Published online before print February 21, 2006, 10.1148/radiol.2383050058
(Radiology 2006;239:263-268.)
© RSNA, 2006
Renal Arteries: Comparison of Steady-State Free Precession MR Angiography and Contrast-enhanced MR Angiography1
Christoph U. Herborn, MD,
David M. Watkins, MD,
Val M. Runge, MD,
Jilene M. Gendron, RT,
Mark L. Montgomery, MD and
L. Gill Naul, MD
1 From the Department of Radiology, Scott and White Clinic and Hospital, Texas A&M University, Temple, Tex. Received January 17, 2005; revision requested March 18; revision received April 18; accepted June 1.
Address correspondence to C.U.H., Department of Diagnostic and Interventional Radiology, University Medical Center Hamburg-Eppendorf, Martinistr 52, 20246 Hamburg, Germany (e-mail: herborn{at}uke.uni-hamburg.de).
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ABSTRACT
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All participants provided informed consent to participate in this study, which was approved by the institutional review board. Breath-hold three-dimensional (3D) steady-state free precession (SSFP) magnetic resonance (MR) angiography was compared with 3D contrast material–enhanced MR angiography in patients suspected of having renal artery stenosis. Two radiologists assessed visualization of renal arteries and detection of vascular disease. With SSFP MR angiography, 39 of 41 renal arteries in 19 patients were correctly detected. Relevant stenoses were correctly identified with SSFP MR angiography in two patients. In two patients, SSFP MR angiographic data sets led to false-positive overgrading of vascular disease. Fast breath-hold 3D SSFP MR angiography appears to be feasible for MR angiography of renal arteries.
© RSNA, 2006
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INTRODUCTION
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Renal artery stenosis due to atherosclerotic vessel wall changes and fibromuscular dysplasia is a well-recognized cause of secondary arterial hypertension and often initiates a vicious pathophysiologic circle toward impaired renal function, which might end in extracorporeal dialysis. In addition to medical therapy, effective treatment options for significant renal artery constriction include minimally invasive endovascular repair by means of angioplasty with and without stent implantation and surgical procedures. Thus, accurate detection and classification of renovascular disease at an early stage is of paramount importance. Despite its invasiveness, inherent complication risks, and the use of potentially nephrotoxic contrast agents, conventional angiography is regarded as the standard of reference for evaluation of the renal arteries. Several alternative imaging modalities, however, have become clinically available and are increasingly applied for initial assessment of the renal arteries to exclude relevant disease (1).
Currently, both contrast material–enhanced computed tomography (CT) angiography and three-dimensional (3D) magnetic resonance (MR) angiography have been established as safe and reliable techniques for detection and classification of renal artery disease. Because of the lack of need for a nephrotoxic contrast agent and ionizing radiation, 3D contrast-enhanced MR angiography is particularly attractive for patients at risk of renal failure (2,3). During the past decade, this technique has been shown to be robust and easily implemented even in community hospitals and private practices, yet it is not without limitations (4). Fast imaging with steady-state free precession (SSFP) has become available (5). The sequence is characterized by a complex T2 and T1 contrast. Favorable imaging features inherent in the SSFP sequence include homogeneous high blood vessel signal intensity relatively independent of flow and very short acquisition times. These characteristics render the SSFP sequence a natural candidate for MR angiographic applications. Heretofore, SSFP MR angiography has been successfully implemented for evaluation of the coronary arteries (6,7). Recently, the technique also has been assessed for use with free-breathing MR angiography of the renal arteries by using slab-selective prepulses (8). The aim of our study, therefore, was to compare breath-hold 3D SSFP MR angiography with the reference standard of 3D contrast-enhanced MR angiography in patients who are suspected of having renal artery stenosis.
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MATERIALS AND METHODS
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Subjects
The study met all criteria set forth by the local institutional review board that approved our study, and all participants gave informed consent prior to inclusion in the study. Between October 2004 and January 2005, 21 consecutive patients who were referred for exclusion of renal artery stenosis due to arterial hypertension of unknown origin were enrolled in the study. All patients lacked any contraindications to MR imaging. There were 13 men (age range, 35–71 years; mean age, 59.3 years) and eight women (age range, 17–77 years; mean age, 61.4 years). The mean blood pressure values were 156.8 mm Hg ± 13 (standard deviation) for men and 96 mm Hg ± 10 for women; the mean serum creatinine value was 1.8 mg/dL ± 0.7 (159 µmol/L ± 62, and the mean serum urea nitrogen level was 51.3 mg/dL ± 42.4 (18.3 mmol/L ± 15.1).
MR Imaging
All examinations were performed with a 1.5-T whole-body superconducting magnet (Magnetom Sonata; Siemens Medical Solutions, Erlangen, Germany) equipped with a powerful gradient system (gradient strength, 40 mT · m–1; rise time, 200 msec) and a circular polarized phased-array surface coil. Parallel imaging techniques were not employed. After performance of a localizer sequence, which consisted of three imaging stacks oriented in the transverse, sagittal, and coronal planes, a coronal two-dimensional SSFP sequence was performed for localization of the origin of the renal arteries. Next, a transverse breath-hold fat-saturated 3D SSFP sequence was performed. This sequence was characterized by the following parameters: repetition time msec/echo time msec, 3.8/1.55; flip angle, 65°; field of view, 380 mm; matrix, 180 x 320; number of sections per slab, 30; spatial resolution, 1.4 x 1.2 x 1.6 mm; and acquisition time, 23 seconds. A transverse acquisition was chosen to minimize pulsation artifacts from the aorta and the inferior vena cava. Coronal 3D gradient-recalled-echo sequences (3.44/1.17; flip angle, 25°; field of view, 280 mm; phase-encoding direction, 100%; matrix, 288 x 384; number of sections per slab, 56; spatial resolution, 1.0 x 0.7 x 1.8 mm; and acquisition time, 21 seconds) were performed before and after the intravenous administration of a bolus of a paramagnetic contrast agent (gadodiamide, Omniscan; GE Healthcare, Princeton, NJ) at a dose of 0.2 mmol/kg. The contrast agent was tracked with a bolus-tracking technique (Care-Bolus; Siemens Medical Solutions, Erlangen, Germany) and was administered with an automated injector (Spectris; Medrad, Pittsburgh, Pa) at a rate of 2.0 mL/sec.
Image Analysis
All data were transferred to and evaluated with a dedicated postprocessing workstation (Leonardo, Siemens Medical Solutions). Both sequences were performed and assessed together. To eliminate any recognition bias, all patient-related data were masked on the digitally stored images from the examinations. Maximum blood vessel length as visible on the maximum intensity projections was recorded for SSFP MR angiographic and contrast-enhanced MR angiographic sequences, respectively, by one author (C.U.H., with 4 years of experience with MR imaging evaluation of the renal arteries). Signal-to-noise ratios within the first third of the main renal artery were measured on the source images at each site with equally sized (size range, 40–60 pixels) and locally adapted regions of interest with the following calculation: SIrart/SDnoise, where SIrart is the signal intensity of the renal artery and SDnoise is the standard deviation of noise from a signal intensity measurement in a circular region of interest in the air outside the patient.
Blood over soft-tissue contrast-to-noise ratio values were calculated in the same manner by placing the region of interest in paravertebral muscle by using the following calculation: (SIrart – SImus)/SDnoise, where SImus is signal intensity of muscle. These measurements were performed by another author (D.M.W., with 2 years of MR imaging experience). Image quality of the maximum intensity projection was assessed in consensus by two radiologists (L.G.N. and M.L.M., both with more than 10 years of MR imaging experience) with a four-point Likert-type scale as follows: 1, nondiagnostic (no signal enhancement within the vessel lumen, complete venous overlay); 2, moderate (signal enhancement within the vessel lumen but still inhomogeneous, incomplete delineation of the vessel border, slight venous overlay, evaluation possible with low diagnostic confidence); 3, good visualization (good signal enhancement within vessel lumen, almost completely homogeneous; almost no venous overlay; incomplete delineation of vessel border; evaluation possible with satisfactory diagnostic confidence); and 4, excellent visualization (superb and completely homogeneous signal enhancement within vessel lumen, optimal delineation of vessel border, no venous overlay, evaluation possible with high diagnostic confidence). Maximum reduction of the luminal diameter for each lesion (<50%, 
50%, or occlusion) was assessed in consensus by two experienced readers (C.U.H. and V.M.R., with more than 10 years of experience with MR angiography) on maximum intensity projections of both MR angiographic data sets in random order.
Statistical Analysis
All parameters were recorded in an electronic data sheet (Excel XP; Microsoft, Redmond, Wash), and statistical analysis was performed by using software (SPSS for Windows, version 12, 2003; SPSS, Chicago Ill). While signal-to-noise ratios and contrast-to-noise ratios and maximal visible blood vessel length were analyzed with a nonparametric Wilcoxon signed rank test, image quality of SSFP MR angiographic images and that of contrast-enhanced MR angiographic images was compared with a Mantel-Haenszel test for ordinal data. Differences with P < .05 were considered statistically significant in all cases. Sensitivity and specificity of SSFP MR angiography for the detection of significant stenoses (luminal narrowing exceeding 50%) were calculated for each artery by using contrast-enhanced MR angiography as the standard of reference. The 95% confidence intervals were calculated for all computed sensitivity and specificity values on the basis of binominal distribution.
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RESULTS
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Venous access for contrast material injection was impossible in one female patient who therefore underwent MR angiography on the basis that SSFP MR angiographic images revealed no hemodynamically relevant stenosis. In one male patient, the SSFP sequence failed because of technical problems. Thus, MR data acquisition for the comparative analysis was fully accomplished in a total of 19 patients.
Arteries
A total of 39 (96.1%) of 41 renal arteries in these 19 patients were correctly detected with SSFP MR angiography (Fig 1). Two supernumerary arteries were missed in the SSFP data sets; one of those was not included in the field of view for the SSFP images. The maximal visible blood vessel length was more limited on the SSFP images compared with that on the contrast-enhanced MR angiographic images (Fig 2). The maximal visible blood vessel length for the right renal artery was 38 mm on the SSFP images, whereas it was 51 mm on the contrast-enhanced images; for the left renal artery, these values were 31 and 44 mm, respectively (P < .04).
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Figure 1a: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (3.44/1.17; flip angle, 25°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (3.8/1.55; flip angle, 65°) in a 68-year-old woman. Main renal arteries are displayed equally well on both images. An accessory right renal artery (arrow) is well depicted on a, whereas it was considered a lumbar artery on b.
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Figure 1b: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (3.44/1.17; flip angle, 25°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (3.8/1.55; flip angle, 65°) in a 68-year-old woman. Main renal arteries are displayed equally well on both images. An accessory right renal artery (arrow) is well depicted on a, whereas it was considered a lumbar artery on b.
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Figure 2a: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (4.6/1.8; flip angle, 30°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (4.6/1.8; flip angle, 30°) in a 61-year-old man. Maximum lengths and branching are better depicted on a, the contrast-enhanced image.
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Figure 2b: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (4.6/1.8; flip angle, 30°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (4.6/1.8; flip angle, 30°) in a 61-year-old man. Maximum lengths and branching are better depicted on a, the contrast-enhanced image.
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Signal-to-Noise Ratio, Contrast-to-Noise Ratio, and Image Quality
The mean signal-to-noise ratio of the renal arteries on the SSFP images amounted to 31 ± 12 and was significantly lower than that on the contrast-enhanced images (44 ± 11; P < .03). Likewise, contrast-to-noise ratios were significantly lower on the SSFP images as compared with those on the contrast-enhanced images (mean, 23 ± 13 vs 35 ± 9; P < .02).
Overall SSFP data sets had an image quality score of 3.1 ± 0.2. Image quality of the contrast-enhanced data sets, however, was significantly higher, with a mean score of 3.5 ± 0.4 (P < .05). Especially on SSFP images, overlay from the renal veins and the inferior vena cava often hampered the evaluation of the more distal parts of the renal arteries.
Stenosis
Two patients had relevant renal artery stenosis (>50%), and the stenoses were correctly identified with SSFP MR angiography (Fig 3). In two patients in whom the readers found a stenosis of less than 50% luminal diameter on the basis of contrast-enhanced MR angiographic image analysis, readout of SSFP data sets led to false-positive overgrading of vascular disease (as >50%) in all of these. One case of fibromuscular dysplasia as determined on the contrast-enhanced images was falsely judged as high-grade stenosis in one renal artery on the SSFP images. Overall sensitivity and specificity of SSFP MR angiography for detection of relevant luminal changes of the renal arteries were 0.92 (95% confidence interval: 0.60, 0.98) and 0.81 (95% confidence interval: 0.40, 0.95), respectively.
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Figure 3a: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (3.44/1.17; flip angle, 25°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (3.8/1.55; flip angle, 65°) in a 72-year-old man. Severe stenosis of left renal artery is displayed on both images.
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Figure 3b: Anteroposterior coronal maximum intensity projections from 3D MR angiography of abdominal aorta and renal arteries obtained with (a) fast low-angle shot sequence (3.44/1.17; flip angle, 25°) after injection of 0.2 mmol/kg gadodiamide and (b) SSFP sequence (3.8/1.55; flip angle, 65°) in a 72-year-old man. Severe stenosis of left renal artery is displayed on both images.
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DISCUSSION
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Three-dimensional SSFP is an extremely fast gradient-echo sequence that provides display of the abdominal vasculature with high conspicuity in combination with high spatial and temporal resolution. The SSFP sequence generates a complex contrast mixture with high blood pool signal intensity exclusively provided by rapid gradient systems. In our study, the SSFP sequence was shown to be a feasible alternative to a standard angiographic protocol for MR imaging of the renal arteries. Although the overall performance of SSFP MR angiography appears to be undeniably inferior to that of contrast-enhanced MR angiography for depiction of the renal arteries in terms of qualitative and quantitative features, we propose endorsement of SSFP MR angiography if contrast-enhanced MR angiography yields images that are not of diagnostic quality or if placement of a venous cannula for contrast material administration is not possible.
As do several other sequences, SSFP allows high-contrast visualization of the renal arteries without the need for intravenous administration of any contrast material. Both two-dimensional and 3D phase-contrast MR angiography of the renal arteries have been successfully used as the nonenhanced technique of choice for a rather long time (9–11). Areas of hemodynamically significant stenosis are detected by means of their associated flow turbulence, seen as signal void on 3D phase-contrast images, indicating a pressure decrease across the area of luminal narrowing. To accurately display turbulent flow, however, both the echo time and the velocity-encoded value have to be optimally adjusted, and this adjustment partly limits the clinical value of this sequence. With optimal parameters, phase-contrast MR angiography is the only MR imaging technique to precisely permit proper quantification of flow volumes and velocities for a comprehensive assessment of the hemodynamic significance of any renal artery stenoses identified (12). Lengthy acquisition times paired with the inherent propensity for artifacts, however, have driven the search for alternative sequences for morphologic display of the renal arteries. Time-of-flight MR angiographic techniques also rely on blood flow and have been widely used for a myriad of vascular territories, including the aorta, the renal arteries, and particularly the peripheral arterial tree (13–15). Both two-dimensional and 3D time-of-flight MR angiographic techniques, however, have been reported to be of only limited value for assessing the entire course of the renal arteries, often with only the origin reasonably displayed (16).
Against this background, the SSFP sequence is highly attractive, as it produces intrinsically high contrast between the blood pool and soft tissues. Moreover, the SSFP sequence is almost flow compensated in all three spatial orientations owing to symmetrically shaped gradient pulses (5). Katoh et al (8) recently introduced a cardiac-triggered navigator-gated 3D SSFP sequence with selective display of the renal arteries during free breathing. As compared with the herein portrayed approach, this SSFP variant has a relatively short acquisition window during late diastole and allows high temporal resolution and minimization of motion artifacts. Conversely, the examination time of the latter technique is much longer. Despite the potential use of the SSFP sequence for imaging the renal arteries and the wide use of SSFP techniques for display of the coronary arteries, SSFP MR angiography was not found to be reliable for accurate assessment of carotid artery disease because of severe artifacts (17).
Independence of flow combined with administration of contrast material almost void of any side effects make 3D contrast-enhanced MR angiography well suited for diagnosing renal vascular disease. The 3D gadolinium-enhanced MR angiographic technique produces a high-contrast arteriogram, but without the risks of ionizing radiation or those associated with administration of iodinated contrast material. Many studies have shown that the diagnostic accuracy for detection and grading renal artery stenosis, as well as for the assessment of other vascular disease, approaches that of conventional angiography (18). For the renovascular system, 3D contrast-enhanced MR angiography requires precise contrast medium bolus timing for data acquisition during the arterial passage of the bolus. Subsequent postprocessing is critical to provide reformations, maximum intensity projections, and optional volume-rendered images to display arteries in an angiographic format for optimal demonstration of any vascular lesions. The same is true for SSFP data sets.
Clearly, contrast-enhanced MR angiography of the renal arteries is not without its limitations (4). Hence, the search for noninvasive and objective imaging alternatives or technical refinements of current methods appears justified. The use of the 3D SSFP sequence without the need for intravenous contrast media and with the option to be repetitively performed is appealing. In patients who are suspected of having renal artery disease, the SSFP sequence has the potential to be a beneficial supplementary sequence. In addition, the SSFP sequence might be advantageous when contrast-enhanced MR angiography is hampered by venous overlay or severe motion artifacts or when peripheral venous access is impossible, as it was in one patient in our study population.
Our study has recognized limitations. First and foremost, contrast-enhanced MR angiography was defined as the standard of reference, which must be regarded as fairly controversial. Nevertheless, conventional angiography of the renal arteries is clinically deemed necessary only when contrast-enhanced MR angiography depicts severe stenosis and color-coded duplex ultrasonography corroborates this finding. Second, spatial resolution and signal strength of the SSFP sequence might be improved by employing navigator echoes for free-breathing data acquisition. Free breathing dramatically lengthens the acquisition time and particularly decreases the time effectiveness. Therefore, the breath-hold SSFP approach is attractive, as it adds a mere 20 seconds to the entire imaging protocol. Researchers in a recent study (8), however, demonstrated an excellent display of the renal arteries both in healthy volunteers and in patients by using a slab-selective inversion prepulse free-breathing 3D SSFP sequence with acquisition times between 3 and 4 minutes. Finally, the spatial resolution of the SSFP sequence, as described in this study, might be ameliorated with parallel imaging techniques; however, a large reduction of signal-to-noise ratio inherent in these new acquisition techniques such as simultaneous acquisition of spatial harmonics, or SMASH, (19) or sensitivity encoding, or SENSE (20), must be considered. In regard to the limitations of the statistics reported for our study, one has to keep in mind that evaluation of detection of disease was based on the renal artery as the unit of analysis. Our results could be biased if there were within-patient clustering, that is, if the results for arteries from the same patient might be more related than are the results for arteries from different patients.
In conclusion, breath-hold 3D SSFP MR angiography of the renal arteries without the need for intravenous contrast material administration appears to be feasible but of inferior quality to contrast-enhanced MR angiography. Thus, SSFP MR angiography is not very likely to displace contrast-enhanced MR angiography. Nevertheless, further analysis of the SSFP sequence for 3D MR angiography of the renal arteries is warranted and will include sequence modification, as well as comparison with conventional angiography to more precisely define the role of this promising new technique for screening patients who are suspected of having renovascular disease.
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ADVANCE IN KNOWLEDGE
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- Breath-hold three-dimensional steady-state free precession MR angiography permits display of the renal arteries, along with renal vascular disease.
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FOOTNOTES
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Abbreviations: SSFP = steady-state free precession • 3D = three-dimensional
Author contributions: Guarantors of integrity of entire study, C.U.H., V.M.R., M.L.M., L.G.N.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, C.U.H., D.M.W., V.M.R.; clinical studies, all authors; statistical analysis, C.U.H., D.M.W.; and manuscript editing, C.U.H., V.M.R., L.G.N.
Authors stated no financial relationship to disclose.
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ABSTRACT
INTRODUCTION
