Etiology:

Adult dAVFs are usually acquired, often idiopathic, but can result from trauma, previous craniotomy, or venous sinus thrombosis (e.g inherited prothrombotic conditions like antithrombin, protein C, and protein S deficiencies). Infant dAVFs are congenital.

Pathology:

Gross pathology is variable depending on location of fistula and venous drainage:

• Several enlarged dural arteries converging to the wall of a dural sinus or cortical vein
• Enlarged cortical draining veins ± dilatation, tortuosity, stenosis

Microscopic features include arterialized veins with irregular intimal thickening.

Pathophysiology:

Dural sinus obliterated by organized thrombus →  Pathological activation of neoangiogenesis → Proliferating capillaries within granulation tissue →  Budding & proliferation of microvascular network in inner dura → connection to plexus of thin-walled venous channels → microfistulae.

Another commonly accepted theory proposed inflammation at the penetrating point of an emissiary vein (EV) on the dura as the inciting factor. Inflammation can be idiopathic or secondary. Local inflammatory reactions induce vessel dilatation and neovascularization, and subsequently create arteriovenous fistula.

Associated abnormalities: 

Cortical venous drainage may occur and arterialized flow in cortical veins/dural sinuses →  high-flow venopathy (venous outflow obstruction) → Venous hypertension →  ↑ risk of intracranial hemorrhage (ICH) , edema and encephalopathy.

Arterial Feeders:

Typically multiple feeders from arteries that supply the relevant meninges and regional scalp vessels give transosseous branches supplying the DAVF:

- Supratentorial and lateral: (external carotid artery)

        middle meningeal artery

        superficial temporal artery 

- Anterior cranial fossa: (internal carotid artery)

        ethmoidal branches of the ophthalmic artery 

- Cavernous sinus: (internal and external carotid arteries)

        meningohypophyseal trunk and inferolateral trunk

        accessory meningeal artery

- Posterior cranial fossa: (vertebral and external carotid arteries)

        vertebral arteries (dural and muscular branches)

        occipital and ascending pharyngeal arteries

Locations:

- Transverse/sigmoid sinus (most common)

         Least likely to have retrograde venous drainage

- Cavernous sinus (indirect carotid-cavernous fistula)

- Superior sagittal sinus, straight sinus, other venous sinuses

- Anterior cranial fossa

         Only ICA supply (related to meningeal supply of this region)

         Frequently has direct venous drainage

- Tentorium

         Frequently has direct venous drainage

Clinical Presentations:

1. Incidental /  asymptomatic

2. Benign:  Symptoms of increased dural sinus drainage

• Pulsatile tinnitus (pulse-synchronous, most common presentation)
• Pulsatile bruit
• Orbital congestion (proptosis, chemosis, ophthalmoplegia, retro-orbital pain)
• cranial nerve palsy
• chronic headache

3. Aggressive: Symptoms or sequelae of cortical venous hypertension

• Intracranial hemorrhage
• Non-hemorrhagic neurological deficits (NHNDs): 
• Seizure
• Cortical deficits and Stroke
• Symptoms of increased ICP (e.g Papilledema)
• Dementia / developmental delay in children

Infants can present with developmental delay, ↑ head circumference, Life-threatening congestive heart failure

Imaging:

Computed tomography (CT)

DAVF may be hard to evaluate on CT, however the following signs can be seen:

Non Enhanced Contrast CT (NECT):

• Dilated vascular channels in the skull due to transosseous feeding arteries
• Ipsilateral enlargement of foramen spinosum (middle meningeal artery commonly supplies dAVFs)
• Complications: Intracranial hemorrhage, cerebral edema (venous hypertension)

Fig. 1: Figure 1 shows dilated vascular channels in the skull (yellow arrows) due to transosseous feeding arteries. Figure 2 show NECT in a different patient with Type III Borden DAVF presented with intracranial hemorrhage (including left sided extra axial hematoma, left parietotemporal intraparenchymal hemorrhage, and diffuse sub-arachnoid hemorrhage). Figure 3 is for a different patient with Borden type 3 DAVF, his NECT at presentation show cerebellar hemorrhage and extension to the fourth ventricle.

Contrast Enhanced CT (CECT):

• Tortuous feeding arteries ± flow-related aneurysms (uncommon), draining veins
• Involved dural venous sinus completely/partially thrombosed or stenotic

CT Angiogram (CTA):

• Standard 3D CTA may be useful in depicting gross angioarchitecture. Dynamic 4D-CTA allows volumetric imaging, detailed spatial/temporal resolution
• Abnormally enlarged and tortuous vessels in the subarachnoid space, corresponding to dilated cortical vein
• Enlarged external carotid artery (ECA) or enlarged tranosseous vessels 
• Abnormal dural venous sinuses and arterialization of contrast phase in the affected sinus due to arteriovenous shunting

Magnetic Resonance Imaging (MRI)

Diagnosis can be difficult without retrograde venous drainage. Dilated pial vessels in the subarachnoid space can be a potential clue.

• T1WI: Isointense thrombosed dural sinus ± flow voids
• T2WI: Isointense thrombosed sinus ± flow voids, Focal hyperintensity in adjacent brain related to retrograde leptomeningeal venous drainage or venous perfusion abnormalities.
• FLAIR: Isointense thrombosed sinus, Adjacent edema in patients with venous hypertension.
• T2* GRE: Thrombosed dural sinus "blooming", Intraparenchymal hemorrhage.
• DWI: venous infarct or ischemia present, otherwise usually normal 
• SWI: venous congestion
• Contrast enhanced T1WI: Chronically thrombosed sinus usually enhances, Regions of white matter edema may also enhance (suggest aggressive DAVF,  high rate of hemorrhage).
• MRA (Magnetic resonance angiography): gross depiction of angioarchitecture and angiodynamics, Time of flight (TOF) MRA may be negative with small or slow-flow shunts.
• MRV (Magnetic resonance venography): Can detect occluded parent sinus and collateral flow

Fig. 2: A 65 years old male with Borden type III DAVF, figure 1 Axial FLAIR MRI showing left extra-axial signal hyper intensity consistent with subdural hemorrhage. Flow voids in the posterior left cerebral hemisphere related to the DAVF demonstrated on all figures.

Conventional Angiography (Catheter digital subtraction angiography DSA)

It is the gold standard for diagnosis as it provides accurate classification of DAVF by systematic evaluation of feeding vessels. It is essential for planning for potential intervention. DSA can demonstrate the presence and extent of retrograde venous drainage. Due to often extensive arterial supply, a six vessel selective angiogram is required (bilateral ICA, ECA and vertebral artery injections). 

Imaging findings on DSA:

• Multiple arterial feeders: Dural/transosseous branches from ECA (most common), Tentorial/dural branches from ICA or VA, Parasitization of pial arteries with larger dAVFs.
• Arterial inflow into parallel venous channel ("recipient pouch")
• Dural sinus often thrombosed or stenotic
• Dural sinus/cortical veins flow reversal (correlates with progressive symptoms, risk of hemorrhage)
• Tortuous engorged pial veins ("pseudophlebitic" pattern) with venous congestion/hypertension (clinically aggressive)
• High-flow venopathy signs : progressive stenosis, outlet occlusion, hemorrhage

Fig. 3: The top row show serial lateral projection of left external carotid artery pre-emoblization DSA demonstrating DAVF between the occipital artery branches with multiple transosseus channels communicating to the transverse sigmoid sinus. Note the early filling of the sinus on Figure A. Post-emolization images of left common carotid artery DSA in the lateral projection show coil placement in the occipital artery with complete occlusion of the arterial feeders of the DAVF

Angiographic Classifications

The two most commonly used are  (1) Cognard and (2) Borden-Schucart classifications. Both published in 1995. Both classifications are centered around the pattern of venous drainage which correlates with a more aggressive clinical course. Borden classification divides DAVF according to the site of location and presence or absence of cortical venous drainage. 

Cognard classification system in addition considers the direction of blood flow within the sinus and presence of venous ectasia. The Borden classification is a simplified version of the Cognard system.

Summary of Angiographic Classifications:

A. Borden-Schucart:

1. Type I: Venous drainage directly into dural venous sinus or meningeal vein
2. Type II: Venous drainage into dural venous sinus with cortical venous reflux (CVR)
3. Type III: Venous drainage directly into subarachnoid veins (CVR only) 

Fig. 4: Left: Schematic diagram of the Borden Type 1 DAVFs with several communications between the occipital artery and the transverse sinus with antegrade flow and no cortical venous reflux Right: Schematic diagram of the Borden Type 2 DAVF also between the occipital artery and the transverse sinus. However there is stenosis of the distal transverse and proximal sigmoid sinuses with retrograde blood flow into the proximal transverse sinus and the cortical vein

Fig. 5: Left occipital artery angiogram in the lateral (A) and AP (B) projections demonstrating a Borden–Shucart Type II DAVF supplied mainly by an enlarged occipital artery and located in the distal left transverse sinus. The venous drainage was entirely via retrograde cortical drainage into the middle cerebral veins, vein of Labbé as well as flow through the mastoid emissary vein into scalp veins. There was no drainage through the confluence of sinuses or the distal sigmoid sinus due to occlusion of the transverse and sigmoid sinuses proximal and distal to the site of the fistula. CT scan at time of presentation (C) demonstrated left temporal lobe hematoma which is one of the imaging features of venous hypertension cdv = cortical draining vein; mev = mastoid emissary vein; occ = occipital artery; Pp = Prowler Plus microcatheter; Ts = transverse sigmoid pouch; 18ga = 18-gauge needle.

Fig. 6: Right common carotid artery lateral projection angiogram (A) demonstrates a Modified Borden-Shucart Type IIIS dAVF (thin arrow) deriving arterial supply from the right occipital artery (arrowhead). Venous drainage occurred via an enlarged vermian vein, refluxing through the vein of Galen (white arrows). At presentation, MRI of the brain showed imaging features of venous hypertension; coronal T1 post-gadolinium MRIs show right greater than left patchy thalamic enhancement (B); Axial FLAIR MRI showing left greater than right bilateral thalamic T2 signal hyperintensities (C).

B. Cognard:

• Grade I: Located in sinus wall, normal antegrade venous drainage; clinically benign
• Grade IIA: Located in main sinus, reflux into sinus but not cortical veins; clinically benign
• Grade IIB: Reflux (retrograde drainage) into cortical veins; 10-20% hemorrhage rate
• Grade III: Direct cortical venous drainage, no venous ectasia; 40% hemorrhage rate
• Grade IV: Direct cortical venous drainage, venous ectasia; 65% hemorrhage rate
• Grade V: Spinal perimedullary venous drainage; associated with progressive myelopathy

Fig. 7: A table summarizing the angiographic classifications of the different types of cranial dural arteriovenous fistula and their characteristic differences. Abbreviations; CVD: cortical venous drainage, CVH: cortical venous hypertension, ICH: intracranial hemorrhage, NHND: non-hemorrhagic neurological deficit.

Natural History and Indications for treatment:

Borden Type 1 has minimal risk for future events, generally conservative treatment. Borden  Types 2 and 3 are at a higher risk if symptomatic, but lower if not. Treatment is usually endovascular or surgical disconnection.

Higher grades are associated with an annual mortality rate of ~10% and an annual risk of intracranial hemorrhage of ~8%. Prognosis & treatment also consider location, venous drainage pattern in addition to type 98% of dAVFs without retrograde venous drainage have benign course, dAVFs with retrograde venous drainage have aggressive clinical course

Treatment:

Goals of treatment:

• preventing complications 
• reducing intolerable symptoms

Treatment options:

1.Conservative: 

• Borden type I and Cognard types I and IIa
• Observation ± carotid compression techniqu

Fig. 8: (A) Right External Carotid artery (ECA) angiogram in the lateral projection showing an abnormal dural based fistulous communication (multiple white arrows) off an ECA branch and directly draining into the right sigmoid sinus. Note early opacification of the right internal jugular vein. (B) a follow up angiogram performed a year later showed marked decrease in these findings indicating spontaneous regression. (C) Further follow up performed two years after baseline showed complete resolution.

2. Non-conservative options if (1) hemorrhage risk exists or (2) for types 1 and 2A with debilitating pulsatile tinnitus.

• Fistula closure with single/staged procedure
• Endovascular: Embolization of arterial feeders with particulate or liquid agents, coil embolization of recipient venous pouch/sinus
• Surgical disconnection
• Stereotaxic radiosurgery: Time delay of 2-3 years for obliteration

Treatment options depend on classification, age and comorbidities of the patient, as well as symptoms. However in general, the treatment of choice nowadays is endovascular with adjuvant radiosurgery or microsurgery when necessary. Only few lesions require microneurosurgery.