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Vascular Imaging |
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
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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, 2025 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.
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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.
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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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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, 60120 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 1214 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 3540 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, 24 mm with zero filling down to 12 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 5060 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.
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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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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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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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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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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.
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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 5060 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 12 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].
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