Clinical Presentation and Imaging Findings of Patients with Dural Arteriovenous Fistulas with an Angiographic Pseudophlebitic Pattern

DISCUSSION

Our study examining the association between the pseudophlebitic pattern on global angiography and clinical symptoms and imaging findings demonstrated a number of interesting findings. First, the presence of a pseudophlebitic pattern was associated with a significantly higher rate of hemorrhage and other nonhemorrhagic neurologic deficits such as cognitive changes, gait dysfunction, and seizure. Regarding fistula classification, we found that the locations most commonly associated with the presence of a pseudophlebitic pattern were tentorial fistulas (>50%) and superior sagittal sinus fistulas (nearly 10%). As expected, a pseudophlebitic pattern was seen exclusively in malignant fistulas as defined by the Borden and Cognard classification scales. A number of cross-sectional MR imaging findings were found to be independently associated with the presence of a pseudophlebitic pattern, including cerebral edema, chronic hemosiderin deposition, and dilated transmedullary veins. These findings are important because they highlight the pseudophlebitic pattern being a reliable prognostic marker for a symptomatic and malignant fistula.

The pseudophlebitic pattern was first described in the setting of cranial dural arteriovenous fistulas by Willinsky et al.⁴ In their series of 122 patients, a pseudophlebitic pattern was seen in 51 patients, (42%) most of whom presented with hemorrhage or nonhemorrhagic neurologic deficits. Similar to our study, Willinsky et al found that most of the lesions associated with a pseudophlebitic pattern were associated with tentorial or superior sagittal sinus fistulas. Fifty-two patients in their series also had brain MRIs, of whom 20% had cerebral edema, and 90% of those with cerebral edema had a pseudophlebitic pattern. Our study adds to this study in that we report more extensively on the MR imaging findings of 191 patients, 95% of the patients included in this study.

Our study highlights additional imaging findings that are unique to those with a pseudophlebitic pattern. First, we found that the prevalence of cerebral edema among patients with a pseudophlebitic pattern was 71%, significantly higher than the 20% reported in previous studies.⁴ This prevalence is likely a function of improved imaging techniques (ie, increased use of FLAIR, routine 1.5T and 3T MR imaging, and so forth). Cerebral edema in these patients is likely a reflection of diffuse venous congestion (congestive edema) resulting in fluid retention in the interstitial tissues. We found that 17% of patients had chronic hemosiderin deposition or microhemorrhage on T2*-weighted imaging, which is likely a function of tiny perivenular microhemorrhages in the setting of severe venous hypertension. Dilated transmedullary veins on SWI or contrast-enhanced T1 imaging were found in nearly 50% of patients with a pseudophlebitic pattern, a unique association, likely a function of rerouting of normal cerebral venous drainage via transmedullary venous pathways.⁷ We did not find any association between venous sinus narrowing or thrombosis and the presence of a pseudophlebitic pattern. This finding is likely because in most cases of dural venous sinus thrombosis–associated dAVFs, the lesions are located in the transverse and sigmoid sinuses and there are multiple venous egress pathways available for the draining cortical veins. Tentorial and ethmoidal dAVFs are less likely to be associated with venous sinus thrombosis or stenosis.

The pseudophlebitic pattern was not independently associated with hemorrhage but was independently associated with the presence of nonhemorrhagic neurologic deficits. Previous studies have suggested that the pseudophlebitic pattern is a risk factor for hemorrhage, but they did not stratify lesions by the presence or absence of retrograde leptomeningeal venous drainage.⁴ When we examined patients who had retrograde leptomeningeal venous drainage, we found that the rate of hemorrhage was similar between those who did and did not have a pseudophlebitic pattern. This finding suggests that the primary driver of hemorrhage is the venous pathology along the draining vein rather than the venous congestion in the affected territory. However, the fact that nonhemorrhagic neurologic deficits such as seizure and cognitive decline are more common among those with a pseudophlebitic pattern suggests that the chronic venous congestion resulting from the normal brain not being able to properly drain in the setting of leptomeningeal venous drainage is the primary driver of these particular symptoms.^3,8⇓-10 This feature has been suggested by prior reports on the characteristics of dAVFs associated with cognitive decline, which have suggested that nearly all of these patients have evidence of medullary venous hypertension with reflux or congestion of the transmedullary veins on conventional imaging and angiography.¹¹ Given the strong association between the pseudophlebitic pattern and nonhemorrhagic neurologic deficits in our study, we think that the presence of this pattern should encourage the neurointerventionalist or neurosurgeon to be more aggressive in treating and curing the fistula to prevent the downstream effects of chronic venous congestion.

One additional interesting finding from our study was the location of most lesions associated with the pseudophlebitic pattern. Most of these lesions were more or less midline in location (ie, tentorial or superior sagittal sinus). Tentorial dAVFs involving the midline tentorial sinuses, the torcula, or the vein of Galen cause significant venous hypertension in the vein of Galen–straight sinus–torcula draining pathway. Thus, in such cases, the primary means by which the deep venous system drains into the dural venous sinuses is under high pressure, resulting in high pressure in the parenchymal veins draining into the deep venous system and a pseudophlebitic congestive pattern. The same is true for superior sagittal sinus fistulas because the cortical veins experience markedly elevated venous pressure resulting in congestion of the parenchymal veins and an associated pseudophlebitic pattern. This feature would be less common in laterally located lesions (ie, transverse sigmoid junction fistulas) because there may be more avenues for venous egress for the parenchymal veins.

Regarding sex, we found that male sex was associated with a pseudophlebitic pattern on angiography. A number of large clinical case series have found that male sex is associated with a more aggressive angioarchitecture of cranial dural arteriovenous fistulas; however, the reason for this association is unclear.^4,12,13 In their review of >300 cranial and spinal arteriovenous fistulas, Geibprassert et al noticed that fistulas associated with more benign locations and angioarchitecture had a female predominance while those in locations associated with more malignant angioarchitecture were much more common in men.¹³ These findings point to a difference in the etiology of cranial dural arteriovenous fistulas by location. We hypothesize that women are more likely to have the more benign fistulas in the cavernous sinus and transverse sigmoid region due to their propensity to have dural venous sinus thromboses, while men are more likely to have aggressive tentorial or anterior ethmoidal fistulas due to higher rates of trauma.