Follow-up of Intracranial Aneurysms Treated by Flow Diverters: Evaluation of Parent Artery Patency Using 3D-T1 Gradient Recalled-Echo Imaging with 2-Point Dixon in Combination with 3D-TOF-MRA with Compressed Sensing

DISCUSSION

Currently, 3D-TOF-MRA is the most frequently used noninvasive follow-up method for intracranial aneurysms treated using endovascular techniques.²⁰ However, for patients who underwent flow diversion, the magnetic and radiofrequency shielding causes a signal loss in the stent implantation area and often manifests as a false in-stent stenosis or interruption and, consequently, has poor specificity and PPV. To reduce these metallic artifacts, Oishi et al⁵ and Shao et al²² used, respectively, Silent MRA and 3D-T1 SPACE to assess the parent artery status. Regarding the patency of the stented arteries after FD treatment, these sequences were more accurate compared with 3D-TOF-MRA, but they were time-consuming and, consequently, more susceptible to motion artifacts. To reduce the duration of the sequences and reduce the possible motion artifacts and the total duration of the MR imaging examination procedure, we have optimized 2 sequences, which we use together: a 3D-TOF sequence with HyperSense and a LAVA-Flex sequence, both without injection of a contrast agent. The LAVA-Flex sequence allows better study of the flow inside the stent, whereas the 3D-TOF sequence remains necessary to study aneurysmal occlusion because the LAVA-Flex sequence has not proved its effectiveness for this purpose.

Apart from increasing the signal-to-noise ratio, especially intravascular, the compressed sensing technique HyperSense allows a substantial reduction in the acquisition time of the 3D-TOF sequence. Ours had a total acquisition time of 2 minutes 59 seconds. This sequence can also be used to evaluate aneurysmal occlusion, analyze other arteries, but also, when artifacts are low, to evaluate the patency of the parent artery. The LAVA-Flex sequence allows, with a particularly short acquisition time of 1 minute 57 seconds, a 3D-T1-weighted sequence that is less sensitive to metallic artifacts, in particular on the out of phase sequence due to a shorter TE (Fig 1), with, however, a weaker intravascular signal due to an entry section phenomenon less marked than the 3D-TOF with HyperSense sequence. This can be explained by the shorter TR of the LAVA-Flex sequence compared with the 3D-TOF sequence; however, this short TR results in a remarkably decreased acquisition time, without hindering the in-stent flow analysis. MIP reformats of LAVA-Flex MRA are useful to evaluate the caliber of the parent vessel but must always be analyzed in conjunction with the native sections because the selection of the most intense voxels by the MIP algorithm hinders the visualization of the stent, whose signal is low. The total acquisition time for these 2 sequences was, therefore, 4 minutes 56 seconds, more than 2 times shorter than Silent MRA or 3D-T1 SPACE combined with 3D-TOF.

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FIG 1.

3D-TOF with HyperSense MRA (A), LAVA-Flex MRA (B), and DSA (C) of a 61-year-old woman treated with a 4 × 25 Surpass Evolve FD located from the left ICA to the left MCA. There is a significant reduction in metal artifacts on the LAVA-Flex (OutPhase) sequence, which shows the absence of in-stent stenosis, confirmed by DSA. Note that there is not exactly the same projection between MRA and DSA. White arrows indicate the proximal and distal ends of the FDs.

In this study, the joint use of 3D-TOF with HyperSense MRA and LAVA-Flex MRA allowed us to obtain a NC-MRA specificity of 0.83 (95% CI, 0.69–0.93) and a PPV of 0.65 (95% CI, 0.41–0.85) (Fig 2), which were better than those of CE-MRA (0.55; 95% CI, 0.39–0.70; and 0.41; 95% CI, 0.24–0.59, respectively) in the evaluation of the parent artery patency. This result can be explained by an analysis of the TRICKS MRA sequence generally using background-subtracted volumes, which do not permit stent visualization, as well as the use of a delayed-MRA sequence, and not an arterial CE-MRA sequence. Finally, the absence of a contrast-enhanced 3D-T1-weighted sequence can also partially explain these results. With NC-MRA and CE-MRA, we had only 1 false-negative result, which can probably be explained by the delay between MR imaging and arteriography, 4 weeks for this patient, who had stopped the dual antiplatelet therapy on his own after the MR imaging examination, 3 months after FD placement at the M1–M2 junction. Thus, the in-stent stenosis could have developed in the meantime. The sensitivity and NPV remained excellent for NC-MRA (0.93; 95% CI, 0.66–1.00; and 0.97; 95% CI. 0.85–1.00, respectively) and CE-MRA (0.93; 95% CI, 0.66–1.00; and 0.96; 95% CI, 0.79–1.00, respectively).

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FIG 2.

In-stent stenosis in a 50-year-old woman treated with a 5 × 15 Surpass Evolve FD placed in the left VA. This was a complementary embolization of a left PICA aneurysm, initially revealed by a subarachnoid hemorrhage 10 years earlier and treated by coiling at that time. 3D-TOF with HyperSense MRA (A) and LAVA-Flex MRA (Outphase) (B) demonstrates moderate in-stent stenosis (white arrows) predominating a few millimeters upstream of the neck of the still patent aneurysm, 6 months after placement of the FD. Confirmation of a moderate in-stent stenosis (black arrowhead) on angiography without (C) and with (D) digital subtraction. The black arrows show the limits of the FD metallic mesh.

The specificity and PPV tended to be lower for Pipeline Shield FDs and even lower for Surpass Evolve FDs, probably due to more pronounced metallic artifacts (Fig 3). Unlike the criterion standard DSA, MRA is susceptible to the dissimilarities between flow diverters. Halitcan et al¹⁵ suggested that the key factor was the alloy used for the construction of the FDs, with nitinol-based devices being responsible for fewer metallic artifacts. While we agree that this factor influences the extent of artifacts, the marked difference between the artifacts created by Pipeline Shield FDs and Surpass Evolve FDs, which are both cobalt-chromium devices, suggests that other important factors were probably involved, such as the number of wires composing the FD combined with the thickness of the wire. Indeed, Surpass Evolve FDs are made of 64 wires (except for 2.5 mm diameter FD), while Pipeline Shield FDs are made of 48 wires, with an equivalent wire thickness (∼28  and ∼30 µm, respectively). In addition, the tungsten used in combination with platinum for the visibility of cobalt-chromium devices used in this study (while nitinol devices used only platinum) may also play a role.

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FIG 3.

3D-TOF with HyperSense MRA comparison of artifacts created by the 3 types of FDs used in our study. A, A 68-year-old woman treated with a Surpass Evolve FD (3.25 × 17 mm) located in the right VA. B, A 61-year-old woman treated with a Pipeline Shield FD (3.5 × 18 mm) located from the left VA to the basilar artery. C, A 52-year-old woman treated with a Silk Vista Baby FD (2.5 × 20 mm) located in the right anterior cerebral artery (A1–A2). The extent of the metallic artifacts is large for the Surpass Evolve FD, small for the Pipeline Shield FD, and minimal for the Silk Vista Baby FD. White arrows indicate the proximal and distal ends of the FDs.

It is important to keep in mind the shortcomings of each FD in MR imaging when interpreting the parent artery patency, so as not to erroneously conclude in-stent stenosis. Specificity and PPV tended to be lower for patients treated with additional devices than for those treated with FDs exclusively, an outcome expected due to the additional artifacts created by coils, the WEB, or surgical clips. Indeed, these artifacts can appear as false stenosis (ie, false-positives), thus reducing specificity and PPV. MR imaging is essential for the evaluation of potential ischemic and hemorrhagic complications after FD placement and is a relatively reliable screening test for in-stent stenosis because of its excellent sensitivity and NPV. However, DSA remains the criterion standard in parent artery patency evaluation, especially when additional material like coils or surgical clips is used. It, thus, appears useful to systematically perform NC-MRA sequences in addition to classic parenchymal sequences to evaluate in-stent flow. Ideally, an initial concomitant DSA control would indicate any false-positive or false-negative results, which could serve as reference in the long-term follow-up of intracranial stent evaluation with NC-MRA.

Our study has some limitations: First, the small number of patients (n = 56) included. However, this number is comparable with that in the other 2 main studies focused on the analysis of the patency of the parent artery (40 for Shao et al²² and 78 for Oishi et al⁵). Besides, the sample size for each kind of FD is small, possibly introducing systematic error. Second, MR imaging and DSA were not systematically performed on the same day, with a maximum interval of 4 weeks and, therefore, may not reflect the exact same conditions concerning parent vessel status. Third, CTA was not evaluated in our study, notably for patients treated with FDs exclusively for whom it could be a valid option. Although it shares the risks of iodinated contrast media and ionizing radiation of DSA, it is a noninvasive examination that does not share the potential risks of puncture site and neurologic complications. Fourth, interobserver agreement ranged from 0.6 to 0.79 for the NC-MRA and CE-MRA, corresponding to “substantial agreement” and not “almost perfect agreement.”²⁴ These differences mainly concerned the analysis of Surpass Evolve FDs, which produce more pronounced metallic artifacts than the other FDs studied, thus making interpretation more difficult, especially in the presence of additional material like coils and clips.