Classification of Cerebral Arteriovenous Malformations and Intranidal Flow Patterns by Color-Encoded 4D-Hybrid-MRA

Discussion

4D MR angiography and lately also 4D-CTA¹³ have been evolving in clinical routine as noninvasive supplements to DSA. We combined the benefits of 3D TOF MRA and 4D contrast-enhanced MRA to increase spatial resolution and obtain a virtual temporal resolution of up to 0.1-second inflow time points, which serve as a measure of blood flow velocity, are color-coded, and can be adjusted interactively, giving the impression of a contrast bolus flowing through the vessels. This way, arterial, venous, and mixed-phase images can be obtained. For this study, data were acquired in a clinical routine setting at 1.5T and 3T. Due to the curve-fitting algorithm of the postprocessing, the inferior field strength at 1.5T did not influence visualization results compared with 3T datasets.

We found very good agreement for the Spetzler-Martin classification between DSA and 4D-hMRA. The agreement is in line with previous studies on 4D-MRA.^2,14⇓–16 In our study, the differences in Spetzler-Martin scores are attributed to the definition of the drainage pattern and nidus size measurement, while the nidus was located equally well in both examinations. Classification of nidus size and location is intuitively superior with tomographic imaging compared with DSA. In our study, the 3 standard planes were used for size measurements instead of angulated planes, which might produce more precise diameters, so that interrater agreement was reduced. In only 1 patient (patient 27), a difference in size measurement caused a different Spetzler-Martin grade because results were above and below the cutoff value of 3 cm.

Interrater reliability and accordance with DSA regarding depiction of draining veins were excellent for both readers, even though variability was somewhat higher and total agreement was not achieved as reported in the previous studies on 4D-MRA. On 4D-hMRA, more AVMs were seen to drain into the deep system than on DSA. We believe that this is a true advantage of 4D-MRA and was caused by a better depiction of draining veins in tomographic images with inflow–time point encoding. For example, patient 23 has a right parietal AVM fed by ACA, PCA, and MCA branches that angiographically drain into the superior sagittal sinus (Fig 4). On transversal and coronal views of the 4D-hMRA, the ipsilateral internal cerebral vein is dilated as an effect of its overload as a draining vein. An earlier inflow with respect to the contralateral internal cerebral vein is not seen, though. This might be due to a relatively small difference of inflow time points, possibly exceeding the temporal resolution of the 4D-hMRA. An explanation for the poor conspicuity on DSA might be that only a small fraction of blood drains through the internal cerebral vein, resulting in weak attenuation of the x-rays.

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Fig 4.

Patient 23. Axial (A) and coronal (B) color-encoded images show the right (ipsilateral to the AVM) internal cerebral vein dilated with symmetric inflow time points. Note the early inflow in the deep venous system in comparison with the confluens sinuum (column 3). On DSA, a deep venous drainage is not seen (C). Also note the huge aneurysmal dilation of cortical drainage with relatively late filling from its medial portion.

Another example is patient 4 with a right frontal AVM that drains superficially into the straight superior and transverse sinuses, which can be well seen on DSA (Fig 5). The delayed deep drainage into the internal cerebral vein is only faint on DSA and can easily be overlooked. On 4D-hMRA, this deep drainage is seen as a dilated vein, which contrasts with the other venous structures due to its early filling in the late arterial phase as a sign of arteriovenous shunt surgery, in effect offering a higher sensitivity. This is also a good example of the ability to differentiate the sequence of the draining veins with 4D-hMRA. Here, interrater reliability and accordance with DSA are also good. Again, the sequences of more draining veins could be distinguished better with 4D-hMRA than with DSA (Figs 5 and 6). This might, in part, be due to the rather slow rate of 3 frames/second that we use for DSA. Higher frame rates might allow differentiation of the sequences of more draining veins but with the trade-off of higher radiation exposure.

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Fig 5.

Patient 4. A, Two dilated superficial draining veins can be seen, which drain early into the transverse sinus and superior sagittal sinus (pictures 1 and 4). On picture 5, a dilated vein with delayed drainage into the internal cerebral veins is seen. B, DSA shows faint and retarded drainage into the deep venous system (picture 5).

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Fig 6.

Patient 19. Brain arteriovenous malformation fed by the ACA and PCA. Initial drainage into veins draining into the superior sagittal sinus (white arrows), while the posteromedial part of the nidus begins to drain later into the vein of Galen (B and C, single black arrow). Corresponding inhomogeneous intranidal flow pattern with a late inflow time point in the posteromedial part of the AVM nidus (type 2) (A) is seen.

The major drawback of 4D-hMRA lies in the depiction of small vessels. This can be seen in the cases in which the sequences of draining veins were not successfully distinguished and can be ascribed to vessels with a diameter smaller than 2 mm as well as the superior spatial resolution of DSA. The same is true for the depiction of feeding arteries, which is very good in vessels greater than 2 mm but inferior to DSA in arteries smaller than that. Small vessel size is a problem also encountered in previous studies. There, sensitivity could be improved by additional arterial spin-labeling perfusion imaging, with the drawback that only feeders supplying a different vascular territory could be detected. For a reliable detection of all feeding arteries, including vessels smaller than 2 mm, DSA still is needed in addition to 4D-MRA.

As the central anatomic structure, the nidus plays an essential role in the rupture of an AVM and for embolization. Its investigation has only rarely been pursued. 4D-hMRA offers very good insight into flow patterns within the nidus, so fistulas, compartmentation, and “main routes” between feeders and veins are well displayed. Because, in contrast to DSA, all feeding and draining vessels are depicted at the same time, the contribution of each single vessel to the whole nidus perfusion and its main transit routes can be analyzed and related to each other. Complex intranidal flow patterns (type 3, see below), however, can impede this analysis. Here, superselective DSA with a display of each single feeder is an advantage. In color-encoded planar reconstructions of 4D-hMRA, different types of blood flow through the nidus are discernible and can be classified into 3 types: first, a homogeneous flow in 1 direction without branching, being consistent with a major single inflow and a major single outlet as seen in patient 5 (Fig 1). Perfusion types 2 and 3 show a heterogeneous distribution of inflow time points. In type 2, there is a single branching either of 1 inflow point to 2 outflow points or vice versa as seen in patient 9 (Fig 2). Here, early arterial inflow is seen from an MCA feeder in the middle of the convolute. The blood is drained to both sides, laterally and medially, being consistent with a branching of the blood stream to the drainage veins, which are located here.

More complex inflow–time point distributions that exhibit multiple stream debranchings are seen in patient 3 (Fig 3). This flow pattern cannot be explained by only 1 or 2 relevant feeders or draining veins. In Fig 3, early inflow is seen medially, anterolaterally, and posterolaterally. Only delayed inflow is observed in the middle anteriorly and posteriorly, so the nidus is compartmented. In our patient cohort, type 2 was the prevailing flow pattern and was prevalent in almost two-thirds of the patients followed by a homogeneous flow (type 1) and a type 3 pattern. Previously ruptured AVMs do not differ in the type of intranidal flow pattern; also the potential role of different flow patterns, for example in prediction of AVM-related rupture, remains unclear. However, complex flow patterns might indicate a higher probability of turbulence. Turbulent flow increases vessel wall stress and is thought to be associated with AVM rupture. There is a need for a prospective study design to validate this hypothesis with respect to these intranidal perfusion patterns.