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1 Department of Diagnostic and Interventional Radiology, University Hospital
Essen, Hufelandstrasse 55, Essen 45122, Germany.
2 Department of Angiology, University Hospital Essen, Essen 45122,
Germany.
3 Department of Radiology, Catholic Hospitals Essen-Nord, Hospitalstrasse 24,
Essen 45329, Germany.
Received August 12, 2003;
accepted after revision November 25, 2003.
Address correspondence to C. U. Herborn
(christoph.herborn{at}uni-essen.de).
Abstract
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SUBJECTS AND METHODS. Fifty-one patients with clinically documented peripheral arterial occlusive disease referred for DSA of the lower extremity arterial system underwent whole-body MR angiography on a 1.5-T MR scanner. Paramagnetic gadobutrol was administered and five contiguous stations were acquired with 3D T1-weighted gradient-echo sequences in a total scanning time of 72 sec. DSA was available as a reference standard for the peripheral vasculature in all patients. Separate blinded data analyses were performed by two radiologists. Additional vascular disease detected by whole-body MR angiography was subsequently assessed on sonography, dedicated MR angiography, or both.
RESULTS. All whole-body MR angiography examinations were feasible
and well tolerated. AngioSURF-based whole-body MR angiography had overall
sensitivities of 92.3% and 93.1% (both 95% confidence intervals [CIs],
78–100%) with specificities of 89.2% and 87.6% (both CIs, 84–98%)
and excellent interobserver agreement (
= 0.82) for the detection of
high-grade stenoses. Additional vascular disease was detected in 12 patients
(23%).
CONCLUSION. Whole-body MR angiography permits a rapid, noninvasive, and accurate evaluation of the lower peripheral arterial system in patients with peripheral arterial occlusive disease, and it may allow identification of additional relevant vascular disease that was previously undetected.
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The implementation of 3D contrast-enhanced MR angiography as an attractive noninvasive alternative for assessing patients with peripheral arterial disease has been brought about by the development of non-nephrotoxic contrast agents, ways of avoiding ionizing radiation, and equipment that allows high diagnostic accuracy [2–6]. Rapid parenchymal enhancement and contrast dose restrictions previously limited 3D contrast-enhanced MR angiography to the display of the arterial territory contained in a single field of view extending over 40–48 cm. The use of bolus chase techniques after a single injection of contrast medium now allows successive extended coverage to encompass vascular territories including the pelvic, femoral, popliteal, and calf arteries [7–9].
Recent hardware and software refinements have extended the bolus chase technique to whole-body coverage. Thus, an arterial display extending from the carotid arteries to the calf vessels can now be created with five sequential 3D contrast-enhanced MR angiography acquisitions in only 72 sec [10]. Correlation with a limited number of regional digital subtraction angiography (DSA) examinations has revealed limitations in the quality of whole-body MR angiography images of the trifurcation vessels. Quality can be much improved by introducing a sliding torso-surface phased array coil for signal detection (AngioSURF: Angiography System for Unlimited Rolling Field of Views [MR-Innovation]) [11]. The technique has been shown to be feasible [10–14], but a thorough assessment of its diagnostic performance in a larger patient cohort has been lacking.
The goal of this study was to prospectively assess the diagnostic performance of AngioSURF-based whole-body 3D contrast-enhanced MR angiography in comparison with DSA examinations of the lower extremities in 51 patients.
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Whole-Body 3D MR Angiography
All imaging was performed on a 1.5-T MR system (Magnetom Sonata, Siemens)
equipped with a high-performance gradient system characterized by an amplitude
of 40 mT/m, 200 µ sec rise time, a slew rate of 200 mT/m per
millisecond, and a single field of view of 40 cm. Patients were placed
feetfirst in the bore of the magnet and examined in the supine position on a
sliding table platform (AngioSURF, MR-Innovation). The platform is mounted on
seven pairs of roller bearings that are anchored in the existing patient table
and allow sliding movement in the z-direction. The AngioSURF table
platform allows the acquisition of up to six 3D data sets in immediate
succession, each with a field of view of 40 cm. Stepping blocks under the
platform and markers permit adjustment of the desired field of view.
Signal reception is accomplished through posteriorly located spine coils integrated in the patient table and an anteriorly positioned body phased array coil that remains stationary in the center of the bore throughout the examination. The torso phased array surface coil is fastened in a height-adjustable holder that remains fixed to the stationary patient table. While the patient slides on the AngioSURF platform underneath the coil, the holder adjusts to the patient's contours. Thus, data for all stations are collected with an unchanged coil set positioned in the isocenter of the magnet.
Whole-body MR angiography consists of the acquisition of at least five slightly overlapping 3D data sets in immediate succession. The first data set covers the aortic arch, supraaortic branch arteries, and the thoracic aorta; the second data set displays the abdominal aorta with its major branches including the renal arteries. The third data set includes the pelvic arteries, and the last two data sets cover the arteries of the thighs and calves, respectively.
For planning of the five 3D data acquisitions, the "moving vessel scout protocol" was used. For each region, six axial images (every 7.5 cm) are collected (TR/TE, 539/10; inversion time, 300 msec; flip angle, 50°; slice thickness, 8 mm; matrix, 114 x 256; field of view, 400 x 400 mm; acquisition time, 20 sec). The imaging delay for the start of the data acquisition was calculated on the basis of the travel time of a contrast test bolus from the injection site (right antecubital vein in 31 patients, left antecubital vein in 20 patients) to the proximal third of the descending aorta. After the IV injection of a 2-mL test bolus of saline-diluted gadolinium flushed with 20 mL of saline solution both at a flow rate of 1.3 mL/sec, axial single-detector multiphase turbo fast low-angle shot (FLASH) images were collected every second (TR/TE, 1,000/3.2; inversion time, 8 msec; flip angle, 10°; slice thickness, 10 mm; matrix, 128 x 256; field of view, 400 x 400 mm).
The arterial tree was imaged with a 3D FLASH sequence (coronal acquisition; k-space sampling, centric elliptic; 2.1/0.7; flip angle, 25°; 40 partitions interpolated by zero filling to 64; field of view, 390 x 390 mm; matrix, 256 x 225; acquisition time, 12 sec). The slice thickness was interpolated by zero filling and varied between the stations: The true slice thickness for the first station was 2.4 mm (interpolated to 1.8 x 1.5 x 1.5 mm): for the second and third station, 2.9 mm (interpolated to 1.7 x 1.5 x 1.8 mm); and for the two lower stations, 1.9 mm (interpolated to 1.6 x 1.5 x 1.2 mm). The last two stations were always collected before and after contrast enhancement for later subtraction. To avoid gaps, the 3D data sets were overlapped by 5 cm, resulting in a craniocaudal coverage of 180 cm. The first two cranial stations were acquired in breath-hold after deep inspiration to avoid motion artifacts. From the third station onward, patients were allowed to breathe. The AngioSURF platform was manually repositioned to the next station in 3 sec. The total examination time for five stations and four repositionings was 72 sec. A paramagnetic contrast agent (gadobutrol [Gadovist, Schering]) was injected automatically (MR Spectris, Medrad) at a body-weight-adjusted dose of 0.15 mmol/kg of body weight. The gadobutrol was diluted with normal saline to a total volume of 60 mL and was stirred carefully. After the 2-mL test bolus, the rest was injected in a biphasic manner: 30 mL at a rate of 1.3 mL/sec, and 28 mL at a rate of 0.7 mL/sec. The contrast medium was flushed with 30 mL of normal saline from a separate syringe injected at a rate of 1.3 mL/sec.
DSA
DSA of the pelvic and lower extremity vessels was performed on a standard
angiography unit (Ultimax, Toshiba). All 51 patients underwent catheter
angiography extending from the distal aorta (including the renal arteries in
28 patients) to the proximal pedal vessels with a transfemorally inserted
5-French pigtail catheter. The catheter tip was positioned just above the
renal artery origins for DSA of the distal aorta, then pulled back to a
position proximal to the aortic bifurcation for display of the pelvic
arteries, followed by acquisitions encompassing the thigh and lower limbs. At
each station, a bolus between 20 and 35 mL of iodinated contrast material
(iobitridol, [Xenetix, Guerbet]) was automatically injected. The examination
was supplemented by acquisition of one or more oblique views of the pelvic
arteries using 20 mL of contrast material, if required. Selective
catheterization of each lower extremity was not performed.
Image Analysis
For analysis, the arterial tree was divided in 31 segments: 1 to 2, right
and left internal carotid arteries; 3 to 4, right and left common carotid
arteries; 5, brachiocephalic trunk; 6, left subclavian artery; 7, thoracic
aorta; 8, suprarenal abdominal aorta; 9 to 10, right and left renal arteries;
11, infrarenal abdominal aorta; 12 to 13, right and left common iliac
arteries; 14 to 15, right and left external iliac arteries; 16 to 17, right
and left common femoral arteries; 18 to 19, proximal halves of right and left
superficial femoral arteries; 20 to 21, distal halves of right and left
superficial femoral arteries; 22 to 23, right and left popliteal arteries; 24
to 25, right and left tibioperoneal trunk; 26 to 27, right and left anterior
tibial arteries; 28 to 29, right and left peroneal arteries; 30 to 31, right
and left posterior tibial arteries.
DSA and MR angiography examinations were masked and subjected to a prospective qualitative analysis based on a segment-by-segment review using caliper measurements. DSA examinations were documented on film created from images saved on optical disks and were interpreted by a radiologist specialized in vascular interventions. The arterial diameters were measured with electronic calipers. MR angiography examinations were reviewed separately by two experienced radiologists. The DSA observer was unaware of the MR angiography results, and the MR angiography observers were unaware of each other's interpretations and the DSA results. Three-dimensional MR angiography data sets were available on a workstation (Virtuoso, Siemens), allowing review of source images as well as maximum intensity projections and multiplanar reconstructions.
All MR angiography data sets were first assessed for image quality. For this purpose, the depiction of each arterial segment was characterized as either diagnostic or nondiagnostic. Display of an arterial segment was considered diagnostic when image quality allowed reliable detection or exclusion of relevant vascular disease. DSA and MR angiograms were analyzed for the presence of arterial disease as follows: normal, mild stenosis with luminal narrowing not exceeding 50%, severe stenosis with luminal narrowing exceeding 50%, arterial occlusion, or aneurysmal disease. Luminal assessment was based on the most severe reduction or increase of the arterial diameter compared with the most normal-appearing segment proximal or distal to the area of arterial disease, using electronic calipers.
Statistical Analysis
For those arterial segments with DSA correlation, overall sensitivities and
specificities of whole-body 3D contrast-enhanced MR angiography for the
detection of significant stenoses (luminal narrowing > 50%) were calculated
using DSA as the standard of reference. The 95% CIs were calculated for all
computed sensitivity and specificity values on the basis of binomial
distribution. To assess the interobserver concordance of the two reviewers, we
calculated kappa coefficients for all vessel segments as displayed on
whole-body 3D contrast-enhanced MR angiography. The interpretation of the
kappa values followed accepted guidelines; values greater than 0.75 indicated
excellent reproducibility, values between 0.4 and 0.75 indicated good
reproducibility, and values less than 0.4 indicated marginal reproducibility
[15].
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DSA depicted 1,164 of 1,224 potential arterial segments in the 51 study patients. In 16 patients, the suprarenal abdominal aorta could not be assessed because the catheter was directly placed above the level of the renal artery origins, and in 12 patients the catheter tip was positioned at the level of the infrarenal aorta and excluded the renal arteries and suprarenal aorta from evaluation and comparison with MR angiography. Abnormalities were identified in 292 segments (Table 1). In addition to the 1,164 segments depicted on DSA, whole-body 3D contrast-enhanced MR angiography with AngioSURF revealed 417 additional segments for a total of 1,581 arterial segments in the same 51 patients. Atherosclerotic abnormalities were present in 352 (observer 1) and 331 (observer 2) arterial segments, respectively (Table 2).
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Observer 1 misjudged as severely stenosed 14 arterial segments that had been classified as normal or only mildly stenosed on DSA (two renal arteries, four common femoral arteries, two distal superficial femoral arteries, six tibioperoneal trunks). In addition, 12 arterial sections (one distal superficial femoral artery, two tibioperoneal trunks, two posterior tibial arteries, six peroneal arteries, and one anterior tibial artery) were overgraded as occluded on MR angiography but considered severely (n = 7) or mildly (n = 5) stenosed on DSA. Conversely, observer 1 undergraded 11 vessel segments (three tibioperoneal trunks, five posterior tibial arteries, two peroneal arteries, and one anterior tibial artery) that were considered severely stenosed on DSA as normal or mildly stenosed on MR angiography. Sensitivity and specificity for the detection of significant stenoses (luminal narrowing > 50%) were 92.3% (269/292) and 89.2% (778/872; 95% CIs, 78–100% and 84–98%), respectively. Focused on those segments judged as severely stenosed or occluded on DSA, sensitivity and specificity for the detection of vessel occlusions with whole-body 3D contrast-enhanced MR angiography were 90.4% (93/103) and 91.6% (173/189; 95% CIs, 60–98% and 40–97%), respectively.
Observer 2 overestimated 11 arterial segments (one renal artery, one distal
superficial femoral artery, two tibioperoneal trunks, two posterior tibial
arteries, three peroneal arteries, and two anterior tibial arteries) as
severely stenosed that were considered normal (n = 4) or mildly
stenosed (n = 7) on DSA. Ten arterial segments (two distal
superficial femoral arteries, three posterior tibial arteries, four peroneal
arteries, and one anterior tibial artery) that had been regarded as mildly
(n = 4) or severely stenosed (n = 6) on DSA were falsely
estimated as occluded on MR angiography. Nine arterial sections (four
posterior tibial arteries, three peroneal arteries, and two anterior tibial
arteries) were judged as normal or mildly stenosed on MR angiography and
severely stenosed or occluded on DSA. Sensitivity and specificity for the
detection of significant stenoses (luminal narrowing > 50%) for observer 2
were 93.2% (272/292) and 87.6% (764/872; 95% CIs, 78–100% and
84–98%), respectively. MR angiography sensitivity and specificity for
vessel occlusions were 92.2% (95/103) and 93.8% (177/189; 95% CIs,
86–99% and 74–97%), respectively. Interobserver agreement for
whole-body 3D contrast-enhanced MR angiography was excellent ( =
0.82).
Coverage of the entire arterial system with AngioSURF depicted 12 regions of vascular disease in 12 patients that were not clinically suspected before the MR angiography examination: one occlusion of the left superficial femoral artery (Fig. 1A, 1B), four high-grade stenoses of the internal carotid artery in four patients (Fig. 2A, 2B, 2C), two stenoses of the subclavian artery in two patients, one thoracoabdominal and one ascending aortic aneurysm in two patients (Fig. 3A, 3B, 3C), and three hemodynamically relevant renal artery stenoses in three patients who had not undergone DSA of the renal arteries (Fig. 4A, 4B, 4C). However, observer 1 overgraded six renal artery stenoses and observer 2 had three false-positive findings of renal artery stenosis in those patients with initial DSA comparison. The thoracoabdominal and ascending aortic aneurysms measured 4.7 cm and 5.3 cm in diameter, respectively. Carotid artery disease had not been suspected initially, but careful history revealed it to be symptomatic in all cases (e.g., recurring dizziness, transient amaurosis). The subclavian artery stenosis caused intermittent pain in the arm in both cases, and two patients with newly diagnosed renal artery stenosis had arterial hypertension. All patients with unsuspected vascular disease underwent duplex sonography. In addition, three patients with carotid artery disease, both patients with aortic aneurysms, and all patients with renal artery stenosis were subjected to a single-station high-resolution MR angiography examination. Presence and grading of vascular disease were proven in all cases. No false-positive whole-body MR angiography results for the suprarenal arterial vasculature were found.
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The combination of bolus chase techniques with integrated table motion algorithms provided the basis for imaging of contiguous vascular territories. Initial strategies using the body coil for signal reception were handicapped by rather poor signal-to-noise ratios. Spatial resolution was not sufficient to delineate abnormalities in the trifurcation vessels [7, 8]. Dedicated surface coils overcame this limitation; improved signal-to-noise ratio allowed better spatial resolution and improved diagnostic accuracy. Sensitivity and specificity of 92% and 98% have been reported for the detection of stenotic disease of the peripheral arteries [9, 16]. Conventional use of surface coils limits imaging to those body parts contained within the sensitivity range of the coil. We evaluated a strategy that extended the coil sensitivity range to five contiguous body regions by simply sliding the patient through the bore of the scanner and through a coil sandwich consisting of integrated spine and sliding torso coils for signal reception.
The use of a prototypic stepping table with an integrated coil holder and bolus-chase MR angiography of the lower extremities was first described by Wang et al. [17] in 1998. AngioSURF technology extended the technique to the neck, chest, and abdomen [10, 12]. Replacing the body coil with the sliding surface coil results in much better image quality [11]. Similar results have been reported by others using techniques comparable to the AngioSURF technology: Shetty et al. [18] showed excellent signal-to-noise and contrast-to-noise ratios by using a custom-made stepping kinematic imaging platform for the contiguous display of the vessels from the abdominal aorta to the calf arteries. This study confirmed the feasibility of extended-coverage MR angiography using a sliding-coil platform and documented excellent correlation with regional DSA, as evidenced by sensitivity and specificity ranging from 92.3% to 93.1% and from 87.6% to 89.2%, respectively, for the detection of significant arterial disease.
AngioSURF whole-body 3D contrast-enhanced MR angiography allows the assessment of the entire aorta and the supraaortic branches in addition to displaying the peripheral vasculature. In our study cohort of 51 patients with suspected peripheral arterial disease, this technique led to the identification of 12 (23%) patients with additional relevant but clinically unsuspected atherosclerotic lesions. The high prevalence of concomitant arterial disease in patients with peripheral arterial disease accentuates the systemic nature of atherosclerosis. The link between peripheral arterial disease and renovascular disease is well recognized: approximately 34% of patients with peripheral arterial disease also have renal artery stenosis [19]. Three patients (6%) in our study cohort had renal artery disease with luminal narrowing exceeding 50% that was subsequently confirmed. However, MR angiography with better spatial resolution probably would have detected even more renal artery abnormalities than we did.
Similarly, 26–50% of patients with claudication are known to also harbor atherosclerotic disease affecting the carotid arteries [20, 21]. Among our 51 patients, five high-grade carotid stenoses were identified in five patients. Evidence is mounting that high-grade lesions should be treated, although some experts disagree.
The prevalence of aortic aneurysmal disease in patients with peripheral arterial disease is also known to be high [22]. Screening asymptomatic patients for aortic aneurysms is controversial [23–25], but general agreement exists that the concomitant analysis of the thoracoabdominal aorta is desirable in patients who are suspected of having peripheral arterial disease. The increasing availability of covered stents for treatment of aortic aneurysms [26, 27] renders the display of the entire aorta with the AngioSURF technology even more attractive.
To achieve maximal arterial enhancement, we tested a neutral gadolinium chelate (gadubutrol) with high intravascular relaxivity. Although gadobutrol is not approved for MR angiography, it has been found to be superior to gadopentetate dimeglumine even when given at a lower dose [28, 29]. Gadobutrol was applied in a biphasic injection protocol, enhancing the first two (thoracic and abdominal aorta) 3D data sets with a relatively high (1.3 mL/sec) flow rate and the remaining three data sets with a lower (0.7 mL/sec) flow rate. The contrast injection protocol was designed to minimize venous overlap. The protocol proved robust and easy to use, providing diagnostic quality images of the entire arterial tree of the patients. Venous overlap caused by the presence of contrast agent in the portal venous system and in the renal and calf veins did not substantially impair analysis of the arterial tree when the latter was based on multiplanar reformations [28, 29].
This study has several limitations. First, we have not included either the profunda femoral arteries or the dorsal pedal arteries in our analysis. This is in part because the dorsal pedal arteries are not routinely covered in the AngioSURF examination, depending on the patient's height. Also, the use of whole-body MR angiography in patients with critical ischemia remains unclear because we included only five patients with such severe vascular disease in our study. However, monostation high-resolution contrast-enhanced MR angiography for the feet appears feasible.
Second, grading carotid stenoses greater than 50% as severe is not in accordance with the North American Symptomatic Carotid Endarterectomy Trial and Asymptomatic Carotid Artery Atherosclerosis Study criteria [30, 31].
Another limitation relates to the incomplete DSA correlation of the suprarenal abdominal aorta and its branches. In part this limitation was overcome by subjecting patients in whom additional abnormalities were identified to duplex sonography and high-resolution MR angiography. In this manner, all detected abnormalities were confirmed. Negative findings, on the other hand, were not confirmed.
Another limitation refers to the signal changes at the overlapping borders of the five data sets, where relevant abnormalities might be overlooked or falsely detected.
Finally, whole-body contrast-enhanced MR angiography using AngioSURF does not cover the intracranial or coronary arteries. Although rarely affected by atherosclerotic disease in Western patient populations, the intracerebral arteries can be visualized with ease on time-of-flight MR angiography, which would add less than 3 min to the overall examination time. Exclusion of the coronary artery tree is more problematic: the coronary arteries are frequently affected by atherosclerotic disease, and their display with MR angiography requires a complex and highly dedicated imaging approach. To date, MR angiography of the coronary arteries remains under clinical investigation.
Given our data from 51 consecutive patients, we conclude that whole-body 3D contrast-enhanced MR angiography with AngioSURF proved highly accurate in the assessment of peripheral arterial disease. In addition, the strategy permitted the identification of unsuspected, relevant atherosclerotic disease in other arterial regions. Hence, noninvasive whole-body 3D contrast-enhanced MR angiography, which can be completed in less than 10 min, seems an ideal diagnostic technique for patients with peripheral arterial disease.
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