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DOI: 10.1148/radiol.2273020354
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(Radiology 2003;227:897-902.)
© RSNA, 2003

Technical Developments

Metallic Renal Artery MR Imaging Stent: Artifact-free Lumen Visualization with Projection and Standard Renal MR Angiography1

Elmar Spuentrup, MD, Alexander Ruebben, MD, Matthias Stuber, PhD, Rolf W. Günther, MD and Arno Buecker, MD

1 From the Department of Diagnostic Radiology, Technical University of Aachen, Pauwelsstrasse 30, 52057 Aachen, Germany (E.S., A.R., R.W.G., A.B.); Department of Medicine (Cardiovascular Division), Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Mass (E.S., M.S.); and Philips Medical Systems, Best, the Netherlands (M.S.). Received April 4, 2002; revision requested May 30; final revision received September 26; accepted October 15. Address correspondence to E.S. (e-mail: spuenti@rad.rwth-aachen.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
A cardiac-triggered free-breathing three-dimensional (3D) balanced fast field-echo projection renal magnetic resonance (MR) angiographic sequence was investigated for in-stent lumen visualization of a dedicated metallic renal artery stent. Fourteen prototype stents were deployed in the renal arteries of six pigs (in two pigs, three stents were deployed). Projection renal MR angiography was compared with standard contrast material–enhanced 3D breath-hold MR angiography. Artifact-free in-stent lumen visualization was achieved with both projection MR angiography and contrast-enhanced MR angiography. These promising results warrant further studies for visualization of in-stent restenosis.

© RSNA, 2003

Index terms: Magnetic resonance (MR), artifact, 961.93 • Magnetic resonance (MR), vascular studies, 961.12942, 961.12943 • Renal arteries, MR, 961.12942, 961.12943 • Renal arteries, stenosis or obstruction, 961.72 • Stents and prostheses, 961.1268


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
Results
 Discussion
 REFERENCES
 
Metallic stents are frequently used for treatment of renal artery stenosis. Although contrast material–enhanced three-dimensional (3D) magnetic resonance (MR) angiography has been successfully implemented for imaging of the renal arteries noninvasively, currently the in-stent lumen cannot be visualized by using MR angiography because of susceptibility artifacts and radio-frequency shielding (1,2). Although nitinol stents cause smaller artifacts when compared with artifacts caused by stainless steel stents (3,4), even nitinol stents do not allow artifact-free visualization on MR images (4). However, for detection and classification of in-stent restenosis, a metallic stent (independent of MR angiographic imaging sequence, stent diameter, and orientation to the main magnetic field) that allows artifact-free visualization would be favorable.

Projection renal MR angiography (5) allows high spatial resolution and high contrast imaging of the renal arteries and renal artery stenosis without contrast medium. Although aortic spin tagging is used for image contrast (5–10), cardiac triggering (11) and real-time navigator technology (12,13) can be used for motion artifact suppression, and data can be acquired during free breathing. This procedure allows enhanced signal acquisition and high-spatial-resolution imaging. The rationale for applying a 3D steady-state free precession (balanced fast field-echo [FFE]) imaging sequence in the presence of metallic stents is that this sequence has reduced sensitivity to susceptibility artifacts and T2* effects when compared with the sensitivity to artifacts of standard gradient-echo imaging (14,15). This reduced sensitivity may improve in-stent lumen visualization. Thus, the purpose of our study was to evaluate a dedicated metallic renal artery stent for artifact-free in-stent lumen visualization by using two MR angiographic imaging techniques, projection balanced FFE MR angiography and standard contrast-enhanced MR angiography.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
MR Imaging
All studies were performed with an interventional 1.5-T whole-body MR imaging system (Gyroscan ACS-NT; Philips Medical Systems, Best, the Netherlands) equipped with cardiovascular research software (INCA2; Philips Medical Systems) and a commercial gradient system (PowerTrak 6000; Philips Medical Systems), with a maximum amplitude of 23 mT/m and a 219-µsec rise time. An x-ray fluoroscopic unit (BV212; Philips Medical Systems) was positioned in the direct vicinity of the MR unit, which allowed identical repositioning of the study animals between the MR imaging and the x-ray fluoroscopic units prior to and after stent placement.

Study Animals
Projection and contrast-enhanced renal MR angiography were performed in six healthy domestic swine (body weight, 48–61 kg) as approved by the government committee on animal investigations. After premedication with 0.5 mL of intramuscularly administered atropine and 0.2 mL of intramuscularly administered azaperone per kilogram of body weight, an aqueous solution of pentobarbital (dilution, 1:3) was administered intravenously through an ear vein as needed. The animals were intubated, and mechanical ventilation was maintained throughout the study. This allowed for constant free-breathing conditions and motion-free breath holds, which was a major advantage for systematic comparison of the varying sequences performed in this study.

Projection MR Angiography
Principles of projection MR angiography.—A projection MR arteriogram (6–9) allows selective visualization of the arteries by means of spin tagging (spin labeling) upstream of the arteries of interest. The spin tagging pulse (180°) results in a magnetization inversion. During a time delay (labeling delay) between the labeling pulse and the imaging sequence, labeled blood (with an inverted magnetization) flows into the imaging volume. The differences of magnetization at the time of imaging are used for selective visualization of the arterial lumen by means of subtraction of identical data sets, one with and one without the preceding labeling pulse. Consequently, the arterial lumen appears with a high signal intensity on the projection images, whereas signal of the surrounding static tissue is signal suppressed due to subtraction.

Projection renal MR angiographic sequence.—A previously described navigator-gated free-breathing cardiac-triggered 3D segmented k-space balanced FFE sequence (5) was used as the imaging sequence for projection renal MR angiography. Sequence parameters included a field of view of 440 mm, a matrix of 512 x 360 (0.86 x 1.2 mm2 in-plane resolution), 5.0/2.5 repetition time msec/echo time msec, and a flip-angle of a constant 80°. The acquired 3D volume included 29 1.8-mm-thick sections (including interpolation by using zero filling), which resulted in a 1.9-mm3 voxel volume. Twenty-nine radio-frequency excitations with signal sampling resulted in a 145-msec data acquisition window per R-R interval (late diastole) and a scanning time of 5 minutes 45 seconds for a heart rate of 80 beats per minute and one signal acquired. To approach steady-state conditions for the balanced FFE sequence, 20 repetitive start-up cycles preceded each imaging portion of the sequence (16). Data acquisition was timed to late diastole to prevent different inter-view flow velocities or a diameter change of the proximal renal artery caused by the aortic pulse wave (11). The diastolic flow in the renal arteries supports the blood exchange for the projection renal MR angiography. For signal reception, two elements of a synergy spine coil were used. Imaging was performed with an oblique coronal orientation, and the 3D imaging slab was angled in the cranial portion dorsally. This angulation prevented spin saturations (ie, in the left ventricle), which otherwise would result in signal intensity and image contrast reduction in the projection MR angiography (5).

Two-dimensional selective navigator.—A previously described prospective real-time navigator was used for respiratory motion artifact suppression (13) at free-breathing projection renal MR angiography. Such a navigator includes a two-dimensional selective pencil-beam excitation pulse (12), which was positioned on the dome of the right hemidiaphragm (13). The navigator-detected lung-liver interface position was calculated by means of cross correlation (12) between the most recent navigator signal and an end-expiratory reference navigator profile. If the navigator-detected interface position was in a user-specified range (gating window, 5 mm), the data were accepted for image reconstruction; otherwise, the data were discarded and remeasured until the gating window was satisfied.

Two-dimensional selective aortic spin-labeling pulse.—For selective aortic spin labeling (spin tagging), a previously described (8,10) two-dimensional selective spiral inversion pulse with a sinc-shaped radio-frequency excitation (17) and nine cycles in k space was used. This pencil-beam labeling pulse had a 30-mm diameter and was positioned parallel to the suprarenal aorta. A 125-msec labeling time delay was used to allow for subsequent wash-in of labeled blood into the renal arteries. The labeling angle for the nonlabeled and labeled acquisition was changed during the scanning between 0° and 180°, respectively.

Projection renal MR angiographic reconstruction.—For selective visualization of the aorta and renal arteries (with labeled blood), two data sets, one without and one with the preceding labeling pulse, were complexly subtracted, resulting in selective renal MR arteriograms (10,18,19). During subtraction, signal from static tissue and veins was almost completely suppressed.

Three-dimensional Breath-hold Contrast-enhanced Renal MR Angiography
A breath-hold 3D spoiled T1-weighted gradient-echo sequence (5.4/1.44, flip angle of 40°, field of view of 450 x 315 mm2, matrix of 128 x 512, section thickness of 1.5 mm [including interpolation with zero filling], 50 coronal sections, 0.9 x 2.5-mm2 in-plane resolution, and 3.2-mm3 voxel volume) was performed by using automatic bolus tracking to start the imaging sequence. A double dose of gadodiamide (Omniscan; Nycomed, Ismaning, Germany) (0.2 mmol/kg) was administered.

Prototype Renal Artery Stent
The recently developed prototype renal artery MR imaging stent (Aachen Resonance, Aachen, Germany) consisted of a dedicated alloy with a high copper content (>90%) to minimize susceptibility and radio-frequency artifacts (3,4,20,21) (Fig 1). The prototype stent was 12 mm long with a 5-mm diameter, handwoven, balloon mounted, and suitable for dilation from 3 to 7 mm. The stent struts had a width of 100 µm. A closed-cell design yielded diamond-shaped cells that were approximately 2.0 x 2.5 mm. Because of the prototype character of the handwoven stents, no radial strength measurements were performed, but further improvement, if desired, can be obtained by using mechanical weaving.



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  		Figure 1. Prototype metallic renal artery MR imaging stent (stent diameter, 5 mm).

 
Description of Experiments and Data Analysis
MR imaging.—Initially, metallic prototype stents were investigated in vitro in a water bath (projection MR angiography) and in a contrast media solution (contrast-enhanced MR angiography, with a gadolinium and water solution diluted in a ratio of 1:20) by using the head coil. One stent dilated to 5 mm was positioned 0°, 30°, 45°, 60°, and 90° angled to the main magnetic field (B0). The 3D balanced FFE (anatomic image) and 3D gradient-echo imaging sequences with sequence parameters as used for in vivo studies were examined. In vitro images were acquired in the coronal section orientation.

All in vivo MR examinations were performed with each study animal in the supine position. First, coronal oblique projection renal MR angiography was performed before renal intervention. Subsequently, the animal was moved to the x-ray fluoroscopic unit, and the prototype metallic stents were placed in both renal arteries with radiographic guidance through a femoral 9-F introducer sheath (Cordis, Roden, the Netherlands). The stents were mounted on a balloon catheter (Smash; Boston Scientific, Natick, Mass) ranging in size from 3 to 7 mm and positioned over a 0.035-inch guide wire (Terumo, Leuven, Belgium). The balloon size was determined with measurements at conventional renal angiography. Stent localization as derived from conventional angiography with respect to renal artery origin or landmarks such as bifurcations was recorded. Afterward, the animal was repositioned at an identical position in the MR unit, and projection renal MR angiography was repeated. Finally, 3D contrast-enhanced MR angiography with a single breath hold was performed by using bolus tracking for optimized contrast. Contrast-enhanced MR angiography was performed only after projection renal MR angiography, because contrast media injection with T1 shortening potentially reduces contrast in the projection renal MR angiogram (ie, the difference in magnetization between the image with labeling and that without labeling is reduced).

For in vivo investigation, 14 dedicated renal artery metallic stents dilated to varying diameters (3 mm, n = 1; 5 mm, n = 11; 6 mm, n = 1; 7 mm, n = 1) were successfully placed in the main renal arteries (n = 13) or the first segment branch (n = 1) of six pigs (in two pigs, three stents were deployed). All MR images were successfully obtained in all pigs. In all six animals, parallel maximum intensity projections could be obtained with both MR angiographic techniques.

Data analysis.—For in vitro analyses, signal intensity in a region of interest (ROI) inside the stent (ROI including stent lumen and stent wall, 106–121 mm2) and in that outside the stent (the same ROI moved outside the stent) was measured, and signal-to-noise ratios (SNRs) inside and outside were calculated as described later for in vivo investigations. ROIs were positioned by one investigator (E.S.) with respect to the distance to the border of the water bath as derived from macroscopic visualization to ensure correct ROI measurements inside and outside the stent.

For in vivo analyses, maximum intensity projections obtained with both sequences were analyzed by two investigators (A.B., E.S.) who were aware of stent position as determined by using conventional angiography. They were asked to identify stent position on the maximum intensity projection images and to analyze artifacts at the area of stent position in comparison with the area outside the stent in consensus. To do so, they used a two-grade scale as follows: grade 0, which indicated a completely artifact-free vessel lumen and in-stent lumen visualization without any diameter or signal intensity difference, and grade 1, which indicated minor or major artifacts or signal alteration in the portion of the renal vessel with the stent. Furthermore, SNRs inside and outside the stent were calculated on both the navigator-gated free-breathing 3D balanced FFE renal projection MR angiogram and the breath-hold 3D contrast-enhanced renal MR angiogram by using user-specified ROIs (17–67 mm2) placed by one author (E.S.) in the portion of the renal vessel with the stent and those located proximally and distally to the area with the stent as follows: SNRinside = S(ROIinside stent)/SD(ROIair), and SNRoutside = [S(ROIproximally) + S(ROIdistally)/2]/SD(ROIair), where S refers to the signal and SD(ROIair) refers to the SD of the signal in a region of air located dorsally to the animal.

Statistical analysis.—In vivo SNR measurements of all stents were averaged in each swine. Subsequently, SNRs inside and outside the stent were compared by using a two-tailed Student t test for paired groups. A difference with a P value less than .05 was considered significant.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
In vitro signal measurements yielded no significant difference in SNR inside the stent (stent lumen and stent wall) when compared with the SNR outside the stent, independent of the orientation to the main magnetic field or the imaging sequence (with 3D balanced FFE sequence, mean SNRinside was 292.6 ± 4.4 [SD], with a range of 285 to 298, and mean SNRoutside was 291.5 ± 4.8, with a range of 285 to 299 [P = .24]; with 3D gradient-echo sequence, mean SNRinside was 449.3 ± 8.5, with a range of 437 to 461, and mean SNRoutside was 449.7 ± 8.8, with a range of 435 to 462 [P = .73]).

In Figure 2, representative double-oblique coronal projection renal MR images (in concert with the corresponding anatomic image without spin labeling) and the contrast-enhanced MR angiogram are shown as maximum intensity projections. With both techniques, a high signal intensity in both main renal arteries was observed. Both areas of the renal arteries with the stent were visualized completely artifact free with both renal MR angiographic techniques. Furthermore, more distal branching vessels were seen without signal reduction. The signal of the surrounding static soft tissue and renal veins was almost completely suppressed with both techniques (Fig 2a, 2b), which allowed maximal intensity projection display.



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  		Figure 2a. (a) Coronal oblique 3D balanced FFE projection renal MR angiograms obtained in a pig. Left column: Anatomic images. Right column: Projection images. Top row: Images obtained in arteries without stent. Bottom row: Images obtained in arteries with stent. Identical section positioning and imaging parameters were used before and after stent placement. Parameters were as follows: 5.0/2.5, 0.86 x 1.2 mm2 in-plane resolution. (b) Coronal 3D contrast-enhanced MR angiogram (5.4/1.44, 0.9 x 2.5 mm2 in-plane resolution) obtained in a pig. (c) Corresponding anteroposterior digital conventional angiogram obtained in the same pig with stents (arrows) in both renal arteries. With both MR angiographic techniques, the in-stent lumen is completely artifact free.

 


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  		Figure 2b. (a) Coronal oblique 3D balanced FFE projection renal MR angiograms obtained in a pig. Left column: Anatomic images. Right column: Projection images. Top row: Images obtained in arteries without stent. Bottom row: Images obtained in arteries with stent. Identical section positioning and imaging parameters were used before and after stent placement. Parameters were as follows: 5.0/2.5, 0.86 x 1.2 mm2 in-plane resolution. (b) Coronal 3D contrast-enhanced MR angiogram (5.4/1.44, 0.9 x 2.5 mm2 in-plane resolution) obtained in a pig. (c) Corresponding anteroposterior digital conventional angiogram obtained in the same pig with stents (arrows) in both renal arteries. With both MR angiographic techniques, the in-stent lumen is completely artifact free.

 


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  		Figure 2c. (a) Coronal oblique 3D balanced FFE projection renal MR angiograms obtained in a pig. Left column: Anatomic images. Right column: Projection images. Top row: Images obtained in arteries without stent. Bottom row: Images obtained in arteries with stent. Identical section positioning and imaging parameters were used before and after stent placement. Parameters were as follows: 5.0/2.5, 0.86 x 1.2 mm2 in-plane resolution. (b) Coronal 3D contrast-enhanced MR angiogram (5.4/1.44, 0.9 x 2.5 mm2 in-plane resolution) obtained in a pig. (c) Corresponding anteroposterior digital conventional angiogram obtained in the same pig with stents (arrows) in both renal arteries. With both MR angiographic techniques, the in-stent lumen is completely artifact free.

 
In all cases and in all portions of the renal arteries (n = 14) with stents, no artifacts (artifact grade 0) were seen with both renal MR angiographic techniques (projection and contrast-enhanced renal MR angiography) as judged by two investigators. Even direct comparison of the projection renal MR angiograms acquired prior to and after stent placement did not allow stent position detection.

These subjective findings were in good agreement with SNR measurements (Fig 3). With both renal MR angiographic techniques, a similar high SNR inside the stent, when compared with that of the lumen outside (proximally and distally) the stent, was found.



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  		Figure 3. Graph shows objectively assessed image quality of SNR inside and outside the stent for the 3D contrast-enhanced MR angiogram (CE-MRA) and 3D balanced FFE projection renal MR angiogram.

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
REFERENCES
 
Metallic stents are widely used for treatment of stenoses in varying vessel territories. However, in-stent restenosis is frequently observed (22,23). Currently, the standard for in-stent restenosis detection is follow-up conventional angiography (22–24). Although MR angiography can be used to assess flow velocities proximal and distal to the stent as an indirect value for in-stent restenosis (25) (with a notable error as demonstrated in one study [26]), so far, intimal hyperplasia (27) or a thrombus (28) inside metallic stents cannot be directly visualized (2,4). Therefore, MR angiography in the presence of metallic stents is currently not suitable for visualization of in-stent restenosis, an important diagnostic finding for treatment decisions like reintervention. Artifacts caused by stents mainly depend on the stent material, stent design, MR imaging sequence and sequence parameters used, stent orientation with respect to the main magnetic field, and the frequency encoding direction (1,3, 4,21,26,29–34).

In the present study, a prototype metallic renal artery MR imaging stent was investigated for in-stent lumen visualization in vitro and in vivo by using MR imaging. This stent was designed to minimize MR imaging artifacts, such as susceptibility and radio-frequency shielding artifacts, and was investigated with two renal MR angiographic techniques: standard contrast-enhanced renal MR angiography and balanced FFE projection renal MR angiography. Balanced FFE (steady-state free precession) projection MR angiography (5) was also investigated, because projection MR angiography allows high spatial resolution and high image contrast imaging without the need for contrast media application or breath holding. Furthermore, this technique may demonstrate minor sensitivity to susceptibility artifacts, because susceptibility artifacts caused by stents markedly depend on the kind of imaging sequence (such as spin-echo, gradient-echo, and echo-planar imaging) and the sequence parameters (such as echo time) (1,33) and have been shown to be minor with balanced FFE imaging (14,15).

Other nonenhanced renal MR angiographic techniques, such as phase-contrast MR angiography (35,36) or time-of-flight MR angiography (37), are based on gradient-echo techniques, are typically limited to the visualization of the proximal main renal arteries, and tend to contribute to an overestimation of stenoses. In contrast to these techniques, the present balanced FFE projection renal MR angiography is based on a steady-state free precession imaging sequence (with flow compensation in all three spatial coordinates) and has been shown to allow motion artifact–free high-contrast high-spatial-resolution visualization of the renal arteries, including more distal branching vessels and renal artery stenoses (5). Therefore, this technique may be favorably used for in-stent lumen visualization in renal artery stents. High image quality in balanced FFE projection renal MR angiography (5) was obtained by using navigator gating (12) for respiratory motion artifact suppression and cardiac triggering for minimizing flow and pulse-wave artifacts (11).

Sufficient SNR for high-spatial-resolution imaging can be obtained without any time constraints associated with breath-hold MR angiographic techniques (1.9 mm3 voxel size in balanced FFE projection renal MR angiography, 3.2 mm3 voxel size in contrast-enhanced renal MR angiography). Furthermore, selective aortic spin tagging is used for contrast in balanced FFE projection renal MR angiography, which allows repetitive imaging prior to and after stent placement without obscuring of image contrast. Thus, direct comparison of the images prior to and after stent placement was possible, which allowed more accurate determination of artifact and stent localization than did single contrast-enhanced MR angiography (without comparison prior to intervention).

However, findings of our present study show that the metallic renal artery MR imaging stent allows completely artifact-free in-stent lumen visualization with both investigated renal MR angiographic techniques, whereas stent localization cannot be identified. These findings were demonstrated in vitro and in vivo, independent of the orientation to the main magnetic field, which has been shown to markedly influence stent artifact size (1,3,4,29) or the diameter (3–7 mm) of the deployed stents. The almost perpendicular orientation to B0 and the small size of the renal arteries are especially challenging for in-stent lumen visualization in renal MR angiography when they are compared with those of other vessel territories such as the iliac or the femoral arteries (31,38). One limitation of the present study is the small number of swine investigated. In a larger study population, it is possible that a minimal difference in SNR measurements inside and outside the stent probably would be detected. However, no artifacts were seen. We think our study results demonstrate that no clinically relevant SNR alterations occur by using the metallic renal artery MR imaging stent.

Our first promising results warrant further experimental studies for visualization of in-stent restenosis by using the metallic renal artery MR imaging stent.

In conclusion, the metallic renal artery MR imaging stent allows artifact-free in-stent lumen visualization by using both 3D standard renal MR angiography and 3D balanced FFE projection renal MR angiography.


   FOOTNOTES
 
A.B. and A.R. are cofounders of Aachen Resonance, which provided the metallic renal artery MR imaging stents.

Abbreviations: FFE = fast field echo, ROI = region of interest, SNR = signal-to-noise ratio, 3D = three-dimensional

Author contributions: Guarantors of integrity of entire study, E.S., A.B.; study concepts, E.S., A.B.; study design, E.S., A.B., M.S.; literature research, E.S., A.R.; experimental studies, E.S., A.R., A.B.; data acquisition, E.S.; data analysis/interpretation, E.S., A.B.; statistical analysis, E.S., M.S.; manuscript preparation and definition of intellectual content, E.S., A.B.;manuscript revision/review, A.R., R.W.G.; manuscript editing and final version approval, E.S.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 

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