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British Journal of Radiology 74 (2001),495-502 © 2001 The British Institute of Radiology

Full paper

Renal arteriography using gadolinium enhanced 3D MR angiography—clinical experience with the technique, its limitations and pitfalls

T K Mittal, MD, FRCR 1 C Evans, FRCR 2 T Perkins, BSc 2 and A M Wood, MRCP, FRCR 2

1Department of Radiology, Leeds General Infirmary, Great George Street, Leeds LS1 3EX, UK and 2Department of Clinical Radiology, University Hospital of Wales, Heath Park, Cardiff CF4 4XW, UK

Correspondence: Dr T K Mittal, Cardiac MRI Unit, B Floor, Clarendon Wing, Leeds General Infirmary, Great George Street, Leeds LS1 3EX, UK


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
Gadolinium enhanced 3D MR angiography (MRA) is becoming a widely accepted technique for imaging the vascular system. We set out to evaluate its accuracy and reliability in visualization of renal arteries in the clinical setting. Gadolinium enhanced MRA was performed in 15 potential live renal donors and 26 patients suspected of having renal artery stenosis who were referred for digital subtraction angiography (DSA). MRA was performed on a 1.5 T MR scanner in a single breath hold. Images from each study were prospectively analysed for demonstration of number of main and accessory renal arteries and degree of renal artery stenosis in a double blind fashion. All the main and accessory arteries were visualized on MRA in the renal donor group, but in one case a branch was not identified owing to breathing artefact. In one case, an extrarenal vascular anomaly was not demonstrated on MRA. In the renal artery stenosis group, sensitivity, specificity and negative predictive values of 96%, 93% and 96% were obtained for clinically significant stenosis (>50%). Gadolinium enhanced MRA proved to be a useful technique in demonstration of renal arterial anatomy and grading of renal artery stenosis. However, we encountered some pitfalls and limitations of the technique during the process. It is important to be aware of these before accepting it as the sole technique in clinical practice.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Gadolinium enhanced magnetic resonance angiography (MRA) is rapidly becoming the technique of choice for imaging the vascular system, including the renal arteries. This technique, which was first described by Prince et al in 1993 [1], has several advantages over conventional digital subtraction angiography (DSA). In addition to being non-invasive and not using ionizing radiation, gadolinium contrast media have minimal nephrotoxic effects, which is particularly important in patients with concurrent renal insufficiency [2, 3]. MRA provides true anatomical images that are similar to conventional arteriograms and also has the advantage of multiplanar reformatting. High performance MR gradient systems now allow acquisition of three-dimensional (3D) volumes in a single breath hold of less than 30 s to image renal arteries with sufficient spatial resolution [4–9].

Imaging of the renal arteries is important in theevaluation of potential renal donors [10] and in patients suspected of having renal artery stenosis, for which conventional or digital subtraction angiography is the gold standard imaging technique. Owing to the invasive nature and use of ionizing radiation in angiography, there has been a continuous search for a non-invasive technique to detect clinically significant renal artery stenosis. Other techniques such as Doppler ultrasound and captopril scintigraphy are helpful, but have limitations [11]. Contrast enhanced spiral CT can be used to perform renal angiography and has been reported as an accurate non-invasive technique to detect renal artery stenosis [12]. However, it too suffers from disadvantages of requiring a large load of iodinated contrast medium and a considerable radiation dose [13].

MRA with gadolinium enhancement is now a realistic option with the development of fast 3D gradient echo sequences. The use of T1-shortening effect by intravenous injection of paramagnetic contrast material significantly improves vessel imaging by eliminating signal loss from saturation effects, minimizing dependence of the inflow phenomenon and possibly decreasing intravoxel dephasing effects [1, 14, 15].

In this study we review our experience concerning the accuracy and reliability of gadolinium enhanced MRA in the evaluation of renal arteries, with particular emphasis on the limitations and pitfalls associated with the technique.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Potential live renal donors and patients suspected of having renal artery stenosis who were referred for DSA from April 1998 to July 1999 were included in this study. MRA was performed before DSA in all except one case and both studies were performed within a week of each other, most outpatients having both procedures performed on the same day. The purpose of the examination was explained to all subjects and informed consent was obtained.

There were a total of 16 donors, ranging in age from 30 to 55 years, 10 being females and 6 males. MRA could not be performed in one donor because of claustrophobia. This case was thus excluded from further evaluation in the study.

A total of 26 patients suspected of having renal artery stenosis underwent both MRA and DSA during this period. The decision to image the renal arteries was made by the referring physicians on clinical grounds, the indications being hypertension in 19, renal failure in 6 and flash left ventricular failure in 1. The patients were 34–85 years old and consisted of 14 women and 12 men.

MR angiography
All MRI was performed on a 1.5 T Signa scanner (General Electric Medical Systems, Milwaukee, WI) with a torso phased-array coil. Each study comprised the following protocol:

  1. Upper limb venous access (18 or 20 G) in a suitable arm vein, connected to a long line flushed with saline.
  2. Explanation of breath holding to the patient.
  3. Spoiled gradient echo (SPGR) localizer sequence in coronal plane (40 s).
  4. Transverse T2 weighted spin echo (T2W FSE) sequence (TE=85; TR=3000–4000; slice thickness=5 mm with gap of 1 mm; matrix=512 x 256; NEX=3) through the kidneys and the adrenal glands. For the next two sequences, the patient's arms were placed over the head to prevent aliasing.
  5. T1 weighted (T1W) sagittal multiphase gradient echo sequence through the abdominal aorta after a test dose of 2 ml of gadolinium followed by a20 ml saline flush. With this sequence a 15 mm slice was obtained each second through the same sagittal plane for 40 s. A time–signal intensity curve was generated to determine the time taken for the contrast medium to arrive in the aorta (peak enhancement) from the site of injection (contrast travel time).
  6. Gadolinium enhanced 3D MRA using a 3Denhanced fast gradient echo (3defgre) sequence, with the following parameters: TR=6 ms; TE=1.3 ms; flip angle=15°; bandwidth=31.25; slice thickness=2–3 mm; matrix=256 x 160; NEX=0.5–1; field of view=32 cm (range 28–40 cm) and sequential k-space mapping. This was planned using the axial T2W images, making sure to include anteriorly the proximal coeliac axis, superior mesenteric arteries and distal aorta before the bifurcation, and at least the renal hilum posteriorly. Imaging time was kept below 25 s by adjusting the slice thickness, number of locations and number of excitations. The exact acquisition time, obtained after adjusting the above parameters, and the contrast travel time were used to calculate the delay time between injection of contrast medium and starting the image acquisition by the following formula:Go



Initially this sequence was performed without contrast medium to check for any artefacts. If adequate images were obtained, 28 ml of gadolinium chelate (approximately 0.2 mmol per kg body weight gadopentate dimeglumine (Magnevist, Schering) or gadodiamide (Omniscan, Nycomed)) was rapidly injected by hand followed by the 3defgre sequence with a single breath hold after the calculated delay time. Another sequence was performed immediately after the first to obtain a venous phase image.

Digital subtraction angiography
Intraarterial DSA was performed on a GE Advantx TC digital imaging unit (GE Medical Systems, Milwaukee, WI). A 4 F catheter system and non-ionic contrast medium (Omnipaque 300, Nycomed) were used in all cases. A flush aortogram was performed in all of the prospective renal donors followed by selective catheterization only if it was necessary to establish the presence of an accessory artery. In patients with suspected renal artery stenosis, a flush aortogram was followed by selective injection on the side of suspected disease. The pressure gradient across all renal artery stenoses was measured.

Analysis
Both studies were analysed and interpreted in a prospective and blinded fashion. All MRA images were analysed by an experienced cardiovascular radiologist (AMW) on an independent workstation (GE IC software version 5.7). The source images were analysed in each case followed by formation of maximum intensity projections and multiplanar reformations using the available interactive vascular imaging software by the radiologist himself. All DSA examinations were performed and evaluated by a separate consultant radiologist (CE) who was blinded to the results of the MRA studies. Donors were evaluated for the number of main renal arteries, and the presence of any early branches (defined as one arising within 2 cm of the origin of the main renal artery), accessory arteries or any renal artery disease. Patients with suspected renal artery stenosis were analysed for number of main and accessory renal arteries and presence or absence of any stenosis or occlusion. The degree of renal artery stenosis was graded as:normal=Grade 0; 1–49% stenosis=Grade 1; 50–99% stenosis=Grade 2; and occlusions=Grade 3. Arteries that were difficult to evaluate on any imaging modality were classified as being indeterminate. Sensitivity, specificity and predictive values of gadolinium enhanced MRA in the detection of renal artery stenosis greater than 50% (Grades 2 and 3) were based upon the findings at intraarterial DSA.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Potential renal donors
Suboptimal images were obtained in two cases owing to breathing artefacts, although analysis could be performed from the source images. The cause of breathing artefacts in both cases was due to the patient not being able to understand the breathing instructions during the MRA sequence. Both these cases occurred during the early part of this study.

25 main renal arteries without early branches were identified on DSA in 15 potential renal donors included in the study (Table 1Go). MRA correctly identified these 25 arteries. Four of the five renal arteries with early branching identified by DSA were correctly detected with MRA. The early branch was not identified in one renal artery, which was thus inappropriately classified in the former group. This was a donor in which suboptimal images were obtained owing to breathing artefact. There were four accessory arteries, all of which were correctly identified on MRA (Figure 1Go). There was no renal artery with stenosis in this group.


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  		Table 1. Potential renal donors (number of cases=15)

 


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  		Figure 1. Coronal maximum intensity projection magnetic resonance angiography image in a potential renal donor demonstrating an accessory artery on the upper pole of the right kidney.

 
In one potential renal donor, DSA showed occlusion of both coeliac axis and superior mesenteric artery (SMA) with an enlarged inferior mesenteric artery supplying the marginal artery of Drummond and the arch of Riolan (Figure 2aGo). This patient had an abnormal vascular network anterior to the proximal abdominal aorta, supplied by a branch from the right adrenal artery, and was in turn supplying the splenic artery. These collateral arteries, which resulted from coeliac axis and SMA occlusion, were not prospectively identified on MRA (Figure 2bGo). Only the occluded origins of the coeliac axis and SMA were detected on retrospective analysis. These findings led to his exclusion as a donor.



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  		Figure 2. Potential renal donor with abnormal vascular network and collateral vessels demonstrated on digital subtraction angiography (a), but not completely visualized on magnetic resonance angiography (b).

 
Suspected renal artery stenosis
MRA correctly identified all the 52 main renal arteries and 7 accessory arteries shown on DSA in patients with suspected renal artery stenosis. 13 of the 15 arteries reported as being normal (Grade 0) on DSA were similarly graded on MRA. Mild irregularity was identified at the origins of two arteries, thus classifying them as Grade 1 (Table 2Go). Nine renal arteries with Grade 1 on DSA were correctly graded on MRA, while one was over-graded as Grade 2. 20 of the 21 arteries with Grade 2 stenosis on DSA were correctly graded with MRA (Figures 3aGo), while one renal artery was classified as being Grade 1. One renal artery was classified as being Grade 2 on MRA, but was reported on DSA as only being small and thus classified as indeterminate. Further evaluation was not justified as it was supplying an atrophic kidney. All of the five renal arteries with occlusions were correctly identified on MRA.


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  		Table 2. Patients with suspected renal artery stenosis: comparison of degree of stenosis

 


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  		Figure 3. (a) Magnetic resonance angiography demonstrating Grade 2 stenosis in the proximal left renal artery, which corresponds well with the digital subtraction angiography (b).

 
The calculated sensitivities, specificities, and negative and positive predictive values for renal artery stenosis of 50% or greater, with or without occlusions, are given in Table 3. The case with indeterminate stenosis was included and regarded as a positive test result for these calculations.


   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
In this prospective study, gadolinium enhanced MRA has proved to be an accurate method for evaluation of renal arteries in both groups of patients, with the results comparing favourably with that of other studies [6–9, 13, 16–22]. This technique has been applied to study the thoracic aorta [23], pulmonary arteries [24], mesenteric arteries [25], portal venous system [26] and the peripheral arteries [27] besides the renal arteries and abdominal aorta [15]. However, there are limitations to MRA and certain precautions need to be taken while performing and interpreting these studies.

One of the renal arteries with an early branch was not identified on MRA in this study. This was due to suboptimal resolution as a result of inadequate breath holding in a potential renal donor. Identification of early branches and accessory arteries is vital in donors for surgical planning [10]. This demonstrates the importance of prior assessment of each patient's breath-holding capacity and giving proper breathing instructions to the patient before and during the image acquisition [28]. The acquisition time should be tailored to the individual patient by altering the section thickness, number of locations (and thus the coverage) and number of excitations. However, we found that increasing the section thickness by more than 3 mm for renal arteries leads to degradation of spatial resolution, as has been the experience of other authors [18]. With high gradient field strength scanners, most studies can be performed within a single breath hold of 25 s or less. However, these studies can be performed on systems with lower strength MR gradients by selective breath holding, or "keyhole" approach [18, 20], in which the patient is asked to hold the breath during the middle of the scan when the central lines of the k-space are being acquired.

In order to obtain diagnostic images consistently, it is necessary to understand the pulse-sequence architecture as well as to determine accurately the contrast travel time from the intravenous site to the area of interest. For optimal contrast resolution, the maximum arterial gadolinium concentration should occur during the part of the acquisition when central k-space data are being acquired [29, 30]. Central k-spaces can be ordered in several ways, the commonest being sequential acquisition, which is the conventional way, or centric acquisition, in which the central k-spaces are acquired first followed by acquisition of the peripheral k-spaces. Correct timing of the arrival of the contrast medium in the region of interest with acquisition of the central k-space is important to maximize the arterial signal but reduce the overlap caused by venous enhancement. The contrast arrival time can vary widely in patients depending upon their cardiac output, particularly with increasing age and renal failure. This can be calculated by giving a test bolus of gadolinium chelate and scanning repeatedly to form a time–density curve [8, 30, 31], as done in our study, or by automated contrast detection methods [32] like Smartprep (General Electric Medical Systems, Milwaukee, WI). A drawback of the test bolus method is that it increases the total examination time by 5–10 min. In addition, the preliminary gadolinium bolus may interfere with image interpretation by causing venous enhancement or increasing the background signal [13]. Although this may be true for the distal and intrarenal arterial segments, we did not find it to be a problem for the proximal and mid-renal arterial segments, particularly if the source images are analysed.

A more recently introduced technique is to use fluoroscopic imaging for real-time monitoring of the arrival of the bolus of contrast medium fortriggering the 3D MR angiographic sequence [33, 34]. Although a highly reliable method of contrast detection and triggering, this technique is still limited in availability. A novel approach that does not require any bolus timing is to acquire several 3D data sets in a single breath hold with fast multiphase 3D MRA [35]. This technique, which has been considered to be more accurate for depicting the distal renovascular tree, can only be performed on high gradient MR systems.

Resolution of the renal arteries, particularly the distal segment and intrarenal branches, is limited by the spatial resolution and by the contrast in the pelvis and parenchymal enhancement if a test bolus is used. Considering an average field of view of 32 cm and matrix of 256 x 160, the spatial resolution obtainable on our scanner was 1.25 x 2 mm in frequency and phase encoding directions, respectively, while it varied between 2 and 3 mm in slice selection direction. The latter gave better spatial resolution in the potential renal donors as they were relatively healthy people with normal breath-holding capacity. Although this spatial resolution may be enough to identify the accessory renal arteries [18], it may not be able to depict stenosis within them. Also, the subtle irregularities of the distal renal arterial segment in fibromuscular dysplasia may not be demonstrated with MRA [36]. Spatial resolution in slice direction is sometimes sacrificed in order to reduce the acquisition time in patients with inadequate breath-holding capacity. In these patients, who are generally those with chronic renal failure and/or hypertension, this may be justified as it is mainly the proximal renal artery that is of interest.

Gadolinium enhanced MRA requires good co-ordination between the injection of the contrast medium, the breathing instructions and the starting of the scan. A manual injection requires co-ordination between the person injecting the contrast medium and the radiographer performing the acquisition. However, a MR-compatible power injector can perform this function effectively, with a single operator controlling all three functions.

Restriction of imaging volume in the antero-posterior direction when the gadolinium enhanced MRA is performed in the coronal plane is an important limitation of this technique [7, 37], as seen in one case in our study. This is due to the limited number of slice locations that can be performed for a comfortable single breath hold without compromising the section thickness. This means that it is important to position the imaging volume accurately to include the whole of the region of interest. All the vessels imaged should be studied and the significance of any pathology evaluated.

MRA images should always be interpreted by the radiologist on an independent computer workstation with 3D reconstruction capabilities [38]. This should include scrutiny of the individual source images and performing multiplanar reformations and maximum intensity projections in multiple planes. The former is essential as assessment of maximum intensity projections alone has the disadvantage of losing the lower intensity features of the vessels [39], which can result in vessels appearing narrower, overestimation of stenosis and loss of visualization of small vessels. In addition, analysis of source images helps to unravel the arteries free from veins in cases of venous overlap. However, maximum signal intensity projections are helpful for showing long segments of vessels on a single image. Venous overlap can sometimes be cut off by drawing the region of interest around the arteries. These MR capabilities enable one to unfold the course of tortuous vessels, visualize the origins of the renal arteries and evaluate renal arterial pathology from different angles. They should be adequately utilized for proper interpretation of any MRA study.

Some authors recommend 3D phase contrast MRA as an adjunct to gadolinium enhanced MRA in order to demonstrate the haemodynamic severity of renal artery stenosis [40]. We did not add this sequence to our study because of the additional time involved and the lack of objective evidence that it adds to the diagnosis.

Mild over-grading of the degree of renal artery stenosis occurred in four cases in our study. Two of these, which were normal on DSA, had mild irregularity at their origins and were thus classified as being Grade 1. In fact, these irregularities may be real and were detected on MRA because of its multiplanar capability, particularly on the transverse reformats, which are not possible to obtain with DSA. It was difficult to categorize the severity of stenosis precisely into grades in some cases with a moderate degree of stenosis, i.e. between 40% and 60%. In clinical practice, such cases would still have to undergo further evaluation with intra-arterial DSA. Indeterminate results and overgrading on MRA can be caused by signal voids in small arteries or accessory arteries owing to limited spatial resolution. In some instances, dense aortic or renal artery calcification may contribute to local susceptibility-related artefacts [17]. Precise grading of renal artery stenosis may be difficult because of these factors, although it is more important for a screening test to detect the absence of significant stenosis rather than to grade the severity of stenosis accurately.

Gadolinium enhanced 3D MRA is therefore an accurate and clinically useful technique. Like any other imaging modality, strict application of technique is required and avoidance of the pitfalls is essential. One has to become familiar with the particular 3D MRA pulse sequence available on each MR system and the synchronization of this sequence with the injection of contrast medium. One must also adapt to image interpretation interactively at a sophisticated workstation.

In summary, this technique is useful for the pre-surgical evaluation of renal arteries in potential renal donors. It is the non-invasive modality of choice for detecting renal artery stenosis in patients suspected of renovascular hypertension, particularly in patients with renal failure. In our institution, we now routinely perform 3D MRA to detect renal artery stenosis as the first imaging technique. This is followed by intraarterial DSA only when degree of stenosis is Grade 2 or 3 or indeterminate and revascularization is being considered.


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  		Table 3. Statistical analysis in patients with significant renal artery stenosis

 
Received for publication November 14, 2000. Accepted for publication January 24, 2001.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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D. J. Pennell, U. P. Sechtem, C. B. Higgins, W. J. Manning, G. M. Pohost, F. E. Rademakers, A. C. van Rossum, L. J. Shaw, and E. K. Yucel
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Is It Necessary to Study Accessory Arteries When Screening the Renal Arteries for Renovascular Hypertension?
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