Dural Arteriovenous Fistulas of the Foramen Magnum Region: Clinical Features and Angioarchitectural Phenotypes

DISCUSSION

This study represents the largest series of FMR AVFs to date and clarifies the behavior of this uncommon form of intracranial shunt, revealing 4 distinct clinical-angiographic phenotypes. FMR AVFs were under-represented in previous studies, for example, comprising only 1.5% of cases in the cohort from which the Cognard classification was derived.² This study, therefore, builds on prior work^1,3,14 by establishing a classification system specific to FMR AVF, incorporating both risk and symptoms toward appropriate therapy selection.

McDougall et al¹ were the first to systematically describe fistulas of the marginal sinus in a series of 14 patients. They defined 3 clinical phenotypes based on the restriction of jugular outflow and the presence of cortical venous reflux. More recently, Choi et al³ described 10 fistulas of the hypoglossal canal (anterior condylar vein), noting that orbital symptoms and myelopathy were present only in cases with restriction of antegrade sinus outflow, extending the notion that clinical presentation is a manifestation of venous drainage and therefore an overall risk. In a case series and in a systematic review of 120 cases of FMR AVF (115/120, 95.8% from the literature), Spittau et al¹⁴ modified the McDougall taxonomy on the basis of clinical phenotypes, emphasizing the dominant pattern of venous drainage: 1 = antegrade sinus, 2 = retrograde sinus with or without antegrade drainage/cortical venous reflux, and 3 = dominant cortical venous or perimedullary reflux. They showed that this angiographic classification schema corresponds well with clinical manifestations. However, due to inclusion of a subjective element (dominance) and lack of primary angiographic data in >90% of included cases, the reproducibility and generalizability of this scale are uncertain. In addition, the Spittau criteria do not differentiate the binary presence or absence of cortical venous reflux, a feature that has important implications for hemorrhagic risk and mortality.^15,16 We, therefore, differentiated type 2 (60%) and 3 lesions (40%) on the basis of the presence of cortical venous reflux despite a similar prevalence of orbital symptoms (44.3% versus 33.3%, P = 1.0, Fisher exact test) among patients with sinus reflux (Fig 4).

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FIG 4.

A type 3 FMR-AVF with clinical features mimicking a carotid cavernous fistula. MRA of the FMR (A) shows flow-related enhancement in the right hypoglossal canal, corresponding to an anterior condylar vein fistula site. Coronal MRA (B) shows asymmetric flow-related enhancement of the right (white arrowhead) relative to left (clear arrowhead) cavernous sinuses. Lateral-projection DSA of the right ascending pharyngeal artery (C) shows the fistula (asterisk) with antegrade drainage via the IJV (straight arrow) and reflux via the inferior petrosal sinus (IPS, curved arrow) extending to the cavernous sinus (CS) and superior ophthalmic vein (SOV), resulting in proptosis and chemosis. Anterior-posterior DSA of the right vertebral artery (D) shows reflux via the IPS and CS, which continues to the middle cerebral vein (MCV), making this a high-risk type 3 fistula. The asterisk represents the fistulous shunt site. BA indicates the basilar artery.

The principal finding of this study is that nearly all FMR AVFs present symptomatically (96.5%), most with pulsatile tinnitus (82.3%). While AVFs of the sigmoid and transverse sinuses are known causes of pulsatile tinnitus, the correlation of FMR AVF and pulsatile tinnitus is less established. Turbulence in the pressurized condylar veins and petrosal sinuses could plausibly result in conduction across the petrous bone, accounting for a high-pitched, pulse-synchronous tinnitus. In our experience, direct auscultation of the mastoid bone often reveals audible bruit in patients with FMR AVF. Given the observed association of pulsatile tinnitus and FMR AVF, vigilance of the posterior skull base is warranted on noninvasive imaging studies performed to evaluate pulsatile tinnitus. Advanced MR imaging techniques including contrast MR angiography, susceptibility mapping of deoxygenated hemoglobin, and arterial spin-labeling may aid in the diagnosis but care should be taken to avoid misinterpretation of artifactual signal in this region.¹⁷ Our findings also support results of previous work showing that the orbital symptoms are frequent in an FMR AVF with sinus reflux (40% of patients with type 2 or 3), a finding that may clinically mimic carotid cavernous fistula (Fig 4).⁸

In this series, high-risk presenting symptoms (myelopathy, hemorrhage) were seen exclusively in type 3 and 4 lesions. Type 1 and 2 FMR AVFs may, therefore, be considered low-risk when evaluating patients for treatment. This finding corroborates previously well-established risk features from the Borden and Cognard classification systems, in which cortical venous reflux is the key mediator of risk.^2,18 Although the overall incidence of hemorrhage and myelopathy was low (13.7%) relative to other cranial AVFs, the presence of orbital symptoms in >25% of cases has important therapeutic implications. Left untreated, pressurization of the cavernous sinus can result in permanent vision loss and represents an urgent indication for therapy for the FMR AVF.¹⁹ We find that the presence (or absence) of orbital symptoms is a useful heuristic for stratifying patients. Although we did not find statistical difference, orbital symptoms were seen in 40% of patients with angiographic evidence of venous reflux (type 2/3) compared with 14.3% with none (type 1/4). Still, the considerable overlap in orbital symptoms between ostensibly low-risk (type 2) and high-risk (type 3) lesions stresses the importance of angiography in the initial diagnostic work-up.

Djindjian and Merland²⁰ first recognized the disproportionate impact of venous drainage over arterial supply in their taxonomy of cranial AVFs. Subsequent work has confirmed this as a tenet of risk stratification.^15,21,22 Despite the emphasis on venous angioarchitecture, knowledge of the arterial supply is critical to inform treatment strategies. Curative endovascular treatment requires total obliteration of the network of arterial feeders; failure to recognize the contribution of a contralateral feeding artery could result in treatment failure and preclude repeat treatment. Our findings show that a contralateral arterial supply is present in 62.5% of cases. We found that dural supply from the internal carotid artery (48.3% ipsilateral, 31.0% contralateral) and direct vertebral artery supply (89.7% ipsilateral, 27.6% contralateral) were common. Recognition of these and other potential hazardous collaterals is critical to prevent inadvertent reflux if transarterial liquid embolics are used. While this study is insufficiently powered to detect statistical differences in arterial supply across venous angioarchitectural types, we noted a general increase in the number of arterial feeders from type 1 through type 3, with the notable exception of type 4 FMR AVFs, which typically have fewer arterial feeders at presentation. These findings again emphasize the importance of meticulous pretreatment control angiograms to delineate the full extent of the arterial supply in FMR AVFs.

There are several important limitations of the current study. First, although this is the largest comprehensive angiographic review of FMR AVFs, our analysis is underpowered to detect robust differences among angioarchitectural groups. Moreover, we cannot define the natural history of FMR AVFs or the propensity for lesions to attain higher risk features across time, a phenomenon that was reported in 2% of patients in 1 study.¹³ We elected to aggregate fistulas of the FMR, including the condylar veins and marginal sinus, because these share many interconnections and common final drainage pathways.^4,5,7,23 However, it is plausible that subgroups of FMR AVFs (eg, lateral-versus-posterior condylar veins) behave differently.