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Published online before print August 27, 2003, 10.1148/radiol.2291021033
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(Radiology 2003;229:217-223.)
© RSNA, 2003

Cardiac Imaging

Coronary Arteries: Contrast-enhanced MR Imaging with SH L 643A—Experience in 12 Volunteers1

Christoph U. Herborn, MD, Jörg Barkhausen, MD, Ingo Paetsch, MD, Peter Hunold, MD, Marianne Mahler, PhD, Kohkan Shamsi, MD, PhD and Eike Nagel, MD

1 From the Department of Diagnostic and Interventional Radiology, University Hospital Essen, Hufelandstrasse 55, 45122 Essen, Germany (C.U.H., J.B., P.H.); German Heart Institute, Berlin, Germany (I.P., E.N.); Schering, Berlin, Germany (M.M.); and Berlex, Montville, NJ (K.S.). Received August 20, 2002; revision requested October 21; revision received November 18; accepted January 27, 2003. Address correspondence to J.B. (e-mail: joerg.barkhausen@uni-essen.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To assess SH L 643A for three-dimensional breath-hold and respiratory-gated magnetic resonance (MR) imaging in the depiction of coronary arteries.

MATERIALS AND METHODS: Twelve healthy male volunteers underwent either three-dimensional breath-hold (n = 6) or respiratory-gated (n = 6) coronary MR angiography before and after intravenous injection of 0.1 mmol SH L 643A per kilogram of body weight. For nonenhanced and contrast material–enhanced examinations, signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) measurements were obtained. Image quality was assessed in consensus with a five-point scale. Statistical analysis of nonenhanced and contrast-enhanced images was based on a two-tailed paired Student t test. A P value at the .05 significance level was used.

RESULTS: Overall statistically significant improvement in CNR was observed after administration of SH L 643A compared with that on nonenhanced images (8.7 ± 5.3 [SD] vs 23.6 ± 7.2, P < .01). While SNR of contrast-enhanced images showed improvement over that of nonenhanced images, the difference was not statistically significant (25.4 ± 0.8 vs 30.2 ± 16.8, P > .2). Image quality improved from a mean of 3.1 ± 0.8 for nonenhanced images to 4.0 ± 0.8 (P < .01) for contrast-enhanced images.

CONCLUSION: SH L 643A causes significant improvement of the blood-myocardium contrast enhancement at coronary MR angiography compared with that with nonenhanced sequences.

© RSNA, 2003

Index terms: Coronary angiography, contrast media, 511.12142, 511.12143 • Coronary vessels, MR, 54.121412, 54.121413, 54.12142, 54.12143 • Gadolinium • Magnetic resonance (MR), contrast enhancement, 511.12143 • Magnetic resonance (MR), contrast media, 511.12143


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Coronary artery disease is considered the largest cause of mortality and morbidity in the industrialized world (1). Despite a major complication rate of approximately 0.1%, inherent radiation, and excessive cost to the health system (2,3), to date invasive coronary artery angiography is regarded as the standard in the diagnosis of coronary artery disease. Recent technical developments have introduced magnetic resonance (MR) angiography as a feasible and noninvasive alternative that allows visualization of coronary arteries. However, the specificity of current approaches remains insufficient for broad clinical use (4).

Coronary MR angiography so far has been performed with and without application of T1-shortening contrast material. While nonenhanced two-dimensional techniques rely on the inflow of unsaturated spins to increase contrast enhancement between blood and myocardial muscle, this effect is dramatically reduced in three-dimensional (3D) acquisition techniques (5). However, advantageous features inherent to 3D imaging techniques include the acquisition of thin sections, superior signal-to-noise ratio (SNR), and the possibility to postprocess the data set in any desirable plane, which is helpful in particular for small vessels such as coronary arteries. Hence, T1-shortening extracellular gadolinium chelates freely diffusible to the interstitium have been combined with 3D techniques to improve coronary artery delineation (6,7). With reflection about their relatively short intravascular residence time and rapid extravasation into the myocardium, most of the contrast agents currently available have hitherto permitted 3D coronary MR angiography merely during the first arterial pass following intravenous injection (8).

Recent pharmaceutical developments have launched different intravascular contrast agents into preclinical studies. These compounds remain in the blood pool longer than the currently available extravascular agents and simultaneously have higher T1 relaxivity (9–12). Hence, several new blood pool MR contrast agents have recently been reported to improve SNR, as well as contrast-to-noise ratio (CNR), of the blood vessels and the surrounding tissues in animal studies and preliminary clinical trials with coronary MR angiography (13–16). Among other blood pool agents is SH L 643A (Gadomer-17; Schering, Berlin, Germany), which has been shown to be superior to an extravascular agent (gadopentetate dimeglumine) used for coronary MR angiography in a porcine model (17). Since initial volunteer studies of SH L 643A-enhanced MR angiography of the aortoiliac and peripheral arteries provided good image quality and an excellent safety profile (18), the purpose of this bicenter study was to assess SH L 643A for 3D breath-hold and respiratory-gated MR imaging in the depiction of coronary arteries in healthy volunteers.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study was approved by both the institutional review board in Essen, Germany, and the local ethics committee in Berlin, Germany, and informed consent was obtained from all study participants. During a 6-week period, we prospectively enrolled 12 healthy male volunteers (six volunteers each per center; age range, 24–36 years; average age, 32.3 years). Demographic data and medical and surgical history that included current acute and chronic diseases have been assessed 2 weeks prior to the study. In addition, the volunteer’s smoking history; alcohol consumption; diet at present; and any medication received within the past 2 weeks with the indication, total daily dose, and route of administration were noted prior to a general physical examination. All volunteers had electrocardiographic and blood pressure measurements; blood was sampled for hematologic results, coagulation, and clinical chemistry. Urinalysis, virology testing, and drug screening were performed. All laboratory parameters were assessed at a central laboratory (LKF, Kiel, Germany); only drug screening was performed at each study center laboratory.

Inclusion criteria were an age of at least 18 years and no more than 45 years, a body mass index between 20 and 30 kg/m2, and written informed consent. Exclusion criteria were clinically relevant diseases, abnormal electrocardiographic findings, systolic or diastolic blood pressure greater than 140 mm Hg or greater than 90 mm Hg, respectively, as well as positive drug or alcohol screening results, regular intake of medications, and history of any anaphylactic reaction. Any contraindications to MR imaging (eg, metal implants) also resulted in exclusion from the study.

The intravascular contrast agent SH L 643A is a polymer of 24-gadolinium cascades with a molecular weight of 35 kDa. It has gadolinium concentration equimolar to most extravascular compounds (0.5 mmol/mL) combined with a high relaxivity of 13 L/(mmol x sec) at 1.5 T. SH L 643A is eliminated through the kidneys by glomerular filtration; fecal excretion is negligible. SH L 643A does not show considerable extravasation to the interstitial space.

Coronary MR Angiography
For all examinations performed in the 12 subjects, 0.1 mmol SH L 643A per kilogram of body weight was injected with an 18-gauge needle in the left antecubital vein at an individually adjusted flow rate for more than 40 seconds. To guarantee standardized administration of the agent, an automatic injector (MR Spectris; Medrad, Pittsburgh, Pa) was used. The dose was chosen according to previous study findings in which 0.1 mmol/kg yielded high enhancement values during the equilibrium phase (18). All imaging examinations were performed with 1.5-T MR imagers (Magnetom Sonata, Siemens, Erlangen, Germany; and Gyroscan Intera, Philips, Best, the Netherlands) equipped with high-performance three-axis gradient systems. The volunteers were placed in the supine position head first within the bore of the magnet, and a phased-array torso coil with four active coil elements was used. After a transverse localizer sequence was used to identify the origin of the left and right coronary arteries, double oblique fast T1-weighted 3D gradient-echo sequences were performed along the axis of the vessel being evaluated before and after intravenous injection of SH L 643A without the use of a preceding test bolus. For nonenhanced images of the coronary arteries, a T2 preparation pulse was used for the respiratory-gated images (Philips), whereas such a prepulse is not available with the other (Siemens) imager.

While nonenhanced coronary MR angiography was performed without an inversion pulse, contrast-enhanced coronary artery imaging was performed with an inversion-recovery 3D segmented gradient-echo sequence. The inversion-recovery preparation pulse was used to suppress the myocardial signal following contrast material administration and to maximize blood-myocardium contrast enhancement. Inversion times for maximal blood-myocardium contrast enhancement for postcontrast imaging were individually determined for each examination and varied between 180 and 220 msec for the breath-hold examinations, in which fast repetitive images were obtained for time optimization, and were 180 msec for the respiratory-gated examinations. The planes for both imaging techniques were arranged along the main axis of the vessel under investigation. Centric-encoding schemes permitted initial acquisition of low-frequency components in each cardiac cycle when the contrast enhancement between blood and myocardium was high.

Detailed sequence parameters for the breath-hold (Magnetom Sonata) and the respiratory-gated (Gyroscan Intera) examinations are listed in Table 1. An electrocardiogram was recorded during the entire examination, and pulse rate and arterial blood pressure along with oxygen saturation were measured automatically (9500; MR Equipment, Bay Shore, NY) every 5 minutes during the entire examination. Pulse rate; arterial blood pressure; oxygen saturation; an electrocardiogram; and blood samples for hematologic, coagulation, and clinical chemistry tests that included urinalysis were obtained immediately prior to the MR study, as well as 2 and 24 hours following administration of SH L 643A. One author (C.U.H.) reviewed all vital signs, electrocardiograms, and laboratory reports and indicated clinically relevant changes according to a list of normal ranges provided by the central and the local laboratory. Any adverse event that occurred as long as 24 hours after contrast material administration was documented by the same author in a case record form.


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  		TABLE 1. Comparison of Relevant Parameters by Using Either Breath-hold or Respiratory-gated Inversion-Recovery 3D Sequences

 
Breath-hold Imaging
For each image, volunteers were instructed to stop breathing for as long as possible after a deep inspiration. Breath holding was monitored by using navigator echoes collected at the dome of the right diaphragm with a pair of 90° and 180° pulses to ensure intraindividually comparable inspiration levels and supervise motion of the diaphragm during imaging. According to the study protocol, each imaging session started with the left coronary artery to gain comparable data sets; subsequently, the right coronary artery was imaged. The left circumflex artery was imaged hereafter but was not included in the evaluation because of anatomic overlay by the coronary vein. Twelve interpolated sections were collected for each coronary artery with an acquisition time of approximately 30–40 seconds, depending on the heart rate of each volunteer. Three-dimensional breath-hold coronary MR angiography was started during the early arterial phase 20 seconds following initiation of the agent’s application and was constantly repeated following deep inspiration during a total of 30 minutes.

Respiratory-gated Imaging
Real-time adaptive navigator correction with different correction factors (0%, 30%, 60%, 80% of diaphragmatic displacement) was used to correct for respiratory motion in 3D coronary artery imaging (19–21). To reinstate the signal of the liver, which was also suppressed by the inversion prepulse on the contrast-enhanced images to be used for the navigators, a restore pulse was added to the sequence. Contrary to the breath-hold approach, the first contrast-enhanced imaging sequence started within the first steady-state distribution of the compound, roughly 3–4 minutes following the injection of SH L 643A to prevent image artifacts during central k-space acquisition in early arterial phase, and always included the left coronary artery first. There were 20 3D partitions, and the imaging time for each acquisition amounted to 600 cardiac cycles (roughly 8–10 minutes). The entire data acquisition also lasted about 30 minutes and allowed three respiratory-gated acquisitions.

Statistical Analysis
SNR was measured by one author (C.U.H., I.P.) per single center at three localizations within the first 3 cm of the left and right coronary arteries (1, 3, and 5 cm from the origin) with equally sized (20-pixel minimum) and locally adapted regions of interest and was calculated as follows: SIca/SDn, where SIca is the signal intensity of carotid artery and SDn is the noise defined as SD from a signal intensity measurement in a circular region of interest in the lung parenchyma. Noise was measured in the lungs because of the relatively small space outside the patient owing to the coverage of the phased array coil. Blood-myocardium CNR was calculated as follows: (SIca - SIm)/SDn, where SIm is the signal intensity of myocardium, with placement of the region of interest in an adjacent myocardium.

Image quality was assessed in consensus by a radiologist and a cardiologist (I.P., E.N.) with subspecialty training in coronary MR angiography by using the following five-point Likert-type scale: grade 0 represented no visualization (no signal enhancement within vessel lumen); grade 1, poor visualization (low and inhomogenous signal enhancement within vessel lumen, insufficient delineation of vessel border, and no diagnostic evaluation possible); grade 2, moderate visualization (moderate signal enhancement within vessel lumen, but still inhomogeneous, incomplete delineation of vessel border, and evaluation possible with low diagnostic confidence); grade 3, good visualization (good signal enhancement within vessel lumen, almost completely homogeneous, incomplete delineation of vessel border, and evaluation possible with satisfactory diagnostic confidence); and grade 4, excellent visualization (superb and completely homogeneous signal enhancement within vessel lumen, optimal delineation of vessel border, and evaluation possible with high diagnostic confidence). Statistical analysis of nonenhanced and contrast-enhanced images was based on a two-tailed paired Student t test. A P value at the .05 significance level was used.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Coronary MR angiography with and without the blood pool contrast agent SH L 643A was successfully completed in all volunteers. Compared with baseline values obtained prior to the examination, no significant changes in pulse rate, arterial blood pressure, oxygen saturation, and laboratory values were observed following administration of SH L 643A. Neither acute nor late-phase adverse effects were observed in our study cohort.

SNR Results
Overall results of SNR measurements, as well as particular calculations for the left and right coronary arteries, are summarized in Table 2. Both breath-hold and respiratory-gated MR angiography demonstrated improvement of SNR between nonenhanced and contrast-enhanced images that was not statistically significant (breath-hold imaging, mean of 40.2 ± 9.1 [SD] vs 47.6 ± 14.3; respiratory-gated imaging, 12.9 ± 3.3 vs 14.8 ± 7.4).


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  		TABLE 2. Results of SNR and CNR Measurements before and after Administration of SH L 643A

 
CNR Results
Detailed CNR parameters and the corresponding P values are listed in Table 2. Compared with the nonenhanced images, CNR of coronary arteries over myocardial muscle significantly improved on the contrast-enhanced images. A visible example of CNR improvement is shown in Figure 1, where the left coronary artery is nicely displayed following injection of SH L 643A, while it is almost invisible on the nonenhanced data set. Selective analysis of both imaging methods revealed a significant CNR improvement from 9.8 ± 9.1 to 31.0 ± 8.7 (P < .01) for the breath-hold sequence and a trend for improved CNR from 6.4 ± 2.5 to 11.9 ± 7.1 (P = .09) for respiratory-gated MR angiography. One example of SH L 643A-enhanced MR angiography of the right coronary artery with use of either the breath-hold or the respiratory-gated technique is shown in Figure 2.



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  		Figure 1. Breath-hold 3D coronary MR angiograms (oblique inversion-recovery breath-hold T1-weighted gradient-recalled-echo fast low-angle shot). A, On nonenhanced image, the left coronary system (arrow) is poorly seen. B, On contrast-enhanced image, the left main and left anterior descending arteries (arrow) can be nicely delineated 2 minutes after intravenous injection of SH L 643A as a result of considerable increase in blood-to-myocardium CNR.

 


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  		Figure 2. A, Maximum intensity projection from breath-hold 3D coronary MR angiography (oblique inversion-recovery breath-hold T1-weighted gradient-recalled-echo fast low-angle shot) of the right coronary artery system in a 28-year-old volunteer. B, Maximum intensity projection from respiratory-gated coronary MR angiography (oblique inversion-recovery navigator-gated and motion-corrected segmented k-space T1-weighted gradient-echo) of the corresponding anatomic region in a 27-year-old volunteer. Both imaging techniques nicely display the right coronary artery (straight arrow) and proximal parts of the left main coronary artery (curved arrow).

 
As was determined with the breath-hold technique, CNR increased immediately after contrast agent administration and reached the maximum 1–3 minutes after injection. Thereafter, CNR decreased but remained slightly elevated as long as 30 minutes after contrast agent administration (Fig 3). The time course of signal intensity in the blood and myocardium is shown in Figure 4.



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  		Figure 3. Bar graph represents the increase and time course of the blood-to-myocardium CNR following administration of SH L 643A, as acquired in six volunteers with breath-hold coronary MR angiography. Because of shorter image acquisition times compared with those of free-breathing respiratory-gated techniques, this method permits repetitive examinations. Peak CNR is reached as soon as 1-3 minutes after administration of the compound. Error bars = standard errors, * = P < .01 compared with nonenhanced (pre) imaging.

 


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  		Figure 4. Bar graph represents the increase and time course of the signal intensity (SI) of blood (black bars) and myocardium (gray bars) following administration of SH L 643A, as acquired in six volunteers with breath-hold coronary MR angiography. Peak CNR is reached as soon as 1-3 minutes after administration of the compound. Error bars = mean standard errors.

 
Image Quality
The five-point scale was used for both breath-hold and respiratory-gated coronary MR angiography. The overall image quality improved significantly from a mean of 3.1 ± 0.8 to 4.0 ± 0.8 (P < .01) for the contrast-enhanced images. For separate analysis, the breath-hold image quality was rated 3.8 ± 0.4 at contrast-enhanced MR angiography compared with 2.5 ± 0.6 at the nonenhanced study (P < .01), whereas image quality only increased from 3.7 ± 0.5 to 4.2 ± 1.0 (P > .05) at the respiratory-gated examination.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Findings of the present study, in which the blood pool contrast agent SH L 643A was used for coronary MR angiography in healthy volunteers, showed a considerable overall improvement of CNR with both breath-hold and respiratory-gated techniques compared with that with nonenhanced imaging. In addition, image quality was judged significantly better on contrast-enhanced breath-hold images. Besides the satisfactory tolerance of the contrast agent by all study participants, images obtained with SH L 643A at a dose of 0.1 mmol/kg significantly improved coronary artery imaging for at least 10 minutes and caused elevated blood-to-myocardium CNR as long as 30 minutes following intravenous injection. Such long-lasting signal is based on lengthy intravascular retention and strong T1 relaxivity that is inherent to SH L 643A and thus renders the compound well suited for both breath-hold and free-breathing 3D coronary MR angiography. By using the breath-hold sequence, the proximal and medial parts of the coronary tree can be covered with several 3D data sets following a single injection. The improved CNR over 30 minutes allows at least three high-resolution respiratory-gated coronary MR angiograms.

Since coronary MR angiography is electrocardiographically triggered for diastolic data acquisition, it has relatively low imaging efficacy regarding the SNR per segment under investigation. In concert with considerable magnetization recovery of the tissue due to unused time between each imaging cycle, this results in fairly poor contrast enhancement between the blood and myocardium, which substantially impairs sharp delineation of the native coronary arteries. In view of this limitation, several techniques have been introduced to suppress the myocardial signal by using T2 preparation (22–24) and magnetization transfer (25,26) for nonexogenous contrast-enhanced coronary MR angiography or by using steady-state preparations for contrast-enhanced coronary MR angiography (6,13,27). Furthermore, recently introduced fast imaging techniques with steady-state precession (TrueFISP; Siemens Medical Systems, Erlangen, Germany) improve contrast enhancement between blood and myocardial tissue, which allows for sufficient delineation of coronary arteries (28,29). However, contrast-enhanced inversion-recovery imaging with good suppression of the myocardium and barely any influence on the blood signal has become the standard technique for contrast-enhanced coronary MR angiography (15,30). By using a rather high dose of the extravascular contrast material (40 mL gadoteridol), a modified 3D segmented echo-planar technique for contrast-enhanced MR imaging of the coronary arteries recently showed potential, at least when performed separately for the left and right coronary system (31). With regard to SH L 643A, such a dose could be reduced, combined with acceptable drug tolerance observed in the present study group, which might be evaluated in a patient cohort in a future study.

Also in the present work, significant improvements in coronary artery–myocardium CNR, as well as image quality, were achieved. Nevertheless, the choice of an appropriate inversion time for inhibition of the myocardial signal is demanding and needs to be adapted for every single image, as it depends both on the myocardial T1 and the heart rate. In this work, an inversion pulse between 180 and 220 msec was observed to cause sufficient suppression of the myocardium; however, different inversion times should be considered under different circumstances.

In the present study, we used a body weight–adapted dose of the blood pool agent SH L 643A, which previously was shown to significantly improve contrast-enhanced coronary MR angiography, compared with an extravascular standard compound (gadopentetate dimeglumine) used in an animal model with breath-hold and free-breathing techniques (17). This dose also proved suitable for the coverage of the proximal and middle segments of the coronary arteries in our study cohort. A reduced dose may impair the results caused by the long imaging time, especially with the respiratory-gated technique.

Recently, several other new blood pool agents have been evaluated for use in breath-hold and respiratory-gated coronary MR angiography. Either iron particles or gadolinium molecules without and with albumin binding have so far been evaluated. The latter approach with MS-325 caused substantial CNR enhancement of the coronary arteries in humans (15), as did the application of the rapid clearance blood pool agent P792 in swine (32). Iron particles such as superparamagnetic iron oxide (33), NC100150 (34), SHU 555 C (35), and very small superparamagnetic iron oxide particles (36), also have the capability to strongly increase the blood signal, and thus, have been evaluated for coronary MR angiography. Albeit promising results have been reported in both animal and preclinical studies of these compounds, the use of iron agents generally remains challenging due to inherent signal decrease by the pronounced T2 and T2*-shortening effect, especially when it is technically impossible to use minimal echo times (37). Furthermore, iron compounds have a relatively long pharmacologic half-life and accumulate concomitantly in spleen and liver, potentially impairing subsequent examinations of these organs. Hence, SH L 643A, with its good tolerance and fast renal excretion in combination with significantly increased CNR and image quality, holds promise for further clinical evaluation.

In this study, breath-hold coronary MR angiography achieved better results with regard to the improvement in CNR and image quality of contrast-enhanced images compared with respiratory-gated imaging. This partly lies with the rather already high image quality of the nonenhanced sequences of the free-breathing technique. Contrast-enhanced studies might thus be limited to those examinations in which the coronary arteries cannot be sufficiently assessed on nonenhanced MR images. In comparison with respiratory gating, breath-hold coronary MR angiography is generally restricted by lower spatial resolution or by coverage of smaller anatomic portions. However, since healthy volunteers are capable of constantly holding the breath on a certain level for a considerable time, this inherent drawback was well compensated. Furthermore, CNR values were considerably higher with the breath-hold technique, which reflects an increased signal due to the increased pixel size of this technique (1.2 x 0.6 x 2 mm) than that with the respiratory-gated sequence (0.7 x 0.9 x 1.5 mm). Both imaging techniques did not show significant SNR improvement following administration of SH L 643A, which indicates relatively high spatial resolution of the technique, as well as the influence of the inversion pulse of the contrast-enhanced images on SNR measurements. Lengthy retention of the macromolecular compound in the blood pool is reflected by the elevated signal intensity measurements of coronary arteries in comparison with the myocardial signal. The inversion pulse substantially reduces myocardial signal and thus indirectly sustains the T1-shortening effect of paramagnetic contrast agent on increasing blood signal, with consecutively increased blood-to-myocardium CNR.

The outlined study also has some deficits. First, this was a study with a limited number of healthy volunteers and thus without any correlation to the imaging standard, which is coronary angiography. Furthermore, the consensus readout might be a principal limitation of our study, as separate results would have made an interobserver comparison possible. Hence, differences between the sequences used might have become clearer. In addition, calculation of CNR values might call into question whether a separate evaluation of image quality was necessary. However, a more subjective assessment appeared interesting and suggested insignificant qualitative differences between nonenhanced and contrast-enhanced respiratory-gated images, which would not have been detected otherwise.

In conclusion, the blood pool contrast agent SH L 643A, along with an inversion-recovery 3D acquisition technique, improves depiction of the coronary arteries with MR angiography, and thus, we believe, warrants clinical evaluation of breath-hold and respiratory-gated coronary MR angiography in patients with coronary artery disease.


   ACKNOWLEDGMENTS
 
C.U.H. and J.B. thank Michaela Schmidt, Siemens Medical Solutions, Erlangen, Germany, for technical assistance during image acquisition.


   FOOTNOTES
 
Abbreviations: CNR = contrast-to-noise ratio, SNR = signal-to-noise ratio, 3D = three-dimensional

Author contributions: Guarantors of integrity of entire study, all authors; study concepts, M.M., K.S.; study design, M.M., K.S., J.B., E.N.; literature research, C.U.H., J.B., E.N., P.H.; clinical studies, C.U.H., J.B., I.P., E.N.; data acquisition, C.U.H., P.H., J.B., I.P., E.N.; data analysis/interpretation, C.U.H., I.P., E.N.; statistical analysis, C.U.H., I.P.; manuscript preparation, C.U.H., P.H.; manuscript definition of intellectual content and revision/review,, J.B., E.N., K.S.; manuscript editing, C.U.H.; manuscript final version approval, all authors


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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