Natural History and Management Options of Cranial Dural Arteriovenous Fistulas

21 Natural History and Management Options of Cranial Dural Arteriovenous Fistulas

Hugo Andrade-Barazarte, Felix Goehre, Behnam Rezai Jahromi, Zhao Tongyuan, Jiangyu Xue, Zhongcan Cheng, Ajmal Zemmar, Tianxiao Li, and Juha Hernesniemi

Abstract

Intracranial dural arteriovenous fistulas (DAVFs) are pathological anastomoses between meningeal arteries and dural venous sinuses or cortical veins. DAVFs are rare lesions having a documented incidence between 10 and 15% among all intracranial vascular malformations. DAVFs frequently affect patients in their middle-to-later years of life (e.g., 50–60 years of age) and tend to present with a wide variety of symptoms such as intolerable pulsatile tinnitus, exophthalmos and chemosis (when the fistula is in the cavernous sinus), progressive dementia, seizures, or neurological deficits often caused by intraparenchymal hemorrhage. Classification of DAVFs is based on their venous drainage and characteristics, as an attempt to predict their clinical behavior. One of the most important features among these classifications is the distinction (presence or absence) of cortical venous drainage (CVD). The natural history of DAVFs depends on their clinical presentation and the presence of CVD. Therefore, we subdivided the DAVFs in fistulas without CDV or low-grade, and fistulas with CVD or high-grade based on their angioarchitecture and clinical presentation. Low-grade fistulas have a reported annual rate of new neurological event from 0 to 0.6% and an annual mortality rate of 0%. High-grade fistulas have an aggressive natural history and a high risk of early rebleeding of about 35% within 2 weeks after the first hemorrhage with an annual mortality rate of 10.4%. The treatment strategy should be tailored individually to patients considering the anatomical features of the DAVF, the severity of symptoms, and the potential risk of intracranial hemorrhage.

Keywords: dural arteriovenous fistulas DAVF hemorrhage neurological deficit cortical venous drainage venous ectasia

21.1 Introduction

Intracranial dural arteriovenous fistulas (DAVFs) are pathological anastomoses between meningeal arteries and dural venous sinuses or cortical veins.43 They differentiate from brain arteriovenous malformations (AVMs) due to the lack of a parenchymal nidus and the arterial supply vessels only arise from arteries that typically perfuse the dura mater.³⁶ DAVFs are uncommon lesions having a reported incidence of between 10 and 15% among all intracranial vascular malformations (6% supratentorial and 35% infratentorial vascular malformations).³⁷ It has been suggested that there is a slightly higher incidence of DAVFS among Finnish and Japanese populations (incidence of 29–32%).⁴⁰^, ⁴⁵ DAVFs frequently affect patients in their middle to later years of life (50–60 years),⁶ and there is no clear sex predilection or genetic components associated with DAVFs.

Clinical presentation of DAVFs depends on the location of the fistula. Typically, patients may present with intolerable pulsatile tinnitus (transverse–sigmoid sinus junction), exophthalmos and chemosis (cavernous sinus [CS]), progressive dementia (superior sagittal sinus), seizures, or neurological deficits often caused by intraparenchymal hemorrhage.²⁹^, ⁴⁰ DAVFs are frequently located at the transverse–sigmoid junction and also at the CS, superior sagittal sinus, anterior cranial fossa, and tentorium, among others.²⁹^, ³⁶

Various classification systems have been described to predict high-risk fistulas and to guide treatment decision-making. These classification systems are based on angiographic characteristics of the DAVF such as involvement of a venous sinus and presence or absence of retrograde cortical venous drainage (CVD), as well as clinical presentation (hemorrhagic vs. nonhemorrhagic neurological deficits [NHND]).⁴^, ⁶^, ¹³^, ⁵⁶

21.1.1 Pathophysiology

The pathophysiological development of DAVFs remains unclear. It is generally accepted that DAVFs are acquired lesions, with a small subgroup that develops following direct trauma, infection, previous craniotomies, tumors, or venous sinus thrombosis.⁵^, ⁷^, ⁵⁵

One accepted theory regarding DAVF formation is that these lesions arise from progressive stenosis or occlusion of a dural venous sinus. As venous pressure increases, meningeal arteries develop fistulous connections with the dural sinus or cortical veins, which may occur due to the presence of de novo fistulas based on neoangiogenesis or due to the enlargement of preexisting physiological shunts.¹¹^, ²⁶^, ³⁷ These result in a complex network of venous tributaries under arterial pressure with progressing sinus outflow obstruction and venous hypertension. Therefore, the regular and normal antegrade venous flow pattern is altered and reversed resulting in retrograde flow through cortical veins (CVD), which can cause venous hypertension within the surrounding brain.¹¹^, ²⁶^, ³⁷

DAVF formation is a dynamic process since their hemodynamic may change over time due to the recanalization of the respective sinus or in contrary with the recruitment of more arterial feeders (with the possible progression from a low-risk DAVF to a higher grade). It is thought that intracerebral hemorrhage (ICH) occurs when fragile arterialized parenchymal veins rupture due to the presence of unrelenting venous reflux and cortical venous hypertension.⁵^, ⁶^, ¹³^, ²⁶^, ⁵²

Carotid cavernous fistulas (CCFs) involve an abnormal connection between the internal carotid artery (ICA), external carotid artery (ECA), and the CS. These fistulas comprise a particular subgroup among intracranial DAVFs.³ CCFs are defined based on their pathogenesis (spontaneous vs. traumatic), angioarchitecture (direct shunt from the cavernous ICA or its branches, shunt from branches of the ECA, or a combination of both), and hemodynamics (high vs. low flow).³ Commonly, direct CCFs occur as a result of trauma (skull base fracture or iatrogenic) involving the vessel wall at the horizontal segment of the cavernous ICA or because of rupture of an aneurysm at the cavernous ICA, which results in a high-flow fistula between the ICA and the CS.³^, ¹⁰

Indirect CCFs are normally associated with medical comorbidities such as diabetes mellitus, hypertension, collagen vascular disease, and pregnancy, among others. These fistula subtypes are typically low-flow lesions that occur spontaneously.3

Due to the specific characteristics and venous drainage, CCFs have been considered a different pathological entity as DAVFs. Accordingly, their natural history and treatment options are not discussed.

21.1.2 Classification

Classification of DAVFs is based on venous drainage patterns. The most commonly used classifications are the Borden–Shucart and Cognard classifications.⁴^, ¹² One of the most important features among these classifications is the distinction (presence or absence) of CVD.

Borden–Shucart classification: Type I fistula is characterized by the absence of CVD; this type harbors dural arteries that drain exclusively into a dural sinus with antegrade venous flow. Type II and III fistulas are characterized by the presence of CVD. Type II fistulas drain into a dural sinus with venous flow that is both antegrade into the dural sinus and retrograde into the cortical veins, whereas type III fistulas drain exclusively into cortical veins in a retrograde fashion.⁴

Cognard classification: This classification is based on venous drainage characteristics, shunt location, and venous outflow.⁴ The Cognard classification includes five subtypes of DAVF. type I and IIa DAVFs are similar to Borden–Shucart type I (absence of CVD) DAVFs, where type I lesions drain antegrade into a dural sinus and type II lesions drain retrograde into a venous sinus. Type IIb fistulas drain antegrade into a venous sinus and show cortical venous reflux (presence of CVD). Type IIa + IIb DAVFs drain retrograde into a venous sinus and have cortical venous reflux. Type III fistulas drain directly into a cortical veins and type IV fistulas besides draining into cortical veins also show signs of venous ectasia. Type V DAVFs drain directly and exclusively into spinal perimedullary veins.

From these two previous classifications, Borden–Shucart type II and III and Cognard type IIb to V DAVFs are considered high-grade fistulas with a more aggressive natural history due to the presence of CVD.

Additionally, Zipfel et al in 2009 proposed a modified classification based on the Borden–Shucart classification.⁵⁶ This new modification includes clinical data regarding the presentation of the DAVF (asymptomatic, hemorrhage, or NHNDs) besides well-identified angiographic parameters. This simple classification system accurately predicts the risks of hemorrhagic and nonhemorrhagic events. Therefore, it is extremely important for risk stratification to guide further management and treatment.⁵⁶ Table 21.1 summarizes the classifications mentioned earlier.

Table 21.1 Different dural arteriovenous classifications with their respective characteristics, natural history, and management

Borden–Shucart type	Cognard type	Zipfel type	Venous drainage	Presence of CVD	Cortical venous hypertension	Clinical presentation (ICH or NHND)	Risk of ICH (%)	Mortality risk	Management
I	I, IIa	1	Dural sinus	No	No	No	0	0	Conservative
II	IIb, IIa + IIb	2A	Dural sinus	Yes	No	No	1.4–1.5	0	Elective treatment to eliminate risks
II	IIb, IIa + IIb	2S	Dural sinus	Yes	Yes	Yes	7.4–7.6	3.8%	Early treatment
III	III–V	3A	Cortical vein	Yes	No	No	1.4–1.5	0	Elective treatment to eliminate risks
III	III–V	3S	Cortical vein	Yes	Yes	Yes	7.4–7.6	3.8%	Early treatment
Abbreviations: CVD, cortical venous drainage; ICH, intracerebral hemorrhage; NHND, nonhemorrhagic neurological deficit.

Fig. 21.2 (a, b) Axial sections of T2-weighted magnetic resonance imaging study showing large vascular flow voids near the left anterior fossa floor and left Sylvian fissure. Digital subtraction angiography on (c) lateral and (d) anteroposterior views after a left external carotid artery contrast injection showing a Borden–Shucart type III intracranial dural arteriovenous fistula draining into a cortical frontal vein causing venous ectasia and a large venous varix. Digital subtraction angiography on (e) lateral and (f) anteroposterior views after a left internal carotid artery contrast injection showing a Borden–Shucart type III intracranial dural arteriovenous fistula feed by ethmoidal branches of a hypertrophic ophthalmic artery.

21.1.3 Clinical Presentation and Imaging Evaluation

DAVF patients can present with pulsatile tinnitus, exophthalmos, and chemosis among other symptoms due to increased sinus drainage, which may occur in any kind of DAVF with venous sinus drainage (Fig. 21.1). Moreover, patients can present with more aggressive symptoms such as seizures, strong headaches, or decreased conscious level related to the presence of ICH or NHND caused by cortical venous hypertension, which only develops in a DAVF with CVD.²⁹^, ⁴⁰ Hemorrhagic symptoms occur acutely, whereas NHNDs are gradually developed over days to weeks as the product of focal or global cortical venous hypertension that causes different degrees of cerebral ischemia.²³^, ²⁷

Fig. 21.1 Right eye unilateral exophthalmos and chemosis in a patient with caroticocavernous fistula (CCF).

Regarding the initial imaging evaluation, computed tomography (CT) can detect DAVF-related ICH and vasogenic edema caused by cortical venous hypertension. Often, venous varices are the cause of hemorrhage, and these can be located distally from the actual DAVF.¹⁵ Magnetic resonance imaging (MRI) is helpful to identify the anatomy of the DAVF and its location in relation to the brain. On T2-weighted images, it is possible to identify the presence of flow voids from large arterialized draining veins and varices (Fig. 21.2a). Additionally, postcontrast T1-weighted images can show dilated leptomeningeal and medullary vessels, venous ectasia, parenchymal enhancement, and venous sinus occlusion or thrombosis.³¹ Digital subtraction angiography (DSA) still remains the gold standard for diagnosis and it is essential to identify the presence of the fistula, location, angioarchitecture, anatomy of the ECA and its branches, degree of dural sinus stenosis or occlusion, venous ectasia, and presence of CVD (Fig. 21.2b–e). Additionally, it can provide information regarding venous congestion not only by the presence of CVD but also by the presence of a pseudophlebitic pattern (tortuous engorged leptomeningeal veins) in the venous phase.⁵⁴

21.2 Selected Papers on the Natural History of Cranial Dural Arteriovenous Fistula

●Gross BA, Du R. The natural history of cerebral dural arteriovenous fistulae. Neurosurgery 2012;71(3):594–602, discussion 602–603

●Satomi J, van Dijk JM, Terbrugge KG, Willinsky RA, Wallace MC. Benign cranial dural arteriovenous fistulas: outcome of conservative management based on the natural history of the lesion. J Neurosurg 2002;97(4):767–770

●Shah MN, Botros JA, Pilgram TK, et al. Borden-Shucart type I dural arteriovenous fistulas: clinical course including risk of conversion to higher-grade fistulas. J Neurosurg 2012;117(3):539–545

21.3 Natural History of DAVFs

One important parameter when considering the risks of hemorrhage and further treatment decisions is the presence of CVD and the clinical presentation of the patient. Therefore, we subdivided the DAVFs into fistulas without CVD (low grade) and fistulas with CVD (high grade) based on their angioarchitecture and clinical presentation.

21.3.1 Natural History of Low-Grade DAVFs

DAVFs without CVD (Borden–Shucart type I, Zipfel type I, and Cognard types I and IIa) are considered to have a benign natural history and rarely cause ICH or NHND.16^, ²⁰^, ⁴⁶^, ⁴⁷ Based on follow-up studies of patients treated conservatively or through endovascular palliative methods (without complete obliteration of the DAVF), these lesions have a reported annual rate of new neurological event from 0 to 0.6% and an annual mortality rate of 0%.¹⁶^, ²⁰^, ⁴⁶^, ⁴⁷

DAVFs are dynamic lesions that can evolve to become aggressive over time (DAVF with CVD). It is thought that this is due to progressive stenosis or thrombosis of venous outlets, increased arterial flow, or recruitment or extension of the fistulous connections.²⁰^, ⁴⁴^, ⁴⁶

Benign DAVFs have in general a reported conversion rate or risk of developing CVD of about 0.8 to 2%, thus mandating for clinical follow-up review in such cases and the need for new radiological evaluation in the presence of new or modification (improvement or worsening) of previous neurological symptoms.⁴⁶^, ⁴⁷

21.3.2 Natural History of High-Grade DAVFs

DAVFs with CVD (Borden–Shucart types II and III; Zipfel types 2A, 2S, 3A, and 3S; and Cognard types IIb, IIa + b, and III–V) have an aggressive natural history and can frequently cause ICH or NHND.⁶^, ¹⁵^, ¹⁷^, ²⁰^, ⁴²^, ⁴⁹^, ⁵¹^, ⁵⁶ The aggressive nature of these lesions was first reported by Duffau et al¹⁸ in 1999. The authors analyzed 20 patients with Borden–Shucart type II and III DAVFs, and identified a 35% risk of early rebleeding within 2 weeks following the first hemorrhage.¹⁸ Additionally, van Dijk et al retrospectively identified in a subcohort of 20 patients that the presence of cerebral venous reflux (CVR) in cranial DAVFs yields an annual mortality rate of 10.4%.⁵¹ Also, in this series the annual risk for hemorrhage or NHND during follow-up was 8.1 and 6.9%, respectively, resulting in an annual event rate of 15.0%. Table 21.2 summarizes the risks of high-grade DAVFs.⁵¹ Based on these reports, it became clear that DAVFs with CVD are at risk of ICH, NHND, or even death; therefore, in the majority of these patients, treatment should be considered to eliminate those risks.

Table 21.2 Natural history of high-grade DAVFs (Borden–Shucart types II and III; Zipfel types 2A, 2S, 3A, and 3S; and Cognard types IIb, IIa + b, and III–V)

	Risk (%)	Mortality risk (%)
Early rebleeding (within 2 wk from first hemorrhage)¹⁸	35%
Presence of cerebral venous reflux ⁵¹		10.4%.
Annual risk of hemorrhage ⁵¹	8.1%
Annual risk of neurological deficit ⁵¹	6.9%
Abbreviation: DAVFs, dural arteriovenous fistulas.

Clinical presentation plays an important role in DAVFs with CVD since some patients present with aggressive symptoms such as ICH or NHND and others develop benign symptoms such as tinnitus. Söderman et al observed a significant difference in the annual rate of new neurological events between patients presenting with ICH as compared to those without ICH (7.4 vs. 1.5%, respectively).⁵⁰ Additionally, Gross and Du reported a significant difference in the annual rate of ICH in patients presenting with ICH versus those presenting with NHND versus those presenting incidentally or with more benign symptoms of increased sinus drainage (46 vs. 10 vs. 2%, respectively).²⁰ Based on these reports, it can be concluded that a relevant association exists between clinical presentation and natural history of DAVFs with CVD.

Moreover, venous ectasia has been demonstrated to impact the natural history of DAVFs with CVD.²⁰ Bulters et al noted a statistically significant increase in annual risk of hemorrhage between patients with DAVFs having venous ectasia and those with DAVFs without venous ectasia (19.0 vs. 1.4%, respectively).⁷

21.4 Selected Papers on Treatment Outcomes of DAVFs

●Kakarla UK, Deshmukh VR, Zabramski JM, Albuquerque FC, McDougall CG, Spetzler RF. Surgical treatment of high-risk intracranial dural arteriovenous fistulae: clinical outcomes and avoidance of complications. Neurosurgery 2007;61(3):447–457, discussion 457–459

●Piippo A, Niemelä M, van Popta J, et al. Characteristics and long-term outcome of 251 patients with dural arteriovenous fistulas in a defined population. J Neurosurg 2013;118(5):923–934

●Rangel-Castilla L, Barber SM, Klucznik R, Diaz O. Mid and long term outcomes of dural arteriovenous fistula endovascular management with Onyx. Experience of a single tertiary center. J Neurointerv Surg 2014;6(8):607–613

●Söderman M, Edner G, Ericson K, et al. Gamma knife surgery for dural arteriovenous shunts: 25 years of experience. J Neurosurg 2006;104(6):867–875

21.5 Treatment Strategy

In general, treatment options for DAVFs include conservative management, endovascular embolization, microsurgical disconnection, stereotactic radiosurgery (SRS), or a combination of any of these methods.⁸^, ²⁰^, ³⁸^, ⁴⁰^, ⁴⁸^, ⁴⁹^, ⁵¹ However, most DAVFs can be at least partially treated by endovascular methods, which should be the first-line approach to obtain complete occlusion.⁴¹ If complete occlusion is not possible, the patient can undergo SRS or microsurgery depending on the clinical context. Endovascular treatment can also be used as a complementary treatment if there is residual filling after microsurgery or vice versa. Table 21.3 summarizes the treatment options and their respective risks and outcomes.

Table 21.3 Treatment options and respective outcomes

Treatment modality	Angiographic obliteration rate (%)	Complication risk (%)
Endovascular series⁸^, ¹⁹^, ²²	65–95	2
Microsurgery series¹^, ²¹^, ²⁴^, ³³	92–100	7.1–17
Stereotactic radiosurgery series⁹^, ³⁹^, ⁴⁹	68–90	Low complication rate

The treatment strategy should be tailored individually to patients considering the anatomical features of the DAVF, the severity of symptoms, and the potential risk of intracranial hemorrhage. Fig. 21.3 summarizes the treatment algorithm for cranial DAVFs.

Fig. 21.3 Treatment strategy flowchart for cranial DAVFs (CVD, cortical venous drainage; DAVFs, dural arteriovenous fistulas; ICH, intracerebral hemorrhage; NHND, nonhemorrhagic neurological deficit).

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