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Published online before print December 19, 2006, 10.1148/radiol.2422051111

(Radiology 2006;242:610.)

A more recent version of this article appeared on December 1, 2006
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© RSNA, 2006

Vascular and Interventional Radiology

Peripheral Arteries in Diabetic Patients: Standard Bolus-Chase and Time-resolved MR Angiography1

Gustav Andreisek, MD, Thomas Pfammatter, MD, Kerstin Goepfert, RT, Daniel Nanz, PhD, Patrice Hervo, RT, Renate Koppensteiner, MD and Dominik Weishaupt, MD

1 From the Institute of Diagnostic Radiology (G.A., T.P., K.G., D.W.), Department of Internal Medicine, Division of Angiology (R.K.), and Department of Medical Radiology (D.N.), University Hospital Zurich, Raemistrasse 100, CH-8091 Zurich, Switzerland; and GE Healthcare, Buc, France (P.H.). Received July 1, 2005; revision requested September 1; revision received October 26; accepted November 14; final version accepted May 1, 2006. Address correspondence to D.W. (e-mail: dominik.weishaupt{at}usz.ch).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively determine the diagnostic performance of a combination of standard bolus-chase magnetic resonance (MR) angiography and MR angiography with time-resolved imaging of contrast kinetics (TRICKS) for depicting severity of peripheral vascular disease of the lower extremity, including the pedal arteries, in diabetic patients with digital subtraction angiography (DSA) as the reference standard.

Materials and Methods: An ethical committee approved this study; written informed consent was obtained from patients. Standard three-station and TRICKS MR angiography of the calf and foot were performed in 31 consecutive diabetic patients (23 men, eight women; mean age, 67 years; range, 43–81 years). Two readers separately assessed images of arterial segments as diagnostic or nondiagnostic and graded stenosis. Results were compared with those at DSA when the corresponding arterial segments were considered diagnostic at DSA. Wilcoxon signed rank test was used to determine if a significant difference between imaging techniques existed, and {kappa} statistics were used to determine interobserver agreement.

Results: The difference between standard MR angiography and DSA regarding the number of diagnostic segments in the thigh was not significant (P = .50). A significantly higher number of calf and foot segments was considered diagnostic at TRICKS MR angiography than at standard MR angiography (P < .025). Sixteen of 26 segments in the foot that were considered nondiagnostic at DSA were considered diagnostic at TRICKS MR angiography. Average sensitivity of standard MR angiography for depicting hemodynamically significant arterial stenosis was 84% (reader 1) and 83% (reader 2) in the thigh and 78% (reader 1) and 80% (reader 2) in the calf. For both readers, average specificity was 97% in the thigh and 90% in the calf. Sensitivity and specificity of TRICKS MR angiography in the calf and foot were improved compared with those at standard MR angiography.

Conclusion: TRICKS MR angiography of the distal calf and pedal vessels is superior to standard MR angiography regarding the number of diagnostic segments and assessment of the degree of luminal narrowing.

© RSNA, 2006


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
During the past years, contrast material–enhanced magnetic resonance (MR) angiography has become an attractive option for noninvasive imaging of peripheral vascular disease. Results of several studies (13) have shown that contrast-enhanced three-station bolus-chase MR angiography with a single injection depicts hemodynamically significant arterial stenosis and occlusion of the lower extremity and runoff vessels with a sensitivity between 92% and 94% and a specificity between 90% and 99%. However, standard bolus-chase MR angiographic protocols have limitations. Although the field of view encompasses the abdominal aorta and the arteries of the pelvis, thigh, and calf (39), the pedal vessels usually are not covered. The evaluation of the arteries in the calf often is hampered because of venous contamination due to either bolus-timing problems or inflammation of soft tissues (6,1014).

Both limitations are accentuated for patients with diabetes, because the associated peripheral vascular disease typically spares the proximal vessels and mainly affects the more distal arteries in the calf and, in a later stage, the foot (2,1517). The risk of developing critical limb ischemia is 11 times higher for patients with diabetes than for patients without diabetes (18). A clinical assessment of the arterial tree should include the pedal arteries, which may serve as potential target sites for arterial bypass grafts (2,17,19).

Thus, the purpose of our study was to prospectively determine the diagnostic performance of a combination of standard bolus-chase MR angiography and MR angiography with time-resolved imaging of contrast kinetics (TRICKS) for depicting the severity of peripheral vascular disease of the lower extremity, including the pedal arteries, in patients with diabetes by using digital subtraction angiography (DSA) as the reference standard.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients
The local ethical committee approved this prospective study. Written informed consent was obtained from all patients. One author (P.H.) is an employee of GE Healthcare Systems. He gave technical advice. All authors had full control of the data and the information of this study.

During a 6-month period (July 2004 to December 2004), 31 consecutive patients with diabetes and peripheral vascular disease (23 men, eight women; mean age, 67 years; age range, 43–81 years) were referred to our institution to undergo elective DSA of the peripheral arteries of the lower extremity, including the pedal vessels. Five (16%) patients had type 1 diabetes mellitus (insulin dependent), and 26 (84%) patients had type 2 diabetes mellitus (non–insulin dependent, 12 patients; insulin dependent, 14 patients). Patients had intermittent claudication (Fontaine grade IIa or Rutherford grade 1 or 2, 10 patients; Fontaine grade IIb or Rutherford grade 3, 16 patients), rest pain (Fontaine grade III or Rutherford grade 4, one patient), or chronic trophic lesions of the foot with either nonhealing ulceration or focal gangrene (Fontaine grade IV or Rutherford grade 5 or 6, four patients) (20). All patients underwent both elective DSA and standard bolus-chase MR angiography combined with TRICKS MR angiography. DSA was performed first and was followed by MR angiography (delay between DSA and MR angiography: mean, 3 days; median, 1 day; range, 1–29 days).

Conventional DSA
Intraarterial fine-needle DSA of the diseased lower extremity (right lower extremity, 15 patients; left lower extremity, 16 patients) was performed (Integris V3000 or Integris V5000; Philips Medical Systems, Best, the Netherlands) by one angiographer (R.K., 15 years of experience). A standard DSA procedure was followed, with multiple manual injections of a total of 40–60 mL of nonionic iodinated iso-osmolar contrast material (32 mg of iodine per 100 mL of iodixanol, Visipaque 320; Amersham Health, Princeton, NJ) (21) per kilogram of body weight. No vasodilative drugs were administered during the DSA procedure. The number of acquired projections was at the discretion of the angiographer. However, anterior projections for the evaluation of the femoral and popliteal arteries and anterior and lateral projections for the evaluation of the calf and pedal vessels were obtained in all patients.

MR Angiography
The MR angiographic protocol consisted of two parts in a single session. Standard three-station bolus-chase MR angiography was performed in the diseased calf and foot where fine-needle DSA also was performed. TRICKS MR angiography of the diseased calf and foot was then performed. A 1.5-T unit (Signa Excite HD; GE Healthcare, Waukesha, Wis) with a 12-element quadrature phased-array coil (Peripheral Vascular Coil; USA Instruments, Aurora, Ohio) was used for both parts of the examination.

Standard three-station bolus-chase MR angiography was performed (SmartStep; GE Healthcare) (22). This involved acquisition of (a) three three-plane nonenhanced localizer images (repetition time msec/echo time msec, 4.9/1.5; flip angle, 60°) of the abdomen and pelvis (first station), thighs (second station), and calves (third station); (b) a test-bolus timing image by using a 1-mL bolus of gadobutrol (Gadovist 1.0; Schering, Berlin, Germany) at a flow rate of 1 mL/sec; and (c) a contiguous MR angiographic mask image (22,23). The contrast-enhanced MR angiographic imaging was synchronized with a biphasic administration of 12 mL gadobutrol (6 mL gadobutrol injected at a flow rate of 1 mL/sec followed by 6 mL gadobutrol at a flow rate of 0.6 mL/sec) and a 25-mL flush of saline solution at a flow rate of 1 mL/sec by using an automated injector (MR Spectris; Medrad, Pittsburgh, Pa) (13). The parameters of the mask image and the contrast-enhanced images were identical for all three stations (3.4/0.8; inversion time msec [for tissue suppression], 14.0 msec; flip angle, 30°; receiver bandwidth, 83.3 kHz; field of view, 48 x 36 cm; signals acquired, one; slab thickness, 2.4 mm; voxel size before and after interpolation, 1.8 x 1.8 x 2.4 mm and 0.9 x 0.9 x 1.2 mm; acquisition time for each station, 19 seconds). Mask data were subtracted from the corresponding contrast-enhanced data.

At time-resolved MR angiography, a commercialized TRICKS sequence (GE Healthcare) with a temporal resolution of 11.0 seconds was used. In total, 11 three-dimensional TRICKS data sets were acquired 121 seconds after the administration of 6 mL gadobutrol at a flow rate of 1.0 mL/sec. Other parameters were as follows: 5.5/1.2; flip angle, 30°; receiver bandwidth, 31.2 kHz; field of view, 320 x 224 mm; signals acquired, one; slab thickness, 2.4 mm; voxel size before and after interpolation, 1.4 x 1.0 x 2.4 mm and 0.9 x 0.6 x 1.4 mm; and sagittal orientation of the imaging slab. Because of the widely varying circulation time in patients with diabetes, the TRICKS acquisition was synchronized exactly with the arrival of the contrast material in the targeted vessels. The transit time from the injection site (antecubital fossa) to the popliteal artery was measured by administering another 1-mL test bolus of gadobutrol (flow rate, 1 mL/sec) prior to TRICKS MR angiography. TRICKS MR angiography was performed after bolus-chase MR angiography because our experience has shown that the increase in background signal caused by the previous contrast injection is low with the TRICKS data set.

Image Analysis
Two radiologists (T.P., D.W.), who were blinded to all clinical and radiologic data, independently evaluated DSA images and MR angiograms in random order. Only MR angiograms of the diseased leg (where DSA was performed) were analyzed. All MR data, including the source data and the standardized maximum intensity projection images, were evaluated at a workstation (Advantage Windows 4.2; GE Healthcare). The reading session for the standard bolus-chase MR angiograms was separated from that for the TRICKS MR angiograms by a 3-week interval.

The arterial system from the renal arteries to the foot was divided into 20 segments. Analysis of standard bolus-chase MR angiograms included all 20 vascular segments, whereas analysis of TRICKS MR angiograms included segments 10–20. The segments were analyzed in two respects. First, both readers classified depiction of all segments (segments 1–20 on standard bolus-chase MR angiograms and segments 10–20 on TRICKS MR angiograms) as either diagnostic or nondiagnostic. A segment was considered diagnostic if all clinically relevant diagnostic information could be obtained with good differentiation of arterial vasculature from background tissue. Segments were considered nondiagnostic if diagnostic information could not be derived because of blurring of the arterial segment, inadequate vessel enhancement, motion or metal artifacts, venous contamination, or field-of-view limitations.

Second, both readers assessed all segments with a corresponding diagnostic segment on a DSA image as a reference standard for the presence of luminal narrowing or occlusion by using an electronic caliper. For the thigh and calf arteries, the following grading system was used: grade 1, normal vessel or vessel irregularities (<10% luminal narrowing); grade 2, mild arterial stenosis (10%–49% luminal narrowing); grade 3, severe arterial stenosis (50%–99% luminal narrowing); or grade 4, occlusion (1,22). The pedal vessels (segments 17–20) were assessed as follows: grade 1, normal vessel or vessel irregularities (<50% luminal narrowing); grade 2, severe arterial stenosis (50%–99% luminal narrowing); or grade 3, occlusion. There was no grade 4 in the pedal vessels. Stenoses of less than 50% luminal narrowing were considered hemodynamically insignificant, whereas stenoses of more than or equal to 50%–99% luminal narrowing or occlusion were considered hemodynamically significant (24). The most severe stenotic luminal change within an arterial segment was used for grading.

The analysis of the DSA images was performed in consensus by the same two radiologists by using the same criteria and classification system for assessing image quality and presence of luminal narrowing or occlusion that was used at the analysis of MR images. The reading session for DSA images was separated from that for the MR angiograms by a 6-week interval (22).

Because suboptimal contrast material filling of patent vessels is a problem at DSA that may result in a substantial number of nondiagnostic segments (4,24,25), a segment-by-segment evaluation of DSA and MR angiographic reading discrepancies was conducted (5). Both readers performed this evaluation in consensus at a separate reading session. The purpose of this additional subanalysis was to characterize the relevance of nonvisualized vessel segments at DSA for the calculation of true-positive and true-negative findings in the assessment of the diagnostic performance of contrast-enhanced MR angiography.

Statistical Analysis
Descriptive results for image quality (number of diagnostic arterial segments) are reported in absolute and relative numbers. The Wilcoxon signed rank test was used to determine whether a significant difference between the imaging techniques existed with regard to the number of segments classified as diagnostic or nondiagnostic. A Bonferroni correction was used to adjust for multiple comparisons (three modalities with two readers yields four comparisons), which required a P value of .05/6 = .0083 to indicate a significant difference (22).

Interobserver agreement between readers was determined by calculating the Cohen {kappa} coefficient (26). All computations were performed by using software (SPSS, release 11.5; SPSS, Chicago, Ill).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
The number of theoretically analyzable arterial segments was 465 on DSA images (15 segments times 31), 620 on standard bolus-chase MR angiograms (20 segments times 31), and 341 on TRICKS MR angiograms (11 segments times 31).

Diagnostic versus Nondiagnostic Segments
On DSA images (Table 1), 439 (94%) of 465 segments were considered diagnostic and 26 (6%) segments were considered nondiagnostic. All nondiagnostic segments were located in the foot, where 26 (21%) of 124 segments were rated as nondiagnostic because of suboptimal filling and low contrast enhancement.


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Table 1. Nondiagnostic Arterial Segments at DSA, Standard MR Angiography, and TRICKS MR Angiography in 31 Patients with Peripheral Vascular Disease

 
On standard bolus-chase MR angiograms, reader 1 considered 468 (76%) of 620 segments diagnostic and 152 (24%) nondiagnostic. Reader 2 considered 466 (75%) of 620 segments diagnostic and 154 (25%) nondiagnostic. Each reader considered seven (5%) of 155 abdominal and pelvic segments nondiagnostic because of signal void after renal stent graft implantation or because of metal artifacts caused by a hip prosthesis. On standard bolus-chase MR angiograms, 123 (99%) of 124 thigh segments were considered diagnostic by both readers. When compared with the number of diagnostic segments at DSA (all 124 [100%] segments were diagnostic at DSA), this difference was not significant (P = .50 for both readers).

On standard bolus-chase MR angiograms of the calf, reader 1 considered 177 (82%) of 217 calf segments diagnostic, and reader 2 considered 172 (79%) diagnostic (Fig 1). These were significantly lower percentages than that at DSA (P < .001 for both readers), where all 217 (100%) calf segments were diagnostic for both readers. Similarly, the number of diagnostic segments in the foot on standard bolus-chase MR angiograms (reader 1, 20 [16%] of 124; reader 2, 23 [19%]) was also significantly lower (P = .008 for reader 1, P = .004 for reader 2) than that at DSA.


Figure 1
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Figure 1a: MR angiographic and DSA images in 79-year-old man with diabetes and left-sided peripheral vascular disease (Fontaine grade IV). (a) Coronal maximum intensity projection reconstructed from standard bolus-chase MR angiograms shows good delineation of arteries of first (abdomen and pelvis) and second (thigh) station. Visibility of all crural arteries is hampered as a result of venous contamination. After standard bolus-chase MR angiography, sagittal TRICKS MR angiography in left lower leg was performed. (b) TRICKS MR angiogram shows clear delineation of arterial vasculature without venous contamination. Complete chronic occlusion of anterior and posterior tibial arteries (grade 4), as well as occlusion of distal peroneal artery (arrow), is visible. Collateral circulation at ankle and foot is present. (c) Corresponding DSA image of left distal calf and foot illustrates correlation of TRICKS MR angiogram and DSA image.

 

Figure 1
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Figure 1b: MR angiographic and DSA images in 79-year-old man with diabetes and left-sided peripheral vascular disease (Fontaine grade IV). (a) Coronal maximum intensity projection reconstructed from standard bolus-chase MR angiograms shows good delineation of arteries of first (abdomen and pelvis) and second (thigh) station. Visibility of all crural arteries is hampered as a result of venous contamination. After standard bolus-chase MR angiography, sagittal TRICKS MR angiography in left lower leg was performed. (b) TRICKS MR angiogram shows clear delineation of arterial vasculature without venous contamination. Complete chronic occlusion of anterior and posterior tibial arteries (grade 4), as well as occlusion of distal peroneal artery (arrow), is visible. Collateral circulation at ankle and foot is present. (c) Corresponding DSA image of left distal calf and foot illustrates correlation of TRICKS MR angiogram and DSA image.

 

Figure 1
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Figure 1c: MR angiographic and DSA images in 79-year-old man with diabetes and left-sided peripheral vascular disease (Fontaine grade IV). (a) Coronal maximum intensity projection reconstructed from standard bolus-chase MR angiograms shows good delineation of arteries of first (abdomen and pelvis) and second (thigh) station. Visibility of all crural arteries is hampered as a result of venous contamination. After standard bolus-chase MR angiography, sagittal TRICKS MR angiography in left lower leg was performed. (b) TRICKS MR angiogram shows clear delineation of arterial vasculature without venous contamination. Complete chronic occlusion of anterior and posterior tibial arteries (grade 4), as well as occlusion of distal peroneal artery (arrow), is visible. Collateral circulation at ankle and foot is present. (c) Corresponding DSA image of left distal calf and foot illustrates correlation of TRICKS MR angiogram and DSA image.

 
On TRICKS MR angiograms of the calf, reader 1 considered 191 (88%) of 217 calf segments diagnostic, and reader 2 considered 184 (85%) diagnostic; these were still significantly lower percentages than that at DSA (P < .001 for both readers). However, the number of diagnostic segments at TRICKS MR angiography was higher than that at bolus-chase MR angiography.

On TRICKS MR angiograms of the foot, reader 1 considered 99 (80%) of 124 pedal segments diagnostic, and reader 2 considered 97 (78%) diagnostic. The percentages of diagnostic segments did not differ from those at DSA (P = .625 for both readers). However, the percentages of segments considered diagnostic at TRICKS MR angiography in the foot were significantly higher (P = .004 for reader 1, P = .008 for reader 2) than those at bolus-chase MR angiography.

Luminal Narrowing and Diagnostic Performance
The diagnostic performance of standard bolus-chase MR angiography and TRICKS MR angiography for depiction of peripheral vascular disease in patients with diabetes is summarized in Tables 2 and 3. Average sensitivity and specificity, respectively, for assessment of hemodynamically significant stenoses or occlusions (luminal narrowing > 50%) for the arteries in the thigh at bolus-chase MR angiography were 84% and 97% for reader 1 and 83% and 97% for reader 2. Average sensitivity and specificity, respectively, for assessment of hemodynamically significant stenoses or occlusions for the arteries in the calf at bolus-chase MR angiography were 78% and 90% for reader 1 and 80% and 90% for reader 2. Average sensitivity and specificity increased when TRICKS MR angiography was used for assessment of the calf arteries for both readers. Average sensitivity and specificity, respectively, for the arteries in the calf were 82% and 91% for reader 1 and 86% and 93% for reader 2 at TRICKS MR angiography. The significant difference was even more obvious when bolus-chase MR angiography was compared with TRICKS MR angiography in the foot. Because the image quality of standard bolus-chase MR angiography was considered diagnostic in only three patients, the corresponding sensitivity and specificity were not calculated. In contrast, average sensitivity and specificity, respectively, of TRICKS MR angiography in the foot were 58% and 90% for reader 1 and 66% and 88% for reader 2 (Fig 2).


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Table 2. Diagnostic Performance of Standard MR Angiography Compared with that of DSA for Depiction of Hemodynamically Significant Arterial Stenosis

 

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Table 3. Diagnostic Performance of TRICKS MR Angiography Compared with that of DSA for Depiction of Hemodynamically Significant Arterial Stenosis

 

Figure 2
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Figure 2a: MR angiographic and DSA images in 70-year-old man with diabetes and right-sided peripheral vascular disease (Fontaine grade IIb). (a–d) Series of sagittal maximum intensity projection images reconstructed from TRICKS MR angiographic data sets of four time frames corresponding to 62 seconds (frame 2, a), 73 seconds (frame 3, b), 84 seconds (frame 4, c), and 95 seconds (frame 5, d) after start of gadobutrol injection. There is grade 3 stenosis of distal popliteal artery (arrowhead), good contrast material runoff in anterior tibial artery (straight arrow), as well as a grade 3 stenosis of distal peroneal artery (curved arrow). Chronic occlusion (grade 4) of posterior tibial artery is present. TRICKS MR angiographic images display late retrograde filling of pedal arch and lateral plantar artery (arrows in d), which is not visible on (e) corresponding conventional DSA image.

 

Figure 2
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Figure 2b: MR angiographic and DSA images in 70-year-old man with diabetes and right-sided peripheral vascular disease (Fontaine grade IIb). (a–d) Series of sagittal maximum intensity projection images reconstructed from TRICKS MR angiographic data sets of four time frames corresponding to 62 seconds (frame 2, a), 73 seconds (frame 3, b), 84 seconds (frame 4, c), and 95 seconds (frame 5, d) after start of gadobutrol injection. There is grade 3 stenosis of distal popliteal artery (arrowhead), good contrast material runoff in anterior tibial artery (straight arrow), as well as a grade 3 stenosis of distal peroneal artery (curved arrow). Chronic occlusion (grade 4) of posterior tibial artery is present. TRICKS MR angiographic images display late retrograde filling of pedal arch and lateral plantar artery (arrows in d), which is not visible on (e) corresponding conventional DSA image.

 

Figure 2
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Figure 2c: MR angiographic and DSA images in 70-year-old man with diabetes and right-sided peripheral vascular disease (Fontaine grade IIb). (a–d) Series of sagittal maximum intensity projection images reconstructed from TRICKS MR angiographic data sets of four time frames corresponding to 62 seconds (frame 2, a), 73 seconds (frame 3, b), 84 seconds (frame 4, c), and 95 seconds (frame 5, d) after start of gadobutrol injection. There is grade 3 stenosis of distal popliteal artery (arrowhead), good contrast material runoff in anterior tibial artery (straight arrow), as well as a grade 3 stenosis of distal peroneal artery (curved arrow). Chronic occlusion (grade 4) of posterior tibial artery is present. TRICKS MR angiographic images display late retrograde filling of pedal arch and lateral plantar artery (arrows in d), which is not visible on (e) corresponding conventional DSA image.

 

Figure 2
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Figure 2d: MR angiographic and DSA images in 70-year-old man with diabetes and right-sided peripheral vascular disease (Fontaine grade IIb). (a–d) Series of sagittal maximum intensity projection images reconstructed from TRICKS MR angiographic data sets of four time frames corresponding to 62 seconds (frame 2, a), 73 seconds (frame 3, b), 84 seconds (frame 4, c), and 95 seconds (frame 5, d) after start of gadobutrol injection. There is grade 3 stenosis of distal popliteal artery (arrowhead), good contrast material runoff in anterior tibial artery (straight arrow), as well as a grade 3 stenosis of distal peroneal artery (curved arrow). Chronic occlusion (grade 4) of posterior tibial artery is present. TRICKS MR angiographic images display late retrograde filling of pedal arch and lateral plantar artery (arrows in d), which is not visible on (e) corresponding conventional DSA image.

 

Figure 2
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Figure 2e: MR angiographic and DSA images in 70-year-old man with diabetes and right-sided peripheral vascular disease (Fontaine grade IIb). (a–d) Series of sagittal maximum intensity projection images reconstructed from TRICKS MR angiographic data sets of four time frames corresponding to 62 seconds (frame 2, a), 73 seconds (frame 3, b), 84 seconds (frame 4, c), and 95 seconds (frame 5, d) after start of gadobutrol injection. There is grade 3 stenosis of distal popliteal artery (arrowhead), good contrast material runoff in anterior tibial artery (straight arrow), as well as a grade 3 stenosis of distal peroneal artery (curved arrow). Chronic occlusion (grade 4) of posterior tibial artery is present. TRICKS MR angiographic images display late retrograde filling of pedal arch and lateral plantar artery (arrows in d), which is not visible on (e) corresponding conventional DSA image.

 
Interobserver Agreement
Overall, there was good agreement ({kappa} = 0.71 for standard bolus-chase MR angiography, {kappa} = 0.78 for TRICKS MR angiography) between readers for the classification of all arterial stenoses into four grades (grades 1–4). With regard to the differentiation between hemodynamically insignificant and hemodynamically significant arterial stenosis, agreement between readers ranged from good to excellent ({kappa} = 0.75 for bolus-chase MR angiography, {kappa} = 0.82 for TRICKS MR angiography). In general, agreement between readers was better at TRICKS MR angiography than at bolus-chase MR angiography for diagnosing arterial stenoses in the calf and foot. However, these differences were not significant (P > .05).

Discrepancies between DSA and MR Angiographic Findings
The segment-by-segment analysis of the 26 arterial segments that were assessed as nondiagnostic at DSA revealed 10 (38%) segments to be not visible at bolus-chase MR angiography or at TRICKS MR angiography. The remaining 16 nondiagnostic segments were assessable only at TRICKS MR angiography. Nine (56%) of these 16 segments were normal or showed hemodynamically insignificant arterial stenosis (Fig 3). For the seven (44%) remaining segments, a hemodynamically significant arterial stenosis or occlusion was noted on TRICKS MR images.


Figure 3
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Figure 3a: MR angiographic and DSA images in 69-year-old man with diabetes and left-sided peripheral vascular disease (Fontaine grade IIb). (a) Sagittal maximum intensity projection image reconstructed from TRICKS MR angiographic data sets of a late time frame (117 seconds) shows late contrast enhancement of pedal arch with retrograde filling of lateral plantar artery (arrows). (b) Pedal arch and lateral plantar artery are not visible on corresponding DSA image.

 

Figure 3
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Figure 3b: MR angiographic and DSA images in 69-year-old man with diabetes and left-sided peripheral vascular disease (Fontaine grade IIb). (a) Sagittal maximum intensity projection image reconstructed from TRICKS MR angiographic data sets of a late time frame (117 seconds) shows late contrast enhancement of pedal arch with retrograde filling of lateral plantar artery (arrows). (b) Pedal arch and lateral plantar artery are not visible on corresponding DSA image.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
In our study, we demonstrated that the combination of standard bolus-chase MR angiography and TRICKS MR angiography offers a valuable alternative for the assessment of vascular status in patients with diabetes and symptomatic peripheral vascular disease. The complete vascular tree from the infrarenal aorta to the foot could be depicted with good quality at a single imaging session and without changing the radiofrequency coil. With regard to percentage of diagnostic segments, our results demonstrated the combination of both MR angiographic techniques to compensate for the deficits of exclusive use of standard bolus-chase MR angiography. In our study, image quality (percentage of diagnostic segments) and diagnostic performance for detection of hemodynamically significant stenosis or occlusion at the thigh and popliteal arteries were comparable to the results obtained in patients without diabetes by other study groups (3). With the state-of-the-art technique of bolus-chase MR angiography, sensitivity of 88%–100% and specificity of 82%–100% for assessment of hemodynamically significant stenosis of the femoropopliteal vessels can be obtained (3).

The diagnostic performance of the calf station at standard bolus-chase MR angiography for depiction of hemodynamically significant stenosis reported in our study (sensitivity of 46%–93% [reader 1] and 62%–100% [reader 2]) was lower than the values published by other authors (1,3,5,7,27,28). The low values were primarily caused by a high number of nondiagnostic arterial segments at standard bolus-chase MR angiography, which most likely resulted from insufficient arterial filling, venous overlay, and/or soft-tissue enhancement (6,12,13,28,29). Several approaches to overcome venous contamination of calf arteries, which is often also observed in patients without diabetes, have been published. Approaches include external venous compression at either the level of the thigh (30) or the proximal calf (7), as well as a combination of dedicated calf MR angiography and standard bolus-chase MR angiography within the same imaging session (6,7,12,28). Alternatively, venous contamination of calf arteries may be minimized by using time-resolved MR angiography. There are only limited data regarding the performance of time-resolved MR angiography in the assessment of peripheral vascular disease, and all studies were performed in patients without diabetes or in mixed study groups (5,10,15). Results of our study demonstrate TRICKS MR angiography to be helpful with the assessment of the calf arteries in patients with diabetes. Sensitivity and specificity for detection of hemodynamically significant arterial stenosis in the calf significantly increased for both readers when the TRICKS MR technique was used.

Another advantage to performing TRICKS MR angiography as an adjunct to standard bolus-chase MR angiography is the possibility of including the pedal vessels in the imaging volume. There are limited data with regard to MR angiography in pedal vessels (4,24,31). Typically, the feet were positioned in a head coil (24,31). Results of one study (24) found contrast-enhanced MR angiography to be superior to DSA with regard to revealing patent vessel segments of the foot in patients with diabetes and severe arterial occlusive disease.

One group of investigators (27) reported on the diagnostic performance of MR angiography for pedal vessels. Sixty-one patients underwent single-injection bolus-chase MR angiography and dedicated MR angiography in the calf and the pedal vessels. Sensitivity and specificity ranges for detection of hemodynamically significant arterial stenosis in the pedal arteries were 89%–94% and 90%–92%, respectively (27). However, the study sample included a mixed group of patients with diabetes and patients without diabetes (27).

We demonstrated that TRICKS MR angiography could depict hemodynamically significant arterial stenosis in the foot with good diagnostic performance. Whereas the performance of standard bolus-chase MR angiography was too poor to be evaluated, TRICKS MR angiography had sensitivity values of 58% for reader 1 and 66% for reader 2 and specificity values of 90% for reader 1 and 88% for reader 2 for the segments depicted at DSA. TRICKS MR angiography also was found to depict vessel segments that could not be depicted at DSA, most likely because of inadequate opacification of distal vessels caused by incomplete filling and dilution of contrast material after passing through multisegmental occlusions (5,25). Sixteen (62%) of the 26 discrepancies between TRICKS MR angiographic findings and DSA findings were related to vessel segments not visualized at DSA but were graded as patent at TRICKS MR angiography.

We acknowledge several limitations of our study. The selective inclusion of patients with diabetes and severe peripheral vascular disease may have resulted in a selection bias. Our TRICKS MR angiographic acquisition included only a single calf and foot at a time because of the sagittal imaging-slab orientation with the concomitant optimized spatial resolution. Because high-quality TRICKS MR angiography can be performed after previous contrast material injections, however, additional time-resolved MR angiography of the second calf and foot may be performed. There may be a potential bias against TRICKS MR angiography. In our study, TRICKS MR images were acquired after a cumulative injection of 14 mL of a 1 mmol/mL contrast material. This may have resulted in higher systemic T1 values and therefore may have reduced the transient T1 shortening at the first pass of the TRICKS injection. This effect might have reduced the conspicuity of small peripheral vessels, in particular at the level of the foot. The fact that both readers evaluated all MR angiograms and DSA images could have biased the results of the study. However, in all cases, the reading session for DSA images was separated from the reading session for the MR angiograms by 6 weeks.

In conclusion, results of our study have shown that standard bolus-chase MR angiography combined with time-resolved MR angiography with the TRICKS technique is an alternative to conventional DSA for displaying the arteries of the lower extremity, including the pedal arteries, in patients with diabetes. TRICKS MR angiography in the distal calf and pedal vessels is superior to standard single-injection bolus-chase MR angiography with regard to the percentage of diagnostic arterial segments depicted, as well as with regard to the assessment of the degree of luminal narrowing.


    ADVANCES IN KNOWLEDGE
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 


    FOOTNOTES
 

Abbreviations: DSA = digital subtraction angiography • TRICKS = time-resolved imaging of contrast kinetics

See Materials and Methods for pertinent disclosures.

Author contributions: Guarantors of integrity of entire study, G.A., D.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, G.A.; clinical studies, G.A., T.P., K.G., D.N., R.K., D.W.; statistical analysis, G.A.; and manuscript editing, G.A., T.P., K.G., D.N., P.H., D.W.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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