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Published online before print August 16, 2002, 10.1148/radiol.2251011292
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(Radiology 2002;225:43-52.)
© RSNA, 2002

Vascular and Interventional Radiology

Time-resolved Three-dimensional Contrast-enhanced MR Angiography of the Peripheral Vessels1

J. Shannon Swan, MD2, Timothy J. Carroll, PhD, Todd W. Kennell, MD, Dennis M. Heisey, PhD, Frank R. Korosec, PhD, Richard Frayne, PhD3, Charles A. Mistretta, PhD and Thomas M. Grist, MD

1 From the Depts of Radiology (J.S.S., T.W.K., F.R.K., R.F., T.M.G.), Med Physics (T.J.C., F.R.K., R.F., C.A.M., T.M.G.), and Surgery (D.M.H.), Univ of Wisconsin-Madison Med School, Wis. Received Jul 27, 2001; revision requested Sep 4; revision received Dec 19; accepted Feb 19, 2002. Supported by NIH R01 HL51370 and Nycomed-Amersham. Address correspondence to T.J.C., Depts of Radiology and Biomedical Engineering, Northwestern University, 448 E Ontario St, Ste 700, Chicago, IL 60611 (e-mail: t-carroll@northwestern.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare the diagnostic accuracy of time-resolved three-dimensional contrast material–enhanced magnetic resonance (MR) angiography with that of conventional angiography for imaging the lower extremity vasculature.

MATERIALS AND METHODS: Sixty-nine patients who were evaluated for possible surgical intervention underwent conventional angiography (ie, digital subtraction angiography [DSA]) and contrast-enhanced MR angiography (ie, time-resolved imaging of contrast kinetics [TRICKS]). Two independent, blinded readers evaluated vessel stenosis and occlusion at DSA and MR angiographic image readings. Sensitivity, specificity, positive and negative predictive values, and area under the receiver operating characteristic curve were analyzed with repeated-measures analysis of variance. The Cohen {kappa} test was performed to examine interreader variability.

RESULTS: At pooled readings, contrast-enhanced MR angiography had a sensitivity of 78% and a specificity of 98% for detection of occlusion. For detection of significant stenosis (at least one >=50% stenosis), sensitivity and specificity were 77% and 91%, respectively. Interreader agreement was high for detection of both occlusion ({kappa} = 0.76) and significant stenosis ({kappa} = 0.68). Sensitivity increased as MR angiographic technical parameters were optimized. When improvements resulting from coil type and injection protocol were considered, the sensitivity and specificity of TRICKS MR angiography were 89% and 97%, respectively, for occlusion detection and 87% and 90%, respectively, for significant stenosis detection.

CONCLUSION: Contrast-enhanced TRICKS MR angiography is a feasible and minimally invasive means of acquiring angiograms of the peripheral vasculature with high sensitivity and specificity.

© RSNA, 2002

Index terms: Angiography, comparative studies, 92.122, 92.12942, 92.12943, 98.122, 98.12942, 98.12943 • Arteries, stenosis or obstruction, 92.721, 98.721 • Extremities, angiography, 92.122, 92.12942, 92.12943, 98.122, 98.12942, 98.12943 • Magnetic resonance (MR), vascular studies, 92.12942, 92.12943, 98.12942, 98.12943


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Lower extremity arterial occlusive disease is an important cause of morbidity in developing countries, and it results in an estimated 100,000 amputations or surgical bypass procedures annually in the United States alone. Diagnostic evaluation of the presence and extent of lower arterial obstruction generally has been performed with conventional (ie, x-ray) diagnostic intraarterial angiography—that is, digital subtraction angiography (DSA). Magnetic resonance (MR) angiography is emerging as a reasonable adjunct or alternative to the conventional approach of catheter angiography (1). The lower degree of invasiveness and smaller likelihood of complications with MR angiography are well received by patients and thus contribute to arguments promoting the cost-effectiveness of this examination (2–4).

However, the widespread acceptance of MR angiography has been hindered owing to the artifactual signal intensity loss and the lengthy examination time associated with time-of-flight MR image acquisitions. These problems have been addressed with the advent of three-dimensional (3D) contrast material–enhanced MR angiography (5,6). These rapid contrast-enhanced MR angiographic acquisitions have the potential to facilitate accurate noninvasive assessment of the entire vasculature from the abdominal aorta to the pedal arch. Synchronizing the arrival of the contrast agent bolus in the targeted anatomy with image acquisition (7,8) is crucial to the effective use of contrast-enhanced MR angiography. This is normally achieved by performing a test bolus injection (9), fluoroscopic triggering (10,11), or automated triggering (12).

To image arteries of the lower extremities, bolus chase MR angiography, in which automated triggering is combined with table movement with rapid acquisitions at successive levels of the vasculature, similar to bolus chase x-ray angiography, has been introduced (13–17). Early implementations of bolus chase MR angiography have proven to be successful in studies performed with small numbers of patients and volunteers. However, accurate depiction of the distal vasculature has been problematic owing to variability in the time of contrast agent arrival in the distal extremities (18–20).

A different approach to contrast-enhanced MR angiography involves acquiring multiple 3D volumes during the passage of the contrast agent bolus by using time-resolved acquisition (21,22). With one such acquisition—that is, time-resolved imaging of contrast kinetics (TRICKS)—the repeated sampling of the critical central k-space views is combined with temporal interpolation to produce a series of time-resolved 3D images (21). Time-resolved acquisitions such as TRICKS obviate timing tests (21–23) and a separate acquisition of precontrast images for mask-mode subtraction (24). The purpose of our study was to compare the diagnostic accuracy of 3D TRICKS MR angiography with that of DSA for imaging the peripheral vasculature.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients were recruited for a National Institutes of Health–funded study of MR angiography. All patients were enrolled after being scheduled for DSA and before undergoing percutaneous or surgical intervention. Prior to enrollment, patients were screened for standard MR imaging contraindications (ie, cardiac pacemaker, metallic implants, claustrophobia). MR angiography was not performed for treatment planning, and the MR angiographic results were not used to determine whether an individual would undergo DSA. A total of 69 patients (56 male patients, 13 female patients; mean age, 63 years; age range, 44–71 years) were imaged. All patients had symptomatic lower extremity arterial occlusive disease, including claudication, nonhealing ulcers, and rest pain, when they presented to our vascular surgery service. Written informed consent was obtained from all patients prior to their inclusion in the study, in accordance with our institutional review board guidelines.

DSA Technique
All conventional angiographic examinations were performed by using a digital subtraction technique. A Seldinger approach was used to introduce a 5-F angiographic catheter, and then the appropriate test injections were performed by using a nonionic contrast agent (iohexol, Omnipaque; Nycomed-Amersham, Princeton, NJ). DSA images were acquired by using a 38-cm field of view and an image matrix of 1,024 x 1,024 pixels (Integris; Philips, Best, the Netherlands). Sixteen to 20 mL of the contrast agent was injected into each station at a rate of 8–10 mL/ sec by using a power injector (Mark V; MEDRAD, Indianola, Pa), and sequential DSA images were obtained. The patient was then repositioned for imaging of a new area of the anatomy, and the sequence was repeated. A total contrast agent volume of 150–200 mL was administered. The DSA examinations consisted of anteroposterior evaluations of the abdomen, followed by dual oblique views of the pelvis and anteroposterior overlapping evaluations of the lower extremities.

Patients were sedated for the examinations. We observed them for 4–6 hours after imaging to ensure that no hemorrhage or other vascular compromise (ie, damage or thrombosis) had occurred. The DSA studies were recorded on film hard copy in a four images on one film or six images on one film format for evaluation by the radiologists (J.S.S., T.W.K.). Techniques to improve opacification of the distal runoff arteries, such as selective injection, reactive hyperemia, and vasodilation, were performed if clinically indicated and as determined by the interventional radiologist performing the procedure. Because of the small increased risk associated with these procedures, however, they were not routinely used. For each station, the vascular radiologist selected the best available DSA images, which were used as the reference standards.

MR Angiographic Technique
All MR angiographic examinations were performed with a 1.5-T MR unit (Signa; GE Medical Systems, Waukesha, Wis) equipped with echospeed gradients (23-mT/m gradient strength, 120-mT/m/msec slew rate) operating at a slew rate of 77 mT/m/msec. Localizer MR images were obtained with a two-dimensional fast spoiled gradient-echo sequence in the sagittal plane at each of three stations: abdomen and pelvis, thighs, and lower part of the legs. Localizer image acquisition times were between 23 and 35 seconds, and the abdominal station was imaged during a breath hold.

Three separate TRICKS acquisitions were performed at the levels of the abdomen, thighs, and calves to image the structures that were enhanced during the first pass of the contrast agent bolus in three separate injections. The delay between injections varied from examination to examination but was typically longer than 5–7 minutes. The imaging parameters for a typical TRICKS examination were a coronal plane, 7.8/1.7 (repetition time msec/echo time msec), and a 45° flip angle. The field of view was 48 x 36 cm for the abdomen and thigh stations and 48 x 24 cm for the calf station if the patient’s anatomy allowed. Typically, 24 2.0–5.0-mm partitions were prescribed, depending on the patient’s anatomy, and resulted in reconstruction of 48 1.0–2.5-mm sections after zero filling; this yielded an anteroposterior imaging area of 4.8–12.0 cm. The acquired matrix was 312 x 144 pixels in the abdomen and thigh stations and 312 x 128 pixels in the calf station. These data were reconstructed as 512 x 384- and 512 x 256-pixel matrices, respectively. Typical imaging times were 2 minutes 20 seconds for the pelvis and thigh stations and 2 minutes 7 seconds for the calf station.

With implementation of the TRICKS technique used in this study, the k space was divided into four regions along the phase-encoding direction, and all section-encoding values were collected (21). This protocol allowed 20 temporally interpolated 3D TRICKS image volumes, representing 6–7-second "snapshots," to be reconstructed.

Contrast agent (gadodiamide, Omniscan; Nycomed-Amersham) was administered in the antecubital fossa by using a 21-gauge intravenous catheter. For integrated mask acquisition, the injection of contrast agent had to be sufficiently delayed, typically 28 seconds, to ensure that a contrast-free mask volume had been acquired. Contrast agent administration was cued by an audible pause in the pulse sequence. In the abdominal station, a breath hold was initiated 7 seconds before the pause to allow mask and contrast-enhanced images to be acquired during the same 30-second breath hold.

Precise contrast agent injections were ensured by using an MR-compatible power injector (Spectris; MEDRAD). A total contrast agent dose of 0.3 mmol per kilogram of body weight was administered at three separate injections. A slightly increasing dose was used in the cranial-to-caudal stations (0.078 mmol/kg for abdomen, 0.100 mmol/kg for thighs, and 0.122 mmol/kg for lower part of legs). Increasing the contrast agent dose at subsequent injections facilitated additional transient T1 shortening of arterial blood to compensate for the presence of residual contrast agent from prior injections on the mask image (24). An injection rate of 1.5 mL/sec was used for the majority of the patient cohort. We eventually discovered that this injection rate was causing a transient blurring of blood vessels at some examinations (25); therefore, in the last 17 patients, the injection rate for the thigh and calf stations was reduced to 0.5 mL/sec.

At all examinations, the abdominal station was imaged by using a body coil. However, two different coil configurations were used in the lower stations. At earlier examinations, a body coil was used for the thigh station and a torso phased-array coil was used for the calf station. At later examinations, a prototype peripheral vascular phased-array coil (Peripheral Vascular Coil; Medical Advances, Wauwatosa, Wis) was available for use in both the thigh and calf stations.

Reconstruction of raw MR data was performed by using an offline workstation (Impact R10000; Silicon Graphics, Mountain View, Calif) with software that was developed in house. Subsequently, mask-subtracted images were recorded in the image database for inspection and postprocessing. The principal investigator (J.S.S.) reviewed the maximum intensity projection images to determine the peak arterial time frame(s) prior to recording images on film. Targeted reprojections of the peak arterial time frame were recorded on film, in a six images on one film format, at 30° intervals for further analysis. Source images were available for review to verify that the anatomic coverage of the prescribed volume included the targeted blood vessels and to identify potential signal intensity dropout caused by metallic susceptibility artifact on images. However, only the film hard-copy images were used in the final image evaluation.

Image Evaluation
Prior to reading, images were marked to ensure that the readers evaluated equivalent areas of coverage on the MR angiographic and DSA images. Two radiologists (J.S.S., T.W.K.) with extensive experience in body MR angiography, who were blinded to the results of the other examination, read the DSA and MR angiographic studies. The readers evaluated the images independently; a consensus approach was not used. One reader monitored all MR angiographic examinations, but the second reader was not involved in monitoring either DSA or MR angiographic examinations. Weeks to months later, the MR angiographic studies were read first, followed by the DSA studies. We did not read the MR angiographic and DSA studies in the temporal order in which the patients were accrued into the study and imaged. The order was randomized for the readings. No other clinical information was provided with the images. The area of coverage ideally included the infrarenal aorta, common and external iliac arteries, common and deep femoral arteries, superficial femoral arteries, above- and below-the-knee popliteal arteries, and runoff of the trifurcation vessels to the ankle and proximal part of the foot. Some vessels (trifurcation vessels) were divided into thirds for readings. Renal arteries were not evaluated in this study.

The grading system of the American College of Radiology multiinstitutional trial of peripheral MR angiography (1) was used: 0 meant normal; 1, minimal stenosis of less than 50%; 2, one lesion with 50% or greater stenosis; 3, more than one lesion with 50% or greater stenosis; and 4, occlusion. The readers were instructed to record a grade of 9 to denote vessels that could not be adequately evaluated.

Statistical Analysis
The statistical design and subsequent analysis of this study were performed by a dedicated statistician (D.M.H.). Multiple segments within each patient were evaluated by the two readers. Only those segments for which valid (grade 0–4) DSA and MR angiographic readings were performed by both readers were retained in the data set. DSA results were considered to be the reference standard, with significant stenosis indicated by a score greater than 1 and occlusion indicated by a score of 4. MR angiographic results were similarly defined. The sensitivity, specificity, positive predictive value, negative predictive value, and area under the receiver operating characteristic curve (Az) were computed for descriptive purposes by using all 2,850 interpretations. To account for the lack of statistical independence within each patient, the Az, sensitivity, and specificity of MR angiography for detection of vascular disease in each patient (ie, for each reader and location) were estimated by using all of the available vessel segments. These patient-by-patient summary statistics were then analyzed with repeated-measures analysis of variance by using a computer software program (SAS PROC MIXED; SAS Institute, Cary, NC), which accommodates for the correlations that exist as a result of two readers observing multiple vessel segments within a single patient. Cohen {kappa} statistics were used to examine interreader agreement.

The analyses were weighted by the number of diseased arteries in a patient that comprised the denominator of each estimated quantity. If, for example, there were no occluded segments (at DSA) above the knee in a patient, the sensitivity could not be computed, so a weight of 0 was assigned and that particular case was removed from the analysis. The effects of several factors on the overall results were evaluated at subsequent analyses of the data. The factors evaluated were location (above vs below the popliteal trifurcation) and injection rate (fast [1.5 mL/sec] vs slow [0.5 mL/sec]).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The three-station 3D TRICKS examination was tolerated well by all patients. There were no substantial adverse events following the injection of the gadolinium-based contrast agent. At all TRICKS examinations, at least one arterial phase image was acquired prior to venous opacification in all three stations. The 1.4-m superoinferior field of view of the combined three-station examination facilitated depiction of the major arteries from the abdominal aorta to the pedal arch (Figs 1, 2) without the need for any sophisticated measure to ensure coordination of image acquisition with contrast agent arrival. Temporal resolution was observed to be beneficial in the setting of severe vascular disease. When delayed filling occurred distal to altered flow in the superoinferior field of view, or when the filling patterns were asymmetric in the extremities (Figs 2, 3), TRICKS enabled the acquisition of images of the targeted blood vessels.



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  		Figure 1a. DSA and TRICKS angiographic visualization of the peroneal arteries in a 59-year-old man. (a) Peak arterial time frames from a 3D TRICKS examination (7.8/1.7) performed by using fast contrast agent injection (1.5 mL/sec). Composite image of coronal maximum intensity projections from the 3D TRICKS examination demonstrates the anatomic coverage typically achieved in a three-station protocol. Multiple stenoses (arrows) in both superficial femoral arteries are seen and were confirmed at x-ray DSA. Brackets in the lower station enclose the region of interest magnified in b and c. (b) Coronal maximum intensity projections from the distal station of a 3D TRICKS examination (7.8/1.7) demonstrate normal peroneal arteries (arrows) bilaterally. Trifurcation vessels are well visualized despite the modulation artifact that resulted from the fast injection rate and manifested as a ghost artifact along the length of the vessels. (c) DSA image demonstrates left peroneal artery filling (thick arrow), but the right distal peroneal artery is absent (thin arrow). The right distal peroneal artery was judged to be occluded by both readers.

 


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  		Figure 1b. DSA and TRICKS angiographic visualization of the peroneal arteries in a 59-year-old man. (a) Peak arterial time frames from a 3D TRICKS examination (7.8/1.7) performed by using fast contrast agent injection (1.5 mL/sec). Composite image of coronal maximum intensity projections from the 3D TRICKS examination demonstrates the anatomic coverage typically achieved in a three-station protocol. Multiple stenoses (arrows) in both superficial femoral arteries are seen and were confirmed at x-ray DSA. Brackets in the lower station enclose the region of interest magnified in b and c. (b) Coronal maximum intensity projections from the distal station of a 3D TRICKS examination (7.8/1.7) demonstrate normal peroneal arteries (arrows) bilaterally. Trifurcation vessels are well visualized despite the modulation artifact that resulted from the fast injection rate and manifested as a ghost artifact along the length of the vessels. (c) DSA image demonstrates left peroneal artery filling (thick arrow), but the right distal peroneal artery is absent (thin arrow). The right distal peroneal artery was judged to be occluded by both readers.

 


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  		Figure 1c. DSA and TRICKS angiographic visualization of the peroneal arteries in a 59-year-old man. (a) Peak arterial time frames from a 3D TRICKS examination (7.8/1.7) performed by using fast contrast agent injection (1.5 mL/sec). Composite image of coronal maximum intensity projections from the 3D TRICKS examination demonstrates the anatomic coverage typically achieved in a three-station protocol. Multiple stenoses (arrows) in both superficial femoral arteries are seen and were confirmed at x-ray DSA. Brackets in the lower station enclose the region of interest magnified in b and c. (b) Coronal maximum intensity projections from the distal station of a 3D TRICKS examination (7.8/1.7) demonstrate normal peroneal arteries (arrows) bilaterally. Trifurcation vessels are well visualized despite the modulation artifact that resulted from the fast injection rate and manifested as a ghost artifact along the length of the vessels. (c) DSA image demonstrates left peroneal artery filling (thick arrow), but the right distal peroneal artery is absent (thin arrow). The right distal peroneal artery was judged to be occluded by both readers.

 


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  		Figure 2a. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 2b. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 2c. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 2d. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 2e. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 2f. Efficacy of TRICKS imaging demonstrated in a 69-year-old man with aortic occlusion. (a) Composite of coronal maximum intensity projection images from the peak arterial time frames of a 3D TRICKS examination (7.8/1.7) show the entire lower extremity vascular tree (note aortoiliac occlusions). Arrow points to occlusion of the right superficial femoral artery. (b) Correlating DSA image shows aortic occlusion (arrow). (c) DSA image shows collateral vessels establishing flow through the common femoral arteries (arrows). (d) Runoff DSA image shows minimal opacification of vessels (arrows), particularly in the right leg. (e) Advantages of time-resolved acquisition are reflected in 3D TRICKS time frames (7.8/1.7) demonstrating the peak arterial filling of the aortorenal arteries just above the occlusion at 28 seconds (short arrows) and the maximum signal intensity of the common femoral arteries at 42 seconds (long arrows). (f) Coronal maximum intensity projection 3D TRICKS time frames (7.8/1.7) acquired 28-91 seconds after contrast agent injection from the distal runoff station. The left leg is only intermittently filled, and the right leg becomes more obscured by veins in later time frames. The imaging of runoff vessels in this patient probably would have been problematic with use of a non-time-resolved approach.

 


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  		Figure 3a. Insufficient vessel opacification at DSA in a 52-year-old man. (a) DSA image shows right iliac artery stenosis (thick arrows), but no left iliac artery opacification (thin arrows) is depicted. No femoral popliteal artery opacification was seen at a later DSA examination. (b) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows right iliac artery stenosis (thick arrows). However, the left side shows retrograde filling of a stenotic external iliac artery (thin arrows) and a normal common femoral artery. (c) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows normal left lower extremity arteries (arrows) past the left iliac occlusion.

 


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  		Figure 3b. Insufficient vessel opacification at DSA in a 52-year-old man. (a) DSA image shows right iliac artery stenosis (thick arrows), but no left iliac artery opacification (thin arrows) is depicted. No femoral popliteal artery opacification was seen at a later DSA examination. (b) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows right iliac artery stenosis (thick arrows). However, the left side shows retrograde filling of a stenotic external iliac artery (thin arrows) and a normal common femoral artery. (c) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows normal left lower extremity arteries (arrows) past the left iliac occlusion.

 


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  		Figure 3c. Insufficient vessel opacification at DSA in a 52-year-old man. (a) DSA image shows right iliac artery stenosis (thick arrows), but no left iliac artery opacification (thin arrows) is depicted. No femoral popliteal artery opacification was seen at a later DSA examination. (b) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows right iliac artery stenosis (thick arrows). However, the left side shows retrograde filling of a stenotic external iliac artery (thin arrows) and a normal common femoral artery. (c) Three-dimensional TRICKS MR angiogram (7.8/1.7) shows normal left lower extremity arteries (arrows) past the left iliac occlusion.

 
Pooled Results
After removal of those segments for which either reader assigned a grade of 9 at DSA or MR angiography, the remaining vessels were subjected to further analysis. The sample of vessels graded as 9 was dominated by the number of DSA segments for both reader 1 (89 at DSA, 38 at MR angiography) and reader 2 (128 at DSA , 63 at MR angiography). A total of 2,850 observations (two observations per vessel) were performed in the 69 patients: 1,470 above and 1,380 below the knee. When results were pooled over reader, injection rate, and location, readings indicated a sensitivity of 78% and a specificity of 98% for MR angiographic detection of occlusion and values of 77% and 91%, respectively, for MR angiographic detection of significant stenosis. Interreader agreement was high, but when analyses of vessel location and injection rate were performed, significant trends emerged.

Interreader Variability
Interreader agreement (Table 1) was high for detection of both occlusion ({kappa} = 0.83) and significant stenosis ({kappa} = 0.74) at DSA. Results were similar, although slightly lower, for detection of occlusion ({kappa} = 0.76) and significant stenosis ({kappa} = 0.68) at MR angiography. Separate receiver operating characteristic analyses of the detection of occlusive and significant disease by readers 1 (Az = 0.90 and 0.87, respectively) and 2 (Az = 0.95 and 0.91, respectively) indicated slightly higher scores for reader 2 (Fig 4).


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  		TABLE 1. Interreader Agreement on Depiction of Occlusion and Stenosis at MR Angiography and DSA

 


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  		Figure 4a. (a) Receiver operating characteristic curves for detection of occlusion by readers 1 (Az = 0.90) and 2 (Az = 0.95) after pooling over location and injection rate. (b) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) by readers 1 (Az = 0.87) and 2 (Az = 0.91) after pooling over location and injection rate.

 


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  		Figure 4b. (a) Receiver operating characteristic curves for detection of occlusion by readers 1 (Az = 0.90) and 2 (Az = 0.95) after pooling over location and injection rate. (b) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) by readers 1 (Az = 0.87) and 2 (Az = 0.91) after pooling over location and injection rate.

 
Location Effects
The sensitivity and specificity of MR angiography for depiction of vessels above the knee were significantly (P < .05) higher. When pooled over reader and injection rate, the results for above-the-knee vessels yielded a sensitivity of 86% and a specificity of 98% (Az = 0.96) for occlusion detection and values of 82% and 90% (Az = 0.92), respectively, for significant stenosis detection. Below-the-knee data yielded a sensitivity of 68% and a specificity of 98% (Az = 0.89) for occlusion detection and values of 69% and 92% (Az = 0.84), respectively, for significant stenosis detection (Fig 5).



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  		Figure 5a. (a) Receiver operating characteristic curves for detection of occlusion above the knee with fast (Az = 0.95) and slow (Az = 0.98) contrast agent injections indicate a trend toward higher sensitivity and specificity with the slow injection rate examinations. (b) Receiver operating characteristic curves indicate a similar trend for detection of occlusion below the knee with fast (Az = 0.87) and slow (Az = 0.95) injections. (c) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) above the knee with fast (Az = 0.91) and slow (Az = 0.95) contrast agent injections indicate a trend toward higher sensitivity and specificity with slow injection rate examinations. (d) Receiver operating characteristic curves indicate a similar trend for detection of significant stenosis below the knee with fast (Az = 0.83) and slow (Az = 0.89) injections.

 


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  		Figure 5b. (a) Receiver operating characteristic curves for detection of occlusion above the knee with fast (Az = 0.95) and slow (Az = 0.98) contrast agent injections indicate a trend toward higher sensitivity and specificity with the slow injection rate examinations. (b) Receiver operating characteristic curves indicate a similar trend for detection of occlusion below the knee with fast (Az = 0.87) and slow (Az = 0.95) injections. (c) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) above the knee with fast (Az = 0.91) and slow (Az = 0.95) contrast agent injections indicate a trend toward higher sensitivity and specificity with slow injection rate examinations. (d) Receiver operating characteristic curves indicate a similar trend for detection of significant stenosis below the knee with fast (Az = 0.83) and slow (Az = 0.89) injections.

 


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  		Figure 5c. (a) Receiver operating characteristic curves for detection of occlusion above the knee with fast (Az = 0.95) and slow (Az = 0.98) contrast agent injections indicate a trend toward higher sensitivity and specificity with the slow injection rate examinations. (b) Receiver operating characteristic curves indicate a similar trend for detection of occlusion below the knee with fast (Az = 0.87) and slow (Az = 0.95) injections. (c) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) above the knee with fast (Az = 0.91) and slow (Az = 0.95) contrast agent injections indicate a trend toward higher sensitivity and specificity with slow injection rate examinations. (d) Receiver operating characteristic curves indicate a similar trend for detection of significant stenosis below the knee with fast (Az = 0.83) and slow (Az = 0.89) injections.

 


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  		Figure 5d. (a) Receiver operating characteristic curves for detection of occlusion above the knee with fast (Az = 0.95) and slow (Az = 0.98) contrast agent injections indicate a trend toward higher sensitivity and specificity with the slow injection rate examinations. (b) Receiver operating characteristic curves indicate a similar trend for detection of occlusion below the knee with fast (Az = 0.87) and slow (Az = 0.95) injections. (c) Receiver operating characteristic curves for detection of significant stenosis (ie, at least one >=50% stenosis) above the knee with fast (Az = 0.91) and slow (Az = 0.95) contrast agent injections indicate a trend toward higher sensitivity and specificity with slow injection rate examinations. (d) Receiver operating characteristic curves indicate a similar trend for detection of significant stenosis below the knee with fast (Az = 0.83) and slow (Az = 0.89) injections.

 
Injection Rate
When the effect of injection rate was considered and pooled over readers, we observed an improvement in the sensitivity of MR angiography for depiction of both significant stenosis and occlusion. However, there was a lack of statistical power in the data to conclude that the differences were significant. When pooled over location and reader, the slow injection rate examinations yielded a sensitivity of 89% and a specificity of 97% (Az = 0.97) for MR angiographic detection of occlusion and values of 87% and 90% (Az = 0.92), respectively, for detection of significant stenosis (Table 2). These results are demonstrated graphically in Figure 5. However, given the lack of randomization, it is impossible to rule out time dependence as the source of these improvements.


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  		TABLE 2. Performance Values for MR Angiography

 
DSA Errors
In some cases, discrepant DSA and MR angiographic cases were inspected side by side in an unblinded fashion to validate the results of the blinded readings. We found that 20 of the 64 discrepant findings of one reader resulted from the visualization of vessels that appeared to be patent at MR angiography, but, because of catheter placement or dilution of the contrast agent, were not filled at DSA (Figs 1–3). When adjusted for this effect, the sensitivity of TRICKS MR angiography for depiction of occluded vessels below the knee (pooled over injection rate and reader) increased from 68% to 78%.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The 3D TRICKS pulse sequence has proven to be a robust, easy-to-use, and accurate method of acquiring contrast-enhanced MR angiograms of the lower extremities. With a three-station protocol, we were able to perform an examination with a superoinferior extent of 1.4 m, which facilitated the depiction of vessels of the abdomen, pelvis, and lower extremities in less than 30 minutes. During this study, we developed image-processing capabilities that enabled physicians to see 3D data sets that showed peak arterial time frames from all three stations before the patients left the MR suite. This achievement was due to software optimization that enabled the quick and automatic identification of the data that formed the peak arterial time frame prior to image reconstruction (26).

Patients tolerated the examination well. This was proven by the results of a health services survey that was conducted in a separate analysis of this patient cohort and that indicated a clear preference for the MR angiographic experience as opposed to the conventional angiographic experience (2,3). The conclusions of that work suggest an optimistic outlook for the cost-effectiveness of MR angiography. When learning curve effects were taken into account, TRICKS examinations resulted in high sensitivity and specificity with minimal patient discomfort as compared with the more invasive x-ray DSA examinations.

An additional important aspect of the feasibility of TRICKS was demonstrated by its capability to consistently yield pure arterial phase images, particularly in the calf station. This factor sets the TRICKS approach apart from other techniques (18–20), not only because arterial phase images are obtainable but also because they are obtainable without consideration of injection timing. Additionally, our evaluations of the peripheral vessels were aided by the temporal resolution achieved with the TRICKS approach in cases of extensive occlusive disease and/or asymmetric filling of patent vessels in one extremity relative to the other.

The data presented here were accrued during the years of 1996–1998 when 3D TRICKS was an emerging technique undergoing development. Improvements in injection protocol, streamlining of the examination for greater patient comfort, coil development, and software upgrades all contributed to improvements in image quality during this period. Therefore, in a comparison of slow versus fast injection rates, time-dependent effects cannot be ruled out as the source of improvement, even though ghost artifacts and vessel blurring have been shown to be significantly reduced with lower injection rates (25). Such improvements are expected of any emerging technology during its early implementation. Therefore, a more accurate assessment of sensitivity and specificity might be determined from the subset of later examinations.

We believe that this study represents the first clinical evaluation of the feasibility and diagnostic accuracy of a new solution to some of the problems encountered during MR angiography of the lower extremity arteries. Investigators have proposed several approaches for imaging the lower extremity arteries with or without the use of contrast agents. Initial reports of the accuracy of two-dimensional time-of-flight methods indicated excellent sensitivity in infrapopliteal vessel detection when a tailored examination of a single lower part of the leg was performed (27). Despite these successes, time-of-flight examinations are subject to lengthy examination times and artifactual signal intensity losses that result from saturation effects.

In a multicenter trial, Baum et al (1) later observed that the two-dimensional time-of-flight method had diagnostic accuracy similar to that of intraarterial DSA when both techniques were compared with intraoperative angiography as the reference standard. It should be noted that in this study, DSA had a sensitivity of 77% and a specificity of 92% for depicting significant stenosis and a sensitivity of 83% and a specificity of 81% for depicting occlusion. Suboptimal filling of patent distal vessels is a known problem with DSA as the reference standard (27–29). Motivated by this fact, we conducted a side-by-side evaluation of DSA and MR angiographic reading discrepancies. We found that below the knee, 27% of the discrepancies between MR angiography and DSA for one of the readers were due to vessels that were not visualized at DSA but were graded as patent at TRICKS MR angiography.

We have seen a trend toward lower specificity in the distal runoff station that results from miscategorization of the location of stenoses. When we divided runoff vessels into thirds, determining which vessel segment was stenotic (ie, middle or distal third) became a source of error. The distal vessels become quite small and difficult to see at DSA as well. This shortcoming may be relevant to reader experience in this case. We noted that an additional 10 segments (exclusive of the vessel segments not filled at DSA) for which there were discrepancies between MR angiography and DSA were involved with diminutive peroneal arteries, which have questionable clinical importance in this circumstance.

Several investigators (30–35) have proposed alternate approaches for performing lower extremity contrast-enhanced MR angiography. Their reports demonstrated sensitivities that ranged from 88% to 100% and specificities that ranged from 94% to 100% for pelvic vessel detection. Our study results for the proximal vessels demonstrated similar accuracy, although our aim of imaging the entire lower extremity vasculature necessitated the use of a lower dose of contrast agent in the proximal station. Several of the studies in which high accuracy in infrapopliteal vessel detection was demonstrated were performed with only a two-station examination, which made it difficult to see the distal infrapopliteal vessels (30,31). Subsequently, Ho et al (14–16) and Meany et al (17) reported on an MR angiographic technique that incorporates fast imaging and rapid table motion for evaluation of the entire lower extremity. Initial reports of high sensitivity and specificity with this technique have been followed by recent reports that describe limitations below the knee, where image quality may be compromised by venous overlay in up to 30% of cases (18–20). A sensitivity of 79% for detection with MR angiographic techniques in the peroneal artery has been reported in previous studies (14).

The study presented here was not without limitations. In light of the observed discrepancies between DSA and MR angiography, independent evaluation of patency with intraoperative DSA would have been beneficial. In addition, we did not perform evaluation of the foot vessels, which may be useful in determining the appropriate surgical intervention. The vessels of the foot were not evaluated primarily because of the lack of an appropriate coil at the time this study was performed. In fact, during the earliest phase of patient accrual, no peripheral vascular coils were available and a torso coil with limited superior-inferior coverage was used. Furthermore, without a reference standard that is more accurate than DSA, evaluation of the foot vessels with MR angiography could result in more discrepant findings. Finally, we did not compare time-resolved MR angiography with other contrast-enhanced MR angiographic techniques in this study. However, initial patient results of comparing time-resolved contrast-enhanced MR angiography with a bolus chase technique indicate that more vessels are visualized with the time-resolved technique (20).

It is possible that the specificities and sensitivities reported here can be improved with the use of higher spatial resolution examinations, particularly in assessments of the patency of small arteries of the lower part of the leg. In this work, we traded spatial for temporal resolution: Any increase in spatial resolution resulted in a proportionate decrease in temporal resolution. In this regard, the spatial resolution of TRICKS examinations would improve with shorter repetition times (36). To use a consistent set of acquisition parameters, we fixed the repetition time at the value that was achievable at the beginning of patent accrual (ie, in 1996). We are currently acquiring images with higher spatial resolution by using the same temporal resolution. In addition, we are exploring undersampled projection techniques for further improvements in spatial and temporal resolution (37,38).

In conclusion, we have evaluated time-resolved contrast-enhanced MR angiography for assessment of the severity of peripheral vascular occlusive disease. Three-station 3D TRICKS was used to acquire MR angiograms of the peripheral vasculature with high sensitivity and specificity while achieving a combined coverage of 1.4 m in less than 30 minutes.


   ACKNOWLEDGMENTS
 
The authors acknowledge the contributions of Mary Ellen Hagenauer, BS, and Bret J. Borowski, RTR. Contrast media was supplied by Amersham Health, Princeton, NJ.


   FOOTNOTES
 
2 Current address: Department of Radiology, Indiana University School of Medicine, Indianapolis. Back

3 Current address: Department of Clinical Neurosciences and Radiology, University of Calgary, Alberta, Canada. Back

Abbreviations: Az = area under receiver operating characteristic curve, DSA = digital subtraction angiography, TRICKS = time-resolved imaging of contrast kinetics, 3D = three-dimensional

Author contributions: Guarantors of integrity of entire study, J.S.S., T.J.C., T.M.G.; study concepts and design, all authors; literature research, T.J.C., T.M.G.; clinical studies, J.S.S., T.W.K., T.M.G.; experimental studies, J.S.S., F.R.K., R.F.; data acquisition, J.S.S., T.J.C., F.R.K., R.F.; data analysis/interpretation, all authors; statistical analysis, J.S.S., D.M.H.; manuscript preparation, all authors; manuscript definition of intellectual content, J.S.S., T.J.C., D.M.H., F.R.K., R.F., C.A.M., T.M.G.; manuscript editing, J.S.S., T.J.C., F.R.K., T.M.G.; manuscript revision/review and final version approval, all authors.


   REFERENCES
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 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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