Patterns of aortic involvement in Takayasu arteritis and its clinical implications: Evaluation with spiral computed tomography angiography

Article Outline

• Abstract
• Materials and methods
• Results
• Discussion
• Conclusion
• Author contributions
• References
• Copyright

Objective

Although the luminal changes of Takayasu arteritis are well depicted with conventional angiography, its mural changes can be best evaluated with spiral computed tomography (CT) angiography. Here, the authors investigated the patterns of aortic involvement in Takayasu arteritis by using CT angiography.

Methods

CT angiography was performed from the carotid bifurcation to the iliac bifurcation in a consecutive 85 patients (M:F = 10:75, mean age: 37 years) with Takayasu arteritis. Two radiologists interpreted axial images and three-dimensional reconstructed images by consensus with respect to disease extent, lesion continuity, and disease activity based on mural and luminal changes on CT angiography.

Results

Eighty-one (95%) patients had aortic involvement with or without aortic branch involvement, and the other four (5%) patients had only aortic branch involvement. In terms of aortic branches, the left common carotid artery (77%) and the left subclavian artery (76%) were most commonly involved. Extent of disease involvement assessed by mural change was wider than that assessed by luminal change in 52 (61%) patients. Although arterial involvement was contiguous in 69 (81%) patients, skipped lesions were identified in 16 (19%) patients. An analysis of mural findings revealed the coexistence of active and inactive lesions in nine (11%) patients.

Conclusions

Aortic involvement in Takayasu arteritis can occur from the aortic root to below the iliac bifurcation, and isolated branch vessel involvement is also possible. In most patients, aortic involvement occurs in a contiguous, synchronous fashion. However, skipped involvement and the coexistence of active and inactive lesions also occur.

Takayasu arteritis (TA) is a chronic inflammatory and obliterating disease of the aorta, its branches, and of the pulmonary artery of unknown etiology. Diagnosis is based on clinical signs and symptoms, laboratory findings, operative and angiographic findings.¹, ², ³ TA is found predominantly in female patients and has a worldwide distribution although it is more commonly seen in Asian and Latin American countries.³, ⁴, ⁵, ⁶, ⁷

The basic pathologic features of TA concern mural changes in great vessels. However, mural changes cannot be evaluated by conventional angiography, and previous reports on the classification of aortic involvement in TA have been based on conventional angiography.², ⁸, ⁹ Diagnosis during early stage disease is often missed or delayed because of a nonspecific clinical presentation and no luminal changes of aorta or of its branches by conventional angiography, which thus, underestimates true disease extent even in the pulseless disease stage.¹, ¹⁰, ¹¹

Unlike conventional angiography, computed tomography (CT) angiography is capable of demonstrating mural and luminal changes in both the aorta and aortic branches, and has greater diagnostic accuracy than conventional angiography.¹², ¹³, ¹⁴, ¹⁵, ¹⁶ Therefore, new interpretation of aortic involvement in TA should be carried out in the era of CT angiography. In the present study, the authors investigated patterns of aortic and aortic branch involvements, based on mural changes in CT angiography.

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Materials and methods 

Patients. Between 1994 and 2003, 1997 CT angiographic examinations in 1254 patients were performed to evaluate suspected aortic pathology, and 157 CT examinations in 113 patients were performed to evaluate suspected Takayasu arteritis. Among them, 85 patients met three or more of six American College of Rheumatology’s diagnostic criteria for TA.¹⁷ Thus, this study included consecutive Korean 85 TA patients (75 females and 10 males) who had CT angiography between 1994 and 2003. Patients were between 11- and 66-years-old (mean, 37 years) and were diagnosed based on clinical, laboratory, and angiographic findings. Chief complaints of 85 patients were dyspnea (n = 15), hypertension evaluation (n = 13), chest pain (n = 13), pulseless arm (n = 7), fever (n = 6), blood pressure difference of both arms (n = 5), headache (n = 5), paresthesia (n = 4), claudication (n = 4), loss of consciousness (n = 3), neck pain (n = 3), cerebral infarct (n = 2), abdominal pain (n = 2), dizziness (n = 1), deafness (n = 1), and abnormal chest radiography (n = 1). In 36 patients, the clinicians suspected the diagnosis of TA on the basis of the clinical characteristics of the patients (ie, ischemic symptoms and signs or fever of unknown origin in young female) and the diagnosis of TA was made after CT angiography. The remaining 49 patients had diagnosed as having TA, 3 months to 17 years (mean, 6.5 year), before CT angiography scanning, and CT angiography was performed for follow-up evaluation of known TA. Fifteen patients had received steroid therapy before CT scanning. Conventional angiography was performed in 59 of these 85 patients a month or less after CT angiography, and echocardiography was undertaken in 48 to confirm possible aortic regurgitation.

CT angiography technique. For CT examinations, a Somatom Plus S (n = 7), a Somatom Plus 4 (n = 54) (Siemens, Erlangen, Germany), and an MX8000 multidetector row CT scanner (n = 24) (Philips Medical Systems, Cleveland, Ohio) were used. CT scans were defined as three distinct phases, ie, the unenhanced, arterial, and delayed phases. Initially, unenhanced images were obtained from the carotid bifurcation to the iliac bifurcation level, with parameters of 5 mm collimation and 10 mm interscan interval.

For the Somatom Plus S and Plus 4 scanners, two consecutive arterial phases were scanned from the carotid bifurcation to the iliac bifurcation using a breath-hold technique. The CT parameters were 3 mm beam collimation, 5-6 mm/s table speed, 3 mm slice thickness, and a 2 mm reconstruction interval. For the MX8000 scanner, single arterial phase was scanned using a breath-hold technique with the following parameters; 2.5 mm detector collimation, 20-30 mm/s table speed, 3.2 mm slice thickness, and a 1.6 mm reconstruction interval. Contrast medium (Ultravist 370, Schering, Berlin, Germany) was injected intravenously into an upper extremity or a lower extremity vein at 3 mL/s and with a bolus of 120-150 mL. Arterial phase delay times were chosen empirically and were in the range 20-30 seconds after injection start. Subsequently, delayed CT scans were also obtained using 5 mm collimation and 10 mm interscan interval from the carotid bifurcation to below the iliac bifurcation. Delayed scans were initiated 30 seconds after arterial phase.

Image analysis. Thin-section axial images were transferred to a personal computer containing three-dimensional (3D) reconstruction software (Rapidia; INFINITT, Seoul, Korea). Volume data was loaded into the 3D program and an experienced radiologist (J.W.C.) performed 3D reconstruction, which included volume rendering, maximum intensity projection, and multiplanar reformation. Two radiologists (Y.H.C., J.W.C.) evaluated patterns of aortic and aortic branch involvement using axial images and 3D images. Evaluations included disease extent, lesion continuity, and disease stage based on mural and/or luminal changes by consensus.

To evaluate disease extent, the aorta was segmented arbitrarily into the following: aortic root; ascending aorta; aortic arch; proximal, middle and distal descending thoracic aorta; and suprarenal, infrarenal and infra-IMA (inferior mesenteric artery) abdominal aorta. Aortic and branch involvements were determined based on the presence of mural or luminal changes. The mural changes indicative of active lesion TA were a thickened arterial wall with mural enhancement and low attenuation ring on delayed phase images (Fig 1, B and D).¹², ¹⁴ The mural changes indicative of inactive lesion TA were a slightly thickened or normal arterial wall with a high attenuation ring or calcifications on unenhanced phase images, and slight mural enhancement without low attenuation ring on delayed phase images (Fig 1, C).¹², ¹⁴ Aortic wall thickening was defined as a wall thickness >1 mm with enhancement on a contrast-enhanced CT image; a previous study revealed that aortic walls are either <1 mm thick or imperceptible in healthy adults.¹², ¹⁴ Luminal changes associated with TA were stenosis, occlusion, and dilatation, and these were primarily evaluated on 3D reconstruction CT angiographic images in conjunction with conventional angiographic images in 59 patients.

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• Fig 1. 

  Takayasu arteritis showing active and inactive lesions in a 25-year-old woman. A, Multiplanar reformation image shows wall thickening of aortic arch and abdominal aorta (arrowheads). Mural calcification and stenosis of descending thoracic aorta (arrow) is noted. B, CT scan shows diffuse wall thickening of ascending and descending thoracic aorta (arrowheads) suggesting active lesion. C, CT scan shows mural calcification and stenosis of descending thoracic aorta (arrowhead) suggesting inactive lesion. D, CT scan shows wall thickening, inner low-attenuated ring, and aneurismal dilation of abdominal aorta (arrowheads) suggesting active lesion.

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Results 

Eighty-one (95%) of the 85 patients showed aortic involvement with or without major aortic branch vessel involvement (Fig 2, Fig 3, Fig 4, Fig 5). TA presented a spectrum of aortic involvements from the aortic root to below the iliac bifurcation (Table I). Aortic roots and infra-IMA aorta were less frequently involved than in other aortic segments. The remaining four patients (5%) showed aortic branch involvement without aortic involvement; ie, only the left subclavian artery in three patients; the innominate artery, both common carotid artery, and superior mesenteric artery in the other one (Fig 6).

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• Fig 2. 

  The spectrum of aortic involvement in patients with Takayasu arteritis. The extent of aortic involvement is presented in 81 patients with aortic involvement. A, line without interruptions indicates contiguous involvement. Interrupted lines in 11 patients indicate the presence of skipped area between the diseased aortas. Four patients without aortic involvement are not presented on the diagram. Root, aortic root; AA, ascending thoracic aorta; Arch, aortic arch; p-DTA, proximal descending thoracic aorta; m-DTA, middle descending thoracic aorta; d-DTA, distal descending thoracic aorta; SR-AA, suprarenal abdominal aorta; IR-AA, infrarenal abdominal aorta; IIMA-AA, infra-inferior mesenteric artery abdominal aorta.

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• Fig 3. 

  Takayasu arteritis involving aorta with skipped segment in a 50-year-old woman. A, Multiplanar reformation image shows wall thickening (arrowheads) of ascending thoracic aorta, aortic arch, proximal descending thoracic aorta, and abdominal aorta. No wall thickening of distal descending thoracic aorta is noted. Motion artifact (pulsation artifact) was not observed in the thickened segment such as aortic arch and abdominal aorta due to stiffness of involved aorta and was observed in the distal descending thoracic aorta (arrows) due to pulsation of the noninvolved segment. B, CT scan at the proximal descending thoracic aorta shows diffuse wall thickening and inner low attenuated ring of ascending (arrow) and descending thoracic aorta (arrowhead). C, CT scan at the distal descending thoracic aorta (arrow) shows no wall thickening of aorta. D, CT scan at the abdominal aorta shows diffuse wall thickening and inner low attenuated ring of abdominal aorta (arrow).

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• Fig 4. 

  Takayasu arteritis involving abdominal aorta and both renal artery in a 20-year-old woman. A, Maximum-intensity-projection image shows severe stenoses of both proximal renal artery (arrows) and luminal irregularity of abdominal aorta (arrowheads). Normal-looking far distal abdominal aorta (yellow line) is noted. B, CT scan at the far distal abdominal aorta shows diffuse wall thickening of abdominal aorta (arrows) suggesting active inflammation of aorta wall despite of no abnormality at maximum-intensity-projection image. C, Volume rendering image after auto-transplantation of both kidneys shows the graft between the left iliac artery and left renal artery, and the right kidney directly anastomosed with right iliac artery.

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• Fig 5. 

  Takayasu arteritis causing complete occlusion of both carotid and subclavian arteries in a 57-year-old woman. A and B, Conventional aortography shows complete occlusion of both common carotid and subclavian arteries. Dilated left vertebral artery (arrow) in noted. Reconstructed left internal carotid artery (arrowhead) is faintly observed. C, Volume rendering image clearly shows reconstituted left internal and external carotid arteries (arrow).

Table I. Involvement of aorta, its branches, and pulmonary artery in patients with Takayasu arteritis

Location	No. of patients evaluated	No. of patients involved	Occlusive lesion	Aneurismal lesion	Wall thickening lesion
Aorta
Aortic root	85	31(36%)	0	10	21
Ascending aorta	85	50(59%)	0	15	35
Aortic arch	85	68(80%)	1	5	62
Proximal descending thoracic aorta	85	69(81%)	6	2	61
Middle descending thoracic aorta	85	66(78%)	11	5	50
Distal descending thoracic aorta	85	64(75%)	16	4	43
Suprarenal abdominal aorta	85	61(72%)	18	1	42
Infrarenal abdominal aorta	85	55(65%)	19	1	35
Infra-IMA abdominal aorta	85	30(35%)	6	0	24
Aortic branches
Innominate artery	81	57(70%)	6	9	42
Right common carotid artery	82	53(65%)	27	2	24
Right external carotid artery	21	2(10%)	1	0	1
Right internal carotid artery	21	1(5%)	0	0	1
Right subclavian artery (proximal)	83	41(49%)	21	6	14
Right subclavian artery (distal)	82	30(37%)	17	2	11
Right vertebral artery	78	5(6%)	3	0	2
Left common carotid artery	83	64(77%)	46	1	17
Left external carotid artery	23	6(26%)	3	0	3
Left internal carotid artery	22	5(23%)	2	0	3
Left subclavian artery (proximal)	84	64(76%)	44	2	18
Left subclavian artery (distal)	81	48(59%)	38	1	9
Left vertebral artery	78	9(12%)	6	0	3
Celiac trunk	83	11(13%)	9	0	2
Superior mesenteric artery	83	28(34%)	20	0	8
Right renal artery	84	27(32%)	26	0	1
Left renal artery	83	34(41%)	34	0	0
Inferior mesenteric artery	82	2(2%)	0	0	2
Right common iliac artery	81	12(15%)	2	0	10
Right external iliac artery	55	1(1%)	1	0	0
Left common iliac artery	81	12(15%)	2	0	10
Left external iliac artery	55	0(0%)	0	0	0
Pulmonary artery	83	22(27%)	20	0	2

Infra-IMA, infra-inferior mesenteric artery; (proximal), proximal to the origin of vertebral artery; (distal), distal to the origin of vertebral artery.

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• Fig 6. 

  Takayasu arteritis involving only aortic branch vessels in a 19-year-old woman A, Multiplanar reformation image shows wall thickening of left common carotid (arrowheads) and superior mesenteric arteries (arrows). B, Arterial phase CT scan at the common carotid artery level shows diffusion wall thickening of left common carotid artery (arrows). C, Delayed phase CT scan at the common carotid artery level shows enhancing thickened wall and inner low-attenuated ring of left common carotid artery (arrows). D and E, CT scan at the descending thoracic aorta level shows no definite wall thickening of aorta (arrow). F, Arterial phase CT scan at the abdominal aorta level shows no wall thickening of abdominal aorta (arrowhead) and wall thickening of superior mesenteric artery (arrows). G, Delayed phase CT scan at the abdominal aorta level shows wall enhancement of superior mesenteric artery (arrows).

Aneurismal lesions commonly involved the ascending thoracic aorta and less commonly descending thoracic aorta (Table I). Aneurismal lesions involved the aorta or aortic branches in 19 patients, and two of 19 patients had partial thrombosis within the aneurismal lesions. Occlusive lesions predominantly involved aortic branches including the carotid, subclavian, and renal arteries, and less commonly abdominal aorta. Three patients had only wall thickening without occlusive or aneurismal lesion.

In 52 (61%) of the 85 patients, the extent of disease involvement assessed by mural changes on CT angiography was wider than that assessed by luminal changes. These 52 patients had at least one vascular segment with normal endoluminal diameter and luminal regularity but with vascular wall thickening (Fig 4).

In a subgroup of 48 patients who underwent echocardiography, aortic regurgitation was observed by echocardiography in 23, and 17 of these 23 patients had an abnormality such as luminal dilation or an increased wall thickness of aortic root by CT angiography (Table II).

Table II. Relation between abnormality on CT angiography and aortic regurgitation demonstrated on echocardiography

TA extended to the carotid bifurcation, the external and internal carotid arteries, and to the external iliac artery. Aortic branch involvement incidences are summarized in Table I. Aortic arch vessels were involved more commonly than abdominal aortic branches, and the left common carotid artery, left subclavian artery, and innominate artery were involved in 77%, 76%, and 70%, respectively. In terms of abdominal aortic branches, the inferior mesenteric artery was involved just only in two (2%) patients.

Complete occlusion of the right or left common carotid artery was present in 13 patients, and CT angiography scanned from internal carotid artery in six of 13 patients. CT angiography in these six patients clearly showed the reconstituted internal carotid arteries, which were hardly perceptible at conventional angiography (Fig 5).

Although vascular involvements were contiguous in 69 (81%) patients, intervening normal arterial segments were identified in 16 patients (19%). Those normal segments were located between involved aortic segments (n = 11) (Fig 3), between an involved aortic segment and an involved branch vessel (n = 2), within involved arch vessel (n = 2) and in one case entirely spared the aorta but with involvement of arch vessels and the superior mesenteric artery (n = 1) (Fig 6).

According to mural changes, 34 patients had active lesions, 34 inactive lesions, and nine synchronously active and inactive lesions (Fig 1). In the remaining eight patients, it was difficult to determine disease activity. In 79 patients in whom erythrocyte sedimentation rate (ESR) was estimated, ESR in patients with active lesions was higher than that in ones with inactive lesions (Table III).

Table III. Relation between activity based on CT angiography and ESR in 79 patients with Takayasu arteritis

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Discussion 

Necessity and rationale to evaluate patterns of aortic involvement in Takayasu arteritis with CT angiography. Conventional angiography continues to be used as a standard tool for the diagnosis and evaluation in TA. The main arterial changes on angiograms are stenosis and occlusion, though dilatation and aneurysm formation are also found. Moreover, the Ueda classification, Ueno’s classification, and the classification of the International Conferences on TA (Tokyo, 1994) were all based on conventional angiography.¹, ², ⁸, ⁹

In TA, early diagnosis and treatment result in early remission and a better prognosis. In early stage disease, mural changes may be the only positive finding. CT angiography is able to demonstrate mural changes as well as luminal changes,¹⁴ whereas conventional angiography shows mainly luminal changes in the aorta and its major branches. Therefore, CT angiography could be used to diagnose TA at an earlier stage, and if so, the classification of aortic involvement should be based on CT angiographic presentations. Park et al¹⁴ classified ten patients as type I (4 patients), type II (3 patients), and type III (3 patients) according to Ueda classification by conventional angiography, but as type I (2 patients), type II (2 patients), and type III (6 patients) by CT angiography. In this study, three patients had only wall thickening without occlusive or aneurismal lesion. If conventional angiography had been performed alone, the diagnosis of TA might be delayed.

In addition, recognition of normal arterial segments without mural inflammation is important when planning bypass surgery, such as, aorto-carotid, aorto-renal, aorto-aortic bypass surgery, for symptomatic occlusive disease. Therefore, aortic involvement in TA requires re-interpretation with respect to CT angiographic finding.

Topographical distribution of aortic involvement. The incidences of specific organ involvements vary in reported series, which may relate to ethnic differences.⁶, ⁹ According to Hata et al,⁹ in Japanese patients, the aortic arch and its branches are mainly affected, whereas in Indian patients, the abdominal aorta and renal arteries are mainly involved. In our study, the aortic arch and its branches were found to be dominantly affected, which is similar to that reported in the Japanese. However, disease extents in TA in this study were more variable as shown in Fig 2. It may be because CT angiography provides more detailed information concerning the scope of vascular involvement and disease extent.

The incidence of aortic involvement in patients with TA is between 50% and 76%.¹, ⁹, ¹⁸, ¹⁹, ²⁰ However, because CT shows abnormalities like aortic wall thickening without luminal change, the incidence of aortic involvement was high, 95% in the present series. The remaining four (5%) patients showed aortic branch involvement only.

The incidence of aortic valve regurgitation in TA patients lies between 13% and 25%, and aortic regurgitation is now considered an important risk factor for mortality TA.²¹, ²², ²³, ²⁴ Aortic regurgitation was found in 23 patients in our study, ie, 27% of the study population. Since aortic regurgitation was demonstrated by echocardiography in 17 of 24 patients with aortic root involvements, we consider that CT angiography helps predict aortic regurgitation.

Approximately 10% to 20% of TA patients experience an ischemic stroke or transient ischemic attack.¹ Common carotid artery involvement with sparing of the internal and external carotid arteries is frequent in TA, and the common carotid artery is often diseased.¹, ²⁵ In the present study, right or left common carotid artery involvement was present in 65% and 77% of the patients evaluated, respectively, and internal and external carotid artery involvements were less than 26%. Aorta-carotid bypass surgery is needed in patients with ischemic symptoms and an awareness of normal internal carotid artery segments is important. Conventional angiography often fails to demonstrate the reconstituted internal carotid artery in case of complete occlusion of the common carotid artery, whereas CT angiography clearly showed the reconstituted internal carotid arteries. This is attributed to the longer scan delay time of CT angiography, which allows contrast material to fill the reconstituted internal carotid artery.

Renovascular hypertension in TA is one of the common indications for intervention and surgical treatment.²⁶, ²⁷, ²⁸ Weaver et al²⁸ recently reported that the detection of an anastomotic region without apparent inflammation is important for preventing graft failure due to inflammation at an anastomotic site. In our series, the extent of disease involvement, assessed by mural changes, was wider than that assessed by luminal changes in 52 (61%) patients. Thus, if surgical treatment is planned, CT angiography plays a key role in selecting sites for graft anastomosis.

Sharma et al¹³ reported that TA involves a contiguous length of aorta, and that it caused wall and luminal changes in certain areas but only wall changes in the intervening segments. In our study, although it was true in 69 (81%) patients, normal intervening aortic segment without wall changes was observed in 16 patients (19%).

Coexistence of active and inactive lesions. Current laboratory markers of disease activity are insufficiently reliable to assess disease activity, and thus, disease activity should be determined based on clinical, laboratory, and imaging findings. According to the reports of Park et al,¹², ¹⁴ early enhancement during the arterial phase, delayed mural enhancement, and an inner concentric, low-attenuation ring in the aorta and pulmonary artery during the arterial and delayed phases of CT scanning, suggest active disease. Lack of mural enhancement in the early and delayed phases, high mural attenuation on precontrast images, and calcification of great vessel walls are disorders more likely to be seen in patients with inactive disease. The high attenuation of these vessel walls, demonstrated on precontrast images, is probably due to mural calcium deposition, which occurs in TA, and the presence of full-thickness calcification may be due to the transmural nature of this inflammatory disease.¹⁴

The relapsing nature of TA often requires repeated courses of medical therapy, in fact 50% of patients experience relapse within 5-years follow-up.¹ Our study also revealed the coexistence of active and inactive lesions in nine (11%) patients. CT scans should be performed from the carotid bifurcation to the iliac bifurcation to evaluate disease activity during follow-up.

The present study has several limitations. First, CT angiography has some shortcomings with regard to evaluating aortic branch involvement.¹⁵ Although aortic branches adjacent to the aortic arch were clearly depicted by CT angiography, those remote from the aortic arch, such as, distal portions of the subclavian artery and vertebral artery, were less clear and often difficult to evaluate. This limitation could be overcome by multidetector CT. Second, various CT scanners, including a single detector CT, were used in this study over a 10-year period. Thus, CT scan ranges were not constant and evaluations of internal carotid artery and external iliac artery were not possible in many patients. Third, there is no pathologic proof for disease involvement. We think the disease extent in this study might be somewhat underestimated because microscopic involvement can not be detected on CT angiography. Fourth, this study did not evaluate the lesions in coronary artery. The involvement of coronary artery is important for the management of patients with TA. With the recent advent of 16 channel- or 64 channel-detector CT scanner, the evaluation of coronary artery can be possible by CT scanner, and this issue should be further studied.

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Conclusion 

In conclusion, TA can involve the internal and external carotid artery and external iliac artery and can involve just only aortic branches. There can be skipped lesion and coexistence of active and inactive lesions. Mural changes in TA are broader than luminal changes that are seen at conventional angiography. Hence, the present study indicates that CT scans should be performed from the carotid to iliac bifurcation to adequately evaluate and diagnose TA.

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Author contributions 

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References 

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