JOURNAL OF MAGNETIC RESONANCE IMAGING 31:149–159 (2010)
Original Research
Direct Comparison of Sensitivity Encoding (SENSE) Accelerated and Conventional 3D Contrast Enhanced Magnetic Resonance Angiography (CE-MRA) of Renal Arteries: Effect of Increasing Spatial Resolution R. Muthupillai, PhD,1,2* E. Douglas, RT,1 S. Huber, PhD,1,2 B. Lambert, RN,1 M. Pereyra, RT,1 G.J. Wilson, PhD,3,4 and S.D. Flamm, MD1,2,5* Conclusion: Despite a reduction in SNR, the higher-resolution SENSE CE-MRA provided improved image quality, reduced artifacts, and increased reader confidence compared to the conventional protocol.
Purpose: To assess the effect of attaining higher spatial resolution in contrast-enhanced magnetic resonance angiography (MRA) of renal arteries using parallel imaging, sensitivity encoding (SENSE), by comparing the SENSE contrast-enhanced (CE) MRA against a conventional CEMRA protocol with identical scan times, injection protocol, and other acquisition parameters.
Key Words: magnetic resonance angiography; renal artery; magnetic resonance imaging; contrast-enhanced magnetic resonance angiography J. Magn. Reson. Imaging 2010;31:149–159. C 2009 Wiley-Liss, Inc. V
Materials and Methods: Numerical simulations and a direct comparison of SENSE-accelerated versus conventional acquisitions were performed. A total of 41 patients (18 male) were imaged using both protocols for a direct comparison. Both protocols used fluoroscopic triggering, centric encoding, breath-holding, equivalent injection protocol, and lasted 30 seconds. Results: Simulated point-spread functions were narrower for the SENSE protocol compared to the conventional protocol. In the patient study, although the SENSE protocol produced images with lower signal-to-noise ratio (SNR), image quality was better for all segments of the renal arteries. In addition, ringing of kidney parenchyma and renal artery blurring were significantly reduced in the SENSE protocol. Finally, reader confidence improved with the SENSE protocol.
1 Department of Radiology, St. Luke’s Episcopal Hospital, Houston, Texas, USA. 2 Department of Radiology, Baylor College of Medicine, Houston, Texas, USA. 3 Philips Healthcare, Cleveland, Ohio, USA. 4 Department of Radiology, Puget Sound VA HCS, Seattle, Washington, USA. 5 Department of Cardiology, St. Luke’s Episcopal Hospital, Houston, Texas, USA. *Present address: S.D.F., MD: the Cleveland Clinic Foundation, Cleveland, OH. *Address reprint requests to: R.M., Dept of Diagnostic Radiology, St. Luke’s Episcopal Hospital, 6720 Bertner Ave., MC 2-256, Houston, TX 77030. E-mail:
[email protected] Received June 2, 2006; Accepted October 6, 2009. DOI 10.1002/jmri.22002 Published online in Wiley InterScience (www.interscience.wiley.com). C 2009 Wiley-Liss, Inc. V
RENAL ARTERY STENOSIS may cause secondary hypertension and, if untreated, may lead to renal impairment. Conversely, early and accurate detection of renal artery stenosis can aid patient management, and appropriate treatment of stenosis may cure or improve renal function. At present, intraarterial digital subtraction angiography (DSA) is considered the gold standard in revealing renal artery morphology, with exquisite contrast and spatial resolution. However, DSA is invasive and 2-dimensional in nature, involves a small but not insignificant risk of serious complications, and is inappropriate for some patients who cannot tolerate the potentially nephrotoxic x-ray contrast media. In recent years, 3D, contrast-enhanced magnetic resonance angiography (CE-MRA) has shown great promise as a noninvasive imaging tool for evaluating renal artery morphology without the limitations associated with invasive x-ray angiography (1–7). Several recent technological and methodological improvements have facilitated the adoption of 3D CEMRA for evaluating renal artery disease in routine clinical practice. Some key developments include the advent of 1) high-performance gradient hardware capable of providing repetition times (TR) and echo times (TE) on the order of a few milliseconds, making it possible to acquire moderate resolution CE-MRA images within a breath-hold; 2) real-time fluoroscopic monitoring eliminating the guesswork involved in
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timing the bolus arrival in the target vasculature (8,9); and 3) centric phase-encode acquisition schemes that capture the arterial enhancement associated with the first pass of the gadolinium (Gd) contrast, with minimal venous contamination even in scans with long acquisition times (10–13). These developments have contributed to the improved robustness of CE-MRA, and numerous published studies have shown high sensitivity and specificity of CE-MRA for evaluating renal artery disease (1–7). Despite these advances, in a recent prospective multicenter study of 402 patients suspected of having renal artery disease, Vasbinder et al (14) found that the sensitivity and specificity of CE-MRA was only 62% and 84%, respectively, even in experienced hands. However, this study population had an unusually large number of patients with fibromuscular dysplasia (38%)—a disease that affects the mid and distal portions of the renal artery. The modest spatial resolution of CE-MRA techniques (in comparison to invasive x-ray angiography or DSA) may make it difficult to distinguish more distal portions of the renal arteries with clinical confidence. Therefore, there is a strong motivation for exploring methods to improve the spatial resolution of 3D CEMRA techniques. The spatial resolution acquired in 3D CE-MRA is constrained by physiologic variables such as the arterial-to-venous transit time, and patient breath-holding ability. In a typical 3D CE-MRA acquisition, for a given anatomic coverage—field of view (FOV) or stepsize in k-space (dk ¼ 1/FOV), the highest k-space value that can be reached within the physiologic constraints along the phase-encoding directions is the ultimate determinant of acquired spatial resolution. In other words, an increase in the rate of k-space traversal would permit attaining a higher spatial resolution for a given dk, within the same physiologic constraints. The traditional approach to traverse k-space faster is by using high-performance gradients in conjunction with high receiver bandwidth (BW) to reduce the TE and TR. Such brute-force reductions in TE and TR to increase the rate of k-space traversal can diminish the signal-to-noisepffiffiffiffiffiffiffiffiffi ratio (SNR) due to increased noise (by a factor of BW as well as the blood-tobackground contrast-to-noise ratiopffiffiffiffiffiffi (CNR), due to a ffi reduction in TR (by a factor of TR ) (15). In this respect, recently described parallel imaging techniques, such as simultaneous acquisition of spatial harmonics (SMASH) or sensitivity encoding (SENSE), offer an attractive alternative to increase the speed of kspace traversal without altering the underlying contrast parameters (16,17). For example, in the case of SENSE, k-space is traversed faster by increasing the phase-encoding step size by a factor proportional to the SENSE acceleration factor (R), and the resulting intentional aliasing is removed with the knowledge of coil sensitivity profiles. When compared to a conventional acquisition without SENSE, the faster rate of kspace traversal may be used either to attain a desired spatial resolution in a shorter acquisition time (18– 21), or to attain a higher spatial resolution in the same time (22–25). Born et al (26) have demonstrated that SENSE could be used either to enhance the qual-
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ity of abdominal artery images by reducing acquisition time or to improve the spatial resolution at a fixed scan time. Fain et al (27) have shown that even modest improvement in spatial resolution with reduced FOV imaging can enhance the visualization of distal renal arteries. The primary purpose of this prospective study was to compare the effect of improved spatial resolution achievable with SENSE in 3D CE-MRA (SenCE-MRA) of the renal arteries to a conventional 3D CE-MRA acquisition without SENSE (ConCE-MRA) that is otherwise identical. Both 3D CE-MRA acquisitions were triggered after monitoring the bolus arrival using a fluoroscopic acquisition, and a centric phase-encode ordering scheme was used for data collection. In addition, the acquisition duration, contrast parameters (such as TR, TE, and flip angle), contrast injection dose, and contrast injection rate were all kept constant for both the SenCE-MRA and ConCE-MRA acquisitions. The difference between the two acquisitions was that the acquired voxel size of the SenCEMRA acquisition was 33% smaller than the ConCEMRA acquisition. To our knowledge, this is the first study to directly compare higher-resolution SENSE accelerated CE-MRA to conventional CE-MRA using the same scan time. In addition, the effects of parallel imaging on blurring of arteries due to contrast agent bolus profile were modeled.
MATERIALS AND METHODS Numerical Simulations The following notations are used throughout the article. FOVy and FOVz represent the desired coverage along the in-plane (y) and through-plane (z) phaseencoding directions; dky (¼ 1/FOVy) and dkz (¼ 1/ FOVz) are the corresponding step-sizes in k-space; and R y and Rz are the SENSE acceleration factors that proportionally decrease FOVy and FOVz. For an elliptical centric phase-encode ordering method described by Wilman et al (13), Fain et al (28) have shown that the area of the ky-kz plane covered after time ‘‘t’’ is a disk centered about the origin with a radius of the kr(t) given by: pkr 2 ðtÞ ¼ Ka t; where Ka ¼ ðdky dkz Þ=TR
½1
Ka is the time rate of k-space area covered. For the same TR, FOVy, and FOVz, if SENSE acceleration is applied along the ky and kz directions with factors R y and Rz, then the time rate of k-space area coverage, Ka-SENSE is given by Ka-SENSE ¼ ðRy Rz dky dkz Þ=TR:
½2
From Eqs. [1] and [2], Ka-SENSE =Ka ¼ Ry Rz ; and
½3a
pffiffiffiffiffiffiffiffiffiffiffiffiffi Kr-SENSE =Kr ¼ Ry Rz :
½3b
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due to fixed scan time. From the PSF, metrics such as full-width at half-maximum (FWHM), and peak amplitude (Ro) were determined. Patient Population From January 2002 to November 2002, 41 patients (18 men, 60 6 15 years) suspected of renal artery disease and clinically referred for renal artery evaluation were enrolled in this Institutional Review Boardapproved study. MRI Acquisition All imaging was performed on a Philips 1.5T NTIntera scanner (Release 8 software, Best, The Netherlands). A standard 4-element SENSE-compatible body array coil was used for signal reception. Figure 1. The k-space radius sampled as a function of time for a 3D CE-MRA scan with and without SENSE is shown above. The curve R ¼ 1 reflects the CE-MRA acquisition without SENSE, and the curve R ¼ 2 reflects the acquisition with a SENSE factor of 2. The rate of k-space traversal was computed from the acquisition parameters used in the study, eg, FOVy, FOVz, repetition times (TR) (Table 2, medium). Note that the SENSE-assisted CE-MRA acquisition reaches a higher spatial frequency compared to a conventional CEMRA acquisition for the same scan time.
In other words, the SENSE acquisition traverses kspace faster, and in the context of this study, for the same imaging time, samples higher values of kr (Fig. 1). The effect of such faster rate of traversal on the achievable image resolution was modeled numerically using MatLab (v. 13, MathWorks, Natick, MA). The change in the rate of traversal maps the contrast bolus variation across k-space differently for the conventional and SENSE-assisted acquisitions. To study the effect of contrast bolus variation during the acquisition, we used the results obtained by Fain et al (28). They directly measured the signal enhancement in the carotid arteries in nine subjects after injecting 20 cc of gadolinium-chelate followed by 20 cc of saline flush injected at 2 cc/s. Fain et al found that a dualphase, gamma-variate function fit the measured signal intensity profile with the least v2 error. In this study, for purposes of modeling, we used the 2-phase, gamma-variate contrast bolus profile (Fig. 2). More details are described in Fain et al (28). All other parameters used in the simulations were taken directly from the acquisition protocol shown in Table 1 (for ‘‘small,’’ ‘‘medium,’’ and ‘‘large’’ protocols, see description in the next section). The amplitude modulation caused by the bolus profile was mapped onto the ky-kz plane with and without SENSE acceleration, as shown in Fig. 3. For both acquisitions, line profiles along kz ¼ 0 are shown in Fig. 4. Both acquisitions were zero padded to a higher matrix (512 512 60) to yield identical reconstruction voxel sizes. Two-dimensional Fourier transformation of the amplitude modulation across k-space was used to estimate the point-spread function (PSF) of the bolus profile. Such numerical estimation of PSF took into account the effect of truncation
Reference Scan Acquisition Coil sensitivity information was acquired using the vendor-provided SENSE reference scan in the following manner (16,29). Since receiver coil sensitivities vary smoothly and slowly over the spatial domain, a coarse sampling of the coil sensitivities is sufficient (30). Complex radiofrequency (RF) receiver coil sensitivity within the entire imaging volume was calculated from a low-resolution fast field echo acquisition with a voxel size of 9 9 9 mm. Coil sensitivities were estimated by interleaving a quadrature body coil acquisition with a phased-array coil acquisition. Moreover, to
Figure 2. The contrast agent concentration variation during the first pass of the bolus is modeled as a biphasic, second-order gamma-variate function, of the form
y ¼ a1 t 2 e t=s1 þ a2 t 2 e t=s2 ., where a1, a2 are scalars, and s1, and s2 are the time constants for the arterial and venous phases. For purposes of simulation, the bolus profile was modeled using the time constants for the arterial and venous phase as measured by Fain et al, with the values of s1 ¼ 4.3 sec, and s2 ¼ 17.2 sec, respectively. Other imaging parameters required for the simulation, eg, FOVs, TR, and matrix, were identical to that of the acquisition protocol described in Table 2 (medium).
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Table 1 Renal MRA Acquisition Parameters: SenCE-MRA vs. ConCE-MRA ConCE-MRA (small)
SenCE-MRA (small)
Number of patients 5/39 Frequency FOV (mm) 368 Phase-FOV (mm) 294 Frequency-matrix 368 Phase-matrix 245 SENSE-factor 1 No. of Acq/Rec. Slices 30/60 Acq/Rec slice_thick (mm) 2.4/1.2 TE (msec) 1.2 TR (msec) 3.7 Flip angle (degrees) 35 BW/pixel (Hz) 434 1.0 1.5 2.4 1.0 Acq. voxel (mm3) Rec. voxel (mm3) 0.7 0.7 1.2 0.7 Centric phase ordering Yes Fluoro triggering Yes Rel. SENSE voxel size
ConCE-MRA (med)
5/39 368 368 368 368 2 30/60 2.4/1.2 1.2 3.7 35 434 1.0 2.4 1.0 0.7 1.2 0.9 Yes Yes 0.67
SenCE-MRA (med)
16/39 448 358 448 314 1 30/60 2.4/1.2 1.2 3.9 35 434 1.5 2.4 1.0 0.9 1.2 0.9 Yes Yes
ConCE-MRA (large)
16/39 448 448 448 448 2 30/60 2.4/1.2 1.2 3.9 35 434 1.0 2.4 1.0 0.9 1.2 1.0 Yes Yes 0.67
SenCE-MRA (large)
18/39 496 397 496 273 1 30/60 2.4/1.2 1.2 4 35 403 1.5 2.4 1.0 1.0 1.2 1.0 Yes Yes
18/39 496 496 496 496 2 30/60 2.4/1.2 1.2 4 35 403 1.0 2.4 1.0 1.2 Yes Yes 0.67
SENSE CE-MRA, sensitivity encoding; ConCE-MRA, conventional contrast-enhanced magnetic resonance angiography; FOV, field of view; Acq., acquisition; Rec., reconstructed; TE, time echo; TR, repetition times; BW, bandwidth; Rel_SENSE voxel, ratio of SenCE-MRA voxel to ConCE-MRA voxel.
Following rapid gradient-echo scout images, an oblique coronal 3D volume was prescribed to cover
the area from the midthoracic aorta to the iliac bifurcation in the cranio-caudal direction, the parenchyma of both kidneys in the right-to-left direction, and a 72mm-thick slab oriented to cover the anterior-posterior excursion of the renal arteries. Three sets of conventional CE MRA and SENSEassisted high-resolution CE-MRA protocols were set up to take into account the body habitus of the patients. The small, medium, and large protocols maintained the same acquired voxel size by adjusting the matrix in proportion to the FOV. The acquisition parameters for the protocols used are shown in detail in Table 1.
Figure 3. Contrast bolus concentration progressively decreases due to dilution during the acquisition, resulting in an amplitude modulation across k-space. This modulation for two acquisitions without (R ¼ 1), and with (R ¼ 2) SENSE acceleration is shown above and below, respectively. A fluoroscopically triggered, centric phase-encode ordering scheme is assumed for both cases.
Figure 4. The line profile at kz ¼ 0 in the images shown in Fig. 3 illustrates the shape of the amplitude modulation across Ky for the 2 3D CE-MRA acquisitions without (R ¼ 1) and with (R ¼ 2) SENSE. Note that the acquisition begins at the center of k-space, and, therefore, the resulting amplitude modulation has the typical characteristics of a ‘‘low-pass’’ filter.
minimize a potential source of misregistration between the reference scan and the actual acquisition due to differences in breathing positions, the low-resolution reference scan was averaged with eight acquisitions (30). The SENSE reference scan was acquired immediately before the SenCE-MRA acquisition and lasted 53 seconds. 3D CE-MRA
Comparison of SENSE and CE-MRA
The SenCE-MRA and the ConCE-MRA protocols were identical in all respects except the acquired spatial resolution. The SENSE assisted CE-MRA protocol used a SENSE factor of 2 in the in-plane phaseencoding direction and, therefore, was able to sample higher spatial frequencies within the same imaging time of the ConCE-MRA acquisition. However, the improvement in spatial resolution was slightly lower than a factor of 2 for the following reason. The ConCE-MRA technique used a reduced FOV in the phase-encoding direction, but the SENSE acquisition did not, since—unlike the SENSE implementation— some amount of aliasing in the in-plane phase encoding direction can be readily tolerated in the ConCEMRA of renal arteries. As a result, independent of the size of the body habitus, the acquired voxel size of ConCE-MRA technique was 1 1.5 2.4 mm3, and the acquired voxel size of SenCE-MRA technique was 1 1 2.4 mm3—a reduction of 33% in voxel volume for the SenCE-MRA technique (see Table 1 for details). SENSE was applied only in the LR direction, as there was no appreciable coil sensitivity variation for this four-element phased-array coil within the centrally located coronal slab thickness of 72 mm to effectively exploit parallel imaging in the AP direction. Contrast Administration and Imaging Protocol Each patient was imaged twice within the same imaging session, once each with the ConCE-MRA and SenCE-MRA techniques. A contrast dose of 0.1 mmol/kg Gd-chelate was used for each of the SenCEMRA and ConCE-MRA acquisitions. The two contrast administrations were separated by at least 15 minutes. The operator recorded the start times of the CE-MRA scans before the administration of the contrast for each patient. To minimize systematic bias due to residual contrast from the first scan, odd-numbered patients had SenCE-MRA first, and even-numbered patients had ConCE-MRA first (Fig. 5). Both acquisitions used a real-time fluoroscopic sequence to monitor contrast bolus arrival. A thick coronal slice (80 mm) centered on the aorta was imaged with a temporal resolution of 0.7 seconds. A commercially available, computer-controlled power injector was programmed to administer 0.1 mmol/kg of Gd-chelate at 2 cc/s, followed by a saline flush of 20 cc at 2 cc/ s, via an intravenous line placed at the antecubital vein. The fluoroscopic sequence was initiated in conjunction with administration of Gd-chelate. After the first three dynamics in the fluoroscopic mode, a realtime complex subtraction was used to observe the arrival of the contrast bolus, and 3D CE-MRA sequence was initiated after the contrast bolus was seen in the descending aorta at the level of the diaphragm. In the temporal gap between the fluoroscopic acquisition and the initiation of centrally encoded 3D CE-MRA (3.2 sec), the patient was instructed to breathe in and hold it. For each acquisition, based on the signal from the external respiratory belt visible at the console, the operator ranked the breath-holding ability of the patient on a scale of 1 to 4: 1 for excellent (held the breath for the entire duration of the scan); 2 for
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Figure 5. Each patient was imaged with a centrally encoded CE-MRA technique with and without SENSE acceleration. For both acquisitions, a single dose of contrast (0.1 mmol/ kg) was administered using a power injector at 2.0 cc/s, and the contrast bolus was monitored using a fluoroscopic imaging technique. In the case of even-numbered patients, the SENSE acquisition preceded the conventional 3D CE-MRA acquisition, and the order of acquisition was reversed for odd-numbered patients. In the temporal gap (15 minutes) between the two acquisitions, other routine postcontrast images (eg, postcontrast T1-weighted images of the kidneys) were acquired.
good (held the breath for 51%–75% of the scan time); 3 for moderate (held the breath for 26%–50% of the acquisition time); and 4 for poor (did not hold breath throughout the scan, or held breath for 20 mm2) were drawn on the source images on the aorta just above the renal bifurcation and on the inferior vena cava (IVC) just below the renal artery. The mean and standard deviation of the signal intensities (SIs) of the respective ROIs were recorded. Because the noise in the SENSE reconstruction is spatially variable (due to coil geometry factors), and because the noise estimated using traditional metrics such as standard deviation of the signal in the air-space can be artificially low due to regularization performed during SENSE reconstruction, the standard deviation (r) of the signal in the IVC (below the level of the renal arteries) was used as an approximation for noise for each scan. The following quantitative metrics were defined and computed: Aortic signal-to-noise ratio (SNR) ¼ (Mean SI of the Aortic ROI)=r; Venous SNR ¼ (Mean SI of the IVC ROI)=r;
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P-value < 0.05 was assumed to reflect statistical significance. RESULTS Computer Simulations
Figure 6. The amplitude of the PSF along y ¼ 0 demonstrates a broader FWHM for the conventional 3D CE-MRA acquisition (3.6 pixels), compared to the SENSE-assisted 3D CE-MRA acquisition (1.9 pixels).
CNR ¼ ðMean SI of the Aortic ROI Mean SI of the IVC ROIÞ=r; and Arterial to venous ratio ¼ ð SI of the IVC ROI Þ=ð SI of the IVC ROI Þ
Qualitative Analysis A radiologist (S.D.F.) with 10 years of experience in vascular MRI blinded to the acquisition technique qualitatively evaluated the CE-MRA image with the following metrics. The renal artery was divided into three segments: proximal (Seg 1) renal artery from the aortic ostia to the first 5 mm, middle renal artery (Seg 2) ranging from segment 1 to first branch, and distal renal artery (Seg 3) ranging from segment 2 to renal parenchyma. The image quality of each segment was ranked on a 4-point scale (1, excellent; 2, good; 3, moderate; and 4, poor). The artifact level was quantified using the following metrics. The ringing of the renal artery, blurring of the renal artery, and the artifact level in the kidney/ parenchyma were ranked on a 4-point scale (1, none; 2, mild; 3, moderate; 4, severe). Overall reader confidence in the diagnosis was scored on a 3-point scale (1, sure; 2, moderate; 3, poor). The reviewer responses were captured by using a custom-designed electronic form. Statistical Analysis Statistical significance of quantitative metrics was assessed using a paired two-tailed t-test, and that of qualitative metrics (ranked on a scale of 1 through 4) was assessed using the Wilcoxon signed-rank test. A
The results from the numerical evaluation were as follows. For the acquisition parameters used in the study (Table 1, medium) the addition of SENSE to a fluoroscopically triggered 3D CE-MRA scan with centric phase-encoding order reduced the FWHM of the PSF as expected. Without temporal apodization (ie, infinite scan time), the theoretical reduction in FWHM was 1.3 pixels for the ConCE-MRA compared to 1.0 pixel for the SenCE-MRA (28). The numerical results, which included the effect of temporal truncation (due to limited scan time), showed that the FWHM of the SenCE-MRA acquisition was 1.9 pixels compared to the ConCE-MRA acquisition of 3.6 pixels (both reconstructed pixels) (Fig. 6). In addition, the peak amplitude of the SenCE-MRA acquisition was 75% greater than the ConCE-MRA acquisition (Fig. 6). Clinical Results Detailed patient demographic information is given in Table 2. Ninety-five percent (39/41) of patients were successfully imaged using both the conventional and SENSE-assisted CE-MRA. Two patients did not complete both acquisitions due to patient discomfort and were excluded from all data analysis. In 19 patients, ConCE-MRA acquisition preceded the SenCE-MRA acquisition, and in the other 20 patients the order of acquisition was reversed. The mean time between the two acquisitions was 16 6 3 minutes. The breathholding ability of the patients, based on the external monitor, was ranked as excellent in 13/39 patients, good in 11/39 patients, moderate in 7/39 patients, and poor in 9/39 patients. For any given patient there was no discernible difference in the breath-holding capacity between the two acquisitions. Some representative images from the ConCE-MRA technique and the SenCE-MRA technique are shown in Figs. 7 and 8. A total of 89 renal arteries from 39 patients were identified. The total number of renal arteries identified Table 2 Patient Demographics Number of patients Male Age y (range) BSA (m2) (range) BMI (kg/m2) (range) Risk Factors Hypertension? (%) History of hypertension? (%) Diabetic? (%) Smoker? (%) Family history of heart disease? (%) Average risk score
39 18 60 6 15 (36-84) 1.9 6 0.2 (1.4 - 2.4) 27.4 6 5.4 (17.6 - 41.1) 31 29 6 4 19
(79) (74) (15) (10) (49)
2.3 6 1
BSA, body surface area; BMI, body mass index.
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Figure 7. Representative maximum intensity projection (MIP) images from a conventional CE-MRA acquisition (A) and SENSE-assisted CE-MRA (C) are shown above. The rectangular region (white lines) around the renal arteries in both images is magnified for better appreciation of image quality for the conventional (B), and SENSE CE-MRA (D). In this patient the conventional CE-MRA images were acquired second, and as a result there is a slightly greater background signal and presence of contrast in the renal veins from the previous CE-MRA acquisition.
included a total of 15 accessory renal arteries (eight on the right, and seven on the left) in 11 patients. Two patients had a single renal artery, and two renal arteries were not visualized and were nonevaluable. Twenty percent or 18/89 renal arteries were judged to have renal artery disease. The results from the quantitative and qualitative evaluation are summarized in Table 3. With respect to quantitative analyses, the SNR of the aortic blood and the CNR between aortic blood and IVC of the SenCEMRA acquisition declined by 24% and 27.3%, respectively, and this reduction was statistically significant (P < 0.05). The arterial-to-venous ratio of the SenCEMRA technique was slightly lower than that of ConCE-MRA, but the difference was not statistically significant. The mean SNR of the IVC in the SENSE CE-MRA and the conventional CE-MRA was low, indicating adequate venous suppression, and the difference in the IVC SNR between the two techniques was not statistically significant. The effect of the order of the acquisition on the quantitative parameters was also evaluated. The mean residual IVC SNR of the second acquisition was 4.3 6 1.6 and was slightly higher than the mean IVC SNR of the first acquisition, 2.4 6 1.4. The results from the qualitative analyses were as follows (Table 3). For the conventional CE-MRA technique the image quality scores progressively declined from segment 1 (near the ostia) to segment 3 distally. For the SenCE-MRA technique the image quality
scores of segment 1 and segment 2 were comparable, but declined slightly in segment 3. Overall, the image quality of segments obtained using SenCE-MRA was better than that of the ConCE-MRA technique in all segments, and this improvement was statistically significant (P < 0.02 or better). With respect to artifacts, renal artery blurring and the artifacts in the kidney/ parenchyma were substantially reduced in the SenCE-MRA technique (P < 0.001). However, there was no statistically significant difference in renal artery ringing. There was little renal artery ringing in either technique, which seems to confirm the equivalently good and correct timing of CE-MRA acquisition with respect to contrast bolus administration. The reader confidence improved in the SenCE-MRA protocol compared to the ConCE-MRA protocol, and this improvement was statistically significant (P < 0.001).
DISCUSSION Parallel imaging techniques such as SENSE offer tremendous flexibility for protocol optimization in a clinical CE-MRA acquisition. For example, SENSE can be used to 1) reduce the breath-hold duration (18–21,31–33); 2) improve spatial resolution (24, 25,34,35); 3) improve venous suppression and minimize spatial resolution loss caused by bolus profile modulation for a given scan time with appropriate triggering and 3D phase-encoding order (34), or any
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Figure 8. Representative maximum intensity projection (MIP) images from a conventional CE-MRA acquisition (A) and SENSE-assisted CE-MRA (C) are shown above. The rectangular region (white lines) around the renal arteries in both images is magnified for better appreciation of image quality for the conventional (B), and SENSE CE-MRA (D). In this patient the conventional CE-MRA images were acquired second, and as a result there is a slightly greater background signal and presence of contrast in the ureter from the previous CE-MRA acquisition.
combination of these uses. In each of these approaches the addition of parallel imaging techniques such as SENSE to conventional CE-MRA allows one to strike different trade-offs to meet the clinical requirements. In the context of the current study for improving spatial resolution using SENSE for a given scan time, the following issues must be discussed. SNR When all other imaging parameters are kept constant, the SNR penalty incurred when using SENSE to
improve spatial resolution over a fixed scan time is given by (35): SNRSenCEMRA 1 ; ¼ SNRConCEMRA g R where g is the coil geometry factor, R is the SENSE acceleration factor, and SNRSenCE-MRA and SNRConCE-MRA are the SNR of the SENSE acquisition and a fully encoded acquisition for the same scan time, respectively. Therefore, with an acceleration factor of 2 and
Table 3 Summary of Results: Quantitative and Qualitative Metrics SENSE CE-MRA Quantitative parameters SNRAorta SNRIVC CNRAorta-IVC AVR Qualitative parameters RA Seg 1 IQ RA Seg 2 IQ RA Seg 3 IQ Kidney/parenchymal artifacts Renal artery ringing Renal artery blurring Reader confidence
22.4 6 8.0 3.3 6 1.7 19.1 6 8.7 8.9866.21 1.19 1.18 1.4 1.69 1.01 1.45 1.11
6 0.39 6 0.38 6 0.56 60.79 6 0.11 6 0.52 6 0.35
ConCE-MRA
P-value
29.6 3.4 26.3 11.5
6 6 6 6
10.6 1.8 10.8 6.8
P P P P
< ¼ < ¼
1.33 1.35 1.74 2.46 1.04 2.0 1.45
6 6 6 6 6 6 6
0.47 0.53 0.77 0.98 0.19 0.62 0.61
p < 0.02 P < 0.002 P < 0.001 P < 0.001 P ¼ NS P < 0.001 P < 0.001
0.001 NS 0.004 NS
SENSE CE-MRA, sensitivity encoding; ConCE-MRA, conventional contrast-enhanced magnetic resonance angiography; SNR, signal-tonoise ratio; IVC, inferior vena cava; AVR, arterial-to-venous ratio; RA, renal artery; IQ, image quality.
Comparison of SENSE and CE-MRA
accounting for the 25% increase in FOV, the SNR of the SenCE-MRA should at best be 67% of the SNR of the ConCE-MRA. A further decrease in SNR in the SenCE-MRA would also be expected from the coil geometry factor. Yet the measured SNR of the SenCEMRA acquisition was 75% of the ConCE-MRA acquisition. The higher-than-predicted SNR may result from a more favorable k-space weighting in the SENSE acquisition (36). Our numerical simulations indicate that faster k-space traversal using SENSE results in a PSF that has narrower FWHM and higher peak amplitude that may partly offset the SNR loss associated with SENSE. This latter effect may also be the source of better-than-expected SNR for a high-resolution SENSE CE-MRA compared to a conventional CE-MRA for the same scan time in a group of normal healthy volunteers (22). An issue in SNR measurements is the difficulty in measuring estimates of noise when using parallel imaging methods such as SENSE, due to the intrinsic spatial variation of noise associated with the coil-geometry factor. We sought to minimize this effect by obtaining noise estimates near the vessel of interest (ie, in the IVC that is very close to the aorta and to the anatomy of interest in the study). Before contrast arrival, very little signal is observed in the IVC; thus, artifacts are minimal in the noise measurements made in the IVC. Artifacts that do arise will inflate the noise measurements. This is a limitation of this method, the impact of which was minimized by alternating the order of the acquisitions. However, a more elegant approach would be to use the method proposed recently by Kellman and McVeigh (37), which is suitable for estimating noise in parallel imaging methods. Venous Enhancement The SNR of the IVC of the ConCE-MRA and SenCEMRA were very low (3.4 versus 3.3, respectively), indicating appropriate triggering and effective venous suppression for both techniques. The relatively modest difference between the SNR of the IVC measured after the first and second administrations of the contrast indicates that the time window between the two acquisitions was adequate for sufficient washout of contrast. There was no statistically significant difference in AVR, presumably reflecting the effectiveness of appropriate triggering in conjunction with centric phase-encode ordering. For a centric phase-encode sampling, at any given time during the scan the SenCE-MRA acquisition is at a greater k-space radius (kr) from the origin (Eq. [3]) than the ConCE-MRA acquisition. As a result, a given venous enhancement is mapped at a proportionally finer kr (ie, to smaller vessels or vessel edges) in SenCE-MRA compared to a ConCE-MRA, resulting in a more effective venous suppression (36,38). Resolution Considerations The image quality of SenCE-MRA was judged to be superior to that of the ConCE-MRA in all segments,
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and the clinical confidence was higher. This presumably is partly due to the increased acquired spatial resolution as well as a narrower FWHM in the SenCEMRA acquisition. It should, however, be noted that while the average image quality of the ConCE-MRA was lower than that of the SenCE-MRA, it was still very good (scores were between 1 and 2). The imaging time in this study was limited to 30 seconds—a time span considered to be within the realm of a reasonable breath-hold for most patients. While theoretical predictions suggest that greater improvement in FWHM may be obtained with longer scan times, such lengthening of time may not be appropriate for thoraco-abdominal CE-MRA acquisitions due to respiratory motion. Other factors, such as intrinsic motion of the renal arteries associated with cardiac pulsation and diaphragmatic drift during the breath-hold (39,40), may play an important role in limiting the achievable spatial resolution with CE-MRA, and other motion-compensated renal artery angiographic techniques may need to be evaluated (41–44). Two specific aspects of the current study design merit some discussion. First, a single dose of contrast (0.1 mmol/kg) was used in this study for both the ConCE-MRA as well as SenCE-MRA. Several studies have shown that single-dose contrast can adequately depict renal artery stenosis and accessory renal arteries (45–48). Several researchers have used double- or triple-dose contrast for the visualization of renal arteries (49,50). Further investigations are necessary to evaluate if a slightly higher dose of contrast injected at a faster rate might further offset the reduction in SNR in the SenCE-MRA scan (21). Second, the separation of 15 minutes between the two contrast injections is not sufficient for complete clearance of contrast from the body. This, however, allowed the entire study to be completed within an hour in a clinical setting. In addition, we alternated the order of the sequences to minimize or eliminate any potential bias. The results from the study underscore subtle but intrinsic benefits of using SENSE in such centrally encoded 3D CE-MRA acquisitions. First, the incorporation of SENSE to a conventional acquisition provides a direct and flexible way to trade off SNR, without necessarily altering the underlying contrast parameters. Second, when improving spatial resolution is the main objective (keeping scan time constant), the addition of SENSE to an appropriately triggered, elliptical centric 3D CE-MRA acquisition results in a narrower PSF and maps venous signal onto much higher k-space values compared to a conventional acquisition. Third, while the relatively modest coil-sensitivity variation within the slab thickness in the slice-select direction for this 4-channel body phased-array coil precluded the effective use of SENSE along the slice direction for this particular application, 3D CE-MRA acquisitions, in general, provide an additional degree of flexibility to accelerate image acquisition along the slice-select direction when using coils with more conducive coil-sensitivity profiles in the slice-select direction. Lastly, when reducing the breath-hold duration is the main objective, the addition of SENSE could minimize motion-
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induced blurring, as well as venous contamination at the cost of a slightly less desirable PSF due to temporal truncation of the bolus profile. A limitation of the current study is the lack of a ‘‘gold standard’’ such as invasive x-ray angiography for independent validation of the clinical results. In addition, the contrast bolus profile used in the numerical solutions was the one measured by Fain et al (28), at the carotid artery. While the specific contrast bolus shape may be different for the renal arteries, the overall conclusions of the numerical simulations should remain valid for the abdominal aorta and renal arteries. Furthermore, the acquired resolution was increased only in the phase-encode (in-plane) dimension in this study. Alternatively, one could expend the same SENSE-provided increase in scan efficiency to increase the slice-encode (through-plane) resolution. Evaluating the trade-offs between in-plane and through-plane resolution for renal artery imaging was beyond the scope of this study design, but the overall conclusions of the numerical simulations should remain valid. In conclusion, the results from this prospective study of 41 clinical patients show that it is feasible to combine SENSE with clinical renal CE-MRA for improving spatial resolution within the same imaging time with a modest reduction of SNR. When all other imaging parameters were kept identical, the improvement in spatial resolution in the SENSE-assisted CEMRA scan, compared to a conventional CE-MRA technique, contributed to images that were judged to have better image quality in the proximal, mid, and distal segments of renal arteries, reduced blurring in renal parenchyma and renal arteries, and improved clinical confidence in the results.
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ACKNOWLEDGEMENTS The authors thank Ms. Rebecca Bartow, PhD, Senior Scientific Editor, Scientific Publications, Texas Heart Institute for her excellent editing of this manuscript.
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