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Published online before print November 24, 2004, 10.1148/radiol.2341040508
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(Radiology 2005;234:250-255.)
© RSNA, 2004

Technical Developments

Lower Extremity: Low-Dose Contrast Agent Intraarterial MR Angiography in Patients—Initial Results1

Deniz Bilecen, MD, PhD, Anja-Carina Schulte, PhD, Hanns G. Heidecker, MD, Markus Aschwanden, MD, Rolf Huegli, MD, Kurt A. Jaeger, MD, Wladimir Ostheim-Dzerowycz, MD and Georg Bongartz, MD

1 From the Departments of Diagnostic Radiology (D.B., H.G.H., R.H., G.B.) and Angiology (M.A., K.A.J.), University of Basel, Petersgraben 4, CH-4031 Basel, Switzerland; Biozentrum, University of Basel, Switzerland (A.C.S.); and Hochrheinklinik, Bad Saeckingen, Germany (W.O.D.). Received March 17, 2004; revision requested May 25; revision received June 17; accepted June 28. Address correspondence to D.B. (e-mail: dbilecen@uhbs.ch).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
Institutional review board approval and patient consent were obtained. A low-dose injection protocol for intraarterial three-dimensional (3D) gadolinium-enhanced magnetic resonance (MR) angiography was derived from femoral flow phantom studies and prospectively evaluated in patients with peripheral arterial occlusive disease (PAOD). All MR angiograms were obtained at 1.5 T with a T1-weighted gradient-echo sequence. MR angiograms of a gadolinium dilution series (0.8–200.0 mmol/L) were acquired in a femoral phantom at different flow rates. Signal-to-noise ratios (SNRs) above the 75% threshold of the measured maximum were considered optimal. The lowest optimal concentration was injected intraarterially in nine patients to obtain 3D MR angiograms of the thigh and calf station. Contrast-to-noise ratios (CNRs) were calculated for four arterial segments. The low optimal concentration of 50 mmol/L (20-mL bolus volume), about 5% of the total permissible dose, showed SNRs larger than the 75% threshold in the phantom study. In patients, this concentration led to high-spatial-resolution angiograms with mean CNRs of 70.0 ± 14.5 (± standard deviation) for the superficial femoral artery and 47.5 ± 13.4 at the infrapopliteal level. Low-dose contrast agent intraarterial 3D MR angiography showed high arterial enhancement, enabling assessment of lower extremity arteries in patients with PAOD and multiple injections—a crucial precondition for MR-guided endovascular interventions.   

© RSNA, 2004


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
Results
Discussion
 REFERENCES
 
Three-dimensional (3D) magnetic resonance (MR) angiography with intravenous injection of paramagnetic contrast material has been developed as a valuable diagnostic tool (1–6). The major advantages of contrast material–enhanced MR angiography compared to digital subtraction angiography include (a) no radiation exposure for patient and examination personnel, (b) no use of iodinated contrast media, (c) a possibility to examine the soft tissue, and (d) 3D vascular depiction. These favorable properties have motivated several investigators to extend MR technology to MR-guided endovascular interventions, which are currently the subject of growing research activity (7–16). The primary goal of these efforts is to provide high-spatial-resolution 3D contrast-enhanced MR angiograms with strong signal enhancement of the vessel lumen during interventional catheter-guided procedures. These images are essential to delineate the baseline vascular anatomy before, during, and after percutaneous transluminal angioplasty (PTA) and to support the tracking of devices like balloon catheters and guidewires through road map overlays. Due to the short half-life of gadolinium in the blood, repetitive injections of gadolinium-based contrast agents will be mandatory for endovascular intervention. Yet conventional intravenous injections are not practical because the permissible total dose of gadolinium according to the approved guidelines of the Food and Drug Administration would soon be exceeded.

Fortunately, results of recent phantom and animal studies have demonstrated that intraarterial administration allows substantial reduction of the required injected dose of gadolinium-based contrast material compared with that of standard intravenous administration (7,12,15). However, because of the paramagnetic properties of gadolinium, the blood concentration of gadolinium has to be within a certain range to obtain optimal arterial enhancement. Blood concentration of gadolinium that is below this range will result in insufficient T1 shortening, while concentration above this range will undergo T2/T2*-dependent signal intensity loss, reducing or even overcompensating the T1-dependent signal intensity gain.

The blood concentration of gadolinium depends on various parameters, such as the blood flow rate in the artery of interest, the concentration of gadolinium in the injected dose of contrast material (hereafter, the injected gadolinium concentration), and the injection rate. Theoretical calculations have been used to estimate the gadolinium concentration in blood and to predict the optimal range for a particular artery (7). These injection protocols have been successfully validated, for example, in the aorta of swine (7). In patients, however, the potential of low-dose intraarterial 3D contrast-enhanced MR angiography of the lower extremity has not been demonstrated.

Thus, the purpose of our study was to derive a low-dose contrast agent injection protocol from femoral flow phantom experiments for intraarterial 3D contrast-enhanced MR angiography and to prospectively evaluate this injection protocol in patients with peripheral arterial occlusive disease.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
MR Imaging
The flow phantom and patient studies were both performed by using a clinical whole-body 1.5-T MR imager (Magnetom Sonata; Siemens Medical Solutions, Erlangen, Germany) equipped with a high-performance gradient system operating at a gradient strength of 40 mT/m and a slew rate of 200 T/m/sec. A phased-array peripheral vascular coil was used for signal reception. Contrast-enhanced 3D data sets were acquired by using a 3D fast low-angle shot gradient-echo sequence with fat suppression. For the 3D contrast-enhanced MR angiograms in the femoral flow phantom and patient studies, a slab of 64 partitions was oriented in the coronal plane. Acquisition parameters were as follows: section thickness, 1.3 mm; field of view, 380 x 380 mm; matrix, 448 x 251; 80% partial Fourier in the phase-encoding and section direction, resulting in a voxel size of 0.8 x 1.2 x 1.0 mm; acquisition time, 27 seconds; repetition time msec/echo time msec, 2.8/1.1; and flip angle, 20°.

Commercially available gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) distributed with a full strength concentration of 500 mmol/L was used in the phantom and patient studies.

Phantom Study
To obtain different injected gadolinium concentrations, gadopentetate dimeglumine was diluted with physiologic saline solution to acquire concentrations of 0.8, 1.6, 3.1, 6.3, 12.5, 25.0, 50.0, 100.0, and 200.0 mmol/L. To ensure a precise injection rate, a computer-controlled power injector (Spectris; Medrad, Indianola, Pa) was used. The gadolinium-based contrast agent was injected through a 4-F insertion sheath at a rate of 1 mL/sec. To ensure coverage of at least 75% of the k-space during the acquisition time (27 seconds), a bolus length of 20 seconds was applied (17). Thus, the total bolus volume was 20 mL. The injection was applied in flow direction.

The femoral flow phantom was an open system with a 60-L container that served as the first reservoir. The human superficial femoral artery was simulated by an acrylic tube with an inner diameter of 6 mm. The insertion sheath was attached to the tube via a Y connector. Water doped with gadopentetate dimeglumine was used to represent blood and was pumped from the reservoir through the tube into a second collecting container. Continuous flow rates were generated by a motorized pump (Cobe Laboratories, Lakewood, Colo). Flow rates in the femoral flow phantom were determined as the time to fill a defined volume in a graduated cylinder. Since the blood flow rate of the superficial femoral artery in healthy humans is 5.0 mL/sec or less (18), flow rates of 0.0 (stasis), 1.0, 2.5, and 5.0 mL/sec were studied

The signal-to-noise ratio (SNR) as a function of injected gadolinium concentration was determined for all four flow rates. The evaluation was based on signal intensity measurements performed in rectangular regions of interest on the unsubtracted source images. The region of interest with a size of 3 cm2 was placed by one author (A.C.S.) in the enhanced lumen of the flow phantom, starting 3 cm distal from the tip of the introducer sheath. The region of interest was copied and applied to all images of the dilution series. SNR was calculated as SNR = SIbld/SDno, where SIbld is the signal intensity of the acrylic tube (representing the vessel lumen) and SDno is the standard deviation of signal intensity measured in a "noise" region of interest outside the phantom.

Patient Study
The study protocol was approved by our institutional review board. After a full explanation of the study was given, written informed consent was obtained from all patients. Within a period of 3 months, nine patients (eight men, one woman; mean age, 66.0 years ± 11.3 [± standard deviation]; body weight, 75.5 kg ± 5.1) were consecutively enrolled. The inclusion criteria were as follows: intermittent claudication (Fontaine classification stage II), high-grade stenosis suitable for catheter-guided intervention detected at duplex sonography (ATL HDI 5000; Philips, Best, the Netherlands), and antegrade or retrograde PTA. Exclusion criteria included all general contraindications for MR imaging (electrically, magnetically, or mechanically activated pacemakers; ferromagnetic implants; claustrophobia). Patients were referred to the radiology department (University of Basel) for radiographically (digital subtraction angiography) guided PTA, which was performed by one author (R.H.; more than 3 years of experience in interventional radiology). The individual PTA procedure performed in each patient is listed in the Table. After PTA, the 4- or 6-F introducer sheath remained in the femoral artery. The connection side of the side port of the introducer sheath was extended by using a plastic tube to enable comfortable intraarterial administration of contrast material.


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  		Summary of Procedures in Nine Patients with Peripheral Arterial Occlusive Disease

 
Patients were transferred from the digital subtraction angiography suite to the MR suite on a stretcher. A continuous infusion of saline solution with a flow rate of approximately 1 mL/min was applied to ensure the patency of the system during transportation. The overall time for patient transportation and repositioning within the magnet was approximately 20 minutes. Patients were examined in the supine position, feet first in the MR imager.

To cover the entire vascular tree of the lower extremity, a two-station MR angiogram acquisition was chosen; the first station covered the femoropopliteal axis, and the second station covered the popliteal and infrapopliteal axis. The time between each acquisition was approximately 5 minutes to allow image reconstruction. For each station, a single 20-second bolus of contrast material was injected manually through the femoral introducer at a rate of approximately 1 mL/sec and at a concentration that had been determined in the femoral flow phantom study to be the lowest optimal injected gadolinium concentration. Intraarterial injection of contrast material and MR data acquisition were started simultaneously. The MR imager was triggered by a board-certified radiologist (D.B. or G.B., with more than 5 and 15 years of experience in MR angiography, respectively) by using a foot switch next to the imager. Prior to contrast material injection, a native image of the respective station was acquired to serve as a mask for digital subtraction of the contrast-enhanced images.

For quantitative analysis of the intraarterial 3D contrast-enhanced MR angiograms, the arterial tree distal to the catheter tip was subdivided into four segments: segment 1, proximal superficial femoral artery; segment 2, distal superficial femoral artery; segment 3, popliteal artery; and segment 4, infrapopliteal arteries. Signal intensity measurements were performed on the unsubtracted source images displaying to best advantage the arterial segment being evaluated. Signal intensity was measured in regions of interest (size: 0.5–3.0 cm2, depending on the segment) placed by one author (D.B.) in the center of the four arterial segments and immediately adjacent to segments in the soft tissue. Contrast-to-noise ratios (CNRs) were calculated for each arterial segment and each patient as follows: CNR = (SIbld – SItis)/SDno, where SIbld refers to signal intensity of the vessel lumen, SItis refers to signal intensity of the adjacent soft tissue, and SDno refers to the standard deviation of signal intensity measured in a noise region of interest outside the body. In addition, all intraarterial MR angiographic data sets were inspected in terms of image artifacts and venous contamination (D.B. and G.B.).


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
Phantom Study
Figure 1 displays contrast-enhanced unsubtracted source images of the flow phantom obtained with the nine injected gadolinium concentrations at a flow rate of 2.5 mL/sec. A strong increase in SNR was observed with increasing concentration from 0.8 to 25.0 mmol/L, and the highest SNRs were seen at 50.0 and 100.0 mmol/L, which was followed by a moderate decrease at 200.0 mmol/L.



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  		Figure 1. Contrast-enhanced 3D MR angiographic source images of nine injected gadolinium concentrations obtained in the femoral flow phantom study (2.8/1.1, acquisition time of 27 seconds). All images were acquired at continuous flow rate of 2.5 mL/sec, injection rate of 1 mL/sec, and bolus length of 20 seconds. For concentrations below 12.5 mmol/L (12.5 mM), weak signal enhancement is observed because of insufficient T1 shortening. Strong signal enhancement is visible for injected gadolinium concentrations of 25, 50, and 100 mmol/L. A mild decrease in signal enhancement is noted for the 200 mmol/L injected gadolinium concentration, caused by T2/T2*-induced signal loss.

 
The results of the quantitative analysis for each of the four flow rates are plotted in Figure 2. For a flow rate of 0 mL/sec (stasis), peak SNR was found at an injected gadolinium concentration of 25 mmol/L, and for a flow rate of 1.0 mL/sec, it was at 50 mmol/L, whereas the maximum SNRs for flow rates of 2.5 and 5.0 mL/sec were found at an injected gadolinium concentration of 100 mmol/L. A rather broad range of injected gadolinium concentrations above the 75% threshold was observed for all four flow rates. Explicitly, the 75% range of injected gadolinium concentration for a blood flow rate of 0 mL/sec was 6.3–50.0 mmol/L, for a flow rate of 1.0 mL/sec was 12.5–100.0 mmol/L, for a flow rate of 2.5 mL/sec was 25–200 mmol/L, and for a rate of 5.0 mL/sec was 50–200 mmol/L. Thus, an injected gadolinium concentration of 50 mmol/L is the lowest measured concentration that can provide a signal enhancement above the 75% threshold for all four flow rates. From these results, it can be expected that this conclusion will also be valid for in vivo flow rates below 5.0 mL/sec. Thus, an injected gadolinium concentration of 50 mmol/L (1:10 of the stock solution) was used for further evaluation in the patient study.



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  		Figure 2. Graphs show quantitative results of the flow phantom study. SNR versus injected gadolinium concentration ([Gd]inj) for all four flow rates (Qblood) (0.0, 1.0, 2.5, and 5.0 mL/sec). Horizontal lines indicate 75% of the corresponding maximum of SNR. For all four flow rates, SNRs for 50 mmol/L of injected gadolinium concentration are above the 75% threshold.

 
Patient Study
A bolus volume of 20 mL of an injected gadolinium concentration of 50 mmol/L was applied for each station of the two-station 3D contrast-enhanced MR angiography. Thus, the mean dose for each station was 0.013 mmol gadolinium per kilogram of body weight, which corresponds to 4.3% of the total permissible dose of 0.30 mmol gadolinium per kilogram of body weight. The intraarterial injection protocol was well tolerated in all patients. No side effects were observed. The low-dose intraarterial MR angiography protocol provided purely arterial 3D MR angiograms of the main arteries of the thigh and calf. Various arterial lesions were observed at both stations.

Figure 3 depicts anteroposterior maximum intensity projections, or MIPs, from all nine patients. The MIPs from patients 1–4 displayed minor arterial lesions, with mild irregularities of the vessel lumen of the superficial femoral artery and a normal infrapopliteal three-vessel runoff. Images obtained in patient 5 revealed an infrapopliteal two-vessel runoff with an obstruction of the anterior tibial artery. An obstruction of the superficial femoral artery was observed in patient 6. In addition, an infrapopliteal one-vessel runoff, with obstructed anterior tibial and peroneal arteries was observed in patient 7. Images obtained in patients 8 and 9 revealed various obstruction and stenosis patterns at the infrapopliteal level, with luminal irregularities along the patent superficial femoral artery. No disturbing venous contamination nor edge or ringing artifacts at the thigh and calf level were observed on the MIPs.



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  		Figure 3. Anteroposterior maximum intensity projections of the lower extremity in each of nine patients with peripheral arterial occlusive disease. Images were obtained at low-dose contrast agent intraarterial 3D MR angiography (2.8/1.1, acquisition time of 27 seconds). The two stations were acquired separately after intraarterial injection of 20 mL of contrast agent with a 50 mmol/L gadolinium concentration at an injection rate of 1 mL/sec. Various arterial lesions are disclosed. Disturbing venous overlay was not observed.

 
The mean CNR and the corresponding standard deviation for the four arterial segments, averaged over all patients, are presented in Figure 4. The highest CNR, which was 70.0 ± 14.5, was obtained for the proximal superficial femoral artery. A mild but continuous decrease of CNR in the infrapopliteal direction is observed with CNRs of 66.7 ± 9.8 for the distal superficial femoral artery, 61.3 ± 17.7 for the popliteal artery, and 47.5 ± 13.4 for the infrapopliteal arteries.



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  		Figure 4. Graph shows CNR ± standard deviation for the four arterial segments from the thigh and calf station, averaged over nine patients. The highest CNR was observed for the proximal superficial femoral artery, with a moderate uniform decrease toward the peripheral segments.

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
REFERENCES
 
One of the important needs in performing catheter MR-guided endovascular interventions is the repetitive visualization of the vessel segments of interest. This requires repeated intraarterial injections of the contrast agent, whereby the limits mandated by the Food and Drug Administration are not to be exceeded. Recently, it was demonstrated by several investigators that the intraarterial low-dose application of gadolinium-based contrast material is feasible to provide optimal signal enhancement of the vessel lumen in animals (7,9,11,19). In our study, we developed and clinically tested for the first time, to our knowledge, a low-dose injection protocol for intraarterial contrast-enhanced MR angiography for the visualization of the vascular tree of the lower extremity in patients with peripheral arterial occlusive disease. The protocol includes an injection volume of 20 mL, an injected gadolinium concentration of 50 mmol/L, and an injection rate of 1 mL/sec. This low-dose contrast agent intraarterial MR protocol provided high-spatial-resolution 3D angiograms with a high CNR of the vessel lumen. For each station, a total dose of only 1 mmol (ie, injected gadolinium concentration x bolus volume) was administered. If we assume a patient body weight between 60 and 80 kg, approximately 20 (ie, between 18 and 24) intraarterial injections will be permissible before the Food and Drug Administration–approved maximal dose of 0.3 mmol per kilogram of body weight is reached.

The results of our phantom and patient studies, as well as those of studies by other authors, underline that the range of injected gadolinium concentration for optimal arterial enhancement is rather broad (7,8,12). In the phantom study, a blood flow rate of, for example, 2.5 mL/sec generated SNRs above the 75% threshold for injected gadolinium concentrations between 25 and 200 mmol/L. For visualization of the femoral flow in patients, a definite injected gadolinium concentration of 50 mmol/L was applied, which yielded high CNRs for all four arterial segments, that is, for blood flow rates of 5 mL/sec or less and hemodynamic stasis (0 mL/sec). This high tolerance to variations in blood flow simplifies intraarterial MR angiography application and minimizes the occurrence of inconsistent arterial enhancement and image quality. A decrease of CNR in the peripheral direction was observed in the patient study. This is a common phenomenon, however, that is also observed with intravenous contrast-enhanced MR angiography (20).

Assuming that no branch vessels occur between the injection and imaging sites and that blood and gadolinium are completely intermixed, the average blood concentration of gadolinium, [Gd]bld, in the vessel can be estimated from the following equation (7):

{r05ja23e01}
where [Gd]inj is the injected gadolinium concentration, and Qbld and Qinj are the blood flow rate and the injection rate, respectively.

In our phantom study, the theoretically predicted blood concentration of gadolinium ranged 8.3–50.0 mmol/L, which corresponds to 1.7%–10.0% of the commercially available stock solution of 500 mmol/L of gadopentetate dimeglumine. These values are in good agreement with the results obtained in other studies, in which the optimal range of concentration of gadolinium in the blood for 3D MR angiography was found to be on the order of 1%–6% (7,12,15).

Although only 4.3% of the total permissible dose administered at each of two stations (2 x 4.3%) was necessary for the depiction of the vasculature of the lower extremity, there still seems to be great potential to even further reduce the required dose of gadolinium-based contrast material. Results of a recent study showed that injected gadolinium concentration levels below the optimal range are still sufficient to obtain diagnostically valuable 3D MR angiograms—even at gadolinium concentrations in the blood as low as 1% (12). Alternatively, at a constant injected gadolinium concentration, the required dose of gadolinium-based contrast material can be reduced by decreasing the injected bolus volume, which can be achieved by (a) decreasing the injection rate at a constant bolus length or (b) decreasing the bolus length at a constant injection rate. A reduction in bolus length will require shorter acquisition times to maintain the 75% injection coverage of k-space and preserve image quality. This can be realized by using partial Fourier acquisition, alternative k-space sampling strategies (21), or faster MR imaging techniques like sensitivity encoding (22). However, a 50% k-space coverage of the bolus without significant loss of SNR was recently demonstrated in a phantom study and might also be applicable for the assessment of the arteries of the lower extremity in patients (14). In summary, exceeding the maximal permissible Food and Drug Administration–approved dose of gadolinium seems to be rather unlikely during an MR-guided endovascular intervention when using repetitive low-dose intraarterial injections.

In conventional intravenous MR angiography, the synchronization of MR data acquisition and contrast agent application is essential to obtain optimal image quality with exclusively arterial filling. In intraarterial MR angiography, where the start of imaging and bolus injection are concurrent, timing errors are virtually excluded. Insufficient arterial enhancement or disturbing venous overlay was not observed at all, neither at the thigh nor at the calf level. Especially at calf level, venous contamination is often hampering to the image quality at intravenous MR angiography. This venous contamination is caused by the accumulation of contrast agent from the previous run. Intraarterial contrast-enhanced MR angiography, however, allows us to acquire a new mask image directly before the next contrast agent injection and thus prevents this venous contamination.

These favorable properties of intraarterial contrast-enhanced MR angiography also facilitate the acquisition of high-quality angiograms in the case of patients with diseases like peripheral arterial occlusive disease, in which arterial lesions may alter the arterial blood flow and thus the arteriovenous transit time in the periphery (23).

Our study had several limitations. First, all intraarterial 3D contrast-enhanced MR angiograms were acquired with a spoiled gradient-echo sequence. Steady-state free precession sequences, such as true fast imaging with steady-state precession, which may lead to an increase in SNR and CNR, were not applied (19). Second, our experiments were limited to the lower extremity. However, it can be expected that the proposed injection protocol can be applied to other vascular territories with similar blood flow rates, which would result in SNR and CNR values comparable to those obtained in our study.

We assessed the image quality of the intraarterial MR angiograms only in terms of SNR and CNR. Yet, in view of MR-guided endovascular intervention, a comparison between low-dose contrast agent intraarterial 3D MR angiography and digital subtraction angiography as the reference standard is necessary to estimate its sensitivity, specificity, and accuracy in the depiction of stenoses and obstructions.

In conclusion, low-dose contrast agent intraarterial MR angiography is a feasible method for the visualization of the thigh and calf vasculature in patients with peripheral arterial occlusive disease. It provides high-spatial-resolution 3D contrast-enhanced MR angiograms with high CNR of the arteries of the lower extremity. This fact, in combination with the possibility of repetitive injections of gadolinium-based contrast material, facilitates the development of MR-guided endovascular interventional procedures in humans, which may become an alternative method to digital subtraction angiography in the near future.


   ACKNOWLEDGMENTS
 
The authors thank Tanja Haas and Phillip Madoerin for their assistance in data acquisition and processing.


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

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, D.B.; study concepts, D.B.; study design, D.B., G.B.; literature research, H.G.H., W.O.D.; clinical studies, D.B., M.A., R.H., G.B., K.A.J.; experimental studies, D.B., H.G.H., A.C.S.; data acquisition, H.G.H.; data analysis/interpretation, D.B., A.C.S.; manuscript preparation and definition of intellectual content, D.B.; manuscript editing, D.B., A.C.S.; manuscript revision/review, A.C.S., M.A., R.H., W.O.D., G.B.; manuscript final version approval, A.C.S., G.B., H.G.H., M.A., K.A.J., R.H., W.O.D.


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TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 

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