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1
Department of Clinical Radiology, Klinikum der LMU, Großhadern,
Marchioninistr. 15, 81377 München,
Germany.
2
Department of Surgery, Klinikum der LMU, Großhadern, 81377
München, Germany.
3
Siemens AG, Medizintechnik, 91052 Erlangen, Germany.
Received January 28, 2000;
accepted after revision April 13, 2000.
Address correspondence to A. Huber.
Abstract
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SUBJECTS AND METHODS. Twenty-four patients with peripheral arterial occlusive disease underwent digital subtraction angiography and were examined on a 1.5-T MR scanner. The transit time for contrast material was determined with a test bolus injection. A T1-weighted three-dimensional gradient-echo sequence with short TR and TE was used for a dynamic measurement at the level of the iliac arteries, the upper leg, and the lower leg arteries. For each level a single dose of gadolinium was injected into an antecubital vein with an MR power injector. Maximal-intensity-projection reconstructions were calculated after subtraction of the first measurement at each level. Two experienced MR radiologists who were unaware of the digital subtraction angiography results interactively evaluated both the MIP reconstructions and the single slices on a workstation, first independently and then in a consensus interpretation.
RESULTS. With digital subtraction angiography, 80 hemodynamically significant stenoses and 39 occlusions were detected. For the stenoses and occlusions, a sensitivity of 100% was found for MR angiography. The specificity for the assessment of stenoses and occlusions was 98% and 94%, respectively, for the iliac arteries; 98% and 94%, respectively, for the upper leg arteries; and 94% and 95%, respectively, for the lower leg arteries. Most false-positive findings of occlusion were due to metal stents present in the iliac (n = 3) and upper leg (n = 4) arteries.
CONCLUSION. The MR imaging technique that we used revealed the arteries from the distal aorta to the ankle and proved to be reliable at showing arterial stenoses and occlusions.
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To accomplish imaging of the peripheral vascular tree, time-of-flight (TOF) techniques [5] and phase-contrast MR angiography [6] have been used. However, both methods are time-consuming, especially if a field of view from the level of aortic bifurcation to the distal lower leg is to be covered. Another disadvantage of TOF techniques and phase-contrast MR angiography is the tendency to overestimate the degree of stenosis because both are flow-related techniques [6].
Gadolinium-enhanced three-dimensional gradient-echo MR angiography is known as a useful and accurate technique in imaging of the aorta and the iliac arteries [7, 8]. However, the field of view is restricted to a maximum of 40-50 cm. The dose of gadolinium used for contrast-enhanced MR angiography varies among studies. Some investigators used a one and one half to a double dose of gadolinium [7,8,9,10], whereas Sueyoshi et al. [11] and Lee et al. [12] used only a single or even lower dose of gadolinium per region. Using a dynamic manual table translation, it was possible to cover the entire aorta and iliac arteries [13] or the peripheral vascular tree [14]. Ho et al. [15] used moving-bed infusion tracking MR angiography (Mobitrak; Philips Medical Systems, Da Best, The Netherlands) to visualize the peripheral vascular tree with a single high-dose gadolinium bolus [15].
The aim of our study was to use gadolinium-enhanced MR angiography with a dynamic measurement at three levels (iliac region, upper leg region, and lower leg region) to visualize the major arteries from the aortic bifurcation to the ankle joint and to compare the results with those of digital subtraction angiography. For each level a small single dose of gadolinium bolus was used. Potential advantages of this imaging procedure compared with moving-bed MR angiography are the ability to use a phased array coil in all regions, especially in the lower leg arteries [16]; the possibility to use this imaging technique with a standard MR imaging system without a moving-bed option or a prototype coil concept; and the possibility to detect enhancement of peripheral arteries with delay on one side. To our knowledge, little has been reported in the current literature about a step-by-step technique of imaging the iliac and leg arteries that was described by Yamashita et al. [16] and Sueyoshi et al. [11].
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Conventional Angiography
In all patients, conventional angiography was performed with an
angiographic unit (Integris 3000, Philips Medical Systems) with a programmable
moving table and a digital subtraction technique. The matrix was 1024 x
1024 and the field of view was 380 cm. A power injector was used for
administration of an iodinated contrast material, iopamidol (Solutrast 300;
Bracco Byk Gulden, Konstanz, Germany). The flow rate was 15 mL/sec and a dose
of 125-200 mL was administered to each patient. All angiographic procedures
were supervised by experienced vascular radiologists. Conventional angiography
was performed by puncturing the common femoral artery and placing the tip of a
4-French pigtail catheter in the distal aorta above the bifurcation. Both legs
were examined in all patients by a nonselective injection in the distal aorta.
The posterior—anterior views were obtained at all levels by digital
subtraction angiography. Oblique views were obtained in the pelvic region in
all patients and, when necessary, in the proximal upper leg (five patients).
The results were documented on hard copies.
The results were assessed twice, first independently and then with a consensus interpretation, by two vascular radiologists who were unaware of the results of MR angiography. The degree of stenosis was categorized with a 6-point scale (0 = no stenosis, 1 = stenosis with narrowing of diameter of 1-25%, 2 = stenosis with narrowing of diameter of 26-50%, 3 = stenosis with narrowing of diameter of 51-75%, 4 = stenosis with narrowing of diameter of 75-99%, and 5 = complete occlusion). The length of the stenoses was determined on the hard copies by the two observers. For both observers, the mean length of each stenosis measured from the digital subtraction angiography hard copies was compared with the corresponding mean values obtained from the MR angiograms.
MR Angiography
Contrast-enhanced three-dimensional (3D) MR angiography was performed at
three levels: one, the iliac region including the distal aorta and the aortic
bifurcation, the common and external iliac arteries, and proximal parts of the
internal iliac arteries; two, the upper leg region including the common
femoral, superficial femoral, deep femoral, and proximal popliteal arteries;
and three, the lower leg region including the distal popliteal, anterior
tibial, posterior tibial, and peroneal arteries.
For the IV administration of the contrast material gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) via an 18-gauge needle in an antecubital vein, an MR imaging—compatible injector (Spectris; Medrad, Volkach, Germany) with two-phase applications (first, gadolinium; second, saline solution) was used. First, the transit time for contrast material was determined by a test bolus application of 2 mL of gadolinium followed by 20 mL of saline solution with a flow rate of 1 mL/sec. During and after the test bolus injection, a dynamic measurement with a T1-weighted two-dimensional (2D) gradient-echo sequence was performed at the level of the distal abdominal aorta and included 40 consecutive measurements with a repetition time of 1 sec.
The MR imaging examinations were performed with a 1.5-T MR imaging unit (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany). After a multiplanar scout view including six slices was obtained, the 3D MR angiography slab was positioned as required by the vessel anatomy at each level. For the pelvic region, a coronal 3D slab with a field of view of 400 x 350 mm and a thickness of 120 mm was used. The matrix was 512 x 192 and the number of partitions was 30. After a slice interpolation algorithm was applied, 60 slices were calculated. Thus the voxel size was 1.7 x 0.8 x 2 mm3 for the pelvic region. For the upper and lower leg we used a field of view of 500 x 300 mm and a thickness of 90 mm. The matrix was 512 x 185 and the number of partitions was 24. The resulting voxel size was 1 x 1.3 x 1.8 mm3 after slice interpolation. The slab for the upper leg was slightly angulated to cover the proximal superficial femoral artery and the common femoral artery anteriorly and the popliteal artery posteriorly. The slab for the lower leg was strictly coronal. A field of view of 400 or 500 mm was imaged at three stations with a body phased array coil that was designed for a 250-mm field of view. To achieve a sufficient signal-to-noise ratio over a 500-mm field of view, the center of the two anterior coil elements was moved 250 mm upward in relation to the two posterior coil elements. For each region, three consecutive measurements with a T1-weighted 3D gradient-echo sequence (TR/TE, 6.8/2.1; flip angle, 25°) were performed. The first was used for subtraction (mask), the second to visualize the arteries with high contrast during the arterial phase, and the third to detect late enhancement of the arteries. The acquisition time for one measurement was 30 sec for the pelvic region with an interval of 10 sec between each of the three measurements. The acquisition time for one measurement in the upper and lower leg was 24 sec with an interval of 15 sec between each of the three measurements.
The bolus timing was performed with identical delay as determined previously with the test bolus injection in the pelvic region, with an additional delay of 6 sec for the upper leg, and yet another delay of 6 sec for the lower leg. For each level a single dose of contrast material (0.1 mmol/kg) was used. The bolus injection was performed with a flow rate of 1 mL/sec for all regions because we used a smaller dose of contrast material than in previous studies of contrast-enhanced MR angiography [13, 14]. To achieve a sufficient contrast-to-noise (C/N) ratio in spite of the use of only a single dose of gadolinium, a subtraction technique was used before maximal-intensity-projection (MIP) reconstructions were calculated. The first data set was subtracted from the second and third data sets for each level. Twenty MIP reconstructions over a 90° sector (-45° to 45°; 0° is the anteroposterior view) around the body axis were calculated for each subtracted data set.
Evaluation of MR Angiography
The signal-to-noise (S/N) ratio (signal intensity / standard deviation
noise) and the C/N ratio ([signal intensity 1 — signal intensity 2] /
standard deviation noise) were determined for the pelvic region as well as for
the upper and lower leg regions. The mean values of S/N ratio of all patients
were calculated for the first, second, and third measurements at each level.
The C/N ratio values of all patients were determined for the first measurement
taken after gadolinium administration with and without subtraction of the
measurement taken before gadolinium administration on each level to determine
if a subtraction technique was necessary.
Two experienced MR radiologists who were unaware of the digital subtraction angiographic results interactively evaluated both the MIP reconstructions and the single slices on a workstation, first independently and then in a consensus interpretation. The degree of stenosis and occlusion was determined as described for the conventional angiography. Cohen's kappa statistic was calculated to determine the interobserver agreement. The following arterial vessel segments were included for comparison of digital subtraction angiographic and MR angiographic results: distal aorta; common and external iliac arteries; common femoral, superficial, deep femoral, and popliteal arteries; and anterior tibial, posterior tibial, and peroneal arteries. To evaluate the diagnostic accuracy of MR angiography, sensitivity and specificity were calculated for all vessel segments.
In addition, the mean length of each stenosis determined on the MIP reconstructions by two observers was compared with the mean length of each stenosis measured from the digital subtraction angiography hard copies. Spearman's rank correlation coefficient was used to compare the length of stenoses found on digital subtraction angiography with those found on MR angiography.
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Adequate MIP reconstructions were obtained only in the upper and lower leg when a subtraction was performed because the S/N ratio (Fig. 3) of the arteries and the C/N ratio of the arteries and the muscles (Fig. 4) were too low after administration of a single dose of contrast material. However, a high C/N ratio was achieved if first a subtraction and then a MIP reconstruction were performed (Fig. 4). In contrast to the result of subtraction in the upper and lower leg regions, subtraction improves the C/N ratio only slightly in the pelvic region (Fig. 4). However, if a subtraction technique and an additional contrast material are used, the C/N ratio of arteries and muscle is higher in the upper and lower leg than the C/N ratio of arteries and surrounding tissue in the pelvic region (Fig. 4). Therefore, diagnostic MIP reconstructions can be calculated for all three regions.
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With digital subtraction angiography, 12 hemodynamically significant stenoses (with narrowing of >50% of vessel diameter) were found in the iliac arteries, 46 in the upper leg arteries, and 22 in the lower leg arteries. In addition four, 14, and 21 occlusions were detected with digital subtraction angiography, respectively. These results were obtained from a consensus interpretation by two experienced vascular radiologists. In our group of patients, seven metal stents were placed in the iliac (n = 3) and upper leg (n = 4) arteries.
MR angiography was highly sensitive and specific for the detection of hemodynamically significant stenoses (sensitivity, 100%; specificity, 96%) and occlusions (sensitivity, 100%; specificity, 93%) in the arterial vessel segments for both observers (Tables 1 and 2). The consensus interpretation showed no understaging of any stenosis or occlusion. However, six upper leg stenoses and 13 lower leg stenoses were overstaged with a difference of less than 25% of the luminal diameter. Seven false-positive findings of occlusion (three in the pelvic region and four in the upper leg) exceeding a 25% overestimation were due to stent grafts, and two stenoses of the lower leg exceeding an 25% overestimation were not due to stent grafts. Overestimation of the degree of stenosis was more common in the lower leg than in the upper leg or in the pelvic region. Most overestimations were less than 25% (n = 19). Seven of nine overestimations with a degree of more than 25% were caused by metal Stent grafts. The length of stenosis highly correlated (r = 0.93, Spearman's rank correlation) with digital subtraction angiography when the first measurement taken after contrast material administration was evaluated. These results improved slightly when both the first and the second measurements taken after gadolinium administration were evaluated (r = 0.97, Spearman's rank correlation). The mean difference of stenosis length determined with digital subtraction angiography and MR angiography was significantly lower (p < 0.05, Student's t test) when both measurements were evaluated (d = 2.1 ± 1.1 mm) than when only the first measurement taken after gadolinium administration was evaluated (d = 4.2 mm ± 1.3 mm). Most false-positive findings of occlusion were caused by stent artifacts (n = 7), and only three and four false-positive stenoses were found by observers 1 and 2, respectively, that were not caused by stent artifacts. Two of these false-positive stenoses were probably found because additional views of MR angiographic MIP reconstructions enabled their identification, whereas they were not detected with digital subtraction angiography because they were hidden behind other arteries. Four false-positive findings of occlusion were found, and five stenoses were missed when only the first measurement taken after gadolinium administration was used for the analysis of the MR angiographic results. However, the five stenoses were found by both observers, and the four false-positive findings of occlusion were not identified when both measurements taken after gadolinium administration were included in the evaluation.
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Decisions for treatment based on the results of digital subtraction angiography were consistent with those based on the results of MR angiography in 23 of 24 patients. In one patient, digital subtraction angiography revealed a mild stenosis (<50%) in the external iliac artery. With MR angiography, however, this stenosis was slightly overestimated as a hemodynamically significant stenosis. Balloon dilatation would have been considered if only the results of MR angiography had been taken into account.
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For imaging the distal runoff arteries in patients with peripheral vascular disease, a phase-contrast rephase or dephase with a subtraction technique has been used [25]. This sequence was found to be superior in comparison with 2D TOF MR angiography. But for each anatomic area, an acquisition time of more than 9 min was necessary. To determine the most suitable vessel for distal anastomosis, the score for MR angiography and digital subtraction angiography agreed in 155 of 198 vessel segments. In this study the sensitivity and specificity for the detection of hemodynamically significant stenosis compared with digital subtraction angiography were not mentioned. Vosshenrich et al. [26] compared contrast-enhanced and TOF MR angiography in the same patients and found that all 160 vessel segments in 20 patients were visualized on contrast-enhanced MR angiography, but only 142 on TOF MR angiography in the lower leg. In addition, the image quality was superior for contrast-enhanced MR angiography, and the grading of stenoses was more accurate with contrast-enhanced MR angiography than with TOF MR angiography. The two major problems with 2D TOF MR angiography when imaging diseased tortuous distal vessels are failure to show in-plane flow and distal signal loss [27]. A more accurate grading of stenosis is possible with contrast-enhanced techniques compared with flow-sensitive MR angiography because poststenotic flow voids, caused by turbulent flow, lead to an overestimation of the degree of stenosis in flow-sensitive techniques [6, 27].
Contrast-Enhanced MR Angiography
Contrast-enhanced MR angiography can be performed during breath-holding
[28] and allows for
subtraction of an unenhanced data set from a postgadolinium data set
[29]. Previous studies showed
that contrast-enhanced MR angiography of the peripheral vascular tree can be
performed with a moving-bed infusion tracking or a dynamic manual table
translation during a single bolus injection
[13,
16,
30]. These techniques can
solve the MR angiography problem of a limited 40- to 50-cm field of view.
However, the moving table technique has several shortcomings.
First, the interval between the unenhanced measurements and the gadolinium-enhanced measurements is longer with a moving-table technique than with a dynamic measurement at each level. Motion artifacts may lead to inaccurate subtraction results, especially in patients with peripheral arterial occlusive disease, who may be uncooperative as a result of cerebral atherosclerotic disease [31]. Second, with a moving-bed technique, the body coil has to be used for two or three regions if no dedicated coil system is available. However, for the lower leg with a small vessel diameter, a phased array body coil is advantageous to achieve a higher S/N ratio with a single dose of contrast material. An alternative method is the use of a dedicated coil system [15], but this generates additional costs and is not available for all standard MR imaging systems. Finally, not all MR imaging systems allow an individual positioning of the 3D slab for each region with a moving-bed examination. Thus wraparound artifacts may hamper the diagnostic accuracy in the pelvic region if a narrow field of view is used. If a large field of view is used, the spatial resolution in the upper and lower leg is reduced or the acquisition time is prolonged [15].
The delay time for the gadolinium bolus from one level to the next can vary from patient to patient. Thus a fixed imaging delay after contrast injection may be inadequate for some of the patients with peripheral arterial occlusive disease, who may also have variable cardiac output due to, for example, ischemic heart disease. Therefore, we used a test bolus injection at the first level to adapt the bolus timing individually. If the delay time between the first and second level is not correct, the second measurement can show a late enhancement of artery segments, and the delay time between the second and third level may be corrected, if necessary. We used a break of 15 sec between each measurement instead of 10 sec in the leg arteries because the acquisition time is shorter in the upper and lower leg (24 sec) compared with the pelvic region (30 sec) because a thinner slab was used in the leg arteries. Moreover, the transit time varies more in the distal arteries than in the pelvic region, where we used a test bolus to determine the transit time.
The dynamic measurement at each level, as used in our study, includes the possibility to detect late enhancement of arteries supplied by collateral arteries or severely stenosed proximal arteries, which may cause time-dependent side different enhancement. Diagnostic accuracy concerning the sensitivity, degree of stenosis, and length of stenosis was improved by the second measurement taken after administration of gadolinium. The main reasons were mistiming because of late enhancement of arteries, a noisy first measurement after gadolinium, completely unenhanced artery segments during the first measurement taken after administration of gadolinium, and reversed arterial flow with delay after occlusions.
Wang et al. [32] investigated a timing algorithm for bolus chase MR angiography. They found variable bolus velocities of 3-4 cm/sec, which were different for the left and right legs. However, our experience in previously examined healthy volunteers and a small number of patients suggests that the bolus velocity, determined after the same injection rate (1 mL/sec) that Wang et al. used, is faster than that found by Wang et al. The results of our study show that the additional delay of 6 sec from station to station seems to be adequate.
The moving-bed infusion tracking uses a fixed timetable for imaging the consecutive anatomic regions. In addition, the acquisition time for each level, usually 20 sec or more, is longer than the bolus first-pass from level to level. Especially in the distal lower leg, deep veins can be enhanced when a moving-table technique is used [10]. The C/N and S/N measurements (Figs. 3 and 4) show how the enhancement of the deep veins was managed in our study. The mean values of the venous S/N ratio increase from proximal to distal. At the third level, the values during the mask and the second measurement are similar to those found for the arteries during the second measurement at the first level (Fig. 4). However, when the deep veins, already enhanced during the mask at the second and third level, are subtracted from the measurements taken after gadolinium administration, a high C/N ratio can be achieved, especially for the upper and lower leg (Fig. 3). The advantage of a subtraction at the pelvic region is not as clear as that for the legs because nearly no venous enhancement occurs (only test bolus previously injected) in the mask and movement of the bowel and respiratory artifacts decrease the quality of the subtraction results.
Earls et al. [13] investigated the S/N ratio for two consecutive measurements in the aorta and the proximal peripheral arteries. These researchers found that the second measurement showed a higher S/N ratio for the arteries, veins, and muscle, but the image quality of the second angiograms did not differ significantly from the first ones. We also did not find a disadvantage associated with an enhancement of the veins and the muscles in the second or third regions. Both the deep veins and the muscles were already enhanced before the first measurement was performed at each level. However, it was possible to subtract the already enhanced structures, and the subtraction results were similar to that obtained from the first region.
A step-by-step technique at three levels, as suggested by Yamashita et al. [16], allows the use of a field of view that includes the iliofemoral arteries from the distal aorta to the lower knee. In this study, the contrast material injection was performed by hand. A 0.2-mmol/kg dose was used for the pelvic region and a dose of only 0.05 mmol/kg was used for the upper leg and knee region. We used a lower dose in the pelvic region and a higher dose in the upper and lower leg (0.1 mmol/kg) to visualize the arteries in the distal lower leg. Future studies with larger subject populations should investigate whether a reduction of the gadolinium dose to 0.05 mmol/kg is possible in the upper and lower leg arteries to visualize the distal lower leg arteries. A slow injection rate and the use of an MR injector that provides a defined infusion rate may help to achieve a high contrast within the vessel lumen over the acquisition time when a small bolus is used.
A step-by-step technique with a body coil at two levels was used by Winterer et al. [33]. They used a fixed delay for contrast material injection at the upper and lower regions. However, the distal lower leg could not be included in the field of view. Moreover, the body coil leads to a lower S/N ratio, which is especially disadvantageous in the distal lower leg where the luminal diameter of the arteries is smaller than in proximal regions. That may be the reason why Winterer et al. did not image the distal lower leg arteries.
A main advantage of the technique we used in our study is that no special equipment, such as special software or coils, is required. In contrast to our imaging technique, many recent advances in MR angiography require costly hardware of software upgrades or custom modifications that are not available for most MR imaging users.
Comparison with Digital Subtraction Angiography
Unlike digital subtraction angiography, contrast-enhanced 3D MR angiography
acquires an entire 3D data set within a short scanning time, allowing a
calculation of projection angiograms from many directions without applying
additional radiation or contrast material. The digital subtraction angiography
is a 2D projection technique, which often requires additional projections or
rotational angiography [34] to
make sure that abnormal findings are not hidden behind overlaying structures.
However, digital subtraction angiography has a superior spatial in-plane
resolution compared with MR angiography. That is why we expect a lower
detection rate of small collateral vessels with MR angiography than with
digital subtraction angiography, but a comparison of both techniques in the
visualization of collateral vessels was not included in this study.
Overestimation of the degree of stenosis with MR angiography is more common in
the lower leg than in the upper leg or in the pelvic region probably because
of the lower vessel diameter in the lower leg arteries.
The triple dose of gadolinium that is necessary for the visualization of the entire peripheral vascular tree down to the ankle joint is a disadvantage of our method because the greater contrast material consumption results in higher costs. On the other hand, hospitalization of a patient is not necessary if digital subtraction angiography can be replaced by MR angiography with IV contrast material application. MR imaging contrast material may become less expensive if higher doses are needed, and digital subtraction angiography may be performed without hospitalization when modern catheters with a small caliber are used [35].
In summary, contrast-enhanced MR angiography of the peripheral vascular tree allows visualization of the major arteries from the distal aorta to the ankle joint with high diagnostic accuracy during short acquisition times. The step-by-step technique can be used on a standard MR system with a strong gradient system without special software or hardware equipment that is necessary for a moving-table technique. A dynamic measurement on each level can provide additional information about late enhancement of arterial vessel segments and improves the diagnostic accuracy of contrast-enhanced MR angiography. Contrast-enhanced MR angiography of the peripheral arterial tree may be used as an alternative imaging technique in patients with renal failure or allergic reactions to contrast material, who cannot be examined with digital subtraction angiography.
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