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AJR 2004; 183:1041-1047
© American Roentgen Ray Society


Vascular Imaging

Decreased Venous Contamination on 3D Gadolinium-Enhanced Bolus Chase Peripheral MR Angiography Using Thigh Compression

Hong Lei Zhang1, Bernard Y. Ho1, Minh Chao1, K. Craig Kent1, Harry L. Bush1, Peter L. Faries1, Alan I. Benvenisty2 and Martin R. Prince1

1 Cornell MRI, Weill Medical College of Cornell University, 416 E 55th St., New York, NY 10022.
2 Department of Surgery, Columbia University College of Physicians and Surgeons, 630 W168 St., New York, NY 10032.

Received October 29, 2003; accepted after revision March 16, 2004.

 
Address correspondence to H. Zhang (hoz2005{at}med.cornell.edu).


Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. We evaluated the potential for improving bolus chase peripheral MR angiography in patients with fast arterial flow using thigh compression to prevent venous contamination.

SUBJECTS AND METHODS. We performed bolus chase peripheral MR angiography in 32 consecutive patients in whom the travel time for a contrast agent to reach the popliteal artery trifurcation was less than 25 sec. Thigh compression was applied by a tourniquet (n = 13) or blood pressure cuff inflated to 60 mm Hg (n = 19). We compared the results with those of 36 consecutive patients who underwent angiography without thigh compression. The effect of thigh compression on arterial flow and tissue enhancement was assessed in patients with symmetric travel time in both legs by applying compression to one leg during the time-resolved 2D-projection MR angiography with 6 mL of gadolinium. On 3D bolus chase MR angiography, thigh compression was applied bilaterally. Venous contamination on the 3D images of the calf was graded as 0, none; 1, trace; 2, mild; 3, moderate; and 4, severe. Signal-to-noise ratio was measured in the popliteal artery.

RESULTS. Thigh compression slowed the arterial travel time by a mean ± SD of 4.7 ± 2 sec (p < 0.001) with a blood pressure cuff and 3.1 ± 1 sec (p < 0.001) with a tourniquet. Blood pressure cuffs reduced the score of venous contamination on the calf station from 1.9 to 0.4 (p < 0.05) for intermediate flow (contrast travel time, 20–25 sec) and from 2.5 to 0.9 (p < 0.05) for fast flow (< 20 sec). Thigh compression increased the popliteal artery signal-to-noise ratio (81 vs 52, p < 0.001).

CONCLUSION. Thigh compression with blood pressure cuffs inflated to 60 mm Hg slows down arterial flow, increases arterial signal-to-noise ratio, and reduces venous contamination on 3D gadolinium-enhanced bolus chase peripheral MR angiography.


Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Bolus chase peripheral MR angiography is revolutionizing the diagnosis of peripheral vascular disease [16]. With a single bolus injection of gadolinium, this technique provides contrast arteriography from the abdominal aorta down to the ankles without the risks of ionizing radiation, iodinated contrast material, or arterial catheterization. However, one important limitation has been the difficulty in scanning fast enough with MRI to keep up with the rapid flow of contrast material down the legs [7]. Patients with fast flow tend to have venous enhancement in the third station of a bolus chase peripheral MR angiogram [8, 9]. Excessive venous enhancement obscures arteries and limits diagnostic utility of this MR angiographic technique.

Tourniquets are commonly used in extremities to reduce arterial and venous flow [10]. Tourniquets can be applied lightly to occlude only venous flow or more tightly to reduce or arrest arterial flow. A tight tourniquet that narrows arteries can interfere with the assessment of peripheral vascular disease. However, a tourniquet applied lightly arrests only the venous flow without creating arterial pseudostenoses. Blood pressure cuffs can be used in preference to tourniquets to apply a more reproducible amount of compression over a longer length of leg [11, 12].

The purpose of this study was to determine if thigh compression applied with a typical pressure used for suppressing venous flow can reduce venous contamination on the third station of a bolus chase peripheral MR angiographic examination and to evaluate the relative benefits of using tourniquets versus blood pressure cuffs for this purpose.


Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Patients
From February 23, 2003, to October 10, 2003, 98 consecutive patients underwent bolus chase peripheral MR angiography. For all patients, the time for the contrast material to reach the popliteal artery trifurcation was determined on time-resolved 2D-projection MR angiography using an initial 6-mL gadolinium bolus. Patients with slower flow (i.e., contrast travel time to the trifurcation ≥ 25 sec) were considered unlikely to benefit from thigh compression. In our experience, these patients had no venous contamination even without compression, and accordingly they were excluded from further evaluation of thigh compression. The remaining patients with faster flow (i.e., contrast travel time to the trifurcation < 25 sec) were assigned to one of three groups as follows: group 1, no thigh compression (patients studied from February 23, 2003, to June 24, 2003); group 2, thigh compression with tourniquets (from June 25 to July 25, 2003); and group 3, thigh compression with blood pressure cuffs (from July 26 to October 10, 2003). Demographic details of these three groups of patients are listed in Table 1. This study was approved by the local institutional review board.


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TABLE 1 Demographic Data for 68 Patients with Contrast Travel Time to Popliteal Artery Trifurcation < 25 Sec

 

MRI Techniques
The peripheral MR angiographic examination consisted of time-resolved 2D-projection MR angiography of the calf and then the feet using the head coil followed by 3D bolus chase MR angiography of three overlapping stations covering from supraceliac abdominal aorta to the ankles [1315]. Imaging was performed on a 1.5-T MRI system (Signa EXCITE, GE Healthcare). Gadolinium (Magnevist, Berlex) was injected manually by the same experienced nurse in all patients via a 22-gauge angiocatheter (SmartSet, TopSpins) with a tubing system that allowed automatic switching between the gadolinium contrast injection and saline flush as well as easy reloading of the saline flush for the three injections. The injection rate was approximately 2 mL/sec.

Time-resolved 2D-projection MR angiography.—A spoiled gradient-echo sequence was used with the following parameters: TR/TE, 9/1.9; flip angle, 70°; matrix, 256 x 192; field of view, 38 cm; volume thickness, 60–120 mm; number of excitations, 1; and bandwidth, 16 kHz. Thirty sequential images were acquired at 2 sec per frame to display the trifurcation using the head coil for signal transmission and reception with bolus injection of 6 mL of gadolinium. An image obtained before the arrival of the contrast material (visually identified on unsubtracted images) was used as the mask for complex subtraction from the subsequent image data. Then the head coil was moved down to image the feet at 3 sec per frame using similar parameters and another bolus injection of 6 mL of gadolinium.

Three-dimensional bolus chase MR angiography.—A multiphase 3D spoiled gradient-echo sequence with dynamic k-space sampling was used for the 3D bolus chase MR angiographic acquisition using a 48-cm long-bone phased-array coil (ICG Medical Advances) for signal reception at the calf station and body coil for the proximal and thigh stations. Forty-eight milliliters of gadolinium was injected manually with 40 mL of saline flush. The first station was timed with fluoroscopic triggering, and data were acquired with sequential ordering of k-space during 19 sec of breathholding. Using fluoroscopic monitoring of the abdominal aorta in a sagittal oblique plane, the operator activated the trigger as soon as contrast material appeared convincingly on two consecutive frames. During a 4-sec pause, the patient was instructed to take in a deep breath and hold it before the 3D MR angiographic scanning began. The second station was timed at 12–14 sec with elliptical centric ordering of k-space. The third station also used elliptical centric ordering of k-space, which guaranteed that the lowest order k-space coefficients were indeed collected at the beginning of acquisition, and acquisition time was 35–40 sec depending on the number of slices. The minor variations in total third-station scanning time did not affect the center of k-space acquired at the beginning of the third station and thus were believed to be unlikely to affect venous enhancement. The scanning parameters were TR range/TE, 4.4~4.6/1.1; flip angle, 35°; field of view, 48 cm; slice thickness, 2–4 mm with zero filling down to 1–2 mm; number of excitations, 1; and bandwidth, 62.5 kHz. The matrix was 512 x 160 for the first station, 512 x 160 for the thigh, and 512 x 320 for the calf.

Thigh Compression
Thigh compression was applied as proximally as possible on the thigh. Initially, tourniquets were used to indent skin by 5 mm. Because tourniquets could not be applied remotely and produced an inconsistent degree of thigh compression, we subsequently used two blood pressure cuffs inflated to 60 mm Hg on both legs. The long blood pressure cuff tubing and extra connections caused slow air leakage. Cuff pressure was monitored during scanning, and puffs of air were applied to maintain an inflation pressure of 50–60 mm Hg when the pressure drifted down.

Study Design
The effect of thigh compression was studied in group 2 and group 3 patients by applying thigh compression to only the right leg during time-resolved 2D-projection MR angiography of the trifurcation. To avoid confusion with asymmetric flow caused by disease, we performed time-resolved 2D-projection MR angiography of the feet without compression, and patients with differential contrast travel times were excluded, which eliminated the possibility of differential contrast travel time to the trifurcation caused by lesions at the feet such as ulceration and cellulitis [7]. Although it is possible that bilateral occlusive disease at different levels could still create differential contrast travel times to the trifurcation but symmetric contrast arrival at the feet, these effects would tend to average out between right and left legs.

On the subsequent 3D bolus chase MR angiography, compression was initiated just before the unenhanced mask was acquired so that several minutes elapsed between initiation of thigh compression and initiation of arterial phase imaging. Applying compression before the mask was acquired helped to minimize motion between the mask and arterial phase images.

Image Analysis
The MR angiographic data were analyzed on a computer workstation by two radiologists who were blinded to all clinical information. These two radiologists reviewed the time-resolved 2D-projection MR angiographic images to determine the contrast arrival time to the trifurcation and ankle (on the basis of visualization of the contrast material arriving at the specific arteries) and to grade the venous contamination on the third-station imaging as follows: 0, none; 1, trace contamination; 2, mild contamination but fully diagnostic image quality; 3, moderate contamination with limited diagnostic image quality; and 4, severe contamination with nondiagnostic image quality. Signal-to-noise ratio versus time was determined for the popliteal artery and soft tissues (background) using a region-of-interest technique on time-resolved 2D-projection MR angiography. On the 3D source images, signal-to-noise ratio was measured in the popliteal artery, popliteal vein, and subcutaneous vein (if seen). Contrast-to-noise ratio ([signal in artery – signal in tissue] / noise) was measured relative to subcutaneous fat and muscle. The SD of the signal in the air outside the patient was used as noise for the calculation.

The visibility of small arteries was evaluated by determining the arterial branch order visualized for the third station of the 3D bolus chase examination. Each calf was treated independently because the visualization of vasculature could vary between right and left calves. The popliteal artery was designated as first order. Anterior tibial, posterior tibial, and peroneal arteries were second order, and their branches were third order.

Data Analysis
In patients with identical contrast travel times to the left and right ankles, the paired Student's t test was performed to determine the statistical significance of differences in contrast travel time between legs with and without thigh compression in each patient on the time-resolved MR angiography. For all the patients in the three groups, differences in venous contamination, branch order visualization, and popliteal artery signal-to-noise ratio and contrast-to-noise ratios of patients with and without venous compression on the third station of 3D bolus chase MR angiography were also evaluated using the Student's t test assuming unequal variances.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Overall, 30 of the 98 consecutive patients were identified on time-resolved 2D-projection MR angiography as having a slow arterial flow rate, with contrast travel time to the trifurcation of 25 sec or longer. For these patients, the average venous contamination score was 1.0 without any compression. These patients were considered unlikely to have venous contamination even though no thigh compression was applied and were excluded from further evaluation. In the remaining 68 patients, 36 were studied without thigh compression (group 1) and 32 were in groups 2 and 3 with thigh compression applied by either tourniquets (n = 13) or blood pressure cuffs (n = 19).

Effect of Compression on Contrast Travel Time
Seven patients (two in group 1, one in group 2, and four in group 3) were identified as having differential contrast travel times longer than 3 sec (one frame) between right and left ankles on time-resolved 2D-projection MR angiography of the feet. These patients were excluded from the assessment of the effect of thigh compression on contrast travel time. In group 1 (no compression), the mean difference ± SD of travel time between right and left legs was 0.2 ± 1 sec, with no statistical difference (p = 0.4). Blood pressure cuff compression slowed the contrast arrival time at the trifurcation by 4.7 ± 2 sec (p < 0.001) compared with the contralateral leg without compression, whereas tourniquets slowed contrast arrival by only 3.1 ± 1 sec (p < 0.001) (Table 2 and Figs. 1A and 1B).


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TABLE 2 Effect of Thigh Compression on Contrast Travel Time to Popliteal Artery Trifurcation and Time to Soft-Tissue Enhancement (sec)

 


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Fig. 1A. 67-year-old man with claudication. Time-resolved 2D-projection MR angiogram obtained with blood pressure cuff on right thigh shows contrast travel time of 16 sec (s) to left popliteal artery trifurcation without compression and travel time of 24 sec to right popliteal artery trifurcation with compression. Note at 22 sec, muscle enhancement is seen on left side but not on right side with thigh compression. At 60 sec, right calf shows much less soft-tissue enhancement than left calf.

 


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Fig. 1B. 67-year-old man with claudication. Three-dimensional bolus chase peripheral MR angiography shows high signal-to-noise ratio and no venous contamination with third-order branch visualization. Patient had symmetric travel time to ankle despite asymmetric occlusive disease.

 

Popliteal artery and soft-tissue enhancement curves averaged for all patients who had compression applied by blood pressure cuffs (n = 15) are shown in Figure 2. Blood pressure cuff compression delayed (by approximately 6 sec) and broadened the arterial peak and substantially suppressed background tissue enhancement for the entire duration of 2D imaging. Thigh compression decreased peak arterial enhancement by only 13% versus a 35% decrease in peak soft-tissue enhancement. Veins were not well seen on the 2D-projection MR angiography, which precluded quantifying venous enhancement. However, it was the impression of the observers that the relative suppression of venous enhancement with thigh compression was similar for the deep and superficial veins.



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Fig. 2. Arterial and soft-tissue enhancement curves averaged for all patients with compression applied by blood pressure cuff (n = 15) showing right leg with compression (dashed lines) and left leg without compression (solid lines). To correct for temporal differences, we shifted time axis to define 2 sec before contrast arrival at left popliteal artery trifurcation as 0. Note that blood pressure cuff compression delays arterial peak and substantially suppresses background-tissue enhancement for entire duration of imaging. {blacktriangleup} = artery with compression, {blacksquare} = artery without compression, • = tissue with compression, {diamondsuit} = tissue without compression.

 

Effect of Thigh Compression on Venous Contamination and Signal-to-Noise Ratio
Calf venous enhancement scores are shown in Table 3. Patients were categorized as having fast flow (contrast travel time to trifurcation < 20 sec) or intermediate flow (contrast travel time to trifurcation of between 20 and 25 sec). No reduction in venous enhancement was seen in patients with fast flow when tourniquets were used (Figs. 3A, 3B, and 3C). Blood pressure cuff compression reduced venous enhancement for patients with both fast and intermediate rates of flow. When blood pressure cuffs were used, the mean venous contamination score on the calf station decreased from 1.9 to 0.4 (p < 0.05) for intermediate flow and from 2.5 to 0.9 (p < 0.05) for fast flow.


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TABLE 3 Reduction in Venous Enhancement in the Calf with Thigh Compression

 


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Fig. 3A. Calf stations of 3D bolus chase MR angiography in patients with fast rate of flow (contrast travel time to popliteal artery trifurcation, < 20 sec (s). Contrast travel time to trifurcation on time is shown on each image. On time-resolved 2D-projection MR angiograms obtained without thigh compression, all patients show some venous contamination.

 


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Fig. 3B. Calf stations of 3D bolus chase MR angiography in patients with fast rate of flow (contrast travel time to popliteal artery trifurcation, < 20 sec (s). Contrast travel time to trifurcation on time is shown on each image. Time-resolved 2D-projection MR angiograms were obtained with thigh compression applied by tourniquets (B) and blood pressure cuffs (C). Note that least soft-tissue enhancement and venous contamination occurs with subsystolic thigh compression applied by blood pressure cuffs.

 


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Fig. 3C. Calf stations of 3D bolus chase MR angiography in patients with fast rate of flow (contrast travel time to popliteal artery trifurcation, < 20 sec (s). Contrast travel time to trifurcation on time is shown on each image. Time-resolved 2D-projection MR angiograms were obtained with thigh compression applied by tourniquets (B) and blood pressure cuffs (C). Note that least soft-tissue enhancement and venous contamination occurs with subsystolic thigh compression applied by blood pressure cuffs.

 

The popliteal artery signal-to-noise ratio and contrast-to-noise ratio (compared with those of fat and muscle) were 50% higher (p < 0.05) in patients with thigh compression, presumably reflecting an improvement in bolus timing with the slower flow (Table 4).


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TABLE 4 Measurements of Popliteal Artery Signal-to-Noise and Contrast-to-Noise Ratios

 

Branch order visualization (relative to popliteal arteries such that visualization of the anterior tibial artery was second order) for patients without compression, with compression by tourniquets, and with compression by blood pressure cuffs was graded 2.7, 2.9, and 3.2, respectively, on the same scale used to grade venous contamination. The difference between patients without compression and those with compression applied by blood pressure cuffs was statistically significant (p < 0.001). In all 15 patients with compression applied by blood pressure cuffs, all second-order branches of the popliteal artery were visualized in their entirety.


Discussion
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Bolus chase MR angiography improves imaging of peripheral vascular disease because it allows a single contrast bolus to be imaged multiple times for high arterial signal-to-noise ratio as it progresses down the legs [16]. Sharing the bolus on bolus chase MR angiography allows more gadolinium to contribute to arterial signal-to-noise ratio at each station. However, in practice, it has been virtually impossible to acquire MRI data and move the scanner table fast enough to keep up with the flow of contrast material down the legs (typically 5 sec per station) [7]. These data from 19 patients show that subsystolic thigh compression to 50–60 mm Hg with a blood pressure cuff slows down arterial flow and arrests venous flow, improving bolus timing and bolus sharing for the calf station and resulting in higher arterial signal-to-noise ratios with virtually no venous contamination.

Data from unilateral thigh compression during time-resolved MR angiography show that the contrast arrival time to the trifurcation is delayed by an average of 3.1 sec with an elastic tourniquet and 4.7 sec with blood pressure cuffs inflated to 50–60 mm Hg. Contrast travel time from the common femoral artery to the popliteal artery reported in the literature is 5 sec [7]; therefore, the tourniquet slows the travel time from the common femoral artery to the popliteal artery by 62% (3.1 / 5 sec), and subsystolic inflation of thigh blood pressure cuffs slows travel time by 94% (4.7 / 5 sec). The improved sharing of the gadolinium contrast bolus between stations presumably results in better correlation of peak arterial enhancement with the center of k-space and correspondingly increases the arterial signal-to-noise ratio.

Time-resolved MR angiography also revealed suppression of soft-tissue enhancement ipsilateral to thigh compression lasting more than 40 sec after the arrival of contrast material in the popliteal artery. This suppression corresponded to the virtual elimination of venous contamination in the calf with blood pressure cuff compression of the thigh compared with venous enhancement that occurred in nearly every patient imaged without thigh compression. We hypothesize that improved venous suppression is due to engorgement of veins with blood before the injection of gadolinium so that when the contrast material eventually arrives in peripheral veins, it is rapidly diluted. If our hypothesis is correct, it would explain why the improvement is so dramatic but the effect on travel time is so minor.

Elastic tourniquets are easy to obtain and apply. They do not loosen during the study, and they do not interfere with positioning of the legs. However, the degree of indentation is hard to control, leading to inconsistent compression. Tourniquets on one patient with intermediate travel time resulted in grade 4 venous contamination on both calves because the tourniquets were knotted too loosely. Data in our study show that another important limitation of tourniquets is that there is no benefit in patients with fastest rate of flow.

The application of the blood pressure cuff created some difficulties. At least 12 feet of coiled extension tubing was required for the inflation bulb and pressure gauge so that monitoring inflation pressure with periodic extra puffs of inflation could be performed conveniently from outside the magnet. Cuffs had to be inflated before the acquisition of the unenhanced mask run to ensure there was no motion between the mask and arterial phase images. Also, venous obstruction lasting several minutes was necessary to attain sufficient venous engorgement. The scanning volume had to be positioned more anteriorly to the superficial femoral artery relative to the position on the localizer image because the artery was lifted 1–2 cm anteriorly by the inflated cuffs. Subtraction of the mask from the enhanced images was not always perfect because of air leakage and minor movement of the thigh, especially for the thigh station images. Setting up and inflating the blood pressure cuffs prolonged the total scanning time, but compared with the improvement in the image quality these shortcomings are deemed acceptable.

Subsystolic inflation pressure of 60 mm Hg was chosen to arrest venous flow without causing arterial compression that could simulate a false stenosis or occlusion. The actual pressure during scanning was less than 60 mm Hg because of slow air leakage at multiple tubing connections. However, periodic puffs of air were given to maintain the inflation pressure above 50 mm Hg. This level of inflation pressure was chosen on the basis of prior work of Bilecen et al. [11] and Herborn et al. [12], who reported improved bolus chase MR angiography with inflation pressures of 40 and 50 mm Hg, respectively.

Our data confirm the observations of both of these groups of investigators as well as those of Meaney and Prince [10], who all found improved bolus chase MR angiography with the application of thigh compression. It is impossible to exclude the possibility that some small vessels were compressed by the inflated blood pressure cuff. There is also the theoretic possibility that lowering the perfusion pressure of the leg may reduce the diameter of all arteries. However, our observation of greater branch vessel visualization with subsystolic thigh compression applied by blood pressure cuffs suggests that this possibility is not a concern. Perhaps the improved visualization of smaller vessels results from the delay and broadening of the bolus. The longer bolus allows the high-spatial-frequency MR angiography data to be acquired while a higher arterial gadolinium concentration is in the small arteries. Improving the quality of the high-spatial-frequency data likely improves visualization of smaller arteries, thereby improving branch order visualization.

Inflation to supraarterial pressure to completely arrest flow has been reported for upper extremity MR angiography [17]. This technique was considered to be impractical in the legs because the need to image arteries in the region of the blood pressure cuff would have resulted in pseudostenosis. Additional potential problems are presented by the compression of calcified femoral arteries in patients with diabetes and by the underdistention of distal arteries with reduction of inflow pressure.

Use of manual injection introduces a potential bias if the injection is not exactly identical for calf, foot, and bolus chase acquisitions. This potential bias cannot be entirely eliminated with the use of power injectors because all power injectors are activated manually. However, the comparison of contrast travel times between legs with and without compression is not affected because both legs were simultaneously studied with the same injection. Another potential limitation of hand injection is that an inconsistent injection rate may interfere with signal-to-noise ratio assessments for the 3D bolus chase MR angiography. We have noticed that our power injectors may also have inconsistent injection rate depending on the IV resistance. Although power injection is routinely used for one- or two-injection examinations [18, 19], it may pose difficulties for multiinjection examinations (such as the one used in this study) in which the power injector does not hold sufficient saline flush for all three injections. Disconnecting the power injector tubing creates the potential risk of introducing an air embolism. Our hand injection system included automatically closing valves that prevented fluid movement and air embolisms when syringes were disconnected for reloading.

Another limitation to consider is that applying thigh compression alters the hemodynamics such that time-resolved information is no longer accurate. Accordingly, thigh compression is not recommended when performing time-resolved peripheral MR angiography.

Slowing the arterial flow and preventing venous contamination in the calf opens opportunities for further improvements that have not yet been explored. In particular, the elliptical centric ordering of k-space acquisition for the third station used in this study allows longer data acquisition with higher resolution [20]. Perhaps 1024 x 1024 matrix acquisition will be possible once the scanner software is modified to allow such high resolution. Combining this technique with a parallel-imaging technique would allow even higher resolution to take advantage of the higher signal-to-noise ratio obtained from faster contrast injection rates and better sharing of the bolus among stations [12, 21, 22].


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

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