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1
Department of Radiology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, 50, Ilwon-dong, Kangnam-ku, Seoul 135-710, Korea.
2
Department of Internal Medicine, Division of Rheumatology, Sungkyunkwan
University School of Medicine, Seoul 135-710, Korea.
3
Department of Internal Medicine, Divsion of Cardiology, Sungkyunkwan
University School of Medicine, Seoul 135-710, Korea.
Received April 1, 1999;
accepted after revision December 22, 1999.
Supported by a grant from the Sunkyunkwan University, Seoul, Korea.
Abstract
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SUBJECTS AND METHODS. High-resolution contrast-enhanced T1-weighted spinecho MR imaging using small fields of view (14-20 cm) and thin slices (4-5 mm) was performed in 26 patients with Takayasu's arteritis and 16 healthy subjects. The degree of aortic mural enhancement was assessed by measuring signal intensity and by visually estimating it in comparison with that of the myocardium.
RESULTS. Contrast-enhanced MR imaging showed more enhancement of thickened aortic wall compared with myocardium, thus suggesting active Takayasu's arteritis on MR imaging in 16 patients. Determination of disease activity using contrast-enhanced MR imaging was concordant with clinical findings in 23 patients (88.5%). Contrast-enhanced MR findings were concordant with laboratory findings in most patients (erythrocyte sedimentation rate in 92.3% [24/26] and C-reactive protein in 84.6% [22/26]). The measured signal intensity of the aortic wall relative to that of myocardium during the early phase of contrast-enhanced MR imaging correlated well with the erythrocyte sedimentation rate (r = 0.78, p < 0.005) and with the C-reactive protein level (r = 0.63, p < 0.005).
CONCLUSION. Contrast-enhanced MR imaging provides information about disease activity of Takayasu's arteritis, which may be useful in the diagnosis and treatment of Takayasu's arteritis.
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Conventional and digital subtraction angiography have been used for the evaluation of arterial stenoocclusive changes or aneurysm in Takayasu's arteritis. During the early phase of Takayasu's arteritis, only mild luminal changes of the arteries without significant stenosis may be present. These changes may not be detectable on angiography. Cross-sectional imaging techniques are better suited for the evaluation of subtle mural changes of the aorta during the early phase of Takayasu's arteritis than angiography. Helical CT has shown potential in the diagnosis and activity determination of Takayasu's arteritis by depicting enhancement at the inflamed segment of the aorta [9]. On helical CT angiography, the thickened aortic wall may enhance during the arterial phase and further enhance during the late phase [9]. However, little information is available about whether the degree of mural enhancement correlates with the severity of Takayasu's arteritis. A high density of contrast medium in the aortic lumen may cause artifacts in the adjacent aortic wall on contrast-enhanced CT scans, and these images may be unsuitable for evaluation of the aortic mural structures. On the contrary, MR imaging has the inherent ability to differentiate between the flowing blood and stationary aortic wall. MR imaging has the capability of revealing mural thickening of the aorta and its branches [10,11,12], and in an experimental model contrast-enhanced MR imaging was sensitive in the detection of vasculitis [13]. We assumed that the degree of the vascular mural contrast enhancement on MR imaging reflects the severity of active inflammation of the thickened walls of the aorta and its branches in patients with Takayasu's arteritis. The purpose of this study was to evaluate the role of contrast-enhanced MR imaging in the determination of the activity of Takayasu's arteritis.
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The duration of Takayasu's arteritis ranged from 2 months to 23 years (mean, 5.4 years). Laboratory tests including complete blood cell counts, erythrocyte sedimentation rate, C-reactive protein level, immunoglobulins, rheumatoid factor, veneral disease, and antinuclear antibodies were performed within 1 week before or after contrast-enhanced MR imaging in all patients.
Criteria for active Takayasu's arteritis were defined clinically by new onset, persistence, or worsening of two or more features of Takayasu's arteritis. The features of active Takayasu's arteritis included systemic features, such as fever and arthralgia; elevated erythrocyte sedimentation rate; features of vascular ischemia or inflammation, such as claudication, bruit, and vascular pain; and typical imaging features [14].
Contrast-enhanced MR imaging was performed to determine disease activity by the degree of aortic wall enhancement in 26 patients. Carotid and extremity sonography were performed using a 7- or 10-MHz transducer in 20 patients within 1 week before or after MR imaging. Intraarterial digital subtraction angiography or cine angiography was performed using 5-French pigtail catheters and iopamidol (Iopamiron 300 mg I/mL [dose, 2-4 mL/kg]; Bracco, Milan, Italy) in eight patients within 1 week after contrast-enhanced MR imaging.
MR Imaging Techniques
Electrocardiography-gated T1-weighted spinecho axial images (TE range =
10-11 msec; 256 x 192 matrix; number of acquistions, two) were obtained
with or without fat saturation for the thoracic and abdominal aorta using a
1.5-T scanner (Signa Horizon Echospeed; General Electric Medical Systems,
Milwaukee, WI) and body coils. For better visualization of aortic mural
changes, we used thin slices (4-5 mm) and smaller fields of view (from 14
x 14 to 20 x 20 cm). T2-weighted spin-echo images (TR = 3-4
x R-R intervals, TE range = 96-102 msec) were also acquired to look for
aortic wall edema or atherosclerotic change in 18 patients.
To determine the degree of aortic wall enhancement, gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) was IV injected (total amount, 0.3 mL/kg; rate of injection, 2 mL/sec). Then T1-weighted spin-echo imaging of the thoracic or abdominal aorta was performed three times in succession (immediately after, 5-10 min after, and 11-20 min after contrast medium injection). Cervical areas were also included in 20 patients.
In control subjects, T1-weighted spin-echo axial images (slice thickness, 5 mm; field of view, 32 cm) were obtained before and after injection of contrast medium (gadopentetate dimeglumine; total amount, 0.2 mL/kg; rate of injection, 2 mL/sec).
Image Analysis in Patients with Takayasu's Arteritis
The degree of aortic wall enhancement was visually assessed by two
radiologists who were unaware of clinical and laboratory findings of the
patients and was also measured using large (10-20 mm2) regions of
interest on picture archiving and communication system (PACS) workstations.
The signal intensity of the myocardium was also measured for comparison with
the aortic mural signal intensity. Two radiologists assessed the degree of
aortic mural edema on T2-weighted images by visual inspection and in
consensus.
Patterns of aortic wall thickening were classified into six types according to the mural morphology (Fig. 1A,1B,1C,1D,1E,1F). In type A, the middle layer was thickest among the three layers of the thickened aortic wall. In type B, the innermost layer was thicker than or equal to the middle layer. In type C, the innermost and middle layers were inseparable. In type D, small areas of signal void that might represent dilated new vessels or vasae vasorum were seen in the middle or outer layers. In type E, the periadventitial area was also infiltrated by the inflammatory process. In type F, focal thinning, pseudoaneurysm, or dissection was found in the aneurysmal segment.
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We considered Takayasu's arteritis active when the degree of aortic mural
enhancement was equal to or greater than that of myocardial enhancement by
visual assessment or when measured aortic mural signal intensity was equal to
or greater than myocardial signal intensity. We chose to use these criteria
based on the assumption that the myocardium has richer vascularity than
fibrotic aortic mural tissue in inactive Takayasu's arteritis. Statistical
tests, including the Student's t test, were performed for comparison
of aortic wall signal intensity relative to myocardial signal intensity
according to the phase of MR imaging in groups classified by erythrocyte
sedimentation rate (
20 versus >20 mm/hr) and in groups classified by
C-reactive protein level (0.8 versus >0.8 mg/dL). Statistical analysis
(Student's t test) was also performed for comparison of aortic wall
thickening in groups classified by erythrocyte sedimentation rate and in
groups classified by C-reactive protein level.
Image Analysis in the Control Group
The thickness of the right, left, and posterior wall of the mid ascending
thoracic aorta and mid descending thoracic aorta and right and left wall of
the aortic arch were measured on a PACS workstation by one observer. One
observer analyzed aortic wall enhancement patterns. The patterns of wall
enhancement used for classification were a single homogeneous ring with or
without surrounding fat and double rings with a low-signal-intensity ring
intervening between the inner enhanced ring and the outer fat layer. The
degree of aortic wall enhancement was compared with that of the myocardium
(Fig. 2).
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High-resolution MR imaging using a small field of view and a thin slice thickness enabled us to analyze aortic wall structures involved with Takayasu's arteritis (Fig. 3A,3B,3C,3D,3E). Analysis of the aortic wall thickening pattern on contrast-enhanced MR imaging revealed type A in eight (30.8%) of 26 patients, type B in 14 (53.8%), type C in 10 (38.5%), type D in two (7.7%), type E in two (7.7%), type F in three (11.5%), and normal aorta in one (3.8%) (Fig. 3A,3B,3C,3D,3E).
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Disease Activity Determination Using Clinical, Laboratory, and MR
Findings
Erythrocyte sedimentation rate was elevated (>20 mm/hr) in 15 patients
and normal in 11 patients. C-reactive protein level was elevated (>0.8
mg/dL) in 12 patients and normal in 14. The disease was presumed to be
clinically active in 13 patients and inactive in 13. In two patients, disease
activity was suspected clinically, although disease duration was more than 10
years.
Quantitative contrast-enhanced MR imaging showed that the aortic wall was more enhanced than the myocardium, suggestive of active Takayasu's arteritis, in 16 patients (Fig. 4A,4B,4C and Table 2) and that the aortic wall was enhanced less than the myocardium in 10 patients (Fig. 5A,5B). The results of determination of disease activity by visual assessment and by quantitative assessment of aortic wall enhancement compared with myocardial enhancement were concordant in 96.5% of patients for observer 1 and 84.5% for observer 2. The kappa values for the two observers were 0.54, 0.56, and 0.71 for the early, intermediate, and late contrast-enhanced MR images, respectively. Overall observer agreement was 82.1%.
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Disease activity determination using contrast-enhanced MR imaging was concordant with clinical findings in 23 patients (88.5%). Contrast-enhanced MR imaging findings were concordant with laboratory findings in most patients (with erythrocyte sedimentation rate in 92.3% [24/26] and with C-reactive protein level in 84.6% [22/26] (Table 2). There was a significant difference in the aortic signal intensity relative to the myocardial signal intensity between the group with a normal erythrocyte sedimentation rate and the group with a high erythrocyte sedimentation rate (>20 mm/hr) on the early (p < 0.01), intermediate (p < 0.001), and late (p < 0.01) contrast-enhanced MR images, respectively (Table 2). There was also a significant difference in the relative aortic signal intensity between the group with a normal C-reactive protein level and the group with a high C-reactive protein level (>0.8 mg/dL) on the early contrast-enhanced MR images (p < 0.001). Aortic wall thickness was also significantly different between the group with a normal erythrocyte sedimentation rate and the group with a high erythrocyte sedimentation rate (p < 0.05) and between the group with a normal C-reactive protein level and the group with a high C-reactive protein level (p < 0.01). The measured signal intensity of the aortic wall relative to that of myocardium on the early phase contrast-enhanced MR images was in good correlation with erythrocyte sedimentation rates (r = 0.78, p < 0.005) (Fig. 6) and with C-reactive protein levels (r = 0.63, p < 0.005) (Fig. 7).
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Of the 18 patients who underwent T2-weighted spin-echo MR imaging, six patients were shown to have clinically active Takayasu's arteritis at the time of MR imaging, and seven patients were determined to have active Takayasu's arteritis on contrast-enhanced MR imaging (Figs. 4A,4B,4C and 5A,5B). Two radiologists agreed completely in determination of the presence of high signal intensity in the arterial wall in three patients and the absence of high signal intensity in the arterial wall in the remaining 15 patients. T2-weighted images revealed high signal intensity in and around the aortic wall in a 4-year-old girl (Fig. 4A,4B,4C), in the right proximal cartoid artery in a 20-year-old woman, and in both common carotid arteries in a 15-year-old girl with significant mural edema in the active phase of Takayasu's arteritis. In these patients, contrast-enhanced MR imaging also showed evidence of active disease.
The origins and intrathoracic segments of the three branches of the aortic arch were significantly thickened and enhanced on contrast-enhanced MR imaging in all patients with aortic arch involvement. Proximal common carotid arteries were markedly enhanced with wall thickening in two patients (Fig. 8A,8B).
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MR Findings in the Control Group
Thickness of the right, left, and posterior wall of the mid ascending
thoracic aorta, mid descending thoracic aorta, and right and left wall of the
aortic arch ranged from imperceptible to 2.5 mm in 16 control subjects; mean
thickness was 1.4, 1.5, 1.8 mm for the ascending thoracic aorta; 1.8, 2.1, 1.9
mm for the descending thoracic aorta; and 1.4 and 1.9 mm for the aortic arch,
respectively (Fig. 2). The
patterns of aortic wall enhancement were a single homogeneous ring with or
without surrounding fat in 13 subjects (81.3%) and double rings with a
low-signal-intensity area intervening between the inner enhanced ring and the
outer fat layer in three subjects (18.8%). The degree of aortic wall
enhancement was minimal or mild enhancement equal to or less than that of back
muscle enhancement in 14 subjects (87.5%) and equal to that of myocardial
enhancement in two subjects (12.5%), although the degree of enhancement of the
thin aortic wall was difficult to compare with that of the myocardium.
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Recently, cross-sectional imaging techniques such as CT, sonography, and MR imaging have noninvasively revealed wall thickening of the aorta and stenosis or occlusion of aortic branches in Takayasu's arteritis [9,10,11,12, 16,17,18,19,20]. These techniques can depict arterial lesions at an earlier stage than angiography. Unenhanced CT scans may reveal a high-density wall of variable thickness in the aorta and branches of the aortic arch and aortic calcifications in Takayasu's arteritis. Helical CT angiography may show enhancement of the thickened aortic wall with active inflammation [9].
Aortic wall thickening and mural thrombi can be more easily detected on MR imaging than conventional angiography. The degree of aortic stenosis or dilatation and extent of inflammation of the involved segments can be assessed on T1-weighted spin-echo MR imaging in the axial and oblique sagittal planes. Aortic regurgitation and dilatation of the ascending aorta are frequent in Takayasu's arteritis. Cine MR imaging can be helpful in the evaluation of aortic regurgitation. MR imaging also can be useful in the evaluation of response to the medical treatment by depicting decreased wall thickness of the involved arteries and aorta [10].
High-resolution T1-weighted MR images showed clear demarcation of thickened intimal and medial layers in our study. There was a tendency of more involvement of the left wall of the aorta. The cause of crescent-like wall thickening is not clear, although chemical shift artifacts can affect the aortic wall configuration [21]. In the healthy control subjects, we saw no significant difference in the thickness among the right, left, and posterior aortic wall on MR images.
According to one experimental study on perigraft inflammation after delivery of various coated stents in the iliac arteries of animals, contrast-enhanced MR imaging showed marked enhancement at the inflamed segment [13]. On T2-weighted images, high signal intensity was seen at the inflamed segment. During the acute phase of Takayasu's arteritis, enhancement of the aortic wall and periadventitial soft tissue can also be observed. Patterns of aortic wall enhancement varied in our study. The thickness of the brighter inner layer and that of the middle gray layer varied among patients and by location in the aorta.
In chronic cases, increased accumulation and delayed washout of contrast medium in the thickened aortic wall may suggest persistent activity of Takayasu's arteritis; contrast-enhanced MR imaging seems to be more sensitive than erythrocyte sedimentation rate and C-reactive protein level in these cases. In the quiescent stage, contrast enhancement may not occur in the aortic wall. Images of this "cold" aortic wall may indicate extensive fibrosis with diminished microscopic vessels. Using our criteria for Takayasu's arteritis activity, we may have erroneously placed patients with chronic active Takayasu's arteritis in the inactive group when the degree of aortic enhancement is less than that of myocardium. Thus, our criteria for Takayasu's arteritis activity determination are not highly sensitive but are highly specific. Focal or segmental enhancement of the aorta and cervical arteries may suggest progression of the disease in a localized region. Aortic wall thickness itself may reflect activity of Takayasu's arteritis [12]. In most patients with inactive Takayasu's arteritis, aortic wall thickness was less than 4 mm. However, most patients with acute or chronic active Takayasu's arteritis showed aortic wall thickness of 5-7 mm in this study.
The sensitivity of T2-weighted imaging in the detection of active Takayasu's arteritis seems to be inferior to that of contrast-enhanced T1-weighted imaging. All three patients in acute phase with high signal intensity on T2-weighted images also had significant enhancement on T1-weighted spin-echo images. However, T2-weighted images were not sensitive in four patients with persistent chronic activity determined on contrast-enhanced T1-weighted MR imaging. Erythrocyte sedimentation rate was also elevated in three of these patients. We speculate that an increased number of vessels in the inflamed aortic wall contributes to enhancement of the aortic wall and that there is no edema in the aortic wall in chronic active cases.
MR imaging appears to be superior to conventional angiography in the early diagnosis of Takayasu's arteritis because in Takayasu's arteritis early changes occur in the vessel wall and luminal stenosis or occlusion is usually a late manifestation. In addition, MR technique appears to provide important information about the disease activity. Therefore, for the early diagnosis of Takayasu's arteritis, we suggest that a ringlike or crescentlike aortic wall thickening of more than 3 mm on MR imaging or CT and a concentric wall thickening of the carotid, subclavian, and vertebral arteries or occlusion of these vessels on sonography or MR imaging be included as major criteria of Takayasu's arteritis.
In conclusion, contrast-enhanced MR imaging may be useful in evaluation of disease extent and disease activity of Takayasu's arteritis as well as for early diagnosis in patients with nonspecific systemic symptoms.
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