sphenoparietal sinus DAVFs, ethmoidal DAVFs, and carotid-cavernous fistulas. Infratentorial DAVFs include transverse-sigmoid sinus, marginal sinus, and inferior petrosal sinus DAVFs.
In decreasing order of frequency, the common types of DAVFs are carotid-cavernous fistula, transverse-sigmoid sinus, and superior sagittal DAVFs. However, these lesions are amenable to endovascular therapy, and the common types of DAVFs in our surgical experience are different. In decreasing order of frequency, the common types of DAVFs treated surgically are straight sinus, transverse-sigmoid sinus, and ethmoidal DAVFs.
Supratentorial Dural Arteriovenous Fistulas
Carotid-Cavernous Fistulas
A CCF is any abnormal communication between the ICA, external carotid artery (ECA), or any of their branches and the cavernous sinus. CCFs can be classified hemodynamically into high-flow and low-flow fistulas, or anatomically into direct and indirect fistulas. The Barrow classification recognizes four types of CCF: type A is a direct fistula between the intracavernous ICA and cavernous sinus; type B is a dural AV shunt between intracavernous branches of the ICA (such as the branches from the meningohypophyseal trunk or inferolateral trunk) and the cavernous sinus; type C is a dural AV shunt between meningeal branches of the ECA (such as the accessory middle meningeal artery or ascending pharyngeal artery) and the cavernous sinus; and type D is a dural AV shunt between intracavernous branches of both the ICA and ECA and the cavernous sinus. Type A CCFs usually occur in the setting of head trauma or as a result of a ruptured cavernous ICA aneurysm. These fistulas have high-flow and produce symptoms related to venous engorgement of the orbit, including pulsatile exophthalmos, chemosis, cranial nerve III, IV and VI paresis, and rarely glaucoma and visual loss. Types B, C, and D CCFs usually occur spontaneously or following minor trauma with symptoms that are less severe and more insidious in their onset. These indirect CCFs may occur at any age, but are more commonly present in women older than 40 years and may be associated with conditions such as vascular Ehlers-Danlos syndrome, hypertension, hypercoagulability, or pregnancy, among others.43 , 44 Their pathogenesis has been hypothesized in some cases to be related to prior, clinically silent, thrombosis of the cavernous sinus with subsequent formation of aberrant vascular connections during recanalization.43
DAVF | Patients | % |
Supratentorial | ||
Superior sagittal sinus | 7 | 8.6 |
Carotid-cavernous sinus | 1 | 1.2 |
Ethmoidal | 11 | 13.6 |
Sphenoparietal sinus | 5 | 6.2 |
Tentorial | ||
Galenic | 7 | 8.6 |
Straight sinus | 14 | 17.3 |
Torcular | 8 | 9.9 |
Tentorial sinus | 2 | 2.5 |
Superior petrosal sinus | 8 | 9.9 |
Incisural | 2 | 2.5 |
Infratentorial | ||
Transverse-sigmoid sinus | 13 | 16.0 |
Marginal sinus | 3 | 3.7 |
Inferior petrosal sinus | 0 | 0.0 |
Total | 81 | 100.0 |
Type A CCFs require treatment to prevent progressive visual loss, reverse unsightly exophthalmos, or eliminate intolerable bruits or pain. The treatment is endovascular, occluding the fistula with a detachable balloon deployed from a microcatheter in the ICA and inflated in the fistula. These Supratentorial CCFs can also be occluded transvenously with coils in the cavernous sinus, deployed using microcatheters that reach the fistula via the internal jugular vein and inferior petrosal sinus.
Cavernous sinus DAVFs (types B, C, and D) have a benign natural history and often resolve spontaneously. Carotid self-compression (20 seconds, three to four times per hour when awake, using the contralateral hand) may promote thrombosis of the DAVF, but is contraindicated in patients with high-grade carotid stenosis or ulcerative plaques. Endovascular intervention is indicated in patients with visual deterioration, progressive intraocular hypertension, obtrusive diplopia, proptosis with corneal exposure, or intolerable bruit. ECA feeding arteries can be embolized safely in patients with types C and D CCFs, usually resulting in cures. Persistent lesions can be treated additionally with transvenous embolization. Selective catheterization of ICA feeding arteries is more difficult, and embolization is associated with an increased risk of cerebral emboli, but type B lesions are rare. Refractory CCFs that fail endovascular therapy and remain with retrograde cortical venous drainage may require surgical intervention to occlude the vein and interrupt the fistula ( Fig. 25.2 ).
Superior Sagittal Sinus Dural Arteriovenous Fistula
Superior sagittal sinus (SSS) DAVFs are uncommon, but the difficulty in curing these lesions endovascularly makes them more prevalent in surgical series. In our experience, seven of 81 patients (9%) had SSS DAVFs with high-risk features. These lesions can present with pulsatile tinnitus, signs of raised intracranial pressure, or signs of raised cavernous sinus pressure from diversion of venous outflow. Local symptoms, such as focal seizures or focal neurologic deficits, can result in venous engorgement or varix formation and mass effect.
Superior sagittal sinus DAVFs are supplied by middle meningeal arteries or their branches. Scalp arteries (superficial temporal and occipital arteries) can also supply these DAVFs, as can cortical arteries. Venous drainage is primarily to the SSS, but these can be Borden type II or III lesions with cortical venous drainage through convexity veins. SSS DAVFs can be embolized transarterially with ease, but numerous meningeal feeding arteries make them difficult to cure. Fistulas with cortical venous drainage can also be difficult to cure endovascularly because there is typically poor access from the venous side.
Superior sagittal sinus DAVFs requiring surgery are exposed with a midline craniotomy over the sinus and the fistula. Cutting the craniotomy flap over the sinus requires careful preservation of the dura, particularly in older patients with adherent dura. Two separate flaps may be needed to first expose the ipsilateral dura and to allow the sinus to be dissected from the inner table of skull before crossing the midline with the second flap. Surgical management of the fistula depends on its Borden type. Type I SSS DAVFs are treated by skeletonizing the SSS extensively, eliminating the arterial supply while preserving normal flow in the sinus. Type III SSS DAVFs are treated by interrupting the fistula on its venous side as it exits the sinus, usually by clipping the vein, cauterizing it, and dividing it. Type II SSS DAVFs are treated with a combination of skeletonization of the sinus and interruption of arterialized veins.
Related posts:
Stay updated, free articles. Join our Telegram channel
Full access? Get Clinical Tree
