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1
Institute of Diagnostic Radiology, University Hospital,
Rämistr. 100,
Zürich, Switzerland.
2
Present address: Institute of Diagnostic Radiology, University Hospital Essen,
Hufelandstr. 55, D-45122 Essen, Germany.
3
Department of General Surgery, University Hospital,
Zürich, Switzerland.
Received August 9, 1999;
accepted after revision May 31, 2000.
Address correspondence to J. F. Debatin.
Abstract
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SUBJECTS AND METHODS. The study included 39 patients with 45 lower limb grafts. Twenty-eight were saphenous vein grafts, 13 were expanded polytetrafluoroethylene, and two were Dacron grafts. Digital subtraction angiography correlation was available for 30 patients (31 grafts). MR angiography was performed on a 1.5-T system with a multichannel quadrature phased array peripheral vascular coil. The scanning delay was determined with a test bolus technique, using half-time to maximum signal intensity in the graft. Arterial imaging was accomplished with two three-dimensional MR angiography acquisitions with gadopentetate dimeglumine administered using an automated injector. The pelvic and femoral arteries were imaged, the MR table was repositioned, and the lower limb arteries were imaged. The three-dimensional MR angiography sequence used the following parameters: TR/TE, 5.2/1.5 msec; inversion time, 28 msec; flip angle, 30°. The proximal anastomosis, graft, and distal anastomosis were characterized as normal, stenosed, occluded, or ectatic or aneurysmatic.
RESULTS. Sensitivity and specificity values for MR angiography regarding the assessment of grafts were 100% for 87 evaluable segments for which digital subtraction angiography correlation was available: stenosis (n = 10), occlusions (n = 9), ectasia or aneurysms (n = 8). Six segments could not be assessed because of the presence of intravascular stents or metallic clips.
CONCLUSION. Contrast-enhanced three-dimensional MR angiography is well suited for the characterization of arterial grafts, for planning subsequent vascular interventions, and for excluding further lesions.
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Peripheral vascular occlusive disease is a widespread condition. Postoperative graft surveillance is of particular importance because flow impairment is the major cause of graft failure. Autologous venous grafts, which have a primary and secondary graft patency superior to that of expanded polytetrafluoroethylene grafts [9,10,11], have a 12% incidence of bypass graft stenosis in the first postoperative year [12]. Early detection of graft stenosis is the best way to improve the secondary bypass patency rate. For venous grafts, the primary and secondary patencies are 63% and 66% at 12 months and 54% and 56% at 24 months. For expanded polytetrafluoroethylene grafts, the primary and secondary patencies are 48% and 54% at 12 months and 31% and 37% at 24 months [9].
Grafts are generally evaluated using duplex sonography or DSA. A noninvasive test is desirable for follow-up after the graft procedure. Duplex sonography is a good means for determining graft patency and, when performed appropriately, can locate stenoses accurately. However, the sonographic approach is limited with respect to identification of collateral blood flow and depends on the skill of the operator [13,14,15]. Morphologic assessment of arterial bypass grafts of the lower limbs requires high spatial resolution and extended coverage of the arterial system from the aortic bifurcation to the ankles. For this reason, analysis of peripheral grafts using DSA is still commonplace.
The purpose of the study was to assess the diagnostic performance of a single-injection, two-station, contrast-enhanced three-dimensional MR angiography protocol for the characterization of peripheral arterial grafts.
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Thirty patients with a history of peripheral grafts who were referred for DSA were asked to undergo MR angiography as well. The other nine patients were referred from clinicians for MR angiography only. All patients underwent three-dimensional contrast-enhanced MR angiography (43 grafts). The postoperative interval ranged from 5 days to 10 years. Although operative reports were available for all patients, DSA was performed within a 3-week interval (mean, 11 days) of the MR angiography examination, but results were available in only 30 patients with 31 grafts.
Contrast-enhanced three-dimensional MR angiography was performed on a 1.5-T system (Signa Echo-Speed; General Electric Medical Systems, Milwaukee, WI). To place the three-dimensional acquisition volumes, broadly spaced 10-mm axial two-dimensional time-of-flight images were acquired through the pelvis, thighs, and lower limbs. For determination of the scanning delay after the contrast bolus injection, axial multiphase gradient-recalled echo images (TR/TE, 6.4/2.0; flip angle, 60°; field of view, 30 cm; matrix, 256 x 160) were collected at the level of the graft after the injection of a 2-mL gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) test bolus. Half-time to maximum signal intensity in the graft was used as the scanning delay. A multichannel quadrature phased array peripheral vascular coil (Peripheral Vascular Array; Medical Advances, Milwaukee, WI), extending from the aortic bifurcation to the ankle, was used for imaging.
A dose of 0.3 mmol of gadopentetate dimeglumine per kilogram of body weight was injected IV over 60 sec using an automated injector (MR Spectris; Medrad, Pittsburgh, PA). The administered flow rate was weight-adjusted and varied between 0.5 and 0.8 mL/sec. The arterial vasculature was imaged in two acquisitions, each lasting 30 sec and extending over 48 cm. The pelvic and thigh arteries were imaged during the first 30 sec followed by a 10-sec imaging break during which the MR table was manually repositioned to the center of the lower imaging volume, which was offset by only 45 cm to ensure some overlap between the two data sets. The lower limb arteries were imaged during the subsequent 30 sec. Craniocaudal coverage thus extended over 90 cm. The three-dimensional contrast-enhanced fast spoiled gradient-echo sequence used the following parameters: TR/TE, 5.2/1.5; inversion time, 28 msec; flip angle, 30°; slice thickness, 2.4 mm; 48 sections. A 48 x 36 cm field of view combined with a matrix size of 256 x 192 rendered a spatial resolution of 1.8 x 1.8 x 2.4 mm. Zero interpolation by a factor of 2 in all three directions improved the spatial resolution to 0.9 x 0.9 x 1.2 mm. The average time for performing the MR angiography ranged from 15 to 25 min, and the reconstruction time ranged from 3 to 5 min.
DSA was performed on two standard angiography units (Digitron 3, Siemens, Erlangen, Germany; or Integris V3000 version 13, Philips Medical Systems, Best, The Netherlands). All patients (n = 30) underwent catheter angiography extending from the distal aorta to the trifurcation arteries of the lower limb with a transfemorally inserted 5-French pigtail catheter (Angiographic Catheter; AngioDynamics, Queensbury, NY). The catheter tip was positioned immediately superior to the aortic bifurcation for DSA of the pelvic arteries. Then multiple acquisitions were performed encompassing the thigh and lower limb. At each station, 20 mL of iodinated contrast material (ioxaglate, 320 mg/mL) was injected. As required, the examination was supplemented by acquisition of one or more oblique images of the pelvic arteries using 15 mL of contrast material.
Two blinded observers separately analyzed the MR angiography and the DSA examinations. Proximal anastomosis, graft course, and distal anastomosis were analyzed separately. Each segment was evaluated as either normal, significantly stenosed (>50% of the graft diameter), occluded, or ectatic or aneurysmatic (>150% of the graft diameter). MR angiography interpretation was based on maximum-intensity-projection and source images. In addition, the three-dimensional data sets were available for interactive multiplanar reformations on a separate advanced workstation on a monitor. Access to the operative reports at the time of study interpretation was provided.
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MR angiography identified graft stenoses involving the proximal (n = 4) (Fig. 3A,3B) and distal anastomoses (n = 3) and the midportion of the graft course (n = 5). With the exception of one stenosis occurring in an expanded polytetrafluoroethylene graft, all other stenoses were found in venous grafts.
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Aneurysmal and ectatic changes were identified involving 12 graft segments. Eleven ectatic segments occurred in venous grafts (Fig. 4A,4B), and one expanded polytetrafluoroethylene graft itself was ectatic just at the proximal anastomosis. The proximal anastomosis (n = 5) and the proximal graft course (n = 6) were predominantly affected.
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One isolated distal occluded anastomosis of a venous (in situ) graft was noted. Four other occluded grafts were of expanded polytetrafluoroethylene (n = 3) and Dacron (n = 1). Ligating titanium clips were recognized on the underlying source images (Fig. 5A,5B,5C,5D).
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MR angiography graft status interpretations correlated with DSA for all segments of all 31 grafts, resulting in sensitivity and specificity values of 100%. With the six segments in which artifacts precluded the evaluation being assessed as occluded, specificity was reduced to 90.9%.
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Duplex sonography surveillance of lower extremity bypass grafts is a means of identifying patients at risk for occlusion. The perceived accuracy of duplex scanning for identifying stenosis may result in missing additional lesions that are threatening patency. For this reason, some authors suggest preoperative arteriography after identification of abnormalities on duplex scans [16,17,18]. In contrast to conventional DSA, three-dimensional MR angiography is virtually noninvasive and eliminates catheterization risks such as graft injury, hemorrhage, or formation of a pseudoaneurysm at the arterial catheterization site. High-performance gradient systems can reduce data collection times sufficiently to permit collection of complex three-dimensional MR image sets during the intraarterial phase of IV-administered extracellular paramagnetic contrast materials [6, 19, 20]. Furthermore, nonnephrotoxic contrast media [21] permit repetitive use of three-dimensional MR angiography even in patients with impaired renal function. Contrast-enhanced three-dimensional MR angiography thus constitutes an ideal imaging technique for the close follow-up frequently required after vascular bypass surgery or revision.
Few contraindications to MR angiography exist: patients with cardiac pacemakers should not be studied with MR angiography, whereas ligating clips in the area to be imaged are no contraindication. Most commercially available metallic vascular clips are titanium clips and are completely safe; they are not measurably attracted to or heated by the magnetic field [22]. Although metallic clips induce a typical susceptibility artifact because of signal void, depending on the clip size [23, 24], degree of K-space coverage, echo time [25, 26], and bandwidth [27], biocompatible clips are not associated with any signal distortion. Metallic clip presence should be ascertained on source images to avoid misinterpretation of clip-induced susceptibility artifacts as stenoses.
Intravascular stents are being widely used to improve vessel patency rates after balloon angioplasty [28, 29]. Duplex sonography for surveillance after intervention has the disadvantage of difficulty in penetrating the stent wall, which complicates the assessment of patency and imaging of vessel walls [30]. MR imaging artifacts associated with an endoprosthesis are related to both stent geometry and the underlying metal composing the stent. The ability to assess stents in peripheral vascular grafts with three-dimensional contrast-enhanced MR angiography depends on the type of stent used. Although most noncovered stents (Easy Wallstent [Schneider, Bülach, Switzerland], Palmaz stent [Cordis, Warren, NJ]) will result in characteristic signal voids on three-dimensional gradient-echo image sets, some covered stents (Cragg stent [Mintec, Bahamas], Passager stent [Boston Scientific, Natick, MA]) do not impair visualization of the vessel lumen [31].
For homogeneous results, attention to technique is crucial. The peripheral vascular coil extending from the aortic bifurcation to the ankles needs to be properly placed. It consists of four coils operating in a phased array manner. The coil diameter gradually decreases from the proximal to the distal portion and needs to closely surround the thigh and calf. The technique used in this study still requires manually moving the table between the two three-dimensional acquisitions. Accurate placement of visible landmarks is mandatory.
A dose of 0.3 mmol of gadopentetate dimeglumine per kilogram of body weight was injected IV. Whereas a lower dose such as 0.2 mmol/kg of body weight might be appropriate in most patients, a higher dose makes the protocol more robust, especially when there is an asymmetry with regard to the contrast travel time between the leg in which a graft was placed and the contralateral leg.
The contrast travel time from injection site to the vascular system cannot be predicted on the basis of physiologic parameters. This time can be reliably and accurately determined by a test bolus injection of a small volume of contrast agent followed by a saline flush during normal breathing [1]. Half-time to maximum signal intensity of the test bolus at the level of the graft was used as the scanning delay, coinciding with the data collection in the center of the K-space.
Limitations of three-dimensional MR angiography with regard to graft patency assessment primarily relate to spatial resolution. A field of view of 48 x 36 cm combined with a 256 x 192 matrix rendered a spatial resolution of 1.8 x 1.8 x 2.4 mm. Zero interpolation by a factor of 2 in all three directions improved the spatial resolution to 0.9 x 0.9 x 1.2 mm. Although the spatial resolution was sufficient to allow an accurate diagnostic assessment of all graft segments, visual comparison of image quality clearly favors DSA. Far more branch vessels are visible on the DSA images than on the MR angiograms (Figs. 1A,1B,2A,2B,2C,3A,3B, 4A,4B,5A,5B,5C,5D). Further shortening the TR could enhance MR angiography spatial resolution. An associated decrease in the signal-to-noise ratio would still remain compensated by the use of the peripheral surface coil. In addition, limitations are imposed by artifacts caused by stents and clips. First, such artifacts must be recognized. Whereas graft patency may still be determined, it is often not possible to correctly determine the caliber of a segment in the presence of a clip or stent.
This study shows that contrast-enhanced three-dimensional MR angiography is an excellent choice for assessing graft morphology. It should be used much like catheter-based conventional DSA as a second-line examination after duplex sonography to exclude tandem lesions and to plan further treatment.
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