Pial Artery Supply as an Anatomic Risk Factor for Ischemic Stroke in the Treatment of Intracranial Dural Arteriovenous Fistulas

BACKGROUND AND PURPOSE:Although intracranial dural arteriovenous fistulas are principally supplied by dural branches of the external carotid, internal carotid, and vertebral arteries, they can also be fed by pial arteries that supply the brain. We sought to determine the frequency of neurologic deficits following treatment of intracranial dural arteriovenous fistulas with and without pial artery supply.MATERIALS AND METHODS:One hundred twenty-two consecutive patients who underwent treatment for intracranial dural arteriovenous fistulas at our hospital from 2008 to 2015 were retrospectively reviewed. Patient data were examined for posttreatment neurologic deficits; patients with such deficits were evaluated for imaging evidence of cerebral infarction. Data were analyzed with multivariable logistic regression.RESULTS:Of 122 treated patients, 29 (23.8%) had dural arteriovenous fistulas with pial artery supply and 93 (76.2%) had dural arteriovenous fistulas without pial arterial supply. Of patients with pial artery supply, 4 (13.8%) had posttreatment neurologic deficits, compared with 2 patients (2.2%) without pial artery supply (P = .04). Imaging confirmed that 3 patients with pial artery supply (10.3%) had cerebral infarcts, compared with only 1 patient without pial artery supply (1.1%, P = .03). Increasing patient age was also positively associated with pial supply and treatment-related complications.CONCLUSIONS:Patients with dural arteriovenous fistulas supplied by the pial arteries were more likely to experience posttreatment complications, including ischemic strokes, than patients with no pial artery supply. The approach to dural arteriovenous fistula treatment should be made on a case-by-case basis so that the risk of complications can be minimized.

Intracranial dural arteriovenous fistulas (DAVFs) are vascular malformations that connect meningeal arteries to dural venous sinuses or cortical veins. DAVFs account for 10%–15% of all intracranial arteriovenous shunting lesions.^1–14 DAVFs are often thought to be acquired, sometimes in the setting of hypercoagulability.¹⁵ DAVF venous drainage determines the natural history risk of spontaneous intracranial hemorrhage. Thus, venous drainage is incorporated into the most commonly used grading systems of DAVF natural history risk: the Borden-Shucart and Cognard grading scales.^2,3 Drainage to cortical veins is the highest risk category because pressurization of these thin-walled venous structures frequently leads to rupture. Although venous angioarchitecture is a key determinant of natural history risk, the risk of endovascular and/or surgical treatment of DAVFs in the modern era related to underlying lesion angioarchitecture is not well-known.Although DAVFs are most commonly fed by dural branches of the internal carotid, external carotid, and vertebral arteries, they can also have pial artery supply. Pial arteries lie on the surface of the brain. They then branch into penetrating arteries and parenchymal arterioles that lie within and supply the brain parenchyma. The mechanism of pial feeder formation is not well-understood but is believed to be like that of dural feeders, with increased vascular endothelial growth factor secretion from the venous sinus and abnormal angiogenesis.^16–24 Embolization of pial AVFs has been suggested to lead to the development of subsequent DAVFs in up to 25% of cases.^25,26 The inflammatory reaction within the DAVF vessel wall after embolization may also lead to angiogenesis.²⁷Transarterial embolization of DAVFs with pial artery supply with agents that can migrate retrograde (ie, from the dural arteries to the pial arteries) could thus block blood supply to the associated brain parenchyma and cause ischemia. Surgical or endovascular point occlusion of DAVFs with pial artery supply at the fistula site might also result in retrograde thrombosis of feeding pial arteries due to decreased flow. We hypothesized that patients with DAVFs with pial artery supply have a higher risk of postoperative stroke than those who do not have pial supply.