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Published online before print April 3, 2003, 10.1148/radiol.2273020671
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(Radiology 2003;227:802-808.)
© RSNA, 2003

Cardiac Imaging

Improved MR Coronary Angiography with Use of a New Rapid Clearance Blood Pool Contrast Agent in Pigs1

Martijn S. Dirksen, MD, Hildo J. Lamb, PhD, Patrik Kunz, PhD, Philippe Robert, MSc, Claire Corot, PhD and Albert de Roos, MD

1 From the Department of Radiology, Leiden University Medical Center, Albinusdreef 2, Rm 62, Post Zone C2-S, 2333 ZA Leiden, the Netherlands (M.S.D., H.J.L., P.K., A.d.R.); and Guerbet Research, Aulnay Sous Bois, France (P.R., C.C.). From the 2001 RSNA scientific assembly. Received June 6, 2002; revision requested July 30; revision received September 3; accepted October 25. Address correspondence to M.S.D. (e-mail: m.s.dirksen@lumc.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate in an animal model the potential for clinical use of a new rapid clearance blood pool contrast agent to improve free-breathing and breath-hold magnetic resonance (MR) coronary angiography.

MATERIALS AND METHODS: Free-breathing and breath-hold MR coronary angiography were performed in a pig model (n = 9) (a) without use of a contrast agent; (b) with P792 (Guerbet Research, Aulnay Sous Bois, France), a monodisperse monogadolinated macromolecular compound that acts as a blood pool contrast agent with rapid clearance properties; and (c) with an extravascular gadolinium-based contrast agent. This resulted in six imaging options, which were compared in terms of contrast-to-noise ratio (CNR), signal-to-noise ratio, and vessel length measurements by using the Student t test.

RESULTS: Use of P792 improved CNR and visible vessel length significantly with both MR respiratory motion correction approaches, as compared with nonenhanced MR imaging (P < .05). CNR was improved by 76% (from 5.0 to 8.6) with the free-breathing approach and by 34% (from 6.2 to 8.2) with the breath-hold approach. Visible vessel length was increased by 27% (from 79.7 to 99.2 mm) with the free-breathing approach and by 90% (from 48.2 to 86.5 mm) with the breath-hold approach. The P792-enhanced free-breathing approach allowed more distal visualization of the coronary arteries than did the P792-enhanced breath-hold approach (P < .05). Use of the extravascular contrast agent did not improve image quality significantly when compared with that of nonenhanced MR images.

CONCLUSION: Use of P792 improves coronary artery MR imaging in conjunction with free-breathing and breath-hold approaches.

© RSNA, 2003

Index terms: Animals • Contrast media, experimental studies • Coronary vessels, MR, 541.12142, 541.12143 • Magnetic resonance (MR), contrast enhancement, 541.12143 • Magnetic resonance (MR), vascular studies, 541.12142


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Numerous investigators have shown the potential role of magnetic resonance (MR) coronary angiography in the diagnosis of coronary artery stenoses, although the reported sensitivities and specificities are suboptimal (1–8). The spatial resolution and contrast-to-noise ratio (CNR) are not sufficient to allow reliable visualization of coronary artery stenoses with MR imaging. Several technical innovations are currently being explored to improve the diagnostic value of three-dimensional MR coronary angiography. The artifacts caused by respiratory motion can be eliminated with use of navigator-gated free-breathing sequences or rapid acquisitions during repeated breath holds (9–11). Furthermore, contrast between the coronary arteries and surrounding tissues can be enhanced by using specific preparation pulses to suppress the signal from epicardial fat and myocardium (12,13). Moreover, various types of contrast media have been shown to be useful for MR coronary angiography, including contrast agents that remain in the circulation without extravasation to the interstitial space (14–18). Recently, blood pool contrast media have been developed that have an initial intravascular distribution and also have rapid renal elimination (19).

The use of P792 (Guerbet Research, Aulnay Sous Bois, France), a gadolinium-based blood pool contrast medium with rapid renal elimination, was recently reported in the depiction of coronary arteries with use of a breath-hold MR sequence (16). P792 is a gadolinium macromolecule that is too large for capillary extravasation but is small enough for rapid renal elimination. In a study by Taupitz et al (16), a breath-hold length of 60–90 seconds was used, and a moderate CNR was reported for the P792-enhanced images when compared with that in studies in which other blood pool contrast agents were used (14,15,17).

Accordingly, the purpose of the present study was to evaluate in an animal model the potential for clinical use of P792 as a rapid clearance blood pool contrast agent to improve free-breathing and breath-hold MR coronary angiography.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Animals and Contrast Agent
Nine female domestic pigs (weight, 32.1 kg ± 3.5 [SD]) were included in the present study. The study protocol was approved by the local animal studies ethics committee.

P792, a monodisperse monogadolinated macromolecular compound with a molecular weight of 6.47 kDa, is based on a gadoterate meglumine (Dotarem; Laboratoire Guerbet, Aulnay-sous-Bous, France) core. Four hydrophilic arms account for its intravascular properties, and excretion is renal. R1 is 27.1 mmol-1 · L · sec-1 ± 1.0 at 1.5 T. P792 has been designed for human use as a rapid clearance blood pool contrast agent (19,20).

Study Design and Animal Preparation
The pharmacokinetics of P792 were evaluated initially. Thereafter, P792 was evaluated for application in MR coronary angiography. Free-breathing and breath-hold MR imaging were performed (a) without use of a contrast agent, (b) with P792, and (c) with a conventional extravascular gadolinium-based contrast agent (gadoterate meglumine). This resulted in six imaging options, which were compared in terms of CNR, signal-to-noise ratio (SNR), and vessel length measurements. In all cases, the right coronary artery was examined. P792 was used at the intended clinical dose of 0.013 mmol per kg of body weight (0.36-mL solution of P792 per kilogram). Gadoterate meglumine was administered at 377 mmol/kg, or 0.2 mL per kilogram of body weight. For each experiment, contrast material was injected at a rate of 2.0 mL/sec by using a Spectris Power Injector system (Medrad, Indianola, Pa).

Animal preparation was performed by members of the animal care laboratory at Leiden University Medical Center. Each experiment started with intramuscular administration of 8 mg/kg zolazepam-tiletamine (Zoletil; Virbac Laboratories, Carros, France). Anesthesia was induced with intravenous administration of 10 mg/kg thiopental (Nesdonal; Rhône-Poulenc, Amstelveen, the Netherlands) and 0.05 mg/kg atropine (Atropinesulfaat; Centrafarm, Etten-Leur, the Netherlands). The pigs were then intubated and ventilated mechanically with oxygen, nitrous oxide, and 1.5% isoflurane (Forene; Abbott, Hoofddorp, the Netherlands). Anesthesia was maintained with intravenous administration of 5 mg/h midazolam hydrochloride (Midazolam; Genthon, Nijmegen, the Netherlands) and 4 mg/h pancuronium-bromide (Pavulon; Organon, Oss, the Netherlands). Catheters were surgically placed in the jugular vein and carotid artery to allow contrast agent administration and blood sampling, respectively. During MR imaging, the carotid artery catheter was combined with a pulse-wave detector and hardware MR interface for cardiac triggering (21).

Pharmacokinetic Experiment
The pharmacokinetics of P792 were evaluated in two pigs. P792 was injected and blood samples were drawn at increasing time intervals during 48 hours (M.S.D., P.R.). In one pig, additional blood samples were drawn at short time intervals to illustrate first-pass pharmacokinetic effects. The blood levels of P792 were determined with atomic-emission spectrophotometry (ICP-AES Optima-3300RL; Perkin Elmer, Norwalk, Conn), and data were processed with KINETICA software (Innaphase, Philadelphia, Pa).

MR Coronary Angiography
A 1.5-T Gyroscan ACS/NT system (Philips Medical Systems, Best, the Netherlands) was used for MR coronary angiography with Powertrak 6000 gradients, the Interactive Cardiac patch, and all five elements of a commercially available cardiac synergy surface coil (Philips Medical Systems). The following free-breathing and breath-hold MR sequences were performed (n = 7): (a) without use of a contrast agent, (b) with P792, and (c) with gadoterate meglumine. MR imaging was initiated after a fixed time delay of 8.5 seconds after contrast medium administration through the jugular catheter by using the power injector. The time delay was determined by using a P792 test bolus (1.0 mL, 0.013 mmol/kg, injected at 2 mL/sec) and a dynamic image acquisition in the first two animals that included correction for filling of the power injector system with contrast material. At least 60 minutes were allowed between repeat injections for renal clearance.

Free-breathing MR sequence.—A three-dimensional turbo field -echo sequence was combined with real-time respiratory navigator gating and tracking with an acceptance window of 5 mm at end expiration (9,13). Total imaging duration was 8–10 minutes, depending on respiratory navigator gating efficiency. The following imaging parameters were used: repetition time msec/echo time msec, 7.1/1.9; flip angle, 30°; matrix, 512 x 266; field of view, 360 x 270 mm; each three-dimensional volume section acquired in 38 shots, with 12 echoes acquired per shot; and 20 overcontiguous sections reconstructed to 1.5-mm section thickness, resulting in 0.70 x 1.01 in-plane resolution. Acquisition duration was 49.8 msec in diastole. Fat suppression and a low-to-high k-space filling order were applied. For optimization of nonenhanced acquisitions, a T2 preparation pulse was applied. T2 preparation suppresses the signal intensity of the perivascular tissues (12,13). For the contrast material–enhanced images, a 90° saturation preparation pulse was applied, whereas T2 preparation was omitted (Fig 1). A 90° preparation pulse was chosen instead of a 180° preparation pulse, since saturation allows shorter repetition times, which is particularly useful for first-pass contrast-enhanced image acquisitions. In addition, image contrast in saturation-recovery imaging was assumed to be less sensitive to fluctuations of cardiac frequency compared with that of inversion-recovery imaging.



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  		Figure 1. MR coronary angiography pulse sequences used in the present study. Upper row: native nonenhanced sequence with use of T2 preparation and navigator and breath-hold approaches. Lower row: contrast-enhanced sequences with use of navigator and breath-hold approaches. Note that for contrast-enhanced acquisitions, a 90° saturation preparation pulse was applied, whereas the T2 preparation pulse was omitted.

 
Breath-hold MR sequence.—One breath-hold duration of 25–30 seconds was applied in a three-dimensional turbo field-echo sequence: 7.5/2.0; flip angle, 30°; matrix, 512 x 120; field of view, 340 x 170 mm; each three-dimensional volume section acquired in 10 shots, with 12 echoes acquired per shot; and 12 overcontiguous sections reconstructed to 1.5-mm section thickness, resulting in 0.66 x 1.42 in-plane resolution. Acquisition duration was 89.6 msec in diastole. Fat suppression and a low-to-high k-space filling order were applied. For the contrast-enhanced images, a 90° preparatory pulse was applied, whereas T2 preparation was omitted (Fig 1).

Image and Statistical Analyses
CNR, SNR, and visible vessel length were calculated with an Easy Vision workstation (Philips Medical Systems) by two readers in consensus (H.J.L., M.S.D.). CNR and SNR were calculated with the following equations (13): CNR = (Signalblood - Signalbackground)/[1/2(SDblood + SDbackground)] and SNR = Signalblood/ SDblood.

Regions of interest were placed in the proximal right coronary artery 10 mm distal from its origin and also in the adjacent background tissue. The regions were oblong, with a size of 2 x 6 pixels, including 12 pixels. Vessel length was measured by using curved multiplanar reformatting. Data were expressed as mean ± SD and were compared by using a two-tailed paired Student t test. Furthermore, mean percentage changes of individual data were calculated. A P value less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Pharmacokinetic Experiment
Figure 2, A, presents blood levels measured after injection of P792 as a function of time. The initial bolus passage was followed by a steady-state phase, which illustrated the blood pool properties. Then P792 was rapidly cleared by means of renal excretion. Figure 2, B, shows measurements of several pharmacokinetic parameters. Figure 3 illustrates a typical comparison of coronary artery MR imaging with use of the blood pool contrast agent and the extravascular contrast agent.



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  		Figure 2. A, P792 pharmacokinetics. The first-pass phase is followed by a steady-state phase and rapid renal clearance (data from one animal). P792 was below detection level after 59.5 minutes. B, Quantification of pharmacokinetics. C5/C0 represents P792 levels at 5 minutes after injection relative to P792 levels immediately after injection. The high C5/C0 ratio and the small distribution volume compared with that of gadoterate meglumine (Gd-DOTA) (26) illustrate the blood pool properties of P792 (data from two pigs). C, Molecular structure of P792 versus that of gadoterate meglumine (Gd-DOTA). P792 has four hydrophilic arms that prevent transcapillary diffusion. Alternatively, gadoterate meglumine may freely pass the capillary endothelium because of its small molecular size.

 


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  		Figure 3. Wash-out time series of MR coronary angiography with use of two types of contrast agents to illustrate the difference between blood pool contrast agents and extravascular contrast agents. Upper series: Application of a blood pool contrast agent (P792) results in selective enhancement of the blood pool during 15 minutes, whereas the background tissues remain unenhanced. Lower series: the conventional agent (gadoterate meglumine) extravasates within 1 minute, causing enhancement of the perivascular tissues, which makes it impossible to identify the coronary artery.

 
MR Imaging Coronary Angiography
The results are summarized in the Table for the navigator and breath-hold approaches.


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  		Comparison of Three MR Coronary Angiography Techniques

 
Navigator approach.—P792-enhanced MR imaging showed a 76% improvement in CNR compared with that of nonenhanced MR imaging (P < .05). However, gadoterate meglumine–enhanced MR imaging resulted in a 58% decrease in CNR compared with that of nonenhanced MR imaging (P < .05). MR imaging with the aid of P792 or gadoterate meglumine showed no significant change in SNR. Measurements of vessel length improved by 27% with use of P792 but decreased by 35% with use of gadoterate meglumine, compared with those of nonenhanced MR imaging (P < .05). Figure 4 illustrates a comparison of nonenhanced and contrast-enhanced MR images obtained with the navigator approach.



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  		Figure 4. MR images illustrate the main study results. The right coronary artery was imaged with a nonenhanced state-of-the-art T2 preparation technique (upper row); with P792 (middle row); and with gadoterate meglumine (lower row). Images were acquired with the navigator approach (each row shows four sections from a stack of 20). The arrow marks the right coronary artery on all images. Image acquisition was started immediately following bolus injection, with 8.5-second bolus arrival delay. Note the low signal intensity of the perivascular tissues on the P792-enhanced images with regard to the other two image types. Coronary background suppression appears most effective on the P792-enhanced images, thereby improving the conspicuity of the coronary vessel.

 
Breath-hold approach.—CNR improved by 34% with the aid of P792 compared with that at nonenhanced MR imaging (P < .05). CNR did not change with use of gadoterate meglumine. Furthermore, SNR did not improve significantly with use of P792 or gadoterate meglumine. Vessel length measurements showed significant improvement with the use of P792 (P < .05) but not with the use of gadoterate meglumine.

Navigator approach versus breath-hold approach.—Use of the navigator approach yielded a higher SNR and better vessel length visualization than did use of the breath-hold approach for nonenhanced MR imaging (P < .05). Use of free-breathing and breath-hold sequences showed improvements similar to those seen in CNR and SNR with the aid of P792 enhancement. Vessel length measurements showed that the navigator approach allowed more distal visualization of the coronary artery than did the breath-hold technique with the use of P792 (P < .05). The breath-hold approach, compared with the navigator approach, showed a higher CNR for nonenhanced MR imaging and for imaging with use of gadoterate meglumine (P < .05).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
The main findings of the study were that (a) a rapid clearance blood pool contrast agent (P792) substantially improves coronary artery depiction in nondiseased coronary arteries with use of MR coronary angiography, (b) respiratory motion correction with the navigator approach allowed more distal visualization of the coronary artery than did the breath-hold approach, and (c) coronary artery visualization with use of a conventional contrast agent was not significantly improved compared with that observed with use of a state-of-the-art T2 preparation technique without exogenous contrast enhancement.

Rapid Clearance Blood Pool Agents
Blood pool contrast agents are particularly useful for MR coronary angiography because of the selective intravascular distribution. Contrast media have been developed that behave as blood pool contrast agents yet have rapid renal clearance. The agent that was used in the current study (P792) is a monodisperse monogadolinated macromolecular compound with a molecular weight of 6.47 kDa, which is too high for transcapillary extravasation but is still low enough for rapid renal elimination (19). In the present study, the rapid clearance properties of P792 were confirmed in the pharmacokinetic experiment.

MR Imaging with P792 and Gadoterate Meglumine
The effectiveness of P792 in improving MR image quality with regard to nonenhanced images was evaluated. Additionally, acquisitions were performed with a clinically available extravascular contrast agent to illustrate the advantages of blood pool contrast agents over extravascular contrast agents and to justify the need for blood pool contrast agents in coronary artery MR imaging.

CNR.—Use of P792 led to improved contrast between the coronary artery and the surrounding tissues with regard to unenhanced MR images. This was observed with both the navigator and breath-hold approaches. This may be explained by two factors: (a) Due to the intravascular containment, P792 allows selective enhancement of the coronary arteries, without signal intensity incrementation of the surrounding tissues; and (b) a suppression preparation pulse was applied for the contrast-enhanced acquisitions, allowing for more effective suppression of the perivascular tissues when compared with that of nonenhanced imaging.

These observations are in agreement with those in other studies. Stuber et al (17) demonstrated that application of a blood pool contrast agent results in considerably improved contrast of the blood and myocardium when compared with that in optimized nonenhanced acquisitions. The contrast agent used in that study was a small-molecular gadolinium compound with albumin-binding affinity, which therefore had no rapid clearance properties. Hofman et al (22) used a blood pool contrast agent combined with a preparatory pulse for MR coronary angiography. The combined use of the blood pool contrast agent and the preparation pulse resulted in good suppression of nonvascular tissues, as reflected by the improved CNR.

SNR.—In the current study, the application of intravascular or extravascular contrast agents did not significantly improve SNR with relation to that on nonenhanced images. This might result from the inclusion of a suppression preparation pulse in the contrast-enhanced imaging sequence. This preparation pulse suppresses part of the blood signal in addition to suppression of nonvascular tissues. This may have resulted in suboptimal incrementation of the blood signal intensity. Similar findings have been reported in other studies. For example, Hofman et al (22) showed that MR coronary angiography with use of a preparation pulse and a blood pool contrast agent had major effects on CNR but only minor effects on SNR. Similar observations were made by Li et al (14) in a study in which different types of contrast media were compared for use with MR coronary angiography. Those two cohorts did not evaluate the effects of blood pool contrast agents on vessel length visualization, however, as was done in the present study.

Vessel length visualization.—The P792-enhanced images allowed more distal visualization of the coronary artery than did nonenhanced images. The improved visualization may be explained by the higher CNR on the P792-enhanced images, which resulted in less pronounced partial volume effects and provided better depiction of small-diameter vessel segments. Improved vessel length visualization was observed for both navigator and breath-hold approaches, although the longest vessel length was observed with use of the navigator approach.

General Considerations
In the present study, only one side of the coronary artery was imaged because of imaging time constraints and anesthetic procedures. The right coronary artery was imaged in all cases. It is not expected that imaging the left coronary artery tree would have caused major differences in the study outcome. Currently, a human phase II trial is underway in which P792 is being used to evaluate both the right and left coronary arteries.

An interesting observation was that use of the extravascular contrast agent did not significantly improve CNR, SNR, or vessel length visualization with regard to those at nonenhanced imaging, not even during the breath-hold acquisitions. This likely results from early extravasation effects of the extravascular contrast agent, which play a considerable role, even shortly after bolus administration. Conversely, other investigators have reported the advantages of using extravascular contrast agents for MR coronary angiography (23–25). This discordance might be explained by the fact that investigators in these studies did not use reference acquisitions that were optimized with T2 preparation. T2 preparation has been shown to effectively suppress the perivascular tissues, resulting in a relatively high CNR of the reference acquisitions in the current study (13).

Recently, Taupitz et al (16) showed that qualitative assessment of the visualization of coronary arteries and their side branches was significantly better with use of P792 than with use of gadopentetate dimeglumine and gadobenate dimeglumine. However, they did not compare their P792 results with those obtained with nonenhanced state-of-the-art MR coronary angiography techniques, such as T2 preparation. The highest CNR reported by Taupitz et al with use of P792 was lower than the CNR reported currently for nonenhanced images acquired with T2 preparation. Furthermore, the currently observed CNR for P792-enhanced breath-hold acquisitions was twofold higher than that reported by Taupitz et al (16). This may be explained by the absence of a preparation pulse in their study.

In conclusion, MR coronary angiography with the use of P792 as a rapid clearance blood pool contrast agent substantially improves coronary artery visualization when compared with use of a state-of-the-art nonenhanced T2 preparation technique. The free-breathing navigator approach allowed more distal visualization of the coronary arteries than did the single breath-hold approach. Use of the extravascular contrast agent showed no significant advantage over nonenhanced MR coronary angiography.

A blood pool contrast agent such as P792 may improve the clinical application of MR coronary angiography because of improved coronary artery visualization compared with that in conventional acquisition protocols. Additionally, rapid clearance allows for multiple bolus injections. Once P792 is tested clinically, it may allow rest-stress myocardial perfusion imaging in addition to coronary artery imaging in a single imaging session. Further studies are needed to illustrate this combined application.


   ACKNOWLEDGMENTS
 
The authors thank Joost Doornbos, PhD, Rob van der Geest, MSc, and Lucia Kroft, PhD, for technical assistance, the animal department for care and surgical procedures (Leiden University Medical Center), and Guerbet Netherlands.


   FOOTNOTES
 
Abbreviations: CNR = contrast-to-noise ratio, SNR = signal-to-noise ratio

Author contributions: Guarantors of integrity of entire study, M.S.D., H.J.L., A.d.R.; study concepts and design, all authors; literature research, M.S.D.; experimental studies, M.S.D., H.J.L.; data acquisition, M.S.D., H.J.L., P.K.; data analysis/interpretation, all authors; statistical analysis, M.S.D., H.J.L., A.d.R.; manuscript preparation, M.S.D., H.J.L., A.d.R.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 

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Contrast-enhanced Coronary MR Angiography [letter] * Dr Dirksen and colleagues respond:
Radiology, June 1, 2004; 231(3): 924 - 924.
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