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Comparison of Intraarterial and IV Gadolinium-Enhanced MR Angiography with Digital Subtraction Angiography for the Detection of Renal Artery Stenosis in Pigs

¹ Department of Radiology, Northwestern University Medical School, 676 N. St. Claire St., Ste. 800, Chicago, IL 60611.
² Department of Radiology, University of Wisconsin-Madison Medical School, 600 Highland Ave., Madison, WI 53792.
³ Department of Medical Physics, University of Wisconsin-Madison Medical School, Madison, WI 53792.

Received April 13, 2001; accepted after revision July 20, 2001.

 
R. A. Omary was supported in part by the 1999 Radiological Society of North America Bracco Diagnostics Scholar Award.

Address correspondence to R. A. Omary.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. Catheter-based intraarterial injections of gadolinium are useful during MR imaging—guided endovascular procedures to generate rapid vascular road maps. Using an animal model of renal artery stenosis, we tested the hypothesis that intraarterial gadolinium-enhanced MR angiography is as accurate as IV gadolinium-enhanced MR angiography and digital subtraction angiography (DSA). We also tested the hypothesis that intraarterial MR angiography uses less gadolinium than IV MR angiography.

MATERIALS AND METHODS. We induced bilateral renal artery stenosis in five pigs. All pigs underwent comparative imaging with DSA, IV MR angiography, and aortic catheter-directed intraarterial MR angiography. For IV and intraarterial MR angiography, we used the same three-dimensional acquisition. We assessed differences in quantitative stenosis measurements among DSA, IV MR angiography, and intraarterial MR angiography using the Wilcoxon's signed rank test.

RESULTS. Mean stenosis measurements (±SD) were as follows: DSA, 58% ± 12%; IV MR angiography, 63% ± 9.3%; and intraarterial MR angiography, 64% ± 11%. There were no statistically significant differences in accuracy between DSA and IV MR angiography (p = 0.06), DSA and intraarterial MR angiography (p = 0.16), or IV and intraarterial MR angiography (p = 0.70). Intraarterial MR angiography used a mean gadolinium dose of 5.6 mL, compared with 9 mL for IV MR angiography.

CONCLUSION. In swine, IV and intraarterial MR angiography have a similar accuracy for detecting renal artery stenosis. Intraarterial MR angiography uses smaller doses of injected gadolinium.

Introduction

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Direct catheter-based intraarterial injections of dilute gadolinium chelates are potentially useful during MR imaging—guided endovascular interventions to generate vascular road maps. The feasibility for intraarterial gadolinium-enhanced MR angiography has been shown in animal models [1,2,3,4] and in limited use in humans [5]. During MR imaging—guided endovascular procedures, the potential benefits of intraarterial MR angiography over standard IV gadolinium-enhanced MR angiography include decreased reliance on complex methods to synchronize contrast material arrival with data acquisition, reduced background tissue enhancement, limited contrast agent dispersion, and reduced contrast agent dose. The major disadvantage of intraarterial injection is its invasiveness. However, in the setting of a MR imaging—guided endovascular intervention, a catheter will already be in place, and the incremental risk for an intraarterial injection will be minimal.

The previously published feasibility studies for intraarterial MR angiography [1,2,3,4] did not examine the diagnostic accuracy of the technique. Determining the accuracy of intraarterial MR angiography is relevant for patients undergoing future MR imaging—guided renovascular interventions. If intraarterial MR angiography is proved accurate, it could be used to document treatment efficacy without requiring confirmatory radiography or subjecting the patient to iodinated contrast medium and ionizing radiation. The anticipated higher gadolinium doses used for IV injections could also be avoided, a benefit during endovascular procedures that requires multiple contrast agent injections. Renovascular interventions could potentially be enhanced through the use of MR imaging to measure renal function [6, 7]. Intraarterial MR angiography could also be used in selected instances as a problem-solving tool in other vascular distributions [5].

The objective of this study was to compare the diagnostic accuracy of intraarterial MR angiography, standard IV gadolinium-enhanced MR angiography, and digital subtraction angiography (DSA) for the detection of renal artery stenosis. Using a swine model of renal artery stenosis, our aim was to test the hypothesis that intraarterial MR angiography is as accurate as IV MR angiography and DSA. We also tested the hypothesis that intraarterial MR angiography uses less gadolinium contrast agent than conventional double-dose (0.2 mmol/kg gadolinium) IV MR angiography. The long-term goal of this research is to establish the accuracy of intraarterial MR angiography for detecting stenoses. This information is needed for endovascular interventions performed under MR imaging guidance.

Materials and Methods

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Animal Model
The Institutional Animal Care and Use Committee approved these experiments. We used Yorkshire cross swine (n = 5), weighing 20 kg, as the animal model for this study. Pigs were selected as the animal model because their size facilitates percutaneous vascular catheterization and because of the close resemblance of their kidneys to human anatomy and physiology [8, 9].

A model of renal artery stenosis was surgically induced using bilateral placement of reverse cable ties [10, 11]. Cable ties (Gardner Bender, Milwaukee, WI; bundle diameter, 1.5-20.6 mm) are available at most local hardware stores. The ties require gas sterilization with ethylene oxide before using in animals.

The surgical procedure involves preparing and draping the pig's abdomen using a sterile technique. After performing a midline abdominal incision, we used blunt and sharp dissection to expose the main renal arteries bilaterally. We then cinched one cable tie in reverse fashion around each renal artery. Our aim was to induce a moderate stenosis in the 50-80% range via extrinsic compression from the cable tie. Our motivation in this experiment was to induce clinically significant stenoses, while minimizing the risk for occlusion. The abdominal incision was closed and each pig was monitored until recovery from anesthesia.

Imaging
Seven to 9 days after cable tie placement, we performed comparative imaging with DSA and MR angiography. In all pigs, imaging was initially performed with DSA, followed immediately by MR angiography.

DSA was performed using a C-arm digital subtraction unit (Stenoscope; General Electric Medical Systems, Milwaukee, WI). In the animal laboratory, we obtained percutaneous access in the common femoral arteries using micropuncture kits. We inserted 5- or 6-French vascular sheaths. Through these sheaths, we advanced conventional 5-French angiographic pigtail catheters (Royal Flush; Cook, Bloomington, IN) into the abdominal aorta in juxtarenal positions. After vascular access was obtained, each pig received 2,000 U of heparin IV. Frontal and bilateral oblique angiography was performed using 10 mL of iohexol (Omnipaque 300; Nycomed, Princeton, NJ) injected for 2 sec.

We then transferred each pig to a 1.5-T dedicated cardiovascular MR scanner (CV/i; General Electric Medical Systems) for subsequent MR angiography using a spine coil. For intraarterial and IV gadolinium-enhanced MR angiography, we used the same breath-hold three-dimensional (3D) fast-spoiled gradient-echo sequence with elliptical centric phase encoding. Scan parameters for 3D MR angiography were as follows: TR/TE, 8.3/1.6; flip angle, 45°; field of view, 24 x 18 cm; acquisition matrix, 512 x 192; reconstruction matrix, 512 x 512; slice thickness, 2.6 mm with 16 partitions (acquired) and 1.3 mm with 32 partitions (reconstructed); and scan duration, 26 sec. We used gadodiamide (Omniscan; Nycomed) as the gadolinium chelate for all 3D contrast-enhanced MR angiograms. To reduce injection order bias, we randomized the order of intraarterial versus IV injections for each pig.

For 3D intraarterial MR angiography, we used a published injection protocol [2] on the basis of the following relationship (equation 1):

(1)

where [Gd]_inj is injected gadolinium concentration (%), Q_aorta is blood flow rate in aorta (mL/sec), Q_inj is injection rate of gadolinium agent (mL/sec), and [Gd]_arterial is desired arterial concentration of gadolinium (%).

To use this injection protocol, knowledge of the aortic blood flow rates was required. We measured the aortic blood flow rate in each pig using two-dimensional cine phase contrast [12] with the following scan parameters: TR/TE, 10.1/4.7; flip angle, 45°; field of view, 24 x 11 cm; slice thickness, 5 mm; acquisition matrix, 256 x 128; reconstruction matrix, 256 x 256; velocity encoding value, 300 cm/sec; and scan duration, 18 sec. Although estimates of swine aortic blood flow base could have been used, we wanted to improve accuracy by tailoring injections to the measured blood flow rates in each pig. To simplify the injection protocol, we selected Q_inj of 1 mL/sec and [Gd] _arterial of 1%. Substitution of these parameters into equation 1 yielded the gadolinium concentrations used for injection. These gadolinium solutions were created by diluting full-strength gadodiamide (0.5 mmol/mL) with normal saline.

Before performing 3D intraarterial MR angiography, we advanced the pigtail catheter approximately 5-7 cm into a suprarenal aortic position. This position was confirmed using MR imaging—guided passive tracking of catheters filled with dilute 4-6% gadolinium [13,14,15]. Our motivation for selecting this suprarenal aortic catheter position was to allow adequate mixing of injected contrast agent with inflowing blood before arrival in the renal arteries. Mixing would be expected to be less for the intraarterial gadolinium injections than for the intraarterial iodinated contrast agent injections because of the difference in injection rates. For 3D intraarterial MR angiography, based on the substitution of parameters into equation 1, we injected 30 mL of 15-22% of gadolinium concentration at an injection rate of 1 mL/sec. On the basis of equation 1, other combinations of injection rate and injected gadolinium concentration might work as well. To allow the contrast agent time to mix with inflowing blood, we initiated the injection 2 sec before the beginning of image acquisition.

For 3D IV MR angiography, we injected 0.2 mmol/kg of gadolinium at 1 mL/sec through a peripheral angiocatheter, followed by 15 mL normal saline flush at 1 mL/sec. To synchronize contrast material arrival with data acquisition, we used a 1-mL gadolinium dose timing sequence before this IV MR angiography injection.

Data Analysis
Comparative source MR angiograms and DSA images were transferred over a network to a personal computer (Macintosh; Apple Computer, Cupertino, CA). We used National Institutes of Health (NIH) Image 1.62 imaging processing software (NIH, Bethesda, MD) to perform manual quantitative measurements at the stenosis and at the proximal renal artery. The proximal uninvolved renal artery was used to represent normal vessel caliber. We calculated diameter percentage stenosis as 1 — (stenosis caliber / normal caliber) x 100%. For DSA, we used the width of the 5-French pigtail catheter to calibrate measurements. For MR angiography, intrinsic measurement capabilities obviated extrinsic calibration.

We used DSA as the reference standard for stenosis measurements. Raw stenosis measurements were graphed using a scatterplot. Differences in raw stenosis measurements among DSA, IV MR angiography, and intraarterial MR angiography were assessed using the Wilcoxon's signed rank test with alpha set at 0.05. After accounting for the effects of the dilution, we computed the total dose of full-strength gadolinium injected for intraarterial MR angiography. We assessed injected gadolinium dose differences between IV MR angiography and intraarterial MR angiography using descriptive statistical measures.

Results

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Using two-dimensional cine phase contrast-enhanced MR angiography, we found that aortic blood flow rates ranged between 14 and 21 mL/sec. Substitution of these blood flow rates into equation 1 was necessary to compute the proper dilution of gadolinium needed for intraarterial MR angiography injections. For intraarterial MR angiography, we injected gadolinium at concentrations of 15-22% at an injection rate of 1 mL/sec to produce an arterial gadolinium concentration of 1%. Intraarterial injections produced images comparable to those obtained with the conventional IV injections. Figure 1A,1B,1C,1D,1E shows sample images from the same pig using DSA, IV MR angiography, and intraarterial MR angiography. The intraarterial injections, unlike the IV injections, did not require a dose-timing bolus of 1 mL of gadolinium.

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Pig that weighed 20 kg 7 days after surgical induction of bilateral renal artery stenosis. Digital subtraction angiogram shows 70% right (R) renal artery stenosis and 53% left (L) renal artery stenosis.

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Pig that weighed 20 kg 7 days after surgical induction of bilateral renal artery stenosis. Contrast-enhanced MR angiogram obtained with IV administration of gadodiamide shows 68% right renal artery stenosis and 65% left renal artery stenosis. MR angiogram is coronal maximum intensity projection obtained from three-dimensional (3D) fast-spoiled gradient-echo acquisition.

View larger version (133K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —Pig that weighed 20 kg 7 days after surgical induction of bilateral renal artery stenosis. Contrast-enhanced MR angiogram obtained with intraarterial administration of gadodiamide shows 65% right renal artery stenosis and 75% left renal artery stenosis. MR angiogram is a coronal maximum intensity projection obtained from same 3D fast-spoiled gradient-echo acquisition.

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —Pig that weighed 20 kg 7 days after surgical induction of bilateral renal artery stenosis. Magnified source contrast-enhanced MR angiogram obtained with intraarterial administration of gadodiamide shows specific locations used for quantitative stenosis measurements of right renal artery. Small arrow depicts site of stenosis, and large arrow depicts proximal uninvolved normal renal artery segment.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1E. —Pig that weighed 20 kg 7 days after surgical induction of bilateral renal artery stenosis. Magnified source contrast-enhanced MR angiogram obtained with intraarterial administration of gadodiamide shows specific locations used for quantitative stenosis measurements of left renal artery. Small arrow depicts site of stenosis, and large arrow depicts proximal uninvolved normal renal artery segment.

In scatterplot format, Figure 2 depicts raw stenosis measurements for each imaging technique. As can be seen, IV and intraarterial MR angiography measurements tended to be similar, although there was a slightly greater variation with intraarterial MR angiography measurements. Both intraarterial MR angiography and IV MR angiography tended to slightly overcall the degree of stenosis when using DSA as the reference standard. Mean stenosis measurements (±SD) were as follows: DSA, 58% ± 12%; IV MR angiography, 63% ± 9.3%; and intraarterial MR angiography, 64% ± 11%. There was no statistical difference between IV and intraarterial MR angiography (p = 0.75), DSA and IV MR angiography (p = 0.06), or DSA and intraarterial MR angiography (p = 0.11). Table 1 lists lists raw stenosis measurements using the three imaging techniques.

View larger version (11K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —Scatterplot shows raw diameter of renal artery stenosis measurements obtained for IV and intraarterial MR angiogram using DSA as reference standard. Note that intraarterial MR angiogram () has slightly greater scatter than IV MR angiogram ([UNK]), indicating larger standard deviation for intraarterial stenosis measurements.

The 3D MR angiography sequence was identical between the IV and intraarterial MR angiograms, but the intraarterial MR angiograms used less contrast agent. The mean injected gadolinium dose (± standard error) for intraarterial MR angiography was 5.6 mL ± 0.52, whereas for IV MR angiography, it was 9.0 mL (±0.00). These results indicated a clinically important 38% reduction in contrast agent dose when using intraarterial injections.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
There was no difference in accuracy among DSA, IV MR angiography, and intraarterial MR angiography for the detection of renal artery stenosis in a swine model. IV and intraarterial MR angiography both slightly overestimated the degree of stenosis when using DSA as the reference standard, but these differences were not clinically or statistically significant. Intraarterial MR angiography required, on average, 38% less contrast agent than conventional double-dose (0.2 mmol/kg gadolinium) IV MR angiography.

Blood vessel depiction using intraarterial MR angiography depends on optimizing the competitive effects of gadolinium on MR imaging signal. Gadolinium causes signal gain through T1-shortening; however, at higher concentrations, T2^* signal loss predominates over this signal gain. Dilution of gadolinium balances the T1-shortening signal gain with the T2^* signal loss [1].

In static phantom experiments, gadolinium concentration of 2-6% produced optimal MR signal, depending on the selected imaging parameters [1]. Animal experiments in the aorta and iliac arterial system showed that an arterial gadolinium concentration of 3% was optimal [2]. Similar results were obtained in the theoretic derivations of Bos et al. [3] and phantom experiments of Serfaty et al. [4]. These studies suggest that using lower ranges of arterial gadolinium concentration maintains acceptable losses in signal and still provides excellent vascular images. Our rationale for using an arterial gadolinium concentration of 1% for intraarterial injections was to reduce the administered contrast agent dose. Previous studies suggested that signal-to-noise ratio could be maintained over a wide range of arterial gadolinium concentration [2,3,4]. We do not know the effect on accuracy of our intraarterial injections if we had aimed for a higher arterial gadolinium concentration, such as 2-3%. However, at these higher concentrations, the administered contrast agent dose would be higher by a corresponding factor of 2 or 3.

For instance, using an arterial gadolinium concentration of 3% would have required the injection of 20 mL of diluted full-strength gadolinium for our pig with aortic blood rate of 21 mL/sec (obtained from equation 1: (21+1)% x 3 x 30 mL injection volume). Because each pig weighed 20 kg, this gadolinium injection would be equivalent to 1 mL/kg or 0.5 mmol/kg, which is over the Food and Drug Administration—approved daily limit for gadolinium. Saving contrast agent is clinically important in the setting of MR imaging—guided endovascular interventions. These interventions require multiple contrast agent injections to define the vascular anatomy before engaging a vessel of interest, to confirm correct positioning of endoluminal devices during an intervention, and to verify technical success of the intervention. If contrast agent is injected without attention to dose, then multiple injections will exceed the Food and Drug Administration—mandated gadolinium dose limitations.

Inflowing blood affects the local delivery of contrast agent into the arteries by causing additional dilution of gadolinium. An injection protocol must account for this effect for satisfactory arterial depiction. To account for this effect, we used an injection protocol [2] that incorporates the injected [gadolinium], injection rate, and blood flow rate. Bos et al. [3] have proposed a similar injection protocol, but their method does not account for the effect of injection rate on overall arterial blood flow rates.

IV MR angiography has gained increasing acceptance as a minimally invasive alternative to DSA. IV MR angiography is highly accurate for detecting renal artery stenosis, with a sensitivity exceeding 95% and a specificity exceeding 90% [16, 17]. Although preliminary, our results in an animal model suggest there is little difference in the accuracy between IV and intraarterial MR angiography. Compared with conventional DSA, IV and intraarterial MR angiography suffer from reduced spatial and temporal resolution. This reduced spatial resolution limits detection of intrarenal branch stenoses.

Compared with DSA, MR angiography has the advantages of no radiation, fewer allergic reactions, lack of nephrotoxicity, and 3D anatomic depiction of a stenosis with a single contrast material injection. Eccentric stenoses (in the anteroposterior axis rather than the craniocaudal axis) considerably reduce the accuracy of conventional DSA. Eccentric stenoses are underestimated with DSA, unless projections are perfectly tangential to the narrowest span of stenosis [18,19,20]. For example, more than one third of carotid artery stenoses are underestimated using standard DSA [21]. Although rotational angiography [21] can overcome the limitations of depicting eccentric stenoses with a single injection, this technology is still not widely available and does not eliminate the risks for iodinated contrast agent and ionizing radiation exposure.

This study has a number of important limitations. First, it was performed in an animal model of main renal artery stenosis. These results cannot necessarily be generalized to human atherosclerotic or fibromuscular disease. Second, our sample size was small. Comparisons in a much larger sample size and in many other vascular distributions will be required to know the true accuracy of intraarterial injections. Although we detected no statistical differences between the paired comparisons, a larger sample size might also have had the power to detect these differences if they existed. Third, in each animal, we performed sequential IV and intraarterial gadolinium injections during the same imaging session. Injecting on different days would have reduced the effects of residual contrast material on image quality and contrast [22]. We attempted to minimize this effect, however, by randomizing the order of IV versus intraarterial injections. Fourth, the Food and Drug Administration has not approved intraarterial injections of gadolinium. These injections represent an off-label route of administration of an approved contrast agent. Although the safety of intraarterial gadolinium injections for MR angiography has not been documented, intraarterial injections have been used safely for diagnostic angiography [23, 24] and endovascular interventions [25, 26] when performed under radiographic guidance.

In conclusion, we confirmed the accuracy of intraarterial MR angiography for detecting renal artery stenosis in a lower number of animals. This method used less contrast agent dose than conventional double-dose IV gadolinium injections. During MR imaging—guided endovascular procedures, interventional radiologists will readily recognize the similarities between this technique and conventional DSA. MR imaging can be used in place of radiographic guidance, and gadolinium injections can be used in place of iodinated contrast agents. The accuracy of intraarterial MR angiography for detecting stenoses in other vascular distributions remains to be defined.

Acknowledgments
 
We thank Alan Rappe for his expert animal care and Toye Spencer for her assistance with preparation of the manuscript.

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