Artifact-Free Coronary Magnetic Resonance Angiography and Coronary Vessel Wall Imaging in the Presence of a New, Metallic, Coronary Magnetic
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循环学杂志 2005年第3期
the Department of Diagnostic Radiology (E.S., A.R., A.M., C.K., T.H.N., R.W.G., A.B.)
Technical University of Aachen, Aachen, Germany, and Johns Hopkins University School of Medicine (M.S.), Baltimore, Md.
Abstract
Background— Coronary in-stent restenosis cannot be directly assessed by magnetic resonance angiography (MRA) because of the local signal void of currently used stainless steel stents. The aim of this study was to investigate the potential of a new, dedicated, coronary MR imaging (MRI) stent for artifact-free, coronary MRA and in-stent lumen and vessel wall visualization.
Methods and Results— Fifteen prototype stents were deployed in coronary arteries of 15 healthy swine and investigated with a double-oblique, navigator-gated, free-breathing, T2-prepared, 3D cartesian gradient-echo sequence; a T2-prepared, 3D spiral gradient-echo sequence; and a T2-prepared, 3D steady-state, free-precession coronary MRA sequence. Furthermore, black-blood vessel wall imaging by a dual-inversion-recovery, turbo spin-echo sequence was performed. Artifacts of the stented vessel segment and signal intensities of the coronary vessel lumen inside and outside the stent were assessed. With all investigated sequences, the vessel lumen and wall could be visualized without artifacts, including the stented vessel segment. No signal intensity alterations inside the stent when compared with the vessel lumen outside the stent were found.
Conclusions— The new, coronary MRI stent allows for completely artifact-free coronary MRA and vessel wall imaging.
Key Words: stents ; artifacts ; restenosis ; magnetic resonance imaging ; coronary disease
Introduction
Metallic stents are frequently used in the treatment of coronary artery stenosis1–3; however, in-stent restenosis, an important finding for therapeutic decisions, is often observed. Although coronary magnetic resonance angiography (MRA) has been successfully implemented for visualization of the native proximal and middle portions of the coronary artery tree, the in-stent lumen cannot now be visualized because of susceptibility artifacts and radiofrequency shielding,4–6 resulting in a local signal void.7,8 Therefore, x-ray angiography follow-up control is still the "gold standard" for detection of in-stent restenosis9,10 because intimal hyperplasia11 or thrombus12 inside the stents cannot be directly visualized by MRA.5 Flow-sensitive coronary MRA sequences or flow-velocity measurements proximal and distal to the stents have been used to assess stent patency.7,8,13,14 One study, however, detected a notable error in flow measurements in the presence of stents.15 Furthermore, detection, direct visualization, and classification of in-stent restenosis are important. Although nitinol stents cause smaller artifacts when compared with stainless steel stents,6,16 even the former are still not artifact-free on MR images6 and do not allow for visualization of in-stent restenosis. Therefore, a completely artifact-free, metallic stent (independent of MRA imaging sequence, stent diameter, and orientation to the main magnetic field [Bo]) would be helpful.
The aim of the present study was to investigate the potential of a newly developed, dedicated, coronary MR imaging (MRI) stent for artifact-free, coronary in-stent lumen visualization and vessel wall imaging. In addition to a T2-prepared, 3D cartesian gradient-echo sequence, as already used in the first clinical studies,17 we also investigated a recently implemented, T2-prepared, 3D spiral gradient-echo sequence, which has been shown to allow improved coronary vessel visualization.18 Furthermore, a newly developed, navigator-gated, free-breathing, cardiac-triggered, 3D steady-state, free-precession (SSFP) coronary MRA sequence19 was investigated. The rationale for applying a 3D SSFP imaging sequence in the presence of metallic stents is its potentially reduced sensitivity to susceptibility artifacts and T2 effects when compared with standard gradient-echo imaging,20,21 which may improve in-stent lumen visualization. Finally, high-resolution coronary vessel wall imaging, which allows direct visualization of the vessel wall and plaque,22,23 was performed in the stented vessel segments.
Methods
Magnetic Resonance Imaging
All studies were performed on a 1.5-T, whole-body MR system (Gyroscan ACS-NT, Philips Medical Systems) equipped with cardiovascular research software (INCA2) and a commercial gradient system (23 mT/m, 219-μs rise time; PowerTrak 6000).
Animal Preparation
Coronary MRA and vessel wall imaging were performed in 15 healthy, domestic swine (45 to 60 kg body weight). The government committee on animal investigations approved the study protocols. After premedication with 0.5 mL IM atropine, azaperone (0.2 mL/kg body weight IM), ketamine (0.1 mL/kg body weight IM), and an aqueous solution of intravenous (ear vein) pentobarbital (1:3, vol/vol) were administered as needed. The animals were intubated, and mechanical ventilation was maintained throughout the study.
Coronary MRA
Coronary Vessel Wall Imaging
A navigator-gated, cardiac-triggered, fat-suppressed, dual-inversion, turbo spin-echo sequence was used for coronary vessel wall imaging.22 This sequence consisted of a 2D T2-weighted turbo spin-echo sequence with a slice thickness of 5 mm, echo train length of 7, and an echo spacing of 6.2 ms. The effective echo time was set to 25 ms to maximize signal from the vessel wall.22 The resulting acquisition window was 43 ms. A repetition time of 2 heartbeats and 3 signal averages were used. Complete black-blood properties were obtained by using a dual inversion-recovery prepulse and heart rate–dependent inversion delays. With a field of view of 320 mm and an image matrix of 512x512, in-plane spatial resolution was 0.625 mmx0.625 mm (reconstructed with a 1024x1024 matrix to 0.312 mmx0.312 mm). Scanning time was 3:52 minutes for an 80-bpm heart frequency.
2D Selective Navigator
All sequences were equipped with a right hemidiaphragm, prospective, real-time navigator for respiratory motion artifact suppression during free-breathing, 3D coronary MRA and 2D vessel wall imaging. A 5-mm navigator gating window was used. For high navigator performance in black-blood coronary vessel wall imaging, a local navigator restore24 directly followed the nonselective inversion pulse.
Prototype Coronary MRI Stent
The newly developed prototypes of the dedicated, coronary MRI stent (Figure 1A through 1C; Aachen Resonance) consist of a dedicated MR alloy composed of copper (75%), silver (8%), platinum (2%), gold (14%), and palladium (1%) to minimize susceptibility and radiofrequency artifacts.25 Three different prototype designs of this stent were used: hand woven (n=9), mechanically woven (n=3), and lasered (n=3). The initial prototypes of hand-woven stents had a low radial force. Consequently, mechanically woven designs were tested as well, which attained a radial force of >0.9 bar (wire thickness, 0.11 mm). The lasered stent used in this study had a strut thickness of 0.12 mm, yielding a radial force of 1.7 bar, which is similar to or even higher than that in currently used stainless steel stents.26
Description of Experiments and Data Analysis
First, metallic prototype MRI stents (hand woven, mechanically woven, or lasered) were investigated in vitro in a water bath. All 3 prototype designs of the stent were dilated to 2.5 and 4 mm and were positioned at 0°, 45°, and 90° to Bo. All coronary MRA sequences and the coronary vessel wall imaging sequence used for in vivo studies were examined. In vitro images were acquired in coronal slice orientation with an artificial ECG at 80 bpm, with the cardiac phase-array coil identically placed for all scans.
For in vivo examination, hand-woven (n=9), mechanically woven (n=3), and lasered (n=3) prototype coronary MRI stents were placed in the coronary arteries (right coronary artery [RCA] n=3; left anterior descending coronary artery [LAD] n=10; and left circumflex artery [LCX] n=2) in 15 pigs under x-ray guidance via a right carotid artery approach and 3.5- (n=10) and 4- (n=5) mm balloon catheters (Boston Scientific). Balloon size was chosen to avoid any overdilation of the coronary vessel lumen (Figure 2A), which was estimated from x-ray angiography and the catheter used. Stent length was 12 (n=12) or 15 (n=3) mm. After stent placement, the animals were positioned in the MR unit (supine position), and coronary MRA and coronary vessel wall imaging were performed. Coronary MRA was performed parallel to the right or left coronary artery by using a 3-point plan-scan tool and a previously described 3D SSFP scout scan,21 whereas coronary vessel wall imaging was performed perpendicular to the main axis of the coronary arteries.22 Because the multidetector computed tomography (CT) angiography for comparison was performed after MRI, the slice position for vessel wall imaging was chosen by stent location, as derived from x-ray angiograms, to ensure vessel wall imaging in the stented vessel segment. Afterward, this position was compared with reconstructions of the CT scans, which also verified vessel wall imaging in the stented vessel segment. Animal-specific trigger delays were used as visually determined by a cine scout scan (cine gradient-echo echoplanar imaging sequence, 40 heart phases, 4-chamber view). For all MRIs, a 5-element cardiac phase-array coil was used.
Finally, the animals were moved to a multislice CT unit, and cardiac-gated, contrast-enhanced coronary CT angiography was performed to determine stent location (Figure 2B). All CT examinations were performed with a 4–detector row multislice spiral CT scanner (SOMATOM Volume Zoom, Siemens) during suspended breathing (mean, 37 seconds) by switching off the respirator. A 4x1-mm collimation, 1.5-mm table feed per rotation (normalized pitch, 0.375), and a tube rotation time of 500 ms were used. Tube voltage was 120 kV with 400 effective mA · s. The scanning delay was determined by injection of a 20-mL test bolus. For vessel enhancement, 120 mL of nonionic contrast material (Ultravist 370, Schering) was injected into an ear vein at a flow rate of 2.5 mL/s, which was followed by a 50-mL saline flush. Multiplanar reformats were calculated, and stent location with respect to landmarks like origin, bifurcation, or branch vessels (eg, sinus–atrial artery or diagonal branches) was measured. CT was used as the reference for stent location to allow precise comparison with a second tomographic imaging modality.
Data Analysis
For in vitro analyses, signal intensity in a region of interest (ROI) "inside" the stent (ROI including stent lumen and stent wall) and "outside" the stent (identical ROI moved outside the stent) was measured for all 3 stent designs, both sizes (2.5 or 4 mm), all 3 investigated orientations, and all 3 coronary MRA and vessel wall imaging sequences. Signal-to-noise ratios (SNRs) inside and outside were calculated as (ROIinside or ROIoutside)=signal (S)(ROIinside or ROIoutside)/SD(ROIair), where SD(ROIair) refers to the standard deviation of the signal measured in air (outside but adjacent to the water bath), which can be assumed to be consistent in the entire data set. Because the stents were not detectable on MR images, ROIs were positioned with respect to the distance to the border of the phantom bath as derived from visualization to ensure correct ROI measurements inside and outside the stent.
For in vivo analyses, source images of the coronary MRA sand coronary vessel wall images were analyzed by consensus of 2 investigators who were aware of stent placement in the coronary vessel. All coronary MRA sequences investigated were presented next to each other for both investigators at the same time. They were asked to identify stent position on coronary MRA images and to analyze stent artifacts on a 2-grade scale (0=artifact-free coronary artery lumen visualization without any diameter/signal difference or any other stent artifacts, 1=minor or major artifacts or signal alteration in the stented portion of the coronary artery when compared with the area outside the stent). Furthermore, they were asked to analyze artifacts on black-blood coronary vessel wall images by using the same grading scale. In vivo SNRs inside and outside the stent were calculated in all 3 coronary MRA sequences by user-specified ROIs placed in the stented vessel segment of the coronary artery and proximally and distally to the stented area as follows: SNRinside=S(ROIinside)/SD(ROIair), and SNRoutside=[S(ROIproximally)+S(ROIdistally)/2]/SD(ROIair). SD(ROIair) refers to the standard deviation of the signal in a region of air located outside the chest. Because stent location could not be detected on coronary MRAs, ROIs were placed in the coronary lumen with respect to stent location as derived from multislice CT scans. Finally, the diameter of the coronary vessel inside and outside the stent was also assessed in the same vessel segments as used for SNR measurements. Because the origin of a larger branch vessel was located adjacent to the stent end in 3 of the 15 animals, diameter could be assessed for only 12 of them.
Statistics
All values are expressed as mean±SD. Quantitative SNR measurements in vitro were analyzed by calculating the relative difference (difference of 2 techniques divided by their mean value) and performing a repeated-measures ANOVA. SNR values of our in vivo feasibility study were compared for each sequence by a 2-tailed, paired Student t test. A value of P<0.05 was considered statistically significant.
Results
In vitro signal measurements yielded only a minimal difference in SNR measurements inside (stent lumen and stent wall) and outside the stent, with a mean relative difference of <3% (Table 2) for all sequences and for all 3 investigated angulations to Bo. For our small number of measurements, however, these differences did not reach statistical significance.
All in vivo MR scans were successfully completed, and image quality and SNR were assessed for all deployed stents. Coronary MRI stents could not be seen on coronary MRA in all cases. Coronary vessel lumen, including the stented vessel segment, was visualized without any artifacts (artifact grade 0) for all 3 prototype stent designs, all 3 coronary MRA sequences, and coronary vessel wall imaging. In Figures 3 and 4, representative double-oblique coronary MRAs parallel to the main axis of both coronary arteries are displayed as maximal-intensity projections. The coronary artery lumen of the stented vessel segment is visualized without any artifacts. In Figure 5, source images, which allow more precise artifact characterization, are shown. Artifact-free coronary artery visualization is demonstrated for all investigated MRA sequences as well as for coronary vessel wall imaging. The vessel lumen in vessel wall images is signal suppressed (black-blood properties), whereas the coronary vessel wall is clearly visualized without any overlying artifacts of the stent. Stent struts were not depictable on coronary MRAs or on coronary vessel wall images.
These subjective findings were in good agreement with the SNR and vessel diameter measurements (Table 3). With all 3 coronary MRA sequences, no significant differences in SNR inside the stent when compared with the area outside the stent, nor differences in vessel diameter without and with the stent, were found. The mean relative difference was <5% for all 3 investigated sequences. For 3D SSFP imaging, however, a smaller vessel diameter was found when compared with 3D cartesian gradient-echo and 3D spiral gradient-echo imaging.
Discussion
During the past several years, variable MRI sequences for coronary MRA as well as coronary vessel wall imaging have been successfully implemented for noninvasive imaging of the arteries.17–19,22–24,27,28 None of these MRI approaches have allowed complete visualization of the coronary artery lumen in the presence of metallic stents because of susceptibility artifacts and radiofrequency shielding of currently available metallic stents.6–8,29,30 Although nitinol stents cause smaller artifacts when compared with stainless steel stents,4,6,16 MRA still does not allow in-stent lumen visualization.6 Coronary in-stent lumen visualization by MRI is especially challenging because of the small diameter of the coronary arteries. Furthermore, coronary arteries are in part oriented almost perpendicular to Bo, which situation is known to cause the largest susceptibility artifacts.4,16,29,31
Because coronary artery stent placement is frequently used for the treatment of stenosis1–3,9 and in-stent restenosis or stent thrombosis is frequently seen in coronary stents,9,12,32 a noninvasive imaging modality for assessment of the in-stent lumen (like coronary MRA) would be advantageous. In the present study, 3 prototype designs (hand woven, mechanically woven, and lasered) of a newly developed, metallic coronary MRI stent were investigated in vitro and in a swine model. In addition to more conventional imaging strategies as used in earlier studies,25,33 in this study we used variable and high-quality state-of-the art coronary MRA sequences, including the recently described spiral gradient-echo imaging and SSFP imaging for improved image quality.18,19 These newer approaches may be needed for high-resolution and high-quality imaging in a clinical setting. Furthermore, a dedicated, coronary vessel wall imaging approach was used.22 Our results demonstrate that the new coronary MRI stents allows in-stent lumen visualization without any visible artifacts, independent of the coronary MRA approach used (T2-prepared, cartesian gradient-echo coronary MRA, spiral gradient-echo coronary MRA, or SSFP coronary MRA). Furthermore, the vessel wall was clearly visualized with high spatial resolution in the presence of the new coronary MRI stent. On the other hand, the new MRI stent is visible on x-ray angiography, thus facilitating conventional x-ray–guided placement.
In vitro examinations yielded only minimal SNR reduction (mean relative difference <3%) in the stented region (stent lumen and wall) when compared with the unstented area; however, this difference did not reach overall statistical significance. Minor water displacement due to the stent struts may reduce the number of protons for signal. Considerable signal attenuation due to artifacts was not seen, however. In vivo, no significant SNR alterations in the area of the stent were found, independent of the coronary MRA sequence orientation or the stent prototype design, indicating that the in-stent lumen can also be visualized in vivo without any artifacts. Furthermore, the diameter of the stented vessel segment did not show any difference when compared with the vessel segment outside the stent. No dedicated MRI techniques are needed, and even spiral gradient-echo coronary MRA, which is more sensitive to susceptibility and off-resonance artifacts,34,35 as well as high-resolution coronary vessel wall imaging, can be performed. Although artifacts caused by stents markedly depend on the kind of imaging sequence (like spin-echo, gradient-echo, or echoplanar imaging) and sequence parameters like echo time,4,30 SSFP sequences are known to be less sensitive to susceptibility artifacts.20,21 In the present study, however, we did not find any advantage with SSFP imaging for in-stent lumen visualization because of the already excellent vessel lumen visualization obtained with the non-SSFP sequences. Because vessel diameter was also unaltered on all 3 investigated coronary MRA sequences, our results indicate that objective assessment of vessel diameters changes (if any) may also be possible. The lower vessel diameter obtained with SSFP imaging compared with that found by cartesian gradient-echo and spiral gradient-echo techniques may be related to the previously described "black rim" at the border of the vessel, which may be caused by the nearly out-of-phase imaging condition of SSFP imaging. This can result in a signal void in the pixel at the vessel border (including fat and water protons).19 Consequently, the readily visible lumen may appear smaller. This may be even more pronounced by the lower spatial resolution of our SSFP imaging approach (Table 1). Although recently implemented coronary MRA approaches, like the 3D cartesian gradient-echo technique, allow visualization of proximal and middle coronary artery lumen and stenoses,17 it is well known that high spatial resolution is crucial for clinical use,36 and it may also be needed for detection of in-stent restenosis.
Coronary vessel wall imaging22,23 is a new technique that allows high-resolution imaging. The black-blood properties of this modality result in a dark vessel lumen, whereas the vessel wall appears bright, yielding high contrast between the patent lumen and the vessel wall. In contrast to coronary lumen imaging, like white-blood coronary MRA, vessel wall thickening and plaque (including plaques without luminal narrowing due to remodeling) can be assessed.22 Typically, coronary vessel wall imaging is performed perpendicular to the main axis of the vessel wall to reduce partial-volume effects. Therefore, with such an imaging approach, only a small portion of the coronary artery tree can be examined in an acceptable measurement time. For follow-up control of stents, vessel wall imaging as an add-on to coronary MRA may be sufficient if imaging focuses on the area of the stent. Furthermore, most recently, high-resolution, in-plane coronary vessel wall imaging37 has also been implemented and may allow for wall imaging of larger portions of the coronary artery tree.
The present study shows that the new coronary MRI stent makes feasible artifact-free, in-stent lumen visualization with all coronary MRA techniques. In contrast to the first investigations with a larger-diameter, prototype MRI stent and more conventional imaging sequences like contrast-enhanced MRA,25,33 in the present study artifact-free, in-stent lumen visualization of smaller-diameter coronary stents by variable state-of-the art coronary MRA sequences without exogenous contrast medium was proved to be possible. These results indicate that the new, dedicated, MRI stents allow diameter-independent, sequence-independent, and vascular territory–independent in-stent lumen visualization with MRA. Furthermore, in addition to the initial hand-woven designs (as used for renal MRA), in the present study mechanically woven and lasered prototype designs with smaller diameters were studied and compared by different sequences.25,33 The possibility to choose between different stent designs and especially to use lasered stents encourages the creation of stents with greater flexibility that maintain radial tension properties. In contrast to former series, the new, lasered stent in this study had a radial force similar to (or even higher than) currently used stainless steel stents. This shows that the lasered stent has mechanical properties suitable for use in the treatment of stenoses. This demonstrates the clinical utility of this stent design, which allows completely artifact-free, in-stent lumen visualization. In principle, this stent can also be loaded with drugs for reduction of in-stent restenosis. Development of such drug-eluting MRI stents is underway.
Other promising techniques for MRI of the in-stent lumen may include actively tuned stents, ie, using the stent in conjunction with capacitors as an antenna.38,39 For clinical use, however, the capacitor design must be minimized, and the potential for visualization of in-stent restenosis and plaque close to the stent, despite locally variable signal intensities, remains to be investigated and may depend on the sequence used. MRI stents with a completely invisible metallic alloy allow sequence-independent and easier visualization of in-stent lumen visualization.
Conclusion
The new Aachen Resonance coronary MRI stent allows artifact-free coronary MRA and coronary vessel wall imaging, independent of the coronary MRA approach used.
Acknowledgments
This study was funded in part by a general research grant from the Technical University of Aachen. We thank R. Kwiecien, Institute for Medical Statistics, Technical University of Aachen, for his help in performing the statistics. Aachen Resonance Inc provided the Aachen Resonance MRI stent.
Disclosure
Drs Buecker and Ruebben are cofounders of Aachen Resonance Inc.
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Technical University of Aachen, Aachen, Germany, and Johns Hopkins University School of Medicine (M.S.), Baltimore, Md.
Abstract
Background— Coronary in-stent restenosis cannot be directly assessed by magnetic resonance angiography (MRA) because of the local signal void of currently used stainless steel stents. The aim of this study was to investigate the potential of a new, dedicated, coronary MR imaging (MRI) stent for artifact-free, coronary MRA and in-stent lumen and vessel wall visualization.
Methods and Results— Fifteen prototype stents were deployed in coronary arteries of 15 healthy swine and investigated with a double-oblique, navigator-gated, free-breathing, T2-prepared, 3D cartesian gradient-echo sequence; a T2-prepared, 3D spiral gradient-echo sequence; and a T2-prepared, 3D steady-state, free-precession coronary MRA sequence. Furthermore, black-blood vessel wall imaging by a dual-inversion-recovery, turbo spin-echo sequence was performed. Artifacts of the stented vessel segment and signal intensities of the coronary vessel lumen inside and outside the stent were assessed. With all investigated sequences, the vessel lumen and wall could be visualized without artifacts, including the stented vessel segment. No signal intensity alterations inside the stent when compared with the vessel lumen outside the stent were found.
Conclusions— The new, coronary MRI stent allows for completely artifact-free coronary MRA and vessel wall imaging.
Key Words: stents ; artifacts ; restenosis ; magnetic resonance imaging ; coronary disease
Introduction
Metallic stents are frequently used in the treatment of coronary artery stenosis1–3; however, in-stent restenosis, an important finding for therapeutic decisions, is often observed. Although coronary magnetic resonance angiography (MRA) has been successfully implemented for visualization of the native proximal and middle portions of the coronary artery tree, the in-stent lumen cannot now be visualized because of susceptibility artifacts and radiofrequency shielding,4–6 resulting in a local signal void.7,8 Therefore, x-ray angiography follow-up control is still the "gold standard" for detection of in-stent restenosis9,10 because intimal hyperplasia11 or thrombus12 inside the stents cannot be directly visualized by MRA.5 Flow-sensitive coronary MRA sequences or flow-velocity measurements proximal and distal to the stents have been used to assess stent patency.7,8,13,14 One study, however, detected a notable error in flow measurements in the presence of stents.15 Furthermore, detection, direct visualization, and classification of in-stent restenosis are important. Although nitinol stents cause smaller artifacts when compared with stainless steel stents,6,16 even the former are still not artifact-free on MR images6 and do not allow for visualization of in-stent restenosis. Therefore, a completely artifact-free, metallic stent (independent of MRA imaging sequence, stent diameter, and orientation to the main magnetic field [Bo]) would be helpful.
The aim of the present study was to investigate the potential of a newly developed, dedicated, coronary MR imaging (MRI) stent for artifact-free, coronary in-stent lumen visualization and vessel wall imaging. In addition to a T2-prepared, 3D cartesian gradient-echo sequence, as already used in the first clinical studies,17 we also investigated a recently implemented, T2-prepared, 3D spiral gradient-echo sequence, which has been shown to allow improved coronary vessel visualization.18 Furthermore, a newly developed, navigator-gated, free-breathing, cardiac-triggered, 3D steady-state, free-precession (SSFP) coronary MRA sequence19 was investigated. The rationale for applying a 3D SSFP imaging sequence in the presence of metallic stents is its potentially reduced sensitivity to susceptibility artifacts and T2 effects when compared with standard gradient-echo imaging,20,21 which may improve in-stent lumen visualization. Finally, high-resolution coronary vessel wall imaging, which allows direct visualization of the vessel wall and plaque,22,23 was performed in the stented vessel segments.
Methods
Magnetic Resonance Imaging
All studies were performed on a 1.5-T, whole-body MR system (Gyroscan ACS-NT, Philips Medical Systems) equipped with cardiovascular research software (INCA2) and a commercial gradient system (23 mT/m, 219-μs rise time; PowerTrak 6000).
Animal Preparation
Coronary MRA and vessel wall imaging were performed in 15 healthy, domestic swine (45 to 60 kg body weight). The government committee on animal investigations approved the study protocols. After premedication with 0.5 mL IM atropine, azaperone (0.2 mL/kg body weight IM), ketamine (0.1 mL/kg body weight IM), and an aqueous solution of intravenous (ear vein) pentobarbital (1:3, vol/vol) were administered as needed. The animals were intubated, and mechanical ventilation was maintained throughout the study.
Coronary MRA
Coronary Vessel Wall Imaging
A navigator-gated, cardiac-triggered, fat-suppressed, dual-inversion, turbo spin-echo sequence was used for coronary vessel wall imaging.22 This sequence consisted of a 2D T2-weighted turbo spin-echo sequence with a slice thickness of 5 mm, echo train length of 7, and an echo spacing of 6.2 ms. The effective echo time was set to 25 ms to maximize signal from the vessel wall.22 The resulting acquisition window was 43 ms. A repetition time of 2 heartbeats and 3 signal averages were used. Complete black-blood properties were obtained by using a dual inversion-recovery prepulse and heart rate–dependent inversion delays. With a field of view of 320 mm and an image matrix of 512x512, in-plane spatial resolution was 0.625 mmx0.625 mm (reconstructed with a 1024x1024 matrix to 0.312 mmx0.312 mm). Scanning time was 3:52 minutes for an 80-bpm heart frequency.
2D Selective Navigator
All sequences were equipped with a right hemidiaphragm, prospective, real-time navigator for respiratory motion artifact suppression during free-breathing, 3D coronary MRA and 2D vessel wall imaging. A 5-mm navigator gating window was used. For high navigator performance in black-blood coronary vessel wall imaging, a local navigator restore24 directly followed the nonselective inversion pulse.
Prototype Coronary MRI Stent
The newly developed prototypes of the dedicated, coronary MRI stent (Figure 1A through 1C; Aachen Resonance) consist of a dedicated MR alloy composed of copper (75%), silver (8%), platinum (2%), gold (14%), and palladium (1%) to minimize susceptibility and radiofrequency artifacts.25 Three different prototype designs of this stent were used: hand woven (n=9), mechanically woven (n=3), and lasered (n=3). The initial prototypes of hand-woven stents had a low radial force. Consequently, mechanically woven designs were tested as well, which attained a radial force of >0.9 bar (wire thickness, 0.11 mm). The lasered stent used in this study had a strut thickness of 0.12 mm, yielding a radial force of 1.7 bar, which is similar to or even higher than that in currently used stainless steel stents.26
Description of Experiments and Data Analysis
First, metallic prototype MRI stents (hand woven, mechanically woven, or lasered) were investigated in vitro in a water bath. All 3 prototype designs of the stent were dilated to 2.5 and 4 mm and were positioned at 0°, 45°, and 90° to Bo. All coronary MRA sequences and the coronary vessel wall imaging sequence used for in vivo studies were examined. In vitro images were acquired in coronal slice orientation with an artificial ECG at 80 bpm, with the cardiac phase-array coil identically placed for all scans.
For in vivo examination, hand-woven (n=9), mechanically woven (n=3), and lasered (n=3) prototype coronary MRI stents were placed in the coronary arteries (right coronary artery [RCA] n=3; left anterior descending coronary artery [LAD] n=10; and left circumflex artery [LCX] n=2) in 15 pigs under x-ray guidance via a right carotid artery approach and 3.5- (n=10) and 4- (n=5) mm balloon catheters (Boston Scientific). Balloon size was chosen to avoid any overdilation of the coronary vessel lumen (Figure 2A), which was estimated from x-ray angiography and the catheter used. Stent length was 12 (n=12) or 15 (n=3) mm. After stent placement, the animals were positioned in the MR unit (supine position), and coronary MRA and coronary vessel wall imaging were performed. Coronary MRA was performed parallel to the right or left coronary artery by using a 3-point plan-scan tool and a previously described 3D SSFP scout scan,21 whereas coronary vessel wall imaging was performed perpendicular to the main axis of the coronary arteries.22 Because the multidetector computed tomography (CT) angiography for comparison was performed after MRI, the slice position for vessel wall imaging was chosen by stent location, as derived from x-ray angiograms, to ensure vessel wall imaging in the stented vessel segment. Afterward, this position was compared with reconstructions of the CT scans, which also verified vessel wall imaging in the stented vessel segment. Animal-specific trigger delays were used as visually determined by a cine scout scan (cine gradient-echo echoplanar imaging sequence, 40 heart phases, 4-chamber view). For all MRIs, a 5-element cardiac phase-array coil was used.
Finally, the animals were moved to a multislice CT unit, and cardiac-gated, contrast-enhanced coronary CT angiography was performed to determine stent location (Figure 2B). All CT examinations were performed with a 4–detector row multislice spiral CT scanner (SOMATOM Volume Zoom, Siemens) during suspended breathing (mean, 37 seconds) by switching off the respirator. A 4x1-mm collimation, 1.5-mm table feed per rotation (normalized pitch, 0.375), and a tube rotation time of 500 ms were used. Tube voltage was 120 kV with 400 effective mA · s. The scanning delay was determined by injection of a 20-mL test bolus. For vessel enhancement, 120 mL of nonionic contrast material (Ultravist 370, Schering) was injected into an ear vein at a flow rate of 2.5 mL/s, which was followed by a 50-mL saline flush. Multiplanar reformats were calculated, and stent location with respect to landmarks like origin, bifurcation, or branch vessels (eg, sinus–atrial artery or diagonal branches) was measured. CT was used as the reference for stent location to allow precise comparison with a second tomographic imaging modality.
Data Analysis
For in vitro analyses, signal intensity in a region of interest (ROI) "inside" the stent (ROI including stent lumen and stent wall) and "outside" the stent (identical ROI moved outside the stent) was measured for all 3 stent designs, both sizes (2.5 or 4 mm), all 3 investigated orientations, and all 3 coronary MRA and vessel wall imaging sequences. Signal-to-noise ratios (SNRs) inside and outside were calculated as (ROIinside or ROIoutside)=signal (S)(ROIinside or ROIoutside)/SD(ROIair), where SD(ROIair) refers to the standard deviation of the signal measured in air (outside but adjacent to the water bath), which can be assumed to be consistent in the entire data set. Because the stents were not detectable on MR images, ROIs were positioned with respect to the distance to the border of the phantom bath as derived from visualization to ensure correct ROI measurements inside and outside the stent.
For in vivo analyses, source images of the coronary MRA sand coronary vessel wall images were analyzed by consensus of 2 investigators who were aware of stent placement in the coronary vessel. All coronary MRA sequences investigated were presented next to each other for both investigators at the same time. They were asked to identify stent position on coronary MRA images and to analyze stent artifacts on a 2-grade scale (0=artifact-free coronary artery lumen visualization without any diameter/signal difference or any other stent artifacts, 1=minor or major artifacts or signal alteration in the stented portion of the coronary artery when compared with the area outside the stent). Furthermore, they were asked to analyze artifacts on black-blood coronary vessel wall images by using the same grading scale. In vivo SNRs inside and outside the stent were calculated in all 3 coronary MRA sequences by user-specified ROIs placed in the stented vessel segment of the coronary artery and proximally and distally to the stented area as follows: SNRinside=S(ROIinside)/SD(ROIair), and SNRoutside=[S(ROIproximally)+S(ROIdistally)/2]/SD(ROIair). SD(ROIair) refers to the standard deviation of the signal in a region of air located outside the chest. Because stent location could not be detected on coronary MRAs, ROIs were placed in the coronary lumen with respect to stent location as derived from multislice CT scans. Finally, the diameter of the coronary vessel inside and outside the stent was also assessed in the same vessel segments as used for SNR measurements. Because the origin of a larger branch vessel was located adjacent to the stent end in 3 of the 15 animals, diameter could be assessed for only 12 of them.
Statistics
All values are expressed as mean±SD. Quantitative SNR measurements in vitro were analyzed by calculating the relative difference (difference of 2 techniques divided by their mean value) and performing a repeated-measures ANOVA. SNR values of our in vivo feasibility study were compared for each sequence by a 2-tailed, paired Student t test. A value of P<0.05 was considered statistically significant.
Results
In vitro signal measurements yielded only a minimal difference in SNR measurements inside (stent lumen and stent wall) and outside the stent, with a mean relative difference of <3% (Table 2) for all sequences and for all 3 investigated angulations to Bo. For our small number of measurements, however, these differences did not reach statistical significance.
All in vivo MR scans were successfully completed, and image quality and SNR were assessed for all deployed stents. Coronary MRI stents could not be seen on coronary MRA in all cases. Coronary vessel lumen, including the stented vessel segment, was visualized without any artifacts (artifact grade 0) for all 3 prototype stent designs, all 3 coronary MRA sequences, and coronary vessel wall imaging. In Figures 3 and 4, representative double-oblique coronary MRAs parallel to the main axis of both coronary arteries are displayed as maximal-intensity projections. The coronary artery lumen of the stented vessel segment is visualized without any artifacts. In Figure 5, source images, which allow more precise artifact characterization, are shown. Artifact-free coronary artery visualization is demonstrated for all investigated MRA sequences as well as for coronary vessel wall imaging. The vessel lumen in vessel wall images is signal suppressed (black-blood properties), whereas the coronary vessel wall is clearly visualized without any overlying artifacts of the stent. Stent struts were not depictable on coronary MRAs or on coronary vessel wall images.
These subjective findings were in good agreement with the SNR and vessel diameter measurements (Table 3). With all 3 coronary MRA sequences, no significant differences in SNR inside the stent when compared with the area outside the stent, nor differences in vessel diameter without and with the stent, were found. The mean relative difference was <5% for all 3 investigated sequences. For 3D SSFP imaging, however, a smaller vessel diameter was found when compared with 3D cartesian gradient-echo and 3D spiral gradient-echo imaging.
Discussion
During the past several years, variable MRI sequences for coronary MRA as well as coronary vessel wall imaging have been successfully implemented for noninvasive imaging of the arteries.17–19,22–24,27,28 None of these MRI approaches have allowed complete visualization of the coronary artery lumen in the presence of metallic stents because of susceptibility artifacts and radiofrequency shielding of currently available metallic stents.6–8,29,30 Although nitinol stents cause smaller artifacts when compared with stainless steel stents,4,6,16 MRA still does not allow in-stent lumen visualization.6 Coronary in-stent lumen visualization by MRI is especially challenging because of the small diameter of the coronary arteries. Furthermore, coronary arteries are in part oriented almost perpendicular to Bo, which situation is known to cause the largest susceptibility artifacts.4,16,29,31
Because coronary artery stent placement is frequently used for the treatment of stenosis1–3,9 and in-stent restenosis or stent thrombosis is frequently seen in coronary stents,9,12,32 a noninvasive imaging modality for assessment of the in-stent lumen (like coronary MRA) would be advantageous. In the present study, 3 prototype designs (hand woven, mechanically woven, and lasered) of a newly developed, metallic coronary MRI stent were investigated in vitro and in a swine model. In addition to more conventional imaging strategies as used in earlier studies,25,33 in this study we used variable and high-quality state-of-the art coronary MRA sequences, including the recently described spiral gradient-echo imaging and SSFP imaging for improved image quality.18,19 These newer approaches may be needed for high-resolution and high-quality imaging in a clinical setting. Furthermore, a dedicated, coronary vessel wall imaging approach was used.22 Our results demonstrate that the new coronary MRI stents allows in-stent lumen visualization without any visible artifacts, independent of the coronary MRA approach used (T2-prepared, cartesian gradient-echo coronary MRA, spiral gradient-echo coronary MRA, or SSFP coronary MRA). Furthermore, the vessel wall was clearly visualized with high spatial resolution in the presence of the new coronary MRI stent. On the other hand, the new MRI stent is visible on x-ray angiography, thus facilitating conventional x-ray–guided placement.
In vitro examinations yielded only minimal SNR reduction (mean relative difference <3%) in the stented region (stent lumen and wall) when compared with the unstented area; however, this difference did not reach overall statistical significance. Minor water displacement due to the stent struts may reduce the number of protons for signal. Considerable signal attenuation due to artifacts was not seen, however. In vivo, no significant SNR alterations in the area of the stent were found, independent of the coronary MRA sequence orientation or the stent prototype design, indicating that the in-stent lumen can also be visualized in vivo without any artifacts. Furthermore, the diameter of the stented vessel segment did not show any difference when compared with the vessel segment outside the stent. No dedicated MRI techniques are needed, and even spiral gradient-echo coronary MRA, which is more sensitive to susceptibility and off-resonance artifacts,34,35 as well as high-resolution coronary vessel wall imaging, can be performed. Although artifacts caused by stents markedly depend on the kind of imaging sequence (like spin-echo, gradient-echo, or echoplanar imaging) and sequence parameters like echo time,4,30 SSFP sequences are known to be less sensitive to susceptibility artifacts.20,21 In the present study, however, we did not find any advantage with SSFP imaging for in-stent lumen visualization because of the already excellent vessel lumen visualization obtained with the non-SSFP sequences. Because vessel diameter was also unaltered on all 3 investigated coronary MRA sequences, our results indicate that objective assessment of vessel diameters changes (if any) may also be possible. The lower vessel diameter obtained with SSFP imaging compared with that found by cartesian gradient-echo and spiral gradient-echo techniques may be related to the previously described "black rim" at the border of the vessel, which may be caused by the nearly out-of-phase imaging condition of SSFP imaging. This can result in a signal void in the pixel at the vessel border (including fat and water protons).19 Consequently, the readily visible lumen may appear smaller. This may be even more pronounced by the lower spatial resolution of our SSFP imaging approach (Table 1). Although recently implemented coronary MRA approaches, like the 3D cartesian gradient-echo technique, allow visualization of proximal and middle coronary artery lumen and stenoses,17 it is well known that high spatial resolution is crucial for clinical use,36 and it may also be needed for detection of in-stent restenosis.
Coronary vessel wall imaging22,23 is a new technique that allows high-resolution imaging. The black-blood properties of this modality result in a dark vessel lumen, whereas the vessel wall appears bright, yielding high contrast between the patent lumen and the vessel wall. In contrast to coronary lumen imaging, like white-blood coronary MRA, vessel wall thickening and plaque (including plaques without luminal narrowing due to remodeling) can be assessed.22 Typically, coronary vessel wall imaging is performed perpendicular to the main axis of the vessel wall to reduce partial-volume effects. Therefore, with such an imaging approach, only a small portion of the coronary artery tree can be examined in an acceptable measurement time. For follow-up control of stents, vessel wall imaging as an add-on to coronary MRA may be sufficient if imaging focuses on the area of the stent. Furthermore, most recently, high-resolution, in-plane coronary vessel wall imaging37 has also been implemented and may allow for wall imaging of larger portions of the coronary artery tree.
The present study shows that the new coronary MRI stent makes feasible artifact-free, in-stent lumen visualization with all coronary MRA techniques. In contrast to the first investigations with a larger-diameter, prototype MRI stent and more conventional imaging sequences like contrast-enhanced MRA,25,33 in the present study artifact-free, in-stent lumen visualization of smaller-diameter coronary stents by variable state-of-the art coronary MRA sequences without exogenous contrast medium was proved to be possible. These results indicate that the new, dedicated, MRI stents allow diameter-independent, sequence-independent, and vascular territory–independent in-stent lumen visualization with MRA. Furthermore, in addition to the initial hand-woven designs (as used for renal MRA), in the present study mechanically woven and lasered prototype designs with smaller diameters were studied and compared by different sequences.25,33 The possibility to choose between different stent designs and especially to use lasered stents encourages the creation of stents with greater flexibility that maintain radial tension properties. In contrast to former series, the new, lasered stent in this study had a radial force similar to (or even higher than) currently used stainless steel stents. This shows that the lasered stent has mechanical properties suitable for use in the treatment of stenoses. This demonstrates the clinical utility of this stent design, which allows completely artifact-free, in-stent lumen visualization. In principle, this stent can also be loaded with drugs for reduction of in-stent restenosis. Development of such drug-eluting MRI stents is underway.
Other promising techniques for MRI of the in-stent lumen may include actively tuned stents, ie, using the stent in conjunction with capacitors as an antenna.38,39 For clinical use, however, the capacitor design must be minimized, and the potential for visualization of in-stent restenosis and plaque close to the stent, despite locally variable signal intensities, remains to be investigated and may depend on the sequence used. MRI stents with a completely invisible metallic alloy allow sequence-independent and easier visualization of in-stent lumen visualization.
Conclusion
The new Aachen Resonance coronary MRI stent allows artifact-free coronary MRA and coronary vessel wall imaging, independent of the coronary MRA approach used.
Acknowledgments
This study was funded in part by a general research grant from the Technical University of Aachen. We thank R. Kwiecien, Institute for Medical Statistics, Technical University of Aachen, for his help in performing the statistics. Aachen Resonance Inc provided the Aachen Resonance MRI stent.
Disclosure
Drs Buecker and Ruebben are cofounders of Aachen Resonance Inc.
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