Simultaneous Arteriovenous Shunting and Venous Congestion Identification in Dural Arteriovenous Fistulas Using Susceptibility-Weighted Imaging: Initial Experience

Discussion

In 5 of 6 patients, it was possible to correctly identify the location of the fistula shown as hyperintense venous structures on SWI. This preliminary result is similar to the high sensitivity of 93% obtained in a recent study including 29 brain vascular malformations (5 DAVFs) associated with arteriovenous shunting.¹⁰ Tsui et al¹¹ also described hyperintensity in a venous varix related to a DAVF. The hyperintense venous sinuses or veins were well depicted in all cases by the use of SWI images. MIPs obtained from the same SWI images enhanced the visualization of venous hyperintensity (Fig 2D and Fig 3E), though this was not necessary for the diagnosis. As expected, the use of mIP negated this finding in most cases. We postulated that CVR would manifest with cortical venous hyperintensity radiating from the fistulous point. This assumption was based on the principle that veins affected by CVR contain rapidly flowing and nonparamagnetic arterial blood. The extent of CVR revealed on SWI was, however, underestimated in 3 cases of robust CVR, whereas it could not be identified in 2 instances of scant CVR. Slow-flowing DAVFs may result in poor flow-related enhancement, which may at least partially explain the lack of venous hyperintensity in these 2 falsely negative cases. Furthermore, oxyhemoglobin contained in CVR might be rapidly diluted in deoxyhemoglobin-rich congested veins.

Given this relative underestimation of CVR on SWI, this preliminary observation suggests that the noninvasive evaluation of CVR should rely on time-resolved MRA or CTA, which have sensitivity >90% with good-to-excellent interobserver agreement.^14–19 It is, nonetheless, possible that slow-flowing CVR or fistulas may be missed by using these techniques, given the lack of selective arterial injection and lesser temporal resolution compared with DSA. This situation has recently been encountered in a series of DAVFs evaluated by dynamic CTA¹⁴ and highlights the persisting role of conventional angiography in DAVF characterization.

Prominent dilated leptomeningeal and medullary veins on SWI were characteristic features of all cases associated with both the PPP and cortical venous drainage. SWI provided excellent depiction of these collateral venous networks, demonstrating more congested veins compared with conventional sequences, a finding enhanced by the use of mIPs. This finding is similar to previous reports on the use of SWI for the depiction of venous congestion secondary to DAVFs.^7–9 Saini et al⁷ also described reduction in the prominence of these cortical veins after treatment in 1 patient. A similar observation has been described in the setting of cortical venous outflow obstruction seen in Sturge-Weber syndrome, in which SWI was more sensitive than contrast-enhanced T1-weighted imaging in the detection of transmedullary veins.²⁰

In our opinion, the dilated hypointense veins identified on SWI in the setting of DAVFs likely represent enlarged and tortuous collateral veins serving to reroute venous blood away from obstructed and/or hypertensive venous drainage pathways.³ The underlying mechanism for increased venous visibility on SWI is probably multifactorial. It has been postulated that venous hypertension secondary to DAVF leads to hypoperfusion and possibly increased oxygen extraction in ischemic tissue, which would then lead to increased deoxyhemoglobin concentration and increased susceptibility effects.⁷ With positron-emission tomography studies, increased oxygen extraction fraction has been demonstrated in a subset of DAVFs associated with decreased cerebral blood flow and venous-drainage impairment when oxygen metabolism was preserved.^21,22 In addition to increased oxygen extraction fraction, the increased volume of deoxyhemoglobin within dilated veins may also explain their conspicuity on SWI.

In rare situations, venous congestion may be seen without accompanying CVR.^3–5 In these instances, there is still the possibility of hemorrhagic or nonhemorrhagic neurologic complications.^3–5 This scenario is usually associated with arteriovenous shunting within dural sinuses producing increased venous pressure and functional outflow obstruction. In this circumstance, SWI would, in theory, be able to demonstrate engorged veins as well as the hyperintense fistulous point, while the fistula would be classified as benign on the basis of the absence of CVR. The possibility of an independent prognostic value of venous congestion identified on SWI needs further assessment in larger longitudinal studies.

SWI can demonstrate hemorrhagic complications of DAVFs, including previous hemorrhagic events such as pial siderosis or chronic intraparenchymal hematoma that may remain occult on other imaging modalities or MR sequences. Subcortical calcifications in DAVFs^23,24 could also be identified on SWI by the use of filtered-phase images.^25,26 Among the disadvantages of SWI is its vulnerability to susceptibility artifacts present at the skull base, as seen in 1 of our cases. Another caveat for SWI in the diagnosis of DAVF is the possibility of fistula obscuration by blood-degradation products as seen in 1 instance in the report from Noguchi et al.⁸ However, in the series from Jagadeesan et al,¹⁰ the depiction of arteriovenous shunt surgery was paradoxically higher in cases of intracerebral hematoma compared with cases without hemorrhage.

The presence of prominent hypointense pial veins on SWI can also be seen in other conditions, though the presence of marked venous tortuosity would be more suggestive of long-standing venous hypertension as encountered in DAVFs. Furthermore, the additional finding of venous hyperintensity at the fistulous point should also suggest the possibility of a DAVF. Potential mimickers include states of increased oxygen extraction in the setting of oligemia, either in acute ischemic stroke or hemodynamically significant arterial stenosis.^25,27 Transient unilateral venous prominence has also been described in migraines.^28,29 Venous congestion secondary to venous thrombosis can also lead to dilated collateral veins, ^25,26,30 but contrary to arterialized veins in DAVFs, the thrombosed veins should appear hypointense from susceptibility effects.³¹ This latter pattern should prompt further evaluation with MR venography because the distinction between patent and thrombosed veins could be difficult on SWI.

The main limitations of this series are the small sample number, retrospective nature, absence of a control arm, and the fact that the readers were aware of the diagnosis of DAVF. In our institution, all dedicated DAVF studies, including post-treatment follow-up MR imaging, include an optimized time-resolved MRA, which is performed on an MR imaging unit without SWI capability, hence the small number of SWI studies available for review. For the same reason, no posttreatment SWI studies were available for review. All imaging was performed on a 1.5T unit; the depiction of venous congestion should theoretically be enhanced at a higher magnetic field, given the higher sensitivity to susceptibility artifacts. The identification of arteriovenous shunting was not altered in the series of Jagadeesan et al,¹⁰ which included patients evaluated both on 1.5T and 3T units. Finally, we acknowledge the fact that small DAVFs associated with mild PPP on SWI might be difficult to differentiate from normal veins when the diagnosis of DAVF is not known. The ability of SWI to distinguish normal venous structures and abnormal congested veins should ideally be evaluated in a larger study including a control group of patients not harboring a DAVF. In our limited experience, the prominent veins seen secondary to venous congestion in DAVFs were generally beyond the expected normal venous anatomy seen in our daily practice and, in fact, led to further investigations in these cases.