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1 Department of Radiology, Section of Angiography and Interventional Radiology,
University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria.
2 Department of Angiology, University of Vienna, A-1090 Vienna, Austria.
Received October 8, 2001;
accepted after revision March 21, 2002.
Address correspondence to C. Loewe.
Abstract
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MATERIALS AND METHODS. This retrospective report includes 106 patients (45 women, 61 men) with known or suspected peripheral vascular occlusive disease who underwent MR angiography and intraarterial digital subtraction angiography of the peripheral arteries. MR angiography was performed on a 1.0-T unit using a moving-bed technique. Every leg was divided into 14 vascular segments, and severity of disease was scored in four categories. Digital subtraction angiography was the standard of reference.
RESULTS. In the 106 patients, 2378 vessel segments were evaluated
with both imaging modalities. In 2156 segments, MR angiography and digital
subtraction angiography were concordant for stenosis classification, in 188
segments the two modalities differed in one category, and in 24 segments they
differed in two categories. MR angiography achieved sensitivity and
specificity of 96.7% and 95.8%, respectively, for differentiating
nonsignificant from hemodynamically significant stenosis (
= 0.91).
CONCLUSION. This study indicates that MR angiography is an accurate imaging modality in clinical practice. Our data support the concept that MR angiography can modify the diagnosis of suspected peripheral vascular occlusive disease.
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Digital subtraction angiography is the gold standard for imaging, treatment planning, and morphologic follow-up of patients with peripheral vascular occlusive disease. However, digital subtraction angiography is an invasive method that carries the risk of potential allergic reactions and kidney failure as a result of the nephrotoxicity of the contrast material. Furthermore, because peripheral vascular occlusive disease is chronic and progressive, patients must undergo repeated digital subtraction angiography and endovascular interventions; such patients have a cumulative risk for complications resulting from arterial puncture, nephrotoxic effects of contrast agent, and repeated radiation exposure. In addition, digital subtraction angiography is still performed in some centers on an in-patient basis, necessitating at least a 2-day hospital stay. Thus, the need is great for a noninvasive imaging modality that will provide precise delineation of disease severity and optimal treatment planning, and many research groups have attempted to develop an ideal imaging alternative to digital subtraction angiography.
MR angiography has evolved into a feasible noninvasive diagnostic imaging option that has gained widespread clinical acceptance for imaging of the aorta and its major branches [3, 4], the carotid arteries [5, 6], and the pelvis [7, 8]. The limitations of flow-dependent, time-of-flight, phase-contrast MR angiographic sequences, such as long acquisition times and flow-related artifacts, could be overcome with the introduction of gadolinium-enhanced, ultrafast, three-dimensional MR angiography [7, 9,10,11,12]. However, clinical use of this modality for evaluating large vascular systems, such as the vessels of the pelvis and lower extremities, has been hampered by a limited field of view, which necessitates repeated bolus injections, prolonged acquisition times, and increased contrast contamination of surrounding tissue at the second or third imaging acquisition. Recently, a new approach—the moving-bed technique—has been used to image the entire vascular tree from the renal arteries to the ankle in a single contrast bolus injection [13,14,15,16,17]. Thus, background noise, acquisition time, and contrast dose can be minimized. However, data regarding the diagnostic efficacy of this new approach are limited by the small number of patients studied [13,14,15,16,17,18].
The aim of our study was to assess the diagnostic efficacy of contrast-enhanced, moving-bed MR angiography for the detection of peripheral vascular occlusive disease in a large patient cohort using digital subtraction angiography as the standard of reference.
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MR Angiography
All MR angiography was performed on a 1.0-T superconducting magnet
(Gyroscan NT 10; Philips, Best, The Netherlands) using a moving-table
technique (MobiTrak; Philips) and a whole-body coil.
Patients were placed in a feetfirst position with the legs fixed in a dedicated leg support to avoid motion artifacts during imaging. Special care was taken to lift the lower legs to minimize venous and tissue contrast enhancement. With the use of a knee support, the calves hung freely. The isocenter was focused in the middle of the calf.
First, a multistation, two-dimensional turbo-field-echo localizer sequence in three stacks, beginning with the calf, was acquired in the axial orientation. The field of view for each stack was 430 mm, with an overlap of 20 mm between the stacks. Thus, a maximum length of 1250 mm could be imaged by moving the table between the stacks. Scanning parameters were TR/TE, 12/6.9; flip angle, 60°; and slice thickness, 3.3 mm, with an interslice gap of 11 mm. Orthogonal maximum intensity projections (MIPs) for all three stacks were reconstructed automatically.
The arrival time of contrast media bolus was determined in the vessel under consideration. The bolus consisted of 2 mL of paramagnetic contrast material (Dotarem [meglumingadoterat], Guerbet, Roissy, France; or Omniscan [gadodiamide], Nycomed-Amersham, Oslo, Norway) followed by a saline flush of 20 mL (flow, 0.5 mL/sec). For bolus timing, a two-dimensional fast-field-echo axial sequence was performed 2 cm above the aortic bifurcation. Sequence parameters were 12.2/4; flip angle, 40°; field of view, 350 mm; and rectangular field of view, 65%. Fifty dynamic scans were acquired in 1 min 15 sec (1.5 sec per image). Delay between the initiation of contrast administration and scanning was calculated by adding 5 sec to the individual contrast bolus time, which resulted in a mean delay of 38 sec (range, 23-69 sec).
Coronal three-dimensional volumes of the MR angiographic acquisitions were positioned using the sagittal MIPs of the localizer scan. A three-dimensional fast-field-echo sequence in three stacks was acquired using an acquisition matrix of 256 x 128 and a reconstruction matrix of 512. Parameters were 5.1/1.6; flip angle, 40°; and field of view, 430 mm, with an overlap of 20-80 mm depending on patient height. The rectangular field of view was adapted according to patient size and ranged between 75% and 80%. Sixty to seventy slices were acquired with an interpolated slice thickness of 1.5 mm (3.0-mm effective slice thickness). The resulting voxel size was 8.6 mm3 (1.8 x 1.6 x 3.0 mm). Acquisition time was 85-120 sec (mean, 101 sec) for all three stacks.
For MR angiography, unenhanced mask images of the three vascular territories under consideration (aortoiliac, femoropopliteal, and calf) were acquired beginning at the calf level. Then, infusion of 40 mL of paramagnetic contrast material (Dotarem or Omniscan) (0.2-0.3 mmol/kg of body weight) was begun with a flow of 0.5 mL/sec, followed by a saline flush of 20 mL (flow rate, 0.5 mL/sec). Thus, infusion time for the contrast material was 80 sec. At the calculated delay time, scanning of the proximal vessel territory (aortoiliac arteries) was initiated. Table movement among the stacks was performed in 3 sec, and acquisition of the next stack could be started immediately. To minimize tissue and venous enhancement, we chose a centric k-space filling technique for the upper and lower leg.
Mask images were automatically subtracted from the contrast-enhanced images, and orthogonal MIPs of all three stacks were reconstructed immediately, allowing continuous delineation of the arterial tree from the aortic bifurcation to the ankle. Postprocessing time between the end of image acquisition and presentation of three orthogonal subtracted MIPs of every stack took as much as 10 min. Finally, eight coronal MIPs with a rotation angle of 22.5° were reconstructed manually for each stack.
Intraarterial Digital Subtraction Angiography
Catheter angiography was performed with a digital subtraction technique
(Multistar; Siemens, Erlangen, Germany). In 14 patients, digital subtraction
angiography was performed after antegrade arterial puncture, which was planned
according to MR angiographic findings. In these patients, the iliac arteries
were not displayed for comparison. Ten patients were examined after selective
catheterization of the contralateral common iliac artery using a cross-over
maneuver. In these patients, the vascular segments of only one leg were
included in the evaluation. In the other 82 patients, the aortic flush
technique was used. This standard protocol included puncturing the common
femoral artery using a Seldinger technique and advancing a 4-French catheter
into the distal aorta above the aortic bifurcation. In patients with bilateral
weak or absent inguinal pulses (n = 7), a transbrachial approach was
used. A mean total of 150 mL (range, 120-210 mL) of nonionic contrast material
(Optiray 320 [ioversol], Mallinckrodt Medical, Hennef/Sieg, Germany; or
Xenetix 300 [iobitriol], Laboratoire Guerbet, Aulnay-sous-Bois, France) was
injected at a rate of 10 mL/sec using a power injector.
Image Interpretation
Arteriograms of both digital subtraction angiography and MR angiography
were interpreted on conventional films by two experienced vascular
radiologists. The interpreters were unaware of the clinical history and the
results of the other examination, and every reviewer diagnosed only one
imaging modality. The names of the patients were not visible to the
interpreter during image interpretation. For interpretation of MR angiograms,
we evaluated manually reconstructed MIP images (eight projections for each
stack).
The arterial vasculature of the extremities was divided into 14 segments. The common and external iliac; the common and deep femoral; the proximal, medial, and distal parts of the superficial femoral artery; and the P1 segment of the popliteal artery (supragenual) were summarized as thigh vessel segments. The infragenual P2 and P3 segments of the popliteal artery, the tibiofibular trunk, the anterior and posterior tibial arteries, and the fibular artery were summarized as calf vessel segments. The severity of stenosis was graded using a 4-point scale: grade 1 (0-29%, patent); grade 2 (30-69%, no hemodynamic significance); grade 3 (70-99%, hemodynamically significant); and grade 4 (100%, occlusion). For each vessel segment, the most severe stenotic lesion was scored.
Statistical Analysis
To assess the diagnostic value of MR angiography, we evaluated the overall
conformity in stenosis classification between the two imaging modalities. For
this factor, precise stenosis gradation for every assessable segment (those
visualized by both MR angiography and digital subtraction angiography) was
compared.
Furthermore, the sensitivity and specificity for the detection of
hemodynamically significant lesions (lesions grade 3 and 4) were evaluated for
the entire population and for vessel segments compared with digital
subtraction angiography. To estimate the discriminatory power between digital
subtraction angiography and MR angiography, we calculated kappa values to
assess poor ( < 0.1), slight ( = 0.1-0.4), fair ( =
0.41-0.6), moderate ( = 0.61-0.8), or almost perfect ( =
0.81-1.00) agreement between the two imaging modalities.
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Therefore, 2378 segments ("comparable segments") were included in the primary evaluation. Of these, 1236 (52%) were judged to be patent (grade 1) on digital subtraction angiography, whereas 1142 segments (48%) were found to have a grade 2-4 lesion (30-100% stenosis). Of these 1142 segments, 497 (43.5%) vascular sections were considered occluded on digital subtraction angiography (Table 1).
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Accuracy in estimating the severity of peripheral vascular occlusive disease by MR angiography versus digital subtraction angiography depended on localization of vessel segments and severity of stenosis.
In 2156 segments, MR angiography results matched those of digital subtraction angiography, for an overall conformity of 90.7% (Table 2). The positive and negative predictive values for overall stenosis detection were 91.2% and 97.3%, respectively. When the 34 nondiagnostic segments were included, the overall conformity dropped slightly to 89.6%, and the positive and negative predictive values were 89.9% and 95.9%, respectively (Figs. 1A,1B and 2A,2B).
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In 188 segments (8.7%), a difference of one grade was noted in scoring the severity of lesions, and in 24 segments (1.1%), the difference was two grades. In 10 segments (0.5%), a mismatch of three grades occurred. Nearly all (9/10) these segments were located in the calf, and venous contamination was observed in all of them. Of all 222 discrepant segments, 164 (73.9%) were overestimated by MR angiography, and 58 (26.1%) were underestimated (Table 2).
Using digital subtraction angiography, we characterized 729 vascular
lesions (30.7%) as hemodynamically significant (grades 3 and 4;
Table 1); 70 mildly stenotic or
patent vessel segments were scored as having more than 69% stenosis or
occlusion on MR angiography. However, MR angiography underestimated 24
significant lesions. Sensitivity and specificity for MR angiography in
differentiating mild and significantly diseased lesions were 96.7% and 95.8%,
respectively, with a high concordance with digital subtraction angiography
( = 0.91) (Table 3). The
positive and negative predictive values for the diagnosis of significant
lesions were 91.1% and 98.6%, respectively (Fig.
3A,3B).
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When the 34 nonassessable segments (13 with significant and 21 with insignificant disease) were included, the sensitivity and specificity for differentiating mild and significantly diseased lesions reached 95.2% and 94.6%, respectively. The positive and negative predictive values for the diagnosis of significant lesions decreased to 88.5% and 97.8%, respectively.
Of 497 occlusions found on digital subtraction angiography, 18 (3.6%) were diagnosed as high-grade stenoses on MR angiography; conversely, 19 hemodynamically significant stenotic vessel segments (3.8%) were characterized as occluded on MR angiography (Fig. 4A,4B). Differences in concordance between both modalities were noted depending on the location of the vessel segments (Table 2). Overall conformity in precise stenosis classification was best for the external iliac artery (96.4%; six segments incorrectly classified using MR angiography) and poorest for the anterior tibial artery (84.5%; 13 stenoses overestimated and 12 underestimated on MR angiography). The conformity of all vessel segments was 92.3% in the thigh and 88.4% in the calf. The sensitivity for diagnosis of significant lesions was slightly greater in the upper leg (97.8%) than in the lower leg (95.8%) segments; the specificity in the thigh was 96.7% and that for the calf was 94.3% (Table 3). In the thigh, nine (2.2%) of the 403 hemodynamically significant stenoses detected on digital subtraction angiography were understimated on MR angiography compared with 14 (4.3%) of 326 lesions underestimated in the calf. Furthermore, only one underrating of two grades was noted in the thigh compared with five in the calf. MR angiography overrated 33 (3.3%) of the 996 insignificantly diseased or patent upper leg segments (Fig. 5A,5B,5C,5D), whereas 37 (5.7%) of the 653 mildly stenotic vessels of the lower legs were overrated.
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The conformity and the sensitivity and specificity in detecting significant stenoses were also evaluated separately for those patients undergoing digital subtraction angiography before and those undergoing digital subtraction angiography after MR angiography. No difference was found between the two subgroups, but the group undergoing digital subtraction angiography first was significantly smaller. The overall conformity of this group was 91.0% compared with 90.7% for the patients undergoing MR angiography first. The sensitivity and specificity for detecting significant stenoses were 96.6% versus 97.0%, and 95.2% versus 96.1%, respectively.
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The advent of contrast-enhanced, ultrafast MR angiography, proposed by Prince in 1995 [3], has dramatically changed the diagnostic approach to arterial disease. However, application of MR angiography to the peripheral vessels has been limited because of the small field of view of older MR scanners and the length of vessels in the lower extremities. Although some authors have described the feasibility of peripheral MR angiography using the acquisition of multiple stacks [12, 19, 20], that technique has not seen widespread clinical acceptance for pre- or posttherapeutic diagnosis of patients with peripheral vascular occlusive disease for various reasons. The imaging of the entire vessel tree requires both repeated placement of the patient in the scanner and multiple administrations of contrast media. The result is higher costs, long examination times, and reduced contrast-to-noise ratio in the stacks that are acquired second and third because of the increased contrast enhancement of the surrounding tissue. In addition, the repeated positioning of the patient could lead to missing some vessel segments between stacks.
The introduction of multiple-station techniques, such as a moving bed or moving table, has minimized or eliminated these shortcomings in imaging of the peripheral vessels. However, the promising results of a limited number of preliminary studies [13,14,15,16,17] that evaluated the diagnostic efficacy of MR angiography have not been confirmed in a large patient cohort.
The small number of underestimated lesions in our study indicates the high accuracy for MR angiography in the diagnosis of peripheral vascular occlusive disease and shows its potential as a screening modality. The differentiation of diseased and patent vessels was possible in nearly all vascular segments. Furthermore, hemodynamically significant lesions were detected with excellent concordance with digital subtraction angiography, and sensitivity exceeded 95% in almost all vascular regions studied. Our results in stenosis classification are comparable to those previously published in various reports (75-100% [13], 81-89% [14], and 97% [19]).
A distinct dependence of diagnostic confidence on location of stenosis was seen in our study, and only a few significant stenoses [2.2%] were underestimated in the thigh. The major reason for the slightly worse detection of hemodynamically significant stenoses in the calf than in the thigh was the relatively large effective slice thickness of 3.0 mm used in these patients. The voxel size in the peroneal artery and the distal part of the calf seems to be too large compared with the small diameter of these arteries and can lead to over- or underestimations of stenosis in these segments. A solution to this problem might be faster scanning, allowing the acquisition of more and thinner slices during the same time. Another approach is the use of more flexible software that would allow individual planning for each of the three stacks. With such software, it is possible to reduce the imaging volume and thus the slice thickness for only the third stack to image the lower leg arteries with a smaller slice thickness than that of the upper leg. An evaluation of this method has been reported recently [17], but the software is still not commercially available.
Another reason for the better diagnostic accuracy in the upper leg arteries is that the contrast-enhanced images of the calf were acquired at the end of all scanning when vessel contrast had decreased. At this point of the image acquisition, venous overlay can also be observed, especially in patients with accelerated artery-to-vein transit times as a result of tissue hyperemia (after arterial ulcerations) or other abnormalities [21]. The venous overlay combined with reduced concentration of contrast material in the arteries can interfere with the correct diagnosis and was the reason for nearly all (9/10) severe misratings (over- or underestimations of three grades) observed in our study. The number of patients with venous enhancement of the calf vessels was small (n = 8) because a special leg support was used that avoided compression and thus venous stasis of the calf, and a slow infusion of contrast material delayed venous enhancement [13, 14, 21]. Nevertheless, further shortening of the acquisition time seems to be desirable to eliminate this drawback.
The success of an interventional treatment and the risk of treatment-related complications depend not only on the morphology of the significant lesion, which should be treated, but also on the morphology of the inguinal vessels, the inflow and outflow of the diseased vascular segments, and the presence of further mild or severe stenosis. Furthermore, when surgical treatment such as bypass graft surgery is contemplated, complete delineation of the peripheral vasculature is mandatory to identify optimal locations for proximal and distal anastomoses [22].
Our results with peripheral moving-bed, contrast-enhanced MR angiography in a large number of patients confirm the high diagnostic accuracy of this noninvasive technique, as indicated in previously published articles about smaller populations [12,13,14,15,16,17]. As clearly shown in a recently published meta-analysis of the diagnostic performance of peripheral MR angiography [23], patient inclusion criteria in most studies were focused on a particular stage of disease (i.e., grade III chronic limb ischemia [24], severe claudication, and rest pain [25]) or the evaluation was limited to distinct vascular regions [7, 10, 26]. Because of the large number of individuals included and the retrospective study design, our study assessed a broad spectrum of clinical conditions. The diagnostic efficacy and the practicability in clinical practice of this relatively new noninvasive imaging modality can be evaluated without bias from patient compliance, severity of stenosis, cardiac function, or physician performance. Although all examinations were performed during a clinical routine, only 27 segments had to be excluded because of technical failures.
Some patients underwent MR angiography before digital subtraction angiography, and some after an interventional treatment, but no difference was seen in diagnostic accuracy between these two subgroups. Therefore, bias can be excluded. Although it is not standard at our institution to perform treatment follow-up using MR angiography after interventional treatment, such follow-up can be useful in patients with reduced kidney function when final angiography is replaced by MR angiography 1-2 days later to decrease the dose of iodinated contrast material. Furthermore, should complications occur during angioplasty (e.g., peripheral embolism with embolectomy, dissection of the vessel wall), an early noninvasive follow-up during the hospital stay can be helpful for the early detection of complications, restenoses, or reocclusions.
Performing digital subtraction angiography after MR angiography allows optimized planning of an interventional treatment based on MR angiography results.
In our study, commercially available moving-bed software and the whole-body coil were used on a standard scanner. To date, no special vascular surface coil for the lower leg is available for the system used at our institution. This fact is important, because some authors have shown improved contrast-to-noise ratio using a dedicated vascular coil and flexible imaging parameters for each field of view [17]. Although diagnostic accuracy was fairly high even in the small calf vessels in our study population, some reports [16, 17] indicate room exists for further improvement of vessel visualization.
More recently, initial results using a multi-injection, time-resolved MR angiography technique for the evaluation of the peripheral arteries were reported [27]. Although evaluated in a small number of volunteers and patients, this established technique has shown promising results, especially for the carotid arteries, compared with the moving-table MR angiography technique used in our study [28]. With this multiinjection protocol, a decrease in venous contamination and an increase in small vessel delineation should be achieved. Nevertheless, the promising early results of this new potential solution for peripheral MR angiography must be confirmed in a large patient cohort using a standard of reference.
One limitation of using MR angiography is that certain artifacts inherent in this technique pose challenges to the goal of uniform intravascular signal intensities. Susceptibility effects in the region of surgical clips and vascular stents will degrade analysis and surveillance of treated lesions. Although a stent must be identified and not misinterpreted as an occlusion or high-grade stenosis, an in-stent restenosis or occlusion may escape diagnosis. However, indirect signs indicating patency of stents, such as missing collateral vessels and frank opacification of the vessel distal to the stent, are useful information and should allow differentiation of high-grade stenoses or occlusions from low-grade stenoses.
Another shortcoming of the acquisition technique used in our study is that reconstruction was time-consuming, requiring as long as 10 min and resulting in low patient throughput. With the use of recently released software, the reconstruction time can be decreased dramatically and now lasts less than 1 min, allowing three to four patients to be examined in 1 hr.
In conclusion, our retrospective analysis of a large patient cohort shows that movingbed, contrast-enhanced MR angiography is an accurate and practical imaging modality for the assessment of peripheral vascular occlusive disease.
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70% Luminal
Narrowing) Stenoses
