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Vascular and Interventional Radiology |
1 From the Department of Radiology (F.D.C., M.V., A.V., M.S., E.A., P.S., A.D.M.), the Epidemiology Unit (M.P.G.), and the Department of Nephrology (R.Q., G.B.), Scientific Institute S Raffaele, University Hospital, Olgettina 60, 20132 Milan, Italy; and the Department of Radiology, Multimedica Hospital, Milan, Italy (S.S.). From the 1998 RSNA scientific assembly. Received February 4, 1999; revision requested April 1; revision received May 10; accepted July 2. Address reprint requests to F.D.C. (e-mail: francesco.decobelli@hsr.it).
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Forty-five patients with clinical suspicion of renovascular disease were prospectively examined with intra- and extrarenal color Doppler US and breath-hold, gadolinium-enhanced MR angiography. Digital subtraction arteriography (DSA) was the standard of reference in all patients for the number of renal arteries and degree of stenosis.
RESULTS: DSA depicted 103 arteries and 52 stenoses. Color Doppler US was nondiagnostic in two examinations. Significantly more of 13 accessory renal arteries were detected with MR angiography (n = 12) than with color Doppler US (n = 3; P < .05). For assessing all stenoses, the sensitivity and accuracy were 94% and 91%, respectively, for MR angiography and 71% and 76%, respectively, for US (P < .05). The sensitivity was higher for MR angiography (100%) than for US (79%; P < .05) in diagnosing stenoses with at least 50% narrowing. The specificity, accuracy, and negative predictive value in diagnosing stenoses of at least 50% narrowing were 93%, 95%, and 100% for MR angiography and 93%, 89%, and 90% for US.
CONCLUSION: Breath-hold, gadolinium-enhanced MR angiography is superior to color Doppler US in accessory renal artery detection. Although the specificity of MR angiography is similar to that of color Doppler US, MR angiography has a better sensitivity and negative predictive value in depicting renal arterial stenoses.
Index terms: Magnetic resonance (MR), comparative studies, 961.12942 • Renal arteries, MR, 961.129412, 961.129416, 961.12942, 961.12943 • Renal arteries, stenosis or obstruction, 961.721 • Renal arteries, US, 961.12983 • Ultrasound (US), comparative studies, 961.12983
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Since 1984, when Doppler US was introduced as a noninvasive screening technique for renal arterial stenosis (9,10), contrasting results of several studies (8–14) have been reported. Whether the main or segmental renal arteries should be examined with color Doppler US is still controversial. It has been suggested (14,33) that the combination of intra- and extrarenal scanning allows the best results with regard to the diagnosis of significant renal arterial stenosis.
MR angiography is emerging as an alternative, noninvasive way to image the renal arteries. Although early studies performed with a phase-contrast technique or a time-of-flight sequence without contrast medium (17–25) yielded good accuracies, gadolinium-enhanced MR angiography has been introduced (26–32) for imaging of the renal arteries. By using a short repetition time and a short echo time, this new technique may be used with breath holding, which allows improved spatial resolution and image quality and shortening of the imaging time.
In clinical studies (8–14,26–32), both color Doppler US and gadolinium-enhanced MR angiography for the detection of renal arterial stenosis have had good results. To our knowledge, there has not been a prospective comparison between color Doppler US and gadolinium-enhanced MR angiography in the diagnosis of renal arterial stenosis in the same patients. We found only an article in which nonenhanced, three-dimensional, time-of-flight MR angiography and color Doppler US have been compared in the assessment of native renal arterial stenosis (34) and an article in which three-dimensional, phase-contrast MR angiography and color Doppler US have been compared in the assessment of stenosis in transplanted renal arteries (35).
The aim of our prospective study was to compare breath-hold, three-dimensional, gadolinium-enhanced MR angiography and color Doppler US in the detection of renal arterial stenosis in a large series of patients.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Forty-four of 45 patients had hypertension. The mean baseline systolic blood pressure ± SEM was 156 mm Hg ± 23, and the mean diastolic blood pressure was 90 mm Hg ± 13. The mean serum creatinine levels were 1.60 mg/dL (SD, 1.65; SEM, 0.26; range, 0.40–8.49 mg/dL [mean, 141 µmol/L; SD, 146; SEM, 23; range, 35–751 µmol/L]). Fifteen patients had renal impairment (mean serum creatinine levels, 2.98 mg/dL; SD, 2.17; SEM, 0.58 [mean, 263 µmol/L; SD, 192; SEM, 51]). Seventeen of the 45 patients also were enrolled in another study, the findings of which already have been published (30).
All patients were included in the study after they had given informed consent. The study was approved by our institutional review board.
MR Imaging Technique
Images were obtained with a 1.5-T superconducting magnet (Signa Horizon; GE Medical Systems, Milwaukee, Wis) by using an enhanced gradient system, with a maximum gradient strength of 23 mT/m and a maximum gradient slew rate of 120 T/m/sec. Operating system software version 5.5 or 5.6 was used. In all cases, the examination was performed with a phased-array multicoil (Torso-Array-Coil, four channel system; GE Medical Systems).
In all patients, transverse or coronal, breath-hold, T1-weighted, fast, multiplanar spoiled gradient-echo imaging (repetition time msec/echo time msec, 125/4.2; 90° flip angle; 10-mm section thickness; data matrix, 256 x 192; 40-cm field of view) was used to localize the aorta and the renal artery ostia and to evaluate the volume and the morphology of the kidneys. The image acquisition time was 20 seconds for each plane.
After fast, multiplanar spoiled gradient-echo localizing imaging, in all patients, multiple, sequential, sagittal, single-level, two-dimensional, fast, spoiled gradient-echo imaging was performed to obtain images in the abdominal aorta every 1.2 seconds for 60 seconds during the injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) with a power injector (Spectris MR Injector; MedRad, Pittsburgh, Pa; flow rate, 2 mL/sec) and with the following parameters: 7.9/1.3, 20° flip angle, 62.5-kHz bandwidth, 10-mm section thickness, data matrix of 256 x 160, 32–36 cm field of view, and one signal acquired. The image acquisition and the injection of a low (2-mL) dose of gadopentetate dimeglumine through an 18-gauge catheter placed in an antecubital vein were started at the same time and were followed by the normal saline flush (20 mL of saline at 2 mL/sec). The delay between the injection and the abdominal enhancement was observed and measured.
For the first 32 patients, MR angiography was performed with a breath-hold, coronal, three-dimensional, fast, spoiled gradient-echo sequence before, during, and after gadopentetate dimeglumine injection. Imaging parameters included 7.0/1.4, a 40° flip angle, 32-kHz bandwidth, 2-mm section thickness, no gap, 28 partitions, data matrix of 256 x 160–192, 40–48-cm 
rectangular field of view, and one signal acquired. The imaging time was 21–23 seconds. The nonenhanced images were used as scout views to ensure the proper placement of the imaging volume. Gadopentetate dimeglumine was injected intravenously through an 18-gauge catheter placed in an antecubital vein. The contrast material was administered by using a power injector at a standard dose (0.1 mmol per kilogram of body weight) at 2 mL/sec; this injection was immediately followed by injection of 20 mL of normal saline at 2 mL/sec to complete delivery of the entire dose of contrast material and to flush the vein.
The circulation time from the injection site to the renal arteries was calculated in an attempt to achieve peak contrast material enhancement during the acquisition of the central third orders of k space. To calculate the delay time, we used the following equation: td = tc - 
ta, where td is the delay time, tc is the estimated circulation time, and ta is the acquisition time. This injection technique was employed to produce a uniform arterial concentration during the central k-space acquisition and to reduce venous superimposition.
For the remaining 13 patients, gadolinium-enhanced MR angiography was performed with a breath-hold, coronal, enhanced fast gradient-echo, three-dimensional sequence. Imaging parameters included 5.4/1.4/30 (repetition time msec/echo time msec/inversion time msec), 30° flip angle, 62-kHz bandwidth, 2-mm section thickness (double section interpolation on the z axis), 40 partitions, 80 reconstructions (slab thickness, 8 cm), a data matrix of 256–320 x 192, a 40–48-cm 
rectangular field of view, and 0.5 signal acquired. The imaging time was 24 seconds. Spectral fat saturation was also used. With this sequence, the low-frequency k-space lines are acquired at the beginning of the acquisition; the delay time formula is the following: td = tc.
The three-dimensional, gadolinium-enhanced images were reconstructed by using a maximum intensity projection technique after regions of interest that included only the aorta and renal arteries were drawn. A maximum intensity projection algorithm was used to provide an angiographic projection from any desired viewing angle around the long axis of the body. Multiplanar reconstruction and subvolume maximum intensity projection images also were obtained by reviewing the source images to identify the minimum number of images required to demonstrate the renal arteries. In some cases, reformation also was obtained in curved planes. A radiologist (F.D.C.) blinded to the results of angiography selected the regions of interest and reconstructed the maximum intensity projection images. The postprocessing time for each patient was approximately 20 minutes.
MR Image Analysis
Two of the authors (F.D.C., A.V.) who were not aware of the angiographic findings graded the vessels on the MR angiograms by consensus. The two readers had to reach a consensus on the following parameters: (a) number of renal arteries visualized; (b) presence of renal arterial stenosis; and (c) degree of the stenosis. According to findings in previous articles (27,28,30–32), mild stenosis was considered to be a reduction of the arterial caliber of less than 50%; severe stenosis was defined as significant (50%–99%) reduction of the diameter of the artery, with normal arterial enhancement distal to the stenosis. Vessel occlusion was total absence of enhancement.
Color Doppler US
All examinations were performed by a vascular radiologist (M.V.) with a 3.5-MHz curvilinear-array transducer by using an echo Doppler unit (HDI 3000, Advanced Technology Laboratories, Bothell, Wash; or Ansaldo AU 590, Esaote, Genoa, Italy) and were started with the patient in the supine position to visualize the origin and proximal course of the main renal arteries and accessory renal arteries (extrarenal arteries). Both color Doppler US and power Doppler US (especially in obese patients) were employed to detect and correctly evaluate the morphology of the entire course of the renal arteries.
Epigastric transverse scans allowed us to identify the main renal arteries, which originate laterally (anterolateral, right artery; posterolateral, left artery) in the abdominal aorta at about 1 cm under the anterior emergence of the superior mesenteric artery and have a proximal course just posterior to the left renal vein in normal conditions.
Color imaging can show the site of stenosis as signs of turbulence in the systolic phase (as yellow and green with our machine setting).
In the first part of the examination, Doppler waveforms were recorded for the entire courses of the renal arteries, with the color Doppler US unit set for high flow velocities (pulse repetition frequency, 4,000–6,000 Hz), to evaluate the peak systolic velocities: The angle correction was essential to obtain the correct measurements.
A significant arterial stenosis produces an increased peak systolic velocity at or immediately distal to the area of narrowing: We have considered peak systolic velocities of 100–200 cm/sec as suggestive of mild stenosis (<50% narrowing) and those higher than 200 cm/sec as suggestive of severe stenosis (50%–99% narrowing).
The second part of the examination, which was for intrarenal vessel evaluation, was performed with the patient in the lateral decubitus position, with the same 3.5-MHz curvilinear probe, and with the color Doppler US unit set for medium flow velocities (pulse repetition frequency, 1,500–2,500 Hz). For a more correct evaluation, we recorded the blood flow in the intrarenal vessels in the superior third, medium third, and inferior third of each kidney: An acceleration time greater than 0.07 seconds with a tardus-parvus waveform was considered diagnostic of severe stenosis of the extrarenal arteries.
Digital Subtraction Arteriography
All patients underwent digital subtraction arteriography (DSA) within 2 weeks of MR angiography and color Doppler US. DSA was considered the standard of reference. DSA was performed with a 5-F pigtail catheter, with the catheter tip positioned through the right or left femoral artery to be just proximal to the renal arteries. Nonionic contrast material (iopamidol [Iopamiro; Bracco, Milan, Italy]; 300 mg of iodine per milliliter) was injected at 20 mL/sec for 2 seconds, and images were obtained in the anteroposterior, left anterior oblique, and right anterior oblique projections. Selective renal catheterization was performed in 37 of the 45 patients.
In all patients, the DSA images were read and graded by one expert vascular interventional radiologist (M.S.) who was unaware of the MR angiographic results. The number of accessory renal arteries was determined, and the presence of stenosis in the renal arteries was noted and visually graded according to the same grading scale used at MR imaging and at color Doppler US.
Pressures also were measured, when indicated, to judge the significance and degree of stenosis.
Statistical Analysis
MR angiography and color Doppler US were prospectively, separately, and blindly evaluated prior to the performance of DSA.
The sensitivity, specificity, accuracy, positive predictive value, and negative predictive value for the detection of any degree of stenosis and for the detection of significant (>50%-narrowing) stenosis were calculated independently for both techniques. The sensitivity for detecting stenosis or occlusion was calculated as the number of true-positive findings at MR angiography or at color Doppler US divided by the number of positive findings at DSA. The specificity was calculated as the number of true-negative findings at MR angiography or at color Doppler US divided by the number of negative findings at DSA. Exact two-sided confidence intervals for binomial proportions at the 95% level for sensitivity, specificity, accuracy, negative predictive value, and positive predictive value were calculated.
The McNemar test was used to evaluate the difference in the depiction of the renal arteries and the arterial stenoses between MR angiography and color Doppler US.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In two of the 45 patients (4%), color Doppler US scans were considered to be technically inadequate, because no accurate depiction could be attained and no Doppler signal could be detected. In these two patients, one artery had mild (<50%-narrowing) stenosis and three had significant (
50%-narrowing) stenosis at angiography.
In all patients, MR angiography was considered technically adequate, and all 90 main renal arteries were visualized.
Of the 13 accessory renal arteries seen at DSA, only three were depicted with color Doppler US, whereas 12 were depicted with three-dimensional, gadolinium-enhanced MR angiography. One accessory artery was missed with MR angiography because of its small caliber. The number of accessory renal arteries depicted was significantly higher with three-dimensional, gadolinium-enhanced MR angiography than with color Doppler US (P = .016). Neither modality showed false-positive accessory renal arteries. The size of the vessels not depicted with color Doppler US was 1–4 mm (mean, 2.6 mm).
In summary, depiction of 89 of 103 arteries (86%) was possible with color Doppler US, and depiction of 102 of 103 arteries (99%) was possible with MR angiography.
Assessment of Stenosis
DSA showed stenosis in 52 of 103 arteries. Of the 52 renal arterial stenoses, DSA revealed 20 mild (<50%-narrowing) stenoses, 30 severe (50%-narrowing) stenoses (Figs 1, 2), and two occlusions.
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Three-dimensional, gadolinium-enhanced MR angiographic findings in the 102 visualized arteries were true-negative in 44 arteries, false-negative in three, true-positive in 49 (Figs 1, 2, 4), and false-positive in six. These results yielded a sensitivity of 94% (95% CI: 84%, 99%), a specificity of 88% (95% CI: 76%, 96%), a positive predictive value of 89% (95% CI: 78%, 96%), a negative predictive value of 94% (95% CI: 83%, 99%), and an accuracy of 91% (95% CI: 84%, 96%) (Table).
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A statistically significant difference between the two modalities (P < .05) in the assessment of all stenoses was found (sensitivity, P < .001; accuracy, P = .001).
Assessment of Significant Stenosis
From a clinical point of view, we can consider together normal vessels and vessels with mild (<50%-narrowing) stenosis. In our series, DSA revealed 32 stenoses with 50%–100% narrowing (Fig 2).
When the ability to use color Doppler US to distinguish renal arteries with stenosis of at least 50% from normal vessels or vessels with stenosis of less than 50% is considered, of the 89 renal arteries depicted with color Doppler US, 57 had true-negative results, four had false-positive results, 22 had true-positive results, and six had false-negative results (Fig 4). These results yielded a sensitivity of 79% (95% CI: 59%, 92%), a specificity of 93% (95% CI: 84%, 98%), a positive predictive value of 85% (95% CI: 65%, 96%), a negative predictive value of 90% (95% CI: 80%, 96%), and an overall accuracy of 89% (95% CI: 78%, 93%) (Table).
The severe stenosis in one artery was graded as a mild stenosis at US, and five severe stenoses were considered as normal. One normal artery and three mild stenoses were incorrectly graded as severe stenoses.
For the detection of significant stenosis, three-dimensional, gadolinium-enhanced MR angiographic findings were true-negative in 65 arteries, true-positive in 32 arteries, and false-positive in five arteries (Fig 3). There were no false-negative findings. These results yielded a sensitivity of 100% (95% CI: 89%, 100%), a specificity of 93% (95% CI: 84%, 98%), a positive predictive value of 86% (95% CI: 71%, 96%), and a negative predictive value of 100% (95% CI: 95%, 100%). The accuracy was 95% (95% CI: 89%, 98%) (Table). Two normal arteries were classified as severe stenoses, and three mild stenoses were classified as severe stenoses.
The MR angiographic sensitivity was significantly higher than the color Doppler US sensitivity (P = .02). No statistically significant difference between MR angiographic and color Doppler US accuracies (P = .15) was found. The two occluded arteries were correctly depicted with both techniques.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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As reported in previous articles (8–14), one major drawback of color Doppler US is that in a certain percentage of patients the examinations are inadequate because of obesity or the presence of bowel gas; in previous articles (8–14,37,38), the percentage of unsuccessful examinations ranged from 0% to 42%. In those studies, in which both intra- and extrarenal evaluations were performed, this percentage was lower than the percentage in studies in which only the main renal artery was scanned. In our study, we examined both the main renal artery and the segmental vessels. Intrarenal parameters were not sampled in two patients (4%) because of obesity in one case and the presence of bowel gas in the other.
All patients in the present study were successfully examined with MR angiography, and in each patient the MR angiogram was adequate for analysis. MR imaging is contraindicated in the occasional patient with a metallic implant (eg, pacemaker). Patients also must be cooperative. Breath holding is necessary during the acquisition of the images, and some patients may have difficulty with the examination. In our experience, almost all patients have been able to hold their breath for 24 seconds. In a few patients, we have noted minor degradation of the entire volume of image data, but individual sections have not been affected out of proportion to the rest of the data, probably because these motion artifacts occurred not during acquisition of central k-space lines but during acquisition of peripheral k-space data.
Color Doppler US is useful for screening for suspected renal arterial stenosis (8–14). Investigators in recent studies (8,14) have reported good sensitivity in the detection of renovascular disease by using both intra- and extrarenal Doppler US evaluations. However, this technique still has some limitations in depicting accessory renal arteries.
Our results confirm that one drawback of color Doppler US is the poor ability to depict accessory renal vessels. In our series, 10 of 13 polar (accessory) arteries were not depicted with color Doppler US. In all cases, the origin of the accessory arteries was far from the main artery and/or the arteries were of small caliber. Renovascular hypertension can be caused by stenosis of a polar artery.
As reported in previous articles (30–32), an important advantage of three-dimensional, dynamic, gadolinium-enhanced MR angiography is its ability to depict accessory renal vessels, mainly because the whole abdominal aorta can be imaged. In our series, all but one accessory artery were prospectively depicted with this modality. The nondepicted artery had a small caliber, and only at a retrospective reconstruction could this artery be depicted. As previously reported (28,30), a maximum intensity projection view of the entire acquired volume can be insufficient for correct accessory renal artery detection: Small vessels may be obscured by the superimposition of other vessels (ie, superior mesenteric arterial branches); thus, artery detection requires an accurate evaluation of source images, reformatted images, and multiplanar reconstruction images.
In the assessment of all stenoses, the sensitivity and negative predictive value of color Doppler US were 71% and 73%, respectively. These low values were due to the high number of false-negative findings, which resulted from the difficulty of using color Doppler US in the evaluation of mild stenoses. In fact, usually in mild stenoses, the intrarenal Doppler US analysis is normal, and the stenosis can be assessed only with the extrarenal morphologic color power imaging evaluation and extrarenal Doppler US waveform analysis.
Difficulties in the accurate identification of the entire course of the renal artery, problems in angle-corrected velocity calculations, and the resultant high percentage of false-negative results are important limiting factors of color Doppler US. So, as already pointed out by Middleton (39), if a stenotic artery is seen only in segments, a normal Doppler US waveform may be obtained from a nonstenotic segment, which results in a technically successful, but false-negative, examination.
An important advantage of MR angiography over color Doppler US and other screening tests is that it enables detection of hemodynamically insignificant stenosis. This is important because of the progressive course of renovascular disease, which may lead to chronic renal insufficiency. In fact, in our series, we had only three false-negative MR angiographic findings for mild stenoses.
With regard to the detection of severe renal arterial stenosis, color Doppler US results were better: The sensitivity was 79%, and the negative predictive value was 90%. The results of color Doppler US were better probably because hemodynamically significant stenosis is reflected by an abnormal poststenotic Doppler waveform in the more distal intrarenal arteries (11–14); therefore, the association between intra- and extrarenal color Doppler evaluations enables easier detection of significant stenosis than of insignificant stenosis.
However, in depicting severe stenosis, the sensitivity of MR angiography (100%) was significantly higher than the sensitivity of color Doppler US. In fact, with fast MR angiography, all 32 stenoses with at least 50% narrowing were correctly graded. With these results, we can assume that if the gadolinium-enhanced angiographic study findings are negative, a significant stenosis can reliably be excluded.
With both color Doppler US and MR angiography, a correct differentiation between severe stenoses and occluded arteries was always possible. This could have a great clinical effect because in patients with a severe stenosis DSA and endovascular treatment are suitable, whereas in patients with occluded arteries they are not. So, with both techniques, we can keep patients with an occluded renal artery from undergoing an invasive examination.
We found similar specificities for both techniques: 82% for color Doppler US and 88% for MR angiography. In the evaluation of significant stenoses, the specificity was 93% for both screening examinations. In fact, we had eight false-positive color Doppler US findings of stenosis and four false-positive US findings of significant stenoses. We had six false-positive MR angiographic findings of stenosis and five false-positive MR angiographic findings of significant stenosis.
We believe that with MR angiography, some degree of overestimation is to be expected. In fact, breath-hold, dynamic, three-dimensional, gadolinium-enhanced MR angiography is not completely independent of artifacts due to blood flow. Also, with this technique, even if the signal loss is less than that for conventional time-of-flight and phase-contrast techniques, the signal loss from turbulent flow at the origin of a renal artery can be confused with luminal narrowing. Furthermore, signal loss from turbulent flow distal to a stenosis will tend to increase the apparent degree of stenosis.
In conclusion, our results suggest that color Doppler US has some limitations. Even if in our series only 4% of all the patients were considered to have undergone nondiagnostic examinations, the accessory vessel detection was low. Moreover, the sensitivity and the negative predictive value, although acceptable, were significantly lower than those for MR angiography. Improved US technology, such as second-harmonic imaging, or the use of US contrast agents may have a role to play in the future. MR angiography is more reproducible and has better accuracy in accessory vessel detection and in screening for renal arterial stenosis. MR angiography and color Doppler US have similar specificities in the diagnosis of renal arterial stenosis and are accurate in the differentiation between high-grade stenosis and occlusion.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, F.D.C.; study concepts, F.D.C., M.V., R.Q.; study design, F.D.C.; definition of intellectual content, F.D.C., A.D.M., G.B.; literature research, F.D.C., E.A.; clinical studies, F.D.C., M.V., A.V., P.S., M.S., E.A.; data acquisition, F.D.C.; data analysis, F.D.C., R.Q.; statistical analysis, F.D.C., M.P.G., R.Q.; manuscript preparation and editing, F.D.C., M.V.; manuscript review, F.D.C., A.V., P.S., S.S., A.D.M.
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