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1
Department of Radiology, Johannes Gutenberg-University Mainz, Langenbeckstr.
1, D-55131 Mainz, Germany.
2
Department of Cardiothoracic and Vascular Surgery, Johannes
Gutenberg-University Mainz, D-55131 Mainz, Germany.
3
Department of Medical Statistics and Documentation, Johannes
Gutenberg-University Mainz, Obere Zahlbacher Str. 69, D-55131 Mainz,
Germany.
4
Department of Endocrinology, III. Medical Clinic, Johannes
Gutenberg-University Mainz, D-55131 Mainz, Germany.
5
Siemens Medical Engineering, Henkestr. 127, D-91318 Erlangen, Germany.
Received April 30, 1999;
accepted after revision June 2, 1999.
Supported in part by Schering AG, Berlin, Germany.
Abstract
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SUBJECTS AND METHODS. Twenty-four feet of 24 consecutive patients with diabetes and limb-threatening lower extremity ischemia were prospectively imaged using an ultrafast three-dimensional fast low-angle shot sequence on a 1.5-T MR scanner. All patients also underwent DSA of the diseased extremity within 5 days. Images were interpreted in a randomized manner by two observers in conference. Each lower extremity was divided into seven potential arterial segments. Image analysis included the detection of patent, stenosed, or occluded vessel segments. A vascular surgeon formulated treatment plans on the basis of findings from DSA and then formulated treatment plans on the basis of findings from both DSA and MR angiography.
RESULTS. MR angiography was significantly better than DSA in revealing peripheral runoff vessels (p < 0.001). In nine (38%) of the 24 patients, MR angiography showed patent pedal vessels suitable for distal bypass grafting that were not revealed by DSA. Because of the results of MR angiography, treatment plans changed in seven of the nine patients in whom patent vessels were subsequently used as target vessels for distal pedal bypass grafts.
CONCLUSION. Contrast-enhanced three-dimensional MR angiography is superior to DSA in revealing patent vessel segments of the foot in diabetic patients with severe arterial occlusive disease. Contrast-enhanced three-dimensional MR angiography should be part of the diagnostic algorithm for patients in whom pedal bypass grafting is a therapeutic option.
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Advances in surgical revascularization techniques in patients with lower limb ischemia require precise preoperative imaging of the peripheral vessels [2, 3]. Intraarterial digital subtraction angiography (DSA) has been considered the preoperative diagnostic imaging standard in the evaluation of peripheral and especially of infrapopliteal arteries [4]. However, some studies have shown that DSA in combination with standard angiography may fail to reveal patent arteries or vessel segments that are suitable for distal bypass grafting in patients with severe arterial occlusive disease. In these studies, MR angiography using two-dimensional (2D) time-of-flight techniques was proven to be a useful adjunct because it provided images that depicted patent arterial segments that were not seen on angiography [5, 6, 7, 8].
However, several limitations are associated with 2D time-of-flight MR angiography such as spin saturation from in-plane flow, intravoxel spin-phase dispersion from turbulent flow, stepladder motion artifacts on reformatted maximum-intensity-projection (MIP) images, elimination of the arterial signal in cases of retrograde flow by inferiorly placed venous saturation pulses, and long imaging times [8, 9]. Most of these problems have been resolved by the introduction of contrast-enhanced three-dimensional (3D) MR angiography using gadolinium chelates as the contrast agent. This became possible by high-performance gradient systems that enable fast imaging sequences [10, 11, 12].
The purpose of our study was to investigate the usefulness of a contrast-enhanced 3D subtraction MR angiography in patients with diabetes mellitus for evaluating distal calf and pedal vessels before distal pedal bypass surgery. We compared the results of MR angiography with those of conventional DSA.
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DSA
All DSA examinations were performed by experienced angiographers either
with an Integris 2000 digital angiographic unit (Philips Medical Systems,
Eindhoven, Netherlands) or with a Multistar unit (Siemens Medical Systems,
Erlangen, Germany). Angiographically, a nonselective technique was used in 14
(58%) of 24 patients: in eight patients, a 5-French pigtail catheter was
placed in the distal abdominal aorta for imaging the area from the distal
aorta to the pedal arteries of both extremities. In six patients, fine-needle
DSA of the diseased extremity was performed: this procedure consisted of
retrograde puncture of the ipsilateral common femoral artery with a 20-gauge
puncture needle that was connected with a slim tube and multiple manual
injections of contrast material. Ten (42%) of 24 patients underwent selective
DSA with crossover antegrade catheterization of the common femoral,
superficial femoral, or popliteal artery using a 5-French side-hole catheter
(Sos Omni Flush; Angiodynamics, Queensbury, NY). The number of projections
that were performed was at the discretion of the angiographer. For
visualization of the complete arterial tree, an average of 90-110 ml of a
nonionic contrast agent (iopromid [Ultravist]; Schering, Berlin, Germany; or
iopremol [Imeron]; Bracco-Byk Gulden, Konstanz, Germany) was necessary. For
selective injections into the arteries of one leg, 40-60 ml of contrast medium
was sufficient. No vasodilative drugs were administered during the DSA
procedure.
Postoperative selective DSA (either fine-needle puncture or crossover catheter angiography) for documentation of bypass graft patency was available in 16 patients. It was used as a reference standard for the pedal vessels in case of a normal postoperative status.
MR Angiography
MR angiography was performed with a transmit-receive head coil and a
standard 1.5-T whole-body imager (Magnetom Vision; Siemens Medical Systems)
equipped with 25 mT/m high-performance gradients that enabled a 600-µsec
rise time. The coil was placed to include the entire foot and as much of the
calf as possible in the imaging volume. In all patients, one foot was placed
in the coil; the other, outside the coil. The feet were usually positioned in
a slight plantar flexion, comfortable to the patient, and immobilized with
foam padding.
For MR angiography, we used a 3D radiofrequency spoiled fast low-angle shot sequence with the following parameters: TR/TE, 3.8/1.3 msec or 4.6/1.8 msec; flip angle, 35° or 30°; rectangular field of view, 290 or 390 mm; image matrix, 150 x 256 or 170 x 512; and receiver bandwidth, 390 Hz per pixel. The 3D volume had a thickness of 90 mm and was subdivided into 40 partitions, resulting in a slice thickness of 1.1 mm after slice interpolation. In-plane resolution ranged between 1.69 x 1.12 mm2 (image matrix of 256) and 1.48 x 0.76 mm2 (image matrix of 512); acquisition time was 18 or 25 sec, respectively. The slab thickness enabled imaging of the whole foot and distal calf in the sagittal plane. Four sets of identical sagittal slabs were acquired consecutively.
Each MR angiography was enhanced by a 20-ml bolus of gadopentetate dimeglumine (Magnevist; Schering). Administration of contrast material was automatically started with the beginning of the first set through a 22-gauge IV needle and an MR imaging-compatible power injector (Spectris; Medrad, Pittsburgh, PA) into an antecubital vein at a constant flow rate of 2 ml/sec. Contrast agent administration was followed by flushing with 20 ml of saline solution. The mean patient weight was 73.5 ± 12.4 kg (range, 55-92 kg), which resulted in a mean gadolinium dose of 0.14 ± 0.05 mmol/kg (range, 0.11-0.18 mmol/kg).
After image reconstruction, the unenhanced data were subtracted from the corresponding enhanced data. Angiograms of the subtracted images were created using the MIP algorithm. A series of 13 MIP images was generated at 15° rotational increments from a right lateral to a frontal to a left lateral view. MIP images were placed in windows and leveled to maximize arterial contrast and minimize the intensity of background signal. These MIP images served as the basis for further interpretation.
Image Analysis
Two reviewers independently reviewed both the MR angiograms and DSA images
in a randomized order. The MR angiograms were evaluated without knowledge of
the patient's identity and the results of conventional DSA. In cases of
disagreement about the degree of vessel stenosis in either imaging technique,
a final consensus interpretation of the MR images or DSA images was
performed.
Seven vascular segments were evaluated in each extremity: the distal anterior tibial, distal posterior tibial, distal peroneal, dorsal pedal artery, lateral plantar, medial plantar arteries, and the pedal arch. Segments were classified as patent or occluded. Patent segments were further classified as having 50% or less stenosis or greater than 50% stenosis. In cases with multiple sites of disease, only the site with the most severe disease was scored.
After this review, each DSA study was paired with the appropriate MR angiographic study, and an assessment was performed of the overall image quality of the angiographic images. Each reviewer independently assigned a relative rank to each pair of examinations. The possible relative rankings ranged from 2 to -2 (2, MR angiography was substantially better than DSA; 1, MR angiography was moderately better than DSA; 0, MR angiography and DSA were of equivalent quality; -1, DSA was moderately better than MR angiography; -2, DSA was substantially better than MR angiography).
A vascular surgeon who was unaware of the patient's identity and the results of MR angiography formulated treatment plans on the basis of DSA findings alone; he then formulated treatment plans on the basis of findings of both DSA and MR angiography. Finally, he subjectively ranked the overall image quality of both imaging techniques using the scoring described previously.
Statistics
Statistical analysis comprised the segment-wide and overall calculation of
Cohen's kappa coefficient and its 95% confidence interval for determination of
the degree of agreement between both methods. The McNemar test was used to
assess the relative superiority of each technique to reveal patent vessel
segments. For analysis of the reviewers' rankings of the relative image
quality, the paired Wilcoxon's signed rank test was used. A p value
of less than 0.05 using Wilcoxon's signed rank test or the McNemar test was
considered to indicate local statistically significant difference; the
p values were not adjusted for multiplicity concerning the seven
arterial segments. Group comparisons were drawn out using Fisher's exact test.
All computations were performed using SAS software (version 6.12; SAS
Institute, Cary, NC).
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Table 2 lists the ratings of the patent vessel segments seen by both imaging techniques. Of 74 vessel segments, 60 (81%) had an identical scoring. In 11 cases, the degree of stenosis was rated as more severe on DSA images, and in three cases, stenosis was scored as more severe on MR angiograms.
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In a patient-by-patient analysis, MR angiography revealed a patent vessel that was not seen on DSA and that would be suitable for distal bypass grafting in nine (38%) of 24 patients. These findings led to a change of treatment plans for seven patients: two patients received a pedal bypass graft instead of amputation of the lower extremity below the knee (Fig. 3A, Fig. 3B, Fig. 3C, Fig. 3D), and five patients underwent femoropedal bypass grafting instead of femorocrural or femoropopliteal bypass grafting. Target vessels of the bypass grafts were the lateral plantar artery in one patient and the dorsal pedal artery in six patients (Figs. 3A, Figs. 3B, Figs. 3C, Figs. 3D and 4A, 4B). Changes of treatment plans were made in two (20%) of 10 patients with a selective DSA technique, and in five (36%) of 14 patients with a nonselective DSA technique (Table 3). This difference was not statistically significant (p = 0.653, Fisher's exact test).
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Sixteen patients underwent fine-needle DSA for bypass control during the immediate postoperative period (Figs. 3 and 5A, 5B, 5C). In two patients with a sequential bypass graft (femorocrural-pedal bypass), there was a graft occlusion between the crural and pedal anastomosis, resulting in a minor opacification of the pedal vessels. Thys, the results of MR angiography in detecting patent pedal vessels could be compared with postoperative fine-needle DSA in 14 patients. For all patients, there were no false-positive findings on MR angiograms. However, postoperative DSA better depicted metatarsal and digital arteries than MR angiography in three patients (Fig. 3E).
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All ratings of the three observers were pooled for the comparative qualitative analysis of the digital subtraction and MR angiographic images. MR angiograms were considered to be of substantially higher quality than DSA images in 21 patients (score = 2), of somewhat higher quality in 18 patients (score = 1), and of equivalent quality in 32 patients (score = 0). DSA images were given a higher score than the corresponding MR angiograms only once by one observer (score = -1). The difference in assessment of overall image quality between digital subtraction and MR angiograms was statistically significant (p < 0.001).
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Intraarterial DSA has been considered an accurate and reliable method in the assessment of infrapopliteal arteries. Selective angiography has proved to be superior to nonselective injection for assessment of pedal circulation [4, 17]. The results of our study indicate that in diabetic patients with severe peripheral arterial occlusive disease, contrast-enhanced MR angiography is superior to DSA for the identification of patent arterial segments in the runoff vessels of the foot—even when compared with a selective DSA technique. In our series, the pedal arch vessels were identified on MR angiograms in 22 (92%) of 24 feet and on DSA images in nine (38%) of 24 feet.
One possible reason for the success of the 3D MR angiography is the use of subtraction to improve background suppression, which has been shown in other studies [9, 11, 12, 18, 19]. However, when subtraction techniques are used, data may be misregistered. Misregistration may occur with patient motion between acquisitions resulting in substantial artifacts [11, 12]. Because of the short duration of the acquisitions, the convenient patient positioning, and the absence of pain during application of IV contrast material, the quality of all MR angiograms was not affected by patient motion in our study.
We did not use a timing run for calculation of contrast circulation times to achieve optimal acquisition of central K-space data [20]. Nevertheless, we did not observe a markedly reduced image quality as a result of the superimposition of enhanced veins. In the present series, four MR examinations showed a slight venous enhancement, but this did not hamper further image analysis (Fig. 5B).
A possible reason for the lack of venous superimposition was the short scan duration of 18 or 25 sec. These short scan times enabled data acquisition in the window during arterial and before venous enhancement. In contrast to other vascular territories, such as the supraaortic or renal arteries, there is a long duration of up to 20 sec after arrival of the contrast agent until all the pedal circulation may be filled [17]. With the acquisition of four consecutive 3D volumes, we could choose those data sets with the best arterial enhancement for image subtraction. In most cases, the arrival of the contrast agent occurred during the second or third data set. However, because of low cardiac output, the contrast agent arrived only during the last data set in two patients. Therefore, we recommend the acquisition of up to four data sets so bolus arrival is not missed in those patients.
Lee et al. [9] found that contrast-enhanced subtraction MR angiography is superior to 2D time-of-flight MR angiography in the depiction of distal calf and pedal circulation. These researchers used a 2D gadolinium-enhanced technique with a high temporal resolution that enabled imaging of the calf and foot vessels without overlaying veins. They noted a superior depiction even of the supramalleolar vessels by subtraction MR angiography. However, a comparison with standard DSA was not provided in their study.
Compared with 2D or 3D time-of-flight MR angiography, contrast-enhanced MR angiography techniques enable a very fast data acquisition [9, 10, 11, 12, 20, 21]. In our study, the time from preparation of the patients to completion of the study was approximately 10 min. After image reconstruction, postprocessing for subtraction and creation of MIP angiograms required 20 additional min. However, this could be performed on a separate workstation so the work flow on the MR scanner was not further interrupted.
We acknowledge several criticisms of the present study. First, there was a strong selection bias, because only diabetic patients with severe arterial occlusive disease and multiple vessel obstructions were included in the investigation.
Second, we did not use a uniform DSA technique partially because angiographic examination of both lower extremities was necessary in many patients who had existing arterial occlusive disease in both legs. In addition, because all patients suffered from diabetes, the angiographers restricted the total amount of iodinated contrast material that was injected to a minimum. This may have prevented the performance of additional selective series for better depiction of the pedal arteries in some patients. However, a selective DSA technique should be attempted whenever possible.
We have shown in this study of patients with multiple obstructions in one extremity that contrast-enhanced MR angiography was superior to DSA even when a selective technique was performed. These findings contradict the results of Brophy et al. (presented at the Radiological Society of North America meeting, November 1997). Their findings showed superior delineation of infrapopliteal vessels by selective intraarterial DSA over contrast-enhanced 3D MR angiography. However, it is unclear from the available data to what extent their patient population differed from ours as far as the sites and severity of vessel obstruction are concerned.
Third, we did not use vasodilative drugs for better visualization of the pedal vessels. Because all patients suffered from chronic ischemia, we speculated that the pedal vessels were already vasodilated to make up for impaired inflow.
Fourth, postoperative DSA, which could have served as a reference standard, was available in only 16 patients. One patient underwent amputation, three patients were lost to postoperative follow-up; in four patients, the intended bypass operation was not performed for various reasons.
Finally, we used two MR angiography sequences with different in-plane resolutions in 12 patients each. Compared with DSA, both sequences lead to a significantly superior detection of patent pedal arteries.
A basic limitation of our MR technique is that only one anatomic area was covered. For a complete peripheral runoff study, it would be necessary to evaluate the vasculature of the whole extremity because all our patients showed additional obstructions of the femoral, popliteal, or proximal crural vessels. There are several reports in the literature that describe different methodic approaches for imaging of both extremities by contrast-enhanced MR angiography, including boluschase MR angiography [22, 23, 24, 25, 26]. These new techniques are very attractive especially for imaging diabetic patients because the administration of iodinated contrast agents could be avoided. At the moment, these techniques require further optimizations, and larger prospective studies are not yet available. Furthermore, it is not clear whether these techniques would enable adequate visualization of pedal vasculature like the technique presented in this study.
In summary, our study has shown that contrast-enhanced 3D subtraction MR angiography is superior to intraarterial DSA in imaging of distal calf and pedal vessels in diabetics with severe arterial occlusive disease. Thus, it proved to be a useful adjunct to DSA in patients for whom pedal bypass grafting was considered. Owing to the results of this study, contrast-enhanced 3D MR angiography of the distal calf and pedal vessels has become a substantial part of the diagnostic algorithm at our institution if DSA provides inadequate visualization of the pedal arteries.
Acknowledgments
We are indebted to M.-C. Schmitt for providing us with results of her
doctoral thesis, which is under preparation. We thank Manfred Siebald for his
critical reading of the manuscript and A. Keuchel and I. Nessler for making
the photographs.
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