Application of zero echo time MR angiography in follow-up of intracranial aneurysm remnant and in-stent lumen after embolization: a comparison study with digital subtraction angiography

Abstract

Background

Intracranial aneurysm with endovascular treatment needs to be followed-up with a proper imaging method.

Purpose

To evaluate the performance of magnetic resonance angiography (MRA) with zero echo time at 1.5-T in assessing the intracranial aneurysm remnant and in-stent lumen as compared with time-of-flight MRA, with digital subtraction angiography as the gold standard.

Material and Methods

A total of 46 patients (17 men; mean age = 56.6±13.7 years) with 54 aneurysms who underwent coil embolization with or without stent were enrolled in this study. The presence of aneurysm remnant and the visualization of in-stent lumen were evaluated. The agreement of remnant identification between MRA with zero echo time and time-of-flight MRA with digital subtraction angiography was evaluated using Cohen’s kappa analysis. The performance of in-stent lumen visualization between MRA with zero echo time and time-of-flight MR angiography was compared with Chi-square test.

Results

Of 54 aneurysms, 27 were found to have remnants by digital subtraction angiography. The kappa value in identification of remnant of aneurysm was 0.852 between MRA with zero echo time and digital subtraction angiography and 0.741 between time-of-flight MRA and digital subtraction angiography. In detecting remnant of aneurysm, the sensitivity, specificity, positive predictive value, and negative predictive value were 96.3%, 88.9%, 89.7%, and 96.0% for MRA with zero echo time and 91.7%, 83.3%, 81.5%, and 92.6% for time-of-flight MRA, respectively. In visualizing in-stent lumen, MRA with zero echo time had better performance than time-of-flight MRA (P < 0.001).

Conclusion

MR angiography with zero echo time might be a better non-invasive approach in assessing remnant of aneurysms and in-stent lumen as compared with time-of-flight MRA.

Keywords

Central nervous system magnetic resonance angiography embolization stents adults aneurysms

Introduction

Intracranial aneurysm is the third most common apoplectic cerebral lesion, accounting for about 25% of all cerebrovascular diseases. Ruptured aneurysm is the most common cause of spontaneous subarachnoid hemorrhage. In recent years, with continuous development in endovascular intervention techniques and equipment, the endovascular embolization with or without stenting become the major treatment strategies for intracranial aneurysms (1). However, a number of studies have shown that 20–30% of intracranial aneurysms, especially the large and wide-necked ones, could re-canalize or recur despite complete embolization after interventional treatment (2,3). In addition, in 15–65% of cases, embolization may not be complete after the first interventional treatment, leaving the remnants of aneurysmal neck or body, and second treatment may be needed in 30–50% of patients (4,5). Thus, long-term regular follow-ups are needed for the patients after embolization treatment of intracranial aneurysms.

Currently, digital subtraction angiography (DSA) is considered as the gold standard (6) for assessing embolization treatment of intracranial aneurysms. However, the inherent risks including arterial access, the use of iodinated contrast media, and ionizing radiation of DSA limit its routine application for follow-up. Furthermore, DSA may be associated with an inherent small rate of transient or permanent neurological deficit (7,8). Therefore, an imaging technique with high sensitivity and minimal invasion is desirable in determining whether the intracranial aneurysm recurs after the interventional treatment. Computed tomography angiography (CTA) is a very good imaging method for intracranial aneurysm follow-up assessment, but it could not be used for the follow-up of coiled aneurysm due to artifact caused by stent and coil. Time-of-flight magnetic resonance angiography (TOF MRA) has been demonstrated to have high sensitivity and specificity in evaluating the intracranial aneurysm after embolization (9). However, the magnetic field non-uniformity caused by the stent and coil could impact the image quality of in-stent lumen, leading to inaccurate evaluation of aneurysmal sac remnants (10,11). Contrast-enhanced MRA improves the sensitivity and reduces the artifacts related to the stent (12,13). But the enhanced thrombosis inside the sac of aneurysm could lead to the false positive of the remnant (14). Magnetic resonance angiography with zero echo time (zTE MRA) has been recently developed as a non-invasive approach. With the use of arterial spin labeling (ASL) and zero TE (zTE) acquisition, the artifacts caused by turbulent blood flow and related to the magnetic susceptibility may be minimized (15).

This study sought to compare the performance of zTE MRA with TOF MRA at 1.5-T in assessing the remnant of aneurysms and in-stent lumen, with DSA as gold standard.

Material and Methods

Study population

Patients with intracranial aneurysms determined by DSA and underwent coil embolization with or without stenting were recruited in this study. Patients with contraindications to MR examination were excluded. The clinical information including age, gender, hypertension (repeated blood pressure >140/90 mmHg or chronic antihypertensive medication), smoke (current smokers or if the time interval since abstinence was <5 years), diabetes (casual plasma glucose ≥200 mg/dL, fasting plasma glucose ≥126 mg/dL, 2 h plasma glucose ≥200 mg/dL or chronic hypoglycemic medications), and history of stroke was collected from the clinical record. The study protocol was approved by Beijing Hospital Institutional Review Board (approval no. 2016BJYYEC-032-02) and the written consent form was obtained from each participant.

MR imaging

All the recruited patients underwent MR imaging (MRI) on a 1.5-T whole-body MR scanner (MR 360, GE Healthcare, USA) with eight-channel head coil. The TOF MRA and zTE MRA were acquired with the following parameters: 3D TOF MRA: TR/TE = 28/6.8 ms, flip angle (FA) = 20°, field of view (FOV) = 220 × 220 mm, slice thickness = 1.4 mm, slice number = 128 slices, bandwidth = 15.63 kHz, excitation number = 1, and scan time = 3 min 57 s; zTE MRA: TR/TE = 1213/0.008 ms, FA = 5°, FOV = 200 × 200 mm, slice thickness = 1.2 mm, slice number = 332 slices, slab number = 3, bandwidth = 20 kHz, excitation number = 2, and scan time = 12 min 21 s.

DSA examination

The interval between MRA and DSA examination was within one week. After the right side femoral artery was punctured using the modified Seldinger’s technique, a 6F sheath was placed and systemic heparinization was performed. The 6F guiding catheter then reached the targeted vessel with the guidance of a 0.035-inch super-smooth guide wire. A conventional DSA was conducted first and then the rotational DSA was performed with three-dimensional (3D) reconstruction.

Image analysis

The 3D TOF MRA and zTE MRA images were reconstructed with maximum intensity projection (MIP) algorithm using MR workstation (Advantage Workstation 4.6, GE Healthcare, Waukesha, WI, USA). Two readers who had >8 years of experience in neurovascular imaging interpreted TOF MRA images blinded to zTE MRA and DSA results. To minimize the memory bias, these two readers interpreted the zTE MRA images blinded to TOF MRA and DSA results with a one-month interval after the image review of TOF MRA. When reviewing MRA images, the readers were required to go through all the raw source images so that they would not miss the aneurysm remnant due to the image reconstruction. To test the intra-reader reproducibility, one reader (Reader A) reviewed the zTE MRA and TOF MRA images for the second time three months later, still with a one-month interval between and blinded with all the information about the patients. DSA images were evaluated by a senior neural intervention clinician with 12 years of experience in neural intervention blinded to MR images.

The aneurysm remnants were categorized into two grades: grade 1 = no remnants or only presence of neck remnants; and grade 2 = presence of remnants of aneurysmal sac (16).

To evaluate the capability of TOF MRA and zTE MRA in visualizing the in-stent lumen of the parent artery in aneurysms treated with coil embolization and stenting, a two-point scale was used: 1 = there was no artifact or a little artifact, the image quality was good enough to delineate the in-stent lumen; and 2 = the image quality was deteriorated due to the obvious artifact and the in-stent lumen could not be delineated clearly. The differentiation between the in-stent stenosis and the artifact induced ill-delineated lumen was important, it was considered to be the ill-delineated lumen when the artery distal to the stent segment was well demonstrated, and the range of signal loss within the in-stent lumen was relatively long with obscure borderline.

Statistical analysis

Continuous variables were described as mean ± standard deviation (SD) and categorical variables were presented with percentage. Cohen’s kappa analysis was utilized to determine the agreement between TOF MRA and zTE MRA with DSA in detecting the aneurysm remnants. The sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) of each method of MRA in evaluating the aneurysm remnants were calculated with DSA as the gold standard. The inter- and intra-reader reproducibility in identification of aneurysm remnants using TOF MRA and zTE MRA was also analyzed using the Cohen’s kappa analysis, respectively. The capability of TOF MRA and zTE MRA in visualizing the in-stent lumen was compared with Chi-square test. A P value of < 0.05 was considered statistically significant. All statistical analyses were conducted by SPSS v.23.

Results

A total of 46 patients (17 men [37%]; mean age = 56.6 ± 13.7 years) were enrolled in this study from December of 2015 to October of 2017. Ten patients (21.7%) had a history of smoking, 28 (60.9%) had hypertension, 8 (17.3%) had diabetes, and 3 (6.5%) had a history of stroke. The follow-up interval between MRA/DSA and surgery was in the range of 2 days to 12 months.

Characteristics of aneurysms

In total, 54 aneurysms were detected from 46 patients. The mean diameter of the aneurysms was 6.5 ± 6.6 mm. No aneurysm rupture occurred in this study cohort. Of the 54 aneurysms, coil embolization with stenting was performed for 42 (77.8%) aneurysms whereas coil embolization without stenting was performed for 12 (22.2%) aneurysms. The location of the 54 aneurysms was as follows: internal carotid artery = 28 (51.9%); middle cerebral artery = 9 (16.7%); basilar artery = 8 (14.8%); posterior inferior cerebellar artery = 1 (1.9%); superior cerebellar artery = 1 (1.9%); vertebral artery = 3 (5.6%); and anterior communicating artery = 4 (7.4%). The types and numbers of stents were as follows: Solitaire 24; Neuroform 10; Lvis 7; LEO 6; and Pipeline 1.

Evaluation of aneurysm remnants

Of the 54 aneurysms, DSA revealed half of them had type 2 aneurysm remnants. As for MRA, 25 (46.3%) and 29 (53.7%) aneurysms were found to have grade 1 and grade 2 remnants on zTE MRA, whereas 30 (55.6%) and 24 (44.4%) aneurysms were found to have grade 1 and grade 2 remnants on TOF MRA, respectively (Figs. 1 and 2). When identifying aneurysm remnants, zTE MRA showed excellent agreement with DSA (k = 0.852, 95% confidence interval [CI] = 0.714–0.990; Table 1); the sensitivity, specificity, PPV, and NPV of zTE MRA were 96.3%, 88.9%, 89.7%, and 96.0%, respectively. In contrast, TOF MRA showed good agreement with DSA (k = 0.741, 95% CI = 0.564–0.918; Table 1) in evaluating aneurysm remnants; the sensitivity, specificity, PPV, and NPV of TOF MRA was 91.7%, 83.3%, 81.5%, and 92.6%, respectively.

Fig. 1.

Right internal carotid artery aneurysm treated by stent-assisted embolization. Both (a) magnetic resonance angiography with zero echo time (zTE MRA) and (c) digital subtraction angiography (DSA) show the sac remnant (arrow), and (a) zTE MRA shows the in-stent lumen (arrow). (b) Time-of-flight magnetic resonance angiography (TOF MRA) does not show the remnant and in-stent lumen due to the signal loss caused by the stent (arrow).

Fig. 2.

Right superior cerebellar artery aneurysm treated by coil embolization. (a) Magnetic resonance angiography with zero echo time (zTE MRA) shows the aneurysmal sac remnant (arrow). (b) Time-of-flight magnetic resonance angiography (TOF MRA) does not detect the aneurysmal sac remnant (arrow). The intervention doctor missed the sac remnant due to the densely packed coil in the small aneurysm on (c) digital subtraction angiography (DSA) (arrow).

Table 1.

Agreement between MRA and DSA in evaluating aneurysm remnant.

	DSA		Kappa (95% CI)	P value
	Grade 1*	Grade 2^†	Kappa (95% CI)	P value
zTE MRA
Grade 1	24	1	0.852 (0.714–0.990)	<0.001
Grade 2	3	26	0.852 (0.714–0.990)	<0.001
TOF MRA
Grade 1	25	5	0.741 (0.564–0.918)	<0.001
Grade 2	2	22	0.741 (0.564–0.918)	<0.001

No remnants or only presence of neck remnants.

†

Presence of remnants of aneurysmal sac.

zTE MRA, magnetic resonance angiography with zero echo time; TOF, time-of-flight; DSA, digital subtraction angiography; CI, confidence interval.

Visualization of in-stent lumen of parent artery

Of the 42 aneurysms undergoing coil embolization with stenting, the in-stent lumen of 36 (85.7%) cases could be well delineated and 6 (14.3%) were ill-delineated by zTE MRA. In contrast, 17 (40.5%) could be well delineated and 25 (59.5%) were ill-delineated by TOF MRA (Fig. 3). Compared with TOF MRA, zTE MRA had a significantly better performance in the visualization of in-stent lumen of parent artery (P < 0.001).

Fig. 3.

Bilateral internal carotid artery aneurysms treated by stent-assisted embolization. (a) Magnetic resonance angiography with zero echo time (zTE MRA) shows the in-stent lumen clearly (arrow). (b) Time-of-flight magnetic resonance angiography (TOF MRA) does not show (right internal carotid artery) or does not show clearly (left internal carotid artery) the in-stent lumen due to the signal loss caused by the stent (arrow).

As for the influence of stent type on image quality, we noticed that most of the stents, whether they were stents with an open cell design (Solitarire, Neuroform) or a close cell design (Lvis, LEO), had a better in-stent lumen delineation on zTE MRA than on TOF MRA (Table 2).

Table 2.

The type of stent and its influence to the in-stent lumen manifestation on MRA.

Type of stent	Used in this study (n)	Ill-delineated on TOF MRA (n)	Ill-delineated on zTE MRA (n)
Solitaire	24	19	6
Neuroform	10	3	1
Lvis	7	3	0
LEO	6	2	1
PiPeline	1	1	1

MRA, magnetic resonance angiography; TOF, time-of-flight; zTE MRA, magnetic resonance angiography with zero echo time.

Reproducibility

When evaluating the aneurysm remnants by zTE MRA, the kappa values of inter-reader and intra-reader agreement were 0.702 (95% CI = 0.513–0.891) and 0.778 (95% CI = 0.612–0.944), respectively. As for TOF MRA, the kappa values for inter-reader and intra-reader agreement were 0.736 (95% CI = 0.555–0.917) and 0.664 (95% CI = 0.465–0.863), respectively (Table 3).

Table 3.

Inter-reader and intra-reader reproducibility.

	Kappa value (95% CI)	P value
zTE MRA
Reader A vs. Reader B	0.702 (0.513–0.891)	<0.001
Intra-reader (A)	0.778 (0.612–0.944)	<0.001
TOF MRA
Reader A vs. Reader B	0.736 (0.555–0.917)	<0.001
Intra-reader (A)	0.664 (0.465–0.863)	<0.001

zTE MRA, magnetic resonance angiography with zero echo time; TOF, time-of-flight; CI, confidence interval.

Discussion

In the present study, we compared the performance of zTE MRA and TOF MRA in evaluating the aneurysm remnant and in-stent lumen delineation in patients undergoing endovascular treatment, using DSA as a gold standard. We found that zTE MRA showed better agreement with DSA in the identification of aneurysm remnants than TOF MRA. Compared with TOF MRA, zTE MRA had a significantly better performance in visualizing the in-stent lumen of the parent artery. Our findings indicate that zTE MRA might be superior to TOF MRA in the follow-up of intracranial aneurysm after endovascular treatment.

We found that TOF MRA showed good agreement with DSA in identification of intracranial aneurysm remnant. Our study exhibited higher sensitivity than in the literature (16,17). A study by Pierot demonstrated that the sensitivity, specificity, PPV, and NPV in the detection of aneurysm remnants by TOF MRA on a 1.5-T MR scanner were 0.54, 0.98, 0.90, and 0.85, respectively (16). Previous studies also showed that TOF MRA was a sensitive and safe technique for evaluating coiled aneurysms (17 –19). However, there are certain levels of false-negatives and false-positives in TOF MRA when evaluating the remnants of intracranial aneurysm with endovascular intervention treatment. False-negatives are mainly attributed to the artifacts caused by stents, coil, and slow or turbulent blood flow inside the sac of aneurysms. Most of the false-positives might be due to the fact that the short T1 signal of thrombosis within the sac of aneurysms mimics the sac remnant.

In the present study, zTE MRA was found to have better agreement with DSA in assessing the remnants of aneurysms compared with TOF MRA. Similar to our study, Shang recently reported that zTE MRA was a better approach than TOF MRA in visualizing the parent artery of intracranial aneurysms with coil (20). The motivation of using zTE MRA was to minimize the artifacts from coils and stents in aneurysms via shortening the echo time. When the echo time is shortened (e.g. 3-T, TE = 2.6 ms; 1.5-T, TE = 6.9 ms), the coil-related artifacts in 3-T are clearly reduced than those in 1.5-T (21). When the echo time is short enough, the phase dispersion of the labeled blood flow signal in the voxel space and the magnetic susceptibility can be minimized. Compared to the 2.4 ms of echo time which was used in Gönner’s study (22), the echo time of zTE MRA in the present study is only 8 µs. This rather short echo time may further reduce the dephasing induced signal loss and artifacts caused by stents and coils. In addition, the fact that the ASL technique was less sensitive to hemodynamics may also contribute to the lower sensitivity of zTE MRA to blood flow conditions. All these technical characteristics of zTE MRA ensured detection of the sac remnant with a more uniform signal as well as clearer and sharper edges compared to TOF MRA in the present study.

As for the detection of aneurysm remnants, there are three more items in this study which need to be highlighted. First, we used a two-point scale to analyze the aneurysm remnant instead of a three-point scale (complete occlusion, neck remnant, sac remnant). Pierot recommended a two-point scale when they studied 126 intracranial aneurysms with coil embolization, because they considered a three-grade scale to be subjective when differentiating neck and sac remnants and it was difficult to differentiate total occlusion and neck remnants (16). In addition, the risk of rupture or re-rupture is probably higher in aneurysm sac remnants than in neck remnants. We therefore chose the two-point scale. Second, the most crucial aspect of MRA is to correctly depict the aneurysm remnant, so the NPV is important. In this study, the NPV of zTE MRA was 96.0%, higher than that of TOF MRA. This reflects a low probability of omitting clinically significant aneurysm remnant when using zTE MRA. Third, zTE MRA detected three more aneurysm remnants than DSA in the present study. DSA, though considered to be the gold standard, may miss some aneurysm remnants, especially when they are small and the coil is packed closely in the sac. zTE MRA is a good supplement to DSA in the follow-up of intracranial aneurysm after endovascular treatment.

In the present study, zTE MRA was superior to TOF MRA in the visualization of in-stent lumen of parent artery, a similar finding with the study by Takano et al. (23). It is crucial to detect the in-stent restenosis because it is an important complication and needs proper treatment. Besides, it is also important to show the path of the parent artery in order to localize the aneurysm and detect the sac remnant. The stent, though safe for MRI, can still lead to some artifacts on TOF MRA due to the inhomogeneity of B₀. As mentioned above, zTE MRA is capable of minimizing the artifacts of stents benefiting from ultra-short echo time, so that most of in-stent lumen can be well detected. This study also indicates that nearly all kinds of stents used nowadays may have a better imaging quality on zTE MRA compared with TOF MRA. Nevertheless, there were still six cases in which the in-stent lumen was not successfully delineated by zTE MRA. The reason might be due to the stent material and structure.

There are several limitations to this study. First, this study was conducted on a 1.5-T MR scanner which requires a prolonged scan time compared to 3-T due to the shorter T1 relaxation rates and lower signal-to-noise ratio (scanning time = 5–6 min at 3-T, scanning time = 12 min at 1.5-T). Future studies are warranted utilizing 3-T MR scanners. Second, there is a lack of comparison with contrast-enhanced MRA which can improve the sensitivity and reduce the artifacts related to the stent (13). Finally, complete blinding is not possible for readers when evaluating the images from the two MRA modalities as zTE MRA had a larger FOV, better background suppression, and a slightly worse granular feeling in image quality compared with TOF MRA.

In conclusion, zTE MRA might be a better non-invasive approach when assessing remnant of aneurysms and in-stent lumen compared with TOF MRA. Patients may rely on the regular zTE MRA follow-ups when no aneurysm remnant or recur is detected.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

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