MRA of the Renal Arteries 29

S. O. Schoenberg, MD

Department of Clinical Radiology, University Hospitals – Gross hadern, Ludwig Maximilian University of Munich, Marchioni nistr. 15, 81377 Munich, Germany

J. Rieger, MD

Department of Clinical Radiology, University Hospitals – Innenstadt, Ludwig Maximilian University of Munich, Pettenkoferstr. 8a, 80336 Munich, Germany

C O N T E N T S

29.1 Controversies in Grading of Renal-Artery Stenosis

29.2 Implementation of 3D-CE-MRA with Parallel Imaging on Standard MRI Systems 321 29.3 The Use of Multi-Channel MRI Scanners 322

29.4 3D-CE-MRA with

Parallel Imaging at 3 Tesla 323 29.5 Multi-Element Coils

29.6 Time-Resolved 3D-CE-MRA with Parallel-Acquisition Techniques

References

MRA of the Renal Arteries 29

Stefan O. Schoenberg and Johannes Rieger

29.1

Controversies in Grading of Renal-Artery Stenosis

Due to the lack of ionizing radiation, nephrotoxic con- trast agents and invasiveness, 3D contrast-enhanced magnetic-resonance angiography (3D-CE-MRA) has become the technique of choice for angiographic imaging of the renal arteries (Vasbinder et al. 2001).

These advantages are further enhanced by the pos- sible addition of a range of functional techniques for assessment of the hemodynamic signifi cance of renal artery stenosis, staging of parenchymal disease and functional evaluation of the urinary outfl ow tract

(Michaely et al. 2006a, 2006b; Schoenberg et al.

2006). These techniques, including ECG-gated fl ow measurements in the renal artery, time-resolved contrast-enhanced perfusion measurements and dynamic MR urography, can be easily combined with 3D-CE-MRA, thereby offering a comprehensive morphologic and functional evaluation of the renal vascular system within a single magnetic-resonance imaging exam. Two recent large meta-analyses have clearly demonstrated the superior accuracy of 3D- CE-MRA compared to all other imaging techniques of the renal artery for grading of renal artery stenosis, including data of publications from almost 1 decade (Vasbinder et al. 2001; Tan et al. 2002). Therefore, 3D-CE-MRA is currently considered the technique of choice for most referring clinicians to detect and grade renal artery stenosis.

One large Dutch multi-center trial (the RADISH study), however, recently reported completely contra- dictory results in terms of the accuracy of both MRI and computed-tomography angiography (CTA) for grading of renal artery stenosis, thereby question- ing the established the role of 3D-CE-MRA for clini- cal routine use (Vasbinder et al. 2004). In this study, substantially worse sensitivities and specifi cities were found for both MRA and CTA, ranging below 80% for the entire study population of 365 patients.

The results were even worse when the results of the relatively large number of fi bromuscular-dysplasia (FMD) patients were assessed alone with a sensitiv- ity of less than 30%. However, even when only the subgroup of atherosclerotic stenoses exceeding 70%

was selectively evaluated, the overall accuracy did not exceed 85%.

Although the overall results were somewhat dis-

couraging for the use of 3D-CE-MRA, they can be

explained to a large degree by several causes that have

been analyzed in various studies. These underlying

causes include the lack of suffi cient spatial resolution,

random motion of the renal arteries, eccentricity of

atherosclerotic disease, evaluation of the diameter

stenosis instead of the area stenosis as well as inter-

observer variability and incomplete accuracy of the standard of reference, i.e., digital subtraction angiog- raphy. In the RADISH study, typical voxel volumes of 4 to 7 mm³ were used, and only the diameter stenosis was reported for numerical grading of the renal artery stenosis. On the other hand, a recent study has shown that isotropic voxel volumes of less than 0.8 mm³ are feasible using 3D-CE-MRA acquisition accelerated by parallel-imaging techniques (Schoenberg et al.

2005). For the fi rst time, not only the reduction of the vessel diameter at the site of a renal artery stenosis was measured, but also the resulting decrease in vessel area in comparison to the normal renal artery down- stream. This measurement of area stenosis has been well established within invasive techniques such as intravascular ultrasounds for exact grading of coro- nary artery stenosis (Hanekamp et al. 1999). Pathol- ogy studies have shown that atherosclerosis does not occur concentrically in the wall of the vessel, but is a non-uniform eccentric process leaving an irregularly shaped residual lumen of the remaining artery (Jer- emias et al. 2000). Therefore, the only exact measure of the true reduction of vessel lumen is by cross sec- tions perpendicular to the long axis of the vessel.

Due to its three-dimensional acquisition, 3D-CE- MRA in principle holds the potential to perform reconstructions along any desired imaging plane, thus allowing assessment of area stenosis (Fig. 29.1).

However, it is well known that due to the short imag- ing time required to perform the entire 3D-CE-MRA scan within a single breath hold of less than 25 s, spa- tial resolution is usually not equal along all three scan orientations. Typically, spatial resolution is the high- est in the frequency-encoding head-feet direction followed by the phase-encoding left-right direction, while the lowest resolution is acquired in the second phase-encoding (or partition-encoding) anterior- posterior direction. For coronal display of the image in maximum-intensity projection, the relatively poor resolution in partition-encoding direction is not visualized; however, it becomes immediately evident when sagittal or oblique reconstructions are per- formed. In this case geometric distortions from non- isotropic voxel sizes result in a decreased accuracy of the vessel-area measurements. The use of isotropic voxel sizes, as shown in one study, enables a distor- tion-free reconstruction of the vessel area in any desired three-dimensional orientation. Good results could be demonstrated in correlation to invasive ref- erence measurements by intravascular ultrasounds of the renal artery (Schoenberg et al. 2005).

The assessment of area stenosis instead of diam- eter stenosis creates another positive effect on the reliability of renal artery stenosis grading by 3D- CE-MRA, namely the reduction of interobserver variability. A number of studies have shown that

Fig. 29.1. Assessment of area stenosis on 3D-CE-MRA with isotropic sub-millimeter spatial resolution. On the coronal MIP view

(left side) the renal artery stenosis appears to be 50–75%. On the cross-section reformats (right side) perpendicular to the vessel

orientation at the site of the stenosis and downstream the stenosis it becomes evident that this stenosis is only of low grade

with a measured lumen reduction of 30%. This was confi rmed by intravascular ultrasound

interobserver variability is at least as important for a reliable grading of renal artery stenosis as the accu- racy of the technique itself (Schoenberg et al. 2002;

van Jaarsveld et al. 1999). Two large studies have reported kappa values ( κ) as a measure of interob- server agreement of less than 0.6, which highlights the problem of the variability of results among differ- ent readers. It could be shown in one study that meas- urement of diameter stenosis is subject to a much higher interobserver variability than assessment of area stenosis (Schoenberg et al. 2005). This is par- ticularly true for stenoses in the range of 30%–70%, for which a tremendous variation of the results could be shown among two observers. These variations are reduced to less than 20% when using the assessment of area stenosis.

One of the most diffi cult problems to solve in 3D- CE-MRA is random motion of the distal renal arter- ies induced by involuntary contractions of the dia- phragm, which cannot be suppressed by breathing suspension or ECG gating. One study therefore con- cluded that the accuracy for grading of distal renal artery stenosis is inherently limited (Vasbinder et al.

2002). Since these contractions occur somewhat peri- odically in the order of several seconds, one possibil- ity would be to reduce the acquisition to less than 10 s for a 3D data set and to use a time-resolved approach.

This time-resolved approach has also proven in another study to be superior in terms of vessel vis- ibility in the distal main renal artery, the anterior and posterior divisions as well as the proximal segmental intrarenal arteries due to the absence of overlaying enhancing renal parenchyma (Schoenberg et al.

1999). The down side of this approach, however, is that in current acquisitions scan times in the order of 20 s are at least required to obtain the mandatory isotropic spatial resolution of 1 mm³ or less. One study has demonstrated the use of spiral echo-planar imaging (EPI) for accelerating the acquisitions in the x-y plane for time-resolved 3D-CE-MRA of the renal arteries; nevertheless, the spatial resolution could not be increased to voxel lengths of less than 1.5 mm (Amann et al. 2002).

In summary, the requirements for state-of-the-art 3D-CE-MRA of the renal arteries raise the need for a substantial acceleration of the acquisition, which ideally can be delivered by use of parallel-imaging techniques. In the following part, the application of parallel imaging is described for standard MRI sys- tems, multi-channel MRI scanners, dedicated multi- element coils as well as at higher fi eld strengths beyond 1.5 T.

29.2

Implementation of 3D-CE-MRA with Parallel Imaging on Standard MRI Systems

Today standard MRI systems are equipped with at least eight independent receiver channels, which allow the use of eight-element phased-array coils for abdominal imaging. Typically, parallel-imaging acceleration fac- tors of R=2 have been used together with this type of coils, thereby accelerating the acquisition twofold. Ini- tial data have been presented by a few centers using the SENSE algorithm already a few years ago (Weiger et al. 2000; Walter et al. 2003). These preliminary studies could demonstrate advantages in terms of either faster acquisitions or higher resolution within the same scan time compared to non-accelerated imaging. Shorter acquisition times resulted in a lesser number of arte- facts from respiratory motion. However, none of these early studies could show a gain in diagnostic accuracy in comparison to the standard of reference: digital sub- traction angiography (DSA). The overall acceptance of parallel imaging was initially limited by the presence of folding artefacts from signal of tissue outside the fi eld of view (FOV) propagated into the center of the image, often referred to as super-aliasing. Therefore, many researchers still used non-accelerated acqui- sitions and spent the additional signal-to-noise on higher bandwidths, shorter repetition times, fractional echo and smaller fi elds of view to also accelerate acqui- sition unrelated to the use of parallel imaging. One study, however, showed that the GRAPPA algorithm, recently introduced into clinical applications, is sub- stantially more robust to super-aliasing as compared to the mSENSE algorithm (Schoenberg et al. 2005;

Griswold et al. 2002). Thus, smaller FOVs tailored to the dimensions of the renovascular tree could be used even without disturbing central aliasing artefacts.

Therefore, the gain in acquisition speed by parallel- imaging acceleration could be fully exploited without the need for larger number of phase-encoding steps in the left-right direction for encoding of a larger FOV.

The use of GRAPPA with an acceleration factor of 2

resulted in isotropic voxel lengths of 0.9 mm and a

scan time of 23 s. Using multiplanar reconstructions,

the largest cross-sectional diameter at the site of the

stenosis was used for comparison with DSA, which

resulted in a signifi cantly improved accuracy as com-

pared with conventional in-plane diameter measure-

ments of renal artery stenosis. The maximum varia-

tion between 3D-CE-MRA and DSA was reduced from

40% to less than 20% (Schoenberg et al. 2005).

One drawback for the use of parallel imaging is the loss of signal-to-noise ratio (SNR), which decreases in the range of 30% for an acceleration factor of 2. This effect can be effectively counterbalanced to a certain degree by the use of contrast agents with higher relaxivities such as 1-molar agents like gadobutrol (Gadovist, Schering AG, Berlin, Germany) or weakly protein-binding con- trast agents such as gadolinium-BOPTA (MultiHance, BRACCO SpA, Milan, Italy) or strongly protein-binding agents (Vasovist, Schering AG, Berlin, Germany). Both Vasovist and Gadovist are now approved for the use of 3D-CE-MRA of the renal arteries, and the approval for MultiHance is expected in the near future.

29.3

The Use of Multi-Channel MRI Scanners

The recent introduction of MRI systems with up to 32 independent receiver channels has further advanced

the possibilities for parallel-imaging acceleration of 3D-CE-MRA. Usually 12 to 18 different coil elements are used for acquisition of a 3D-CE-MRA data set, thereby improving the g-factor of the coil set-up.

Thus, acceleration factors of 3 can be routinely used with no visible loss of image quality despite a numeri- cally higher noise level (Michaely et al. 2006c) (Figs. 29.2a, 29.2b and 29.3). Typically, the acquisition is accelerated in the left-right direction since the coil sensitivity profi les differ the most in this direction.

Acquisition time can be reduced to 16 s for a 3D-CE- MRA scan with a spatial resolution of 1 mm³. One recent study has found better image quality for scans with a threefold acceleration compared to standard twofold acceleration in terms of vessel visibility in particular in the distal segments of the renal vascular bed (Michaely et al. 2006c). Although the calculated noise level was higher by 30%, this did not visu- ally affect image quality. Therefore, these acquisition parameters can be currently recommended as a reli- able approach to high-resolution renal MRA with relatively short acquisition times.

Fig. 29.2. a High-resolution renal MRA at 3 T with a spatial resolution of 0.9×0.8×0.9 mm³ acquired in just 16 s with GRAPPA and acceleration factor R=3 (40 reference lines, phase encoding and acceleration in left-right direction). The entire slab thick- ness is 72 mm. b High-resolution MRA at 3 T acquired with GRAPPA and acceleration factor R=3 (24 reference lines, phase encoding and acceleration in left-right direction) in 18 s with a spatial resolution of 0.9×0.8×0.9 mm³. In contrast to the above shown MRA, this protocol used phase oversampling and a slab thickness of 87 mm to cover a larger volume of the abdominal vessels and to increase the SNR

b

a

29.4

3D-CE-MRA with Parallel Imaging at 3 Tesla

Parallel-acquisition techniques reduce the signal-to- noise ratio by approximately the square root of the accel- eration factor, if the g-factor is not taken into account.

Since SNR increases linearly with the fi eld strength, 3D-CE-MRA could be theoretically performed with an acceleration factor of 4 at 3 T while maintaining the same SNR as compared to 1.5 T without parallel-imag- ing acceleration. Thus, acceleration factors of 3 to 4 can be routinely performed with excellent image quality.

One preliminary study has shown the feasibility of a high-resolution 3D-CE-MRA scan with isotropic voxel sizes of 0.9×0.9×0.9 mm³ in 16 s scan time (Michaely

et al. 2005) (Fig. 29.2a). The authors could demonstrate an excellent vessel visibility up to the level of the seg- mental arteries with almost no artefacts from respira- tory motion. The use of higher acceleration factors is thereby not limited by the signal-to-noise ratio, but by the geometry of the coils. Although 32-channel 3-T MRI systems are now available, the maximum number of different receiver coil elements in the left-right direc- tion does not exceed 4, thus allowing a maximum of fourfold acceleration in the phase-encoding direction (Fig. 29.4). Higher acceleration factors are theoretically possible when using parallel imaging with acceleration in two dimensions, i.e., an acceleration factor of 4 in phase-encoding direction and an acceleration factor of 2 in partition-encoding (3D) direction totalling to an overall acceleration of R=8. The problem of this 2D

Fig. 29.3. FMD at 3 T; typical string-of-bead appearance of fi bromuscular dysplasia (FMD) in a 72-year-old patient with moder-

ate hypertension. The high spatial resolution (0.9×0.8×0.9 mm³) of this MRA allows a clear depiction of these characteristic

changes on multiplanar reformats in the cross-sectional view (lower row). Courtesy of Dr. Paul Finn, UCLA

parallel-imaging acceleration for coronal 3D-CE-MRA is that due to the relatively thin slab (in partition/3D direction) positioned in the core of the human body the sensitivity profi les of the different coil elements located anterior and posterior are not distinct enough to allow reliable parallel imaging in the partition- encoding direction (Fig. 29.5). Thus, the use of parallel imaging in two dimensions is still limited despite the excess of signal-to-noise ratio at 3 T. Nevertheless, other techniques already benefi t from 2D parallel-imaging acceleration even at 1.5 T such as 3D steady-state-free- precession (SSFP) imaging of the small and large bowel (Herrmann et al. 2006). However, the fundamental dif- ference of this technique is that fi rst, the SNR is substan- tially higher for SSFP sequences compared to gradient- echo sequences used for 3D-CE-MRA, and second, this approach requires complete anatomic coverage of the entire anterior-posterior dimension of the human body to provide images free of aliasing. Therefore, images with three- to fourfold acceleration at 3 T using voxel lengths of 0.8 or less and acquisition times of 15 s are currently considered state of the art.

No data from systematic studies exist for the overall gain in accuracy using these highly accelerated acqui- sitions. However, it can be expected that the increase in acquisition speed and resolution is particularly benefi cial to diseases of the renal artery with subtle irregularities of the vascular wall such as fi bromuscu-

lar dysplasia (Fig. 29.3). Accurate detection of stenosis in fi bromuscular dysplasia is challenging for several reasons. First, the dysplastic changes of the vessel wall with the typical string-of-beads appearance often cause multiple stenoses of varying grade. Second, the changes can appear very subtle when looking on the vessel in a coronal view, thereby underestimating the true reduction of lumen diameter. Therefore, it is very important to reconstruct the images perpendicular to the long axes of the vessel to truly see the multiple reductions of the vessel lumen and correctly identify the target site of the maximum degree of stenosis.

Third, FMD typically involves the distal main artery as well as the intrarenal segments, which are not only smaller, and thus require higher spatial resolution to accurately assess stenosis changes, but also require shorter scan times to reduce the amount of overlay- ing enhancing renal parenchyma and random motion from diaphragmatic contractions.

29.5

Multi-Element Coils

Although 32-channel MR systems are now used in clinical routine, dedicated multi-element coils with

Fig. 29.4. “Prototype MRA” acquired

with parallel-imaging acceleration fac-

tor R=4 (GRAPPA, phase encoding and

acceleration in left-right direction) on

a 32-channel 3-T system with a 32-el-

ement coil. The scan time for this se-

quence was 14 s with a spatial resolution

of 1.0×0.8×1.0 mm³ and a 3D slab thick-

ness of 104 mm. Even though 1.0-molar

contrast agent (Gd-BOPTA) was used

to compensate for the SNR penalty with

parallel imaging, there is a perceivable

amount of image noise. Improved re-

construction algorithms may overcome

this problem in the future

more than 30 elements targeted to a single fi eld of view are not provided by the large manufacturers at this point. However, prototypes are available now from independent companies or research units that can be used together with these 32-channel MR sys- tems, cf. Chaps. 14 and 44. One research group has already demonstrated the possibilities of massively accelerated 3D imaging with acceleration factors of up to 16 using a prototype 32-element coil (Zhu et al. 2004). In our own experience, using a dedicated 32-element fl exible phased-array coil on a 32-channel 3-T MR system, acquisition time for a 3D-CE-MRA scan could be reduced to only 13 s at an isotropic spa- tial resolution of 1×1×1 mm³ (Fig. 29.4). Although all these results have to be considered preliminary and experimental at this point, they clearly show the way towards improvement of the accuracy of contrast- enhanced MRA particularly for the assessment of distal renal artery stenosis.

29.6

Time-Resolved 3D-CE-MRA with Parallel- Acquisition Techniques

Time-resolved 3D-CE-MRA of the renal artery has a number of theoretical advantages for the diagnos- tic work up of renal-artery disease. First, vascular structures with substantially different enhancement kinetics such as the true and false lumen in aortic dissections involving also the renal arteries, primary renal-artery dissection as well as renal-artery aneu- rysms with delayed fi lling can be separately visual- ized on the individual time frames (Schoenberg et al. 1999; Schoenberg et al. 2001) (Fig. 29.6). Second, the short acquisition times reduce the amount of overlay from enhanced renal parenchyma, thus allow- ing a better visualization of the intrarenal branches, which is still a limitation of current 3D-CE-MRA as compared to DSA with a high frame rate. This is also the reason that the assessment of vascular dis- ease primarily involving the intrarenal branches is still a domain of DSA, including vasculitis such as polyarteritis nodosa. Third, involuntary motion from diaphragmatic contractions can be reduced when a high frame rate is used for the time-resolved 3D-CE- MRA acquisition.

Despite these clear advantages, time-resolved 3D-CE-MRA has not been widely used due to con- straints in spatial resolution (Fig. 29.6). One study

has already shown a clear advantage of multi-phase time-resolved acquisitions compared to static single- phase scans in terms of visibility of distal vessel seg- ments (Schoenberg et al. 1999). In this study, a frame rate of 6 s per MRI scan with a reconstructed spatial resolution of 1.8×1.8×1.5 mm³ was used. Overall accuracy compared to DSA was good with sensitivi- ties and specifi cities exceeding 90%; however, only a small number of distal renal artery stenosis were present while most of these stenoses were located in

Fig. 29.5. Limitations of parallel acquisition techniques (PAT)

for renal 3D-CE-MRA. With big volumes acquired in phase-

encode direction (most often left-right direction as shown

on top), the coil sensitivities differ enough to reconstruct the

image correctly. With small volumes as in the case of parallel

imaging in anterior-posterior direction in a thin slab (bottom

robust reconstruction. The results are partially aliased images

with increased folding artefacts in the center

the proximal segment of the main renal artery. Due to the increasing demands in spatial and temporal reso- lution, this approach has not been investigated fur- ther until recently despite the number of advantages.

With the introduction of a combined use of view- sharing techniques together with parallel imaging known as “time-resolved echo-shared angiographic technique” (TREAT) frame rates in the order of 1.8 s are feasible while maintaining a spatial resolution of 1.3×1.0×4.3 mm

(Nael et al. 2006). However, no sys- tematic studies have been published on the overall value of this technique for assessment of renal artery stenosis. Nevertheless, a major shift of paradigm for renal 3D-CE-MRA can be expected integrating the demands for spatial and temporal resolution as well as short acquisition times.

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Fig. 29.6. Time-resolved renal MRA in a

patient with bilateral renal artery sten-

oses acquired at 1.5 T. This sequence

used view sharing with parallel imag-

ing (GRAPPA, R=2) to achieve a spatial

resolution of 2×2×3 mm³ with a tempo-

ral resolution of 1.9 s/3D volume. The

kidneys show symmetric enhancement,

the proximal stenosed part of the renal

arteries cannot be seen due to the nar-

row lumen. This fast imaging technique

allows following the course of the con-

trast agent bolus through the abdominal

vessels

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