Heart Vessels (1992) Suppl. 7:60-67
Heart
andl[ T
1
vessels
© Springer-Verlag1992
Takayasu arteritis in Thailand Chaliow Piyachon 1 and Nitaya Suwanwela 2 1Department of Radiology, Faculty of Medicine, Chiangmai University, Chiangmai, Thailand 2 Department of Radiology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
S u m m a r y . Takayasu arteritis is a disease of worldwide distribution. Geographic difference in sex incidence, anatomical distribution, and the type of lesion is observed. Hypertension is very c o m m o n in the present series, as well as in combination with absent or deficit of peripheral pulses. These symptoms correlate well with arteriographic findings of brachiocephalic and renal artery obstructive lesion. While aneurysm and stenotic lesions have a predilection in the abdominal aorta, stenotic lesion of the thoracic aorta occurs more commonly than aneurysm. However, aneurysm of the aorta as well as of the brachiocephalic arteries is seen more frequently than in the reports, of others. The presence of "funnel-shape" resulting from renal artery obstructive lesion and dilatation or aneurysm of contiguous aorta was characteristic of Takayasu arteritis in our series. The material presented in this report reflects not only geographic variation but also the severe form of this disease. Total aortography, coronary arteriography and pulmonary arteriography, are of value not only for the diagnosis of Takayasu arteritis but also for demonstration of anatomical distribution, severity and type of lesion.
Key words: Takayasu disease - Non-specific aortoarteritis- Occlusive t h r o m b o a o r t o p a t h y - Aortography - Pulseless disease
Introduction Takayasu arteritis (TA) is a non-specific inflammatory disease of the arteries, affecting the aorta and its main branches as well as the pulmonary arteries. It is now Address correspondence to: N. Suwanwela
known to be distributed worldwide. The inciclence of the disease in Thailand has not been estimated but it is considered to be uncommon. Previous reports from Thailand, as well as from those in the literature represent rather severe forms of this disease. Thus, it is apparent that most cases of mild or asymptomatic lesions of Takayasu arteritis have escaped clinical identification. To this regard, radiographic and pathologic findings reported in the literature were mainly that of the severe forms. In Thai patients, it was noted that aneurysmal changes of the aorta as well as its branches occurred much more commonly than such findings in the reports from other countries. The variations in anatomical involvement and character of arterial changes have been observed in relation to certain geographic areas and ethnic origin of patients [1-6]. It is our intention to review arteriographic patterns of this disease in Thai patients presenting geographic and racial variation.
Materials and methods Material histories in this study were gathered in 2 periods, 8 years apart at Chulalongkorn Hospital in Bangkok. The first study was made during a 6-year period from 1971-1976 [6]. This study identified 20 cases of Takayasu arteritis, 15 were females and 5 males, a ratio of 3 to 1. The ages ranged from 9 to 35 years [6]. The second study was made during 1985-1990, another 6-year period. Twenty-six cases of Takayasu arteritis were diagnosed. There were 15 females and 11 males, a ratio of 1.36 to 1. The age ranged from 7 to 40 years. The total number of cases in these 2 periods were 46, with a female to male ratio of 1.88 to 1. All the patients were Thai or Thai-Chinese origin. None of them were from the same family. Eight cases had postmortem confirmation of the diagnosis. Otherwise the diagnosis of Takayasu arteritis was mainly based on the arteriographic findings, supported by the clinical and laboratory results. The clinical and laboratory findings in general corresponded to those discribed in the literature [1-7]. The most common presentation was hypertension. This was found in 80% of the cases, while
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
61
Table 1. Clinical findings in Takayasu arteritis (46 cases)
Findings
Cases (n)
Hypertension Absent or weakness of pulses Congestive heart failure Cerebrovascular disease Others: Aortic insufficiency Pericarditis Joint pain Abdominal mass
37 23 13 11 7 3 1 2 1
Table 2. Summary of regional involvement in Takayasu arteritis (38 cases with total angiography) Vessels
Ascending aorta Aortic arch Descending thoracic aorta Abdominal aorta Brachiocephalic artery Innominate artery Subclavian Rt. artery Lt. Common carotid Rt. artery Lt. Vertebral artery Rt. Lt. Visceral branches Celiac artery Superior mesenteric artery Inferior mesenteric artery Renalartery Rt. Lt. Iliac artery Rt. Lt. Total
Findings A
D
S
1 4 13
12 10 3 9
1 1
7 12
1
5 4 3 7 6 1 1
4 12 5 4 4 5
4 6 1 2 4 3
2 3
1
2
4
2
1
4
11
12 10 3 2
2 8 8 3 4
88
61
5 5 2
2 3 35
6 8 4
81
O
Total number I of lesions 2 14 23 1
13 14 28 58 6 19 29 15 12 9 9
16 1 1
49
8 29 25 9 O 314
A, Aneurysm; D, dilatation; S, stenosis; O, occlusion; I, irregular contour; Rt., right; Lt., left abseht or weakness of pulses were presented in 50% of the cases. Congestive heart failure was found in approximately 35%. Aortic insufficiency was present in 5 out of 46 cases, approximately 11%. Other clinical features including vertigo, syncope, visual disturbances, and joint symptoms were also observed (Table 1). One patient also had immune complex membranous proliferative glomerulonephritis diagnosed by renal biopsy. For the treatment, corticosteroids and immunosuppressive therapy were mainly used. Surgical interventions were done in 11 cases, including by-pass procedures and graft in 5, autorenal transplantation in 3, nephrectomy in 2, and renal artery endarterectomy in 1. Percutaneous transluminal angioplasties were performed in 3 cases with improvement of the stenosis. Total aortography was performed in all cases in the earlier study, while in the recent study, total aortography was done in 18 out of 26 cases. Neither pulmonary arteriography nor coronary arteriography was performed.
Fig. 1. Thoracic aortogram. Oblique view demonstrates dilatation of ascending thoracic aorta with no evidence of aortic insufficiency
Results
Arteriographic findings The arteriographic abnormalities in Takayasu arteritis include various forms of irregular contour, stenosis, occlusion, dilatation, aneurysm, or a combination of these changes. In our patients, dilatation and aneurysmal formation in the aorta were more common than stenotic lesions, which is contrary to the more common stenosis or occlusion of the branch arteries. In addition, marked irregularity of the contour of the involved vessels commonly occurred. Arteriographic findings and frequency of the lesions are summarized in Table 2. A s c e n d i n g a o r t a a n d aortic arch Dilatation of both ascending aorta and aortic arch was encountered in 16 cases (Fig. 1) and of the ascending aorta in 5 cases. Descending thoracic aorta Eighteen patients developed lesion of the descending thoracic aorta: diffuse dilatation in 3, a Iong stenotic lesion in 7 (Fig. 2) and both types of lesion in 2 patients. It was noted that a prestenotic dilatation of the ascending aorta accompanied the stenotic lesion in few cases. During aortography, visualization of dilated bronchial arteries were seen in 2 cases with prompt opacification of the pulmonary arterial branches, indirectly indicative of pulmonary stenotic lesion. Abdominal aorta The abdominal aorta was involved in 76% of the cases at the proximal and mid segments; aneurysmal lesions
62
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand in nature. The carotid arterial lesion occurred less commonly. The lesion was obstructive in nature. All obstructive lesions of the brachiocephalic arteries demonstrated good collateral circulation. Their dilatation was commonly seen, probably secondary in order to increase blood flow, as well as a pre-or poststenotic dilatation. Visceral b r a n c h e s o f a b d o m i n a l a o r t a Occlusion or stenosis of the celiac, superior mesenteric or inferior mesenteric arteries at their origin was not common. However ample collatera| circulation was observed in all cases of visceral obstructive lesions (Figs. 4, 8). R e n a l arteries Renal artery occlusion or stenosis was present in 28 patients (74%), 17 of them bilaterally. The lesion involved a short segment of the proximal part of the renal artery in all cases, usually with abrupt tapering, except for a few case which showed elongated narrowing of the longer segment of the main artery. Poststenotic ditatation and aneurysm were demonstrated in 11 cases (Fig. 6). In 6 cases, aortic aneurysm was continuous with prestenotic di|atation of the renal arteries and manifested themselves by a characteristic "funnel-shape" or triangular configuration, as previously reported [6]. Ample collateral circulation was observed in almost all cases of complete or almost complete obstructive lesions of renal arteries Most of the 37 patients with hypertension demonstrated obstructive lesion of renal arteries, with a few cases of renal artery stenosis being normotensive.
Fig. 2. Thoracic aortogram shows an area of narrowing involving a short segment of mid-part of the descending thoracic aorta (arrowhead). The rest of the thoracic aorta appears normal
in 13 cases with 1 case of saccular aneurysm (Figs. 3 - 6 , 8) and stenotic lesion in 12 cases (Fig. 4). Complete occlusion of the abdomina| aorta with extensive collateral circulation was found in one case (Fig. 5). B r a c h i o c e p h a l i c arteries One or more branches of the brachiocephalic arteries were involved in 30 cases (79%) (Fig. 7). The subclavian arteries were the most commonly involved and more than half of the cases were bilateral. The |esions were mainly obstructive, but fusiform aneurysm and saccular aneurysm occurred in approximately one third of the cases. Most of the subclavian obstructive lesions developed at or just distal to the origin of the vertebral artery. A long segmental narrowing of the subclavian artery extension into the axil|ary artery was seen in a few cases. Vertebral arteries were the next commonly involved. All vertebral arterial lesions were the obstructive type, either stenosis or occlusive
Iliac and f e m o r a l arteries Because arteriographic studies of the femoral artery were not included for most of the cases, the true incidence of femoral artery involvement was not assessable. Internal iliac involvement was more common than the common iliac or external iliac arteries. In severe cases, multiple lesion sites were seen. Obstructive lesions occurred in 11 cases, (Fig. 9) while fusiform and saccular aneurysm were seen in 3 cases; each involving the common iliac and femoral arteries.
Discussion A diagnosis of Takayasu arteritis may be suspected on clinical grounds alone, particularly with presence of pulse weakness or deficits and especially in young female patients. However, a more definitive diagnosis is established on the basis of angiographic findings. The study should include the entire aorta and proximal branches [4, 5]. Intravenous digital subtraction angiography is very helpful in depicting the changes and is the preferred investigation in view of its safety. How-
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
63
Fig. 3. A saccular aneurysm is seen in this abdominal aortogram, located just below the origin of the celiac artery. The right renal artery is occluded. Note a stenotic lesion of the proximal part of the left renal artery (arrowhead)
Fig. 4. Abdominal aortogram reveals a long segment of stenotic lesion at its proximal and distal parts (arrowheads) with occlusion of the celiac and superior mesenteric arteries. Note dilated intercostal and lumbar arteries as well as many small vessels originating from the aorta serving collateral pathways. The proximal part of the right renal artery appears stenosed
ever, its use is limited in patients with congestive cardiac failure and the uncooperative patient. Mild involvement of the descending aorta in the region of the diaphragm could not be assessed. Intra-arterial digital subtraction angiography should be the better method for specific areas and details. Computed tomography is another method used for diagnosis and follow-up studies of Takayasu arteritis following steroid therapy [13, 14]. Aortic wall thickening may be demonstrated by CT and the thickening may be partly or largely due to periaortic infiltration. However, the measurement of the thickness of the wall is not always possible because of the limited spatial resolution of CT and the marked variations in caliber of the aorta during the cardiac cycle. Aneurysm
and related hematoma indicating prior aortic rupture or vascular rupture are also well demonstrated on CT scan [15, 16]. Presently, alternative imaging, such as magnetic resonance imaging (MRI) is not yet widely used for one reason, its high cost. Miller et al. [17] have evaluated the ability of MRI to detect vascular abnormalities in 10 patients with Takayasu arteritis, comparing it to angiography in 1985. Adequate MR visualization was consistently achieved only in the aorta, the common iliac arteries, and the inmominate artery. MRI also provided superior information about pulmonary artery patency [18]. With current equipment and technology, MRI may be even more useful as a screening examination, especially the technique of magnetic resonance angiography.
64
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
Fig. 5. a Abdominal aortogram shows a relatively long segment of an aneurysmal dilatation of the proximal abdominal aorta. Complete occlusion of the aorta below the origin of the renal artery is evident. Note dilatation of the gastroduodenal and meandering mesenteric arteries, b Late arterial phase demonstrates ample collateral circulation with retrograde filling of the distal part of the aorta to the level of occlusion (0). There is narrowing of the distal aortic segment just above the aortic bifurcation
Fig. 6. Abdominal aortogram demonstrates a large fusiform aneurysm of its proximal part. There is a complete occlusion of left renal artery near the origin. A stenotic lesion of the right renal artery is seen approximately 0.5cm from the origin
Doppler ultrasonography is another tool that could be useful in diagnosis of vascular abnormalities, but may be timited to certain areas [19-21]. It may be very useful in detection of aortic regurgitation.
Fig. 7. Arch aortogram reveals multiple stenotic lesions of the brachiocephalic arteries with a relatively long segmental involvement (arrowheads). Note occlusion of the right subclavian artery It is weil known that Takayasu arteritis affects females more than male. However, the sex incidence has geographic variations. The committee report in 1975 revealed that 2,148 patients in Japan had Takayasu disease and that 89% were women [8]. On the other hand, the sex incidence is a lesser feature in reports from Africa and Northern European countries [23]. In our series a 1.88:1 female to male ratio is noted.
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
65
Fig. 8. Abdominal aortogram shows aneurysmal dilation of the proximal part. There is occlusion of all visceral branches. Stenosis of the renal arteries is seen with collateral circulation
In the present study, most cases show diffuse anatomical distribution of the lesions. However, the abdominal aorta, particularly its proximal and midsegments is more frequently involved than the thoracie aorta or distal aortic segment. In certain countries such as India, the descending thoracic aorta is the most commonly affected and the ascending aorta is free from disease [24]. Similarly, in China the ascending aorta is rarely involved [25]. In our series, dilatation of the ascending aorta being commonly observed is in agreement with that reported by others [4, 5]. While reports from Midand West African countries show a high incidence of distal aortic involvement [1, 26]. Of the branch arteries, the brachiocephalic arteries are found to be the most frequently involved in most geographic areas [4, 6, 27]. In our series, 79% of the cases were so involved. Obstructive lesions of the renal arteries in the present series, as well as reports from this part of the world appear to be higher than in other geographie areas [2-7]. In out experience, Takayasu arteritis is the most common cause of renal vascular hypertension in patients under 40 years of age. This is in agreement with a report from India [28]. Ample collateral circulation is well known in Takayasu arteritis. This is weil depicted in most cases of renal artery occlusion, as well as occlusion of the other arteries. Vascular lesion type is found to vary geographically. It has been stated that occlusive lesions are common in Japan, Europe, and the United States where aneurysms are rare. In India, Thailand, and Africa aneurysms are common [1, 3, 6]. In a clinicopathologic autopsy study
Fig. 9. Abdominal aortogram shows a complete occlusion of the right common iliac artery at its origin. Note the irregular contour of the aorta
of 8 cases report from Thailand, aneurysm was common in the ascending aorta [3]. Since these aneurysms were small and found at autopsy they would have undoubtedly escaped angiographic detection. Most of these aneurysms are saccular in nature. However, in out series with arteriographic studies, fusiform aneurysms were more common. When destruction of the aortic wall is extensive, there is disruption of the elastic fibres, the weakened aortic wall then balloons out, producing aneurysmal dilation [2, 3]. Such aneurysm may be fusiform or saccular. Diffuse dilatation of the aorta may due to pre- or post-stenosis as weil as due to destruction of the aortic wall. When the abdominal aorta is more than 2cm in diameter, a fusiform aneurysm may be diagnosed, otherwise the term dilatation is applied. On the contrary, saccular aneurysm, if seen on arteriographic studies, is not difficult to diagnose. It is evident from the present series that stenotic and occlusive lesions commonly
66 occur in branch arteries, the brachiocephalic, renal, visceral and iliac arteries, while aneurysm and stenosis affect the aorta with almost equal frequency. Dilatation of the branch vessels encountered in these cases mainly represents increased blood flow secondary to a collateral pathway. However, diseases involving their wall may play some role in producing the dilatation in some cases. In our series, renal artery stenosis occurring in combination with abdominal aortic aneurysm in the region were commonly encountered. Observation of the "funnel-shaped" configuration resulting from this combined occurrence was not rare. This configuration is characteristic of the Takayasu arteritis occurring in out geographic area [6]. The earliest detectable change at arteriographic studies in Takayasu arteritis has been stated to be localized narrowing or irregularity of the aortic wall [9]. A long narrowing was frequently found in out cases. Although it occurred infrequently in this study, the "flame-shaped" termination of a brachiocephalic obstruction may be characteristic of Takayasu arteritis [29]. The lesion occurs predominantly at the proximal part of the brachiocephalic arteries. It has been noted that pulmonary artery involvement in Takayasu arteritis is not u n c o m m o n [25]. In our series, neither pulmonary arteriography not puimonary scintigraphy was performed. These studies are very helpful in demonstrating pulmonary artery lesions. However, aortographic studies, dilatation of the bronchial arteries with prompt visualization of the pulmonary artery branches in out 2 cases, indirectly indicated the presence of a pulmonary stenotic lesion. We believe that the incidence of pulmonary involvement has been underestimated [4, 30]. Involvement of the coronary artery was seen in one case in out series following aortography. The true incidence of coronary artery involvement could not be estimated, since coronary arteriography was not usually performance in these patients. Most of our cases had advanced lesions as depicted by extensive arterial involvement. This is supported by the evidence of lumbar and intercostal arterial obstruction. Iliac and femoral artery occlusions are also higher than the previous reports [4, 5]. This may partly be due to no arteriographic studies of these arteries having been performed.
References 1. Joffe N (1965) Idiopathic panarteritis with aneurysm formation. Clin Radiol 10:251-255 2. Gotsman MS, Beck W, Schrire V (1967) Selective angiography in arteritis of aorta and its major branches. Radiology 88:232-248 3. Vinijchaikul K (1967) Primary arteritis of the aorta and its main branches (Takayasu arteriopathy): A clinicopathological autopsy of eight cases. Am J Med 43:15-27
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand 4. Deutsch V, Wexler L, Deutsch H (1974) Takayasu arteritis: An angiographic study with remarks on ethnic distribution in Israel. AJR 122:13-28 5. Lande A, Rossi P (1975) The value of total aortography in the diagnosis of Takayasu arteritis. Radiology 114: 287-297 6. Piyachon C (1977) Takayasu arteritis in Thailand. Aust Radiol 21:350-361 7. Hall S, Buchbinder R (1990) Takayasu arteritis. Rheum Dis Clin N Am 16(2):411-422 8. Numano F, Ohta N, Sasasuki T (1982) Symposium on clinical problems in aortic diseases. HLA and clinical manifestations in Takayasu disease. Jpn Circ J 46(4): 184-189 9. Lande A, Gross A (1972) Total aortography in the diagnosis of Takayasu arteritis. AJR 116:165-178 10. Matsunaga N, Hayashi K, Aikawa H (1987) Digital subtraction angiography in Takayasu arteritis. Acta Radiol 28:247-252 11. Sharma S, Aggarwal S, Talwar KK, Rajani M (1989) Intravenous digital subtraction angiography in nonspecific aorto-arteritis. Br J Radiol 62:117-120 12. Yamamoto S, Ogawa S, Kitano T, Shima K, Sakamoto T, Shibamiya K, Kondo T, Sotobata I (1987) Complete evaluation of the cardiovascular lesions in 24 patients with Takayasu aortitis using four-image, intravenous digital subtraction angiography. Am Heart J 114:14261431 13. Berkmen YM, Lande A (1975) Chest roentgenography as a window to the diagnosis of Takayasu arteritis. AJR 125:842-846 14. Hayashi K, Fukushima T, Matsunaga N, Zen-ichiro H (1986) Takayasu arteritis: Decrease in aortic wall thickening following steroid therapy, documented by CT. Br J Radiol 59:281-283 15. Peterson IM, Guthaner DF (1986) Aortic pseudoaneurysm complicating Takayasu disease: CT appearance. J Comput Assist Tomogr 10:676-678 16. Disler L, Hide G (1988) An unusual case of occlusive thromboaortopathy (Takayasu disease) - A case report. Angiology 39:401-404 17. Miller DL, Reining JW, Volkman DJ (1986) Vascular imaging with MRI: Inadequacy in Takayasu arteritis compared with angiography. AJR 146:949-954 18. Mayo J, Culham JA (1987) Magnetic resonance imaging in pediatric vascular disease. J Can Assoc Radiol 38(3): 165-169 19. Giles WB, Young AA, Howlin KJ, Cook CM, Trudinger BJ (1987) Doppler ultrasound features of stenosis of the aorta in a pregnancy complicated by Takayasu arteritis. Case report Br J Obstet Gynaecol 94:907-909 20. Fournier AM, Dickinson ZC, Kelly R (1988) Doppler ultrasonography as a guide to management in Takayasu arteritis. J Rheumatol 15:527-528 21. Reid AJ, Fincher RE, Nichols F r (1989) Case report: Takayasu arteritis in a middle-aged Caucasian woman: Clinical course correlated with duplex ultrasound and angiography. Am J Med Sci 298:324-327 22. Committee Report Clinical and Pathological studies of Takayasu Disease (1975) A report by the Ministry of Health and Welfare, Japan 23. Paloheimo JA (1967) Obstructive arteritis of Takayasu type: Clinical, roentgenological and laboratory studies on 36 patients. Acta,Med Scand [Suppl] 468:1-43 24. Kinare SG (1968) Etiopathological aspect of non-specific aortitis. In: Eliakim H, Neufeld HN (eds) Cardiology: Current topics and progress. Academic, New York, pp 322-325
C. Piyachon and N. Suwanwela: Takavasu arteritis in Thailand 25. Zheng DY, Lieu L, Fan D (1990) Clinical studies in 500 patients with aortoarteritis. Chin Med J 103(7):536-540 26. Repler WJ, Simson IW (1959) Occlusive disease of the abdominal aorta associated with panarteritis. AMA Arch Pathol 68:525-532 27. Park JH, Han MC, Kim SH, Oh BH, Park YB, Seo JD (1989) Takayasu arteritis: Angiographic findings and results of angioplasty. AJR 153:1069-1074 28. Sharma BK, Sagar S, Chugh KS, Säkhuga V, Rajachan-
67 dran A, Ma'lik N (1985) Spectrum of renovascular hypertension in the young in north India: A hospital based study on occurrence and clinical features. Angiology 36:370-378 29. Grollman JH Jr, Hanafee W (1964) The roentgen diagnosis of Takayasu arteritis. Radiology 83:387-395 30. Kozuka T, Nosaki T, Sato K, Iharak (1968) Aortitis syndrome with special reference to pulmonary vascular changes. Acta Radiol (Diag) 7:25-32
Heart
andl[ T
1
vessels
© Springer-Verlag1992
Takayasu arteritis in Thailand Chaliow Piyachon 1 and Nitaya Suwanwela 2 1Department of Radiology, Faculty of Medicine, Chiangmai University, Chiangmai, Thailand 2 Department of Radiology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
S u m m a r y . Takayasu arteritis is a disease of worldwide distribution. Geographic difference in sex incidence, anatomical distribution, and the type of lesion is observed. Hypertension is very c o m m o n in the present series, as well as in combination with absent or deficit of peripheral pulses. These symptoms correlate well with arteriographic findings of brachiocephalic and renal artery obstructive lesion. While aneurysm and stenotic lesions have a predilection in the abdominal aorta, stenotic lesion of the thoracic aorta occurs more commonly than aneurysm. However, aneurysm of the aorta as well as of the brachiocephalic arteries is seen more frequently than in the reports, of others. The presence of "funnel-shape" resulting from renal artery obstructive lesion and dilatation or aneurysm of contiguous aorta was characteristic of Takayasu arteritis in our series. The material presented in this report reflects not only geographic variation but also the severe form of this disease. Total aortography, coronary arteriography and pulmonary arteriography, are of value not only for the diagnosis of Takayasu arteritis but also for demonstration of anatomical distribution, severity and type of lesion.
Key words: Takayasu disease - Non-specific aortoarteritis- Occlusive t h r o m b o a o r t o p a t h y - Aortography - Pulseless disease
Introduction Takayasu arteritis (TA) is a non-specific inflammatory disease of the arteries, affecting the aorta and its main branches as well as the pulmonary arteries. It is now Address correspondence to: N. Suwanwela
known to be distributed worldwide. The inciclence of the disease in Thailand has not been estimated but it is considered to be uncommon. Previous reports from Thailand, as well as from those in the literature represent rather severe forms of this disease. Thus, it is apparent that most cases of mild or asymptomatic lesions of Takayasu arteritis have escaped clinical identification. To this regard, radiographic and pathologic findings reported in the literature were mainly that of the severe forms. In Thai patients, it was noted that aneurysmal changes of the aorta as well as its branches occurred much more commonly than such findings in the reports from other countries. The variations in anatomical involvement and character of arterial changes have been observed in relation to certain geographic areas and ethnic origin of patients [1-6]. It is our intention to review arteriographic patterns of this disease in Thai patients presenting geographic and racial variation.
Materials and methods Material histories in this study were gathered in 2 periods, 8 years apart at Chulalongkorn Hospital in Bangkok. The first study was made during a 6-year period from 1971-1976 [6]. This study identified 20 cases of Takayasu arteritis, 15 were females and 5 males, a ratio of 3 to 1. The ages ranged from 9 to 35 years [6]. The second study was made during 1985-1990, another 6-year period. Twenty-six cases of Takayasu arteritis were diagnosed. There were 15 females and 11 males, a ratio of 1.36 to 1. The age ranged from 7 to 40 years. The total number of cases in these 2 periods were 46, with a female to male ratio of 1.88 to 1. All the patients were Thai or Thai-Chinese origin. None of them were from the same family. Eight cases had postmortem confirmation of the diagnosis. Otherwise the diagnosis of Takayasu arteritis was mainly based on the arteriographic findings, supported by the clinical and laboratory results. The clinical and laboratory findings in general corresponded to those discribed in the literature [1-7]. The most common presentation was hypertension. This was found in 80% of the cases, while
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
61
Table 1. Clinical findings in Takayasu arteritis (46 cases)
Findings
Cases (n)
Hypertension Absent or weakness of pulses Congestive heart failure Cerebrovascular disease Others: Aortic insufficiency Pericarditis Joint pain Abdominal mass
37 23 13 11 7 3 1 2 1
Table 2. Summary of regional involvement in Takayasu arteritis (38 cases with total angiography) Vessels
Ascending aorta Aortic arch Descending thoracic aorta Abdominal aorta Brachiocephalic artery Innominate artery Subclavian Rt. artery Lt. Common carotid Rt. artery Lt. Vertebral artery Rt. Lt. Visceral branches Celiac artery Superior mesenteric artery Inferior mesenteric artery Renalartery Rt. Lt. Iliac artery Rt. Lt. Total
Findings A
D
S
1 4 13
12 10 3 9
1 1
7 12
1
5 4 3 7 6 1 1
4 12 5 4 4 5
4 6 1 2 4 3
2 3
1
2
4
2
1
4
11
12 10 3 2
2 8 8 3 4
88
61
5 5 2
2 3 35
6 8 4
81
O
Total number I of lesions 2 14 23 1
13 14 28 58 6 19 29 15 12 9 9
16 1 1
49
8 29 25 9 O 314
A, Aneurysm; D, dilatation; S, stenosis; O, occlusion; I, irregular contour; Rt., right; Lt., left abseht or weakness of pulses were presented in 50% of the cases. Congestive heart failure was found in approximately 35%. Aortic insufficiency was present in 5 out of 46 cases, approximately 11%. Other clinical features including vertigo, syncope, visual disturbances, and joint symptoms were also observed (Table 1). One patient also had immune complex membranous proliferative glomerulonephritis diagnosed by renal biopsy. For the treatment, corticosteroids and immunosuppressive therapy were mainly used. Surgical interventions were done in 11 cases, including by-pass procedures and graft in 5, autorenal transplantation in 3, nephrectomy in 2, and renal artery endarterectomy in 1. Percutaneous transluminal angioplasties were performed in 3 cases with improvement of the stenosis. Total aortography was performed in all cases in the earlier study, while in the recent study, total aortography was done in 18 out of 26 cases. Neither pulmonary arteriography nor coronary arteriography was performed.
Fig. 1. Thoracic aortogram. Oblique view demonstrates dilatation of ascending thoracic aorta with no evidence of aortic insufficiency
Results
Arteriographic findings The arteriographic abnormalities in Takayasu arteritis include various forms of irregular contour, stenosis, occlusion, dilatation, aneurysm, or a combination of these changes. In our patients, dilatation and aneurysmal formation in the aorta were more common than stenotic lesions, which is contrary to the more common stenosis or occlusion of the branch arteries. In addition, marked irregularity of the contour of the involved vessels commonly occurred. Arteriographic findings and frequency of the lesions are summarized in Table 2. A s c e n d i n g a o r t a a n d aortic arch Dilatation of both ascending aorta and aortic arch was encountered in 16 cases (Fig. 1) and of the ascending aorta in 5 cases. Descending thoracic aorta Eighteen patients developed lesion of the descending thoracic aorta: diffuse dilatation in 3, a Iong stenotic lesion in 7 (Fig. 2) and both types of lesion in 2 patients. It was noted that a prestenotic dilatation of the ascending aorta accompanied the stenotic lesion in few cases. During aortography, visualization of dilated bronchial arteries were seen in 2 cases with prompt opacification of the pulmonary arterial branches, indirectly indicative of pulmonary stenotic lesion. Abdominal aorta The abdominal aorta was involved in 76% of the cases at the proximal and mid segments; aneurysmal lesions
62
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand in nature. The carotid arterial lesion occurred less commonly. The lesion was obstructive in nature. All obstructive lesions of the brachiocephalic arteries demonstrated good collateral circulation. Their dilatation was commonly seen, probably secondary in order to increase blood flow, as well as a pre-or poststenotic dilatation. Visceral b r a n c h e s o f a b d o m i n a l a o r t a Occlusion or stenosis of the celiac, superior mesenteric or inferior mesenteric arteries at their origin was not common. However ample collatera| circulation was observed in all cases of visceral obstructive lesions (Figs. 4, 8). R e n a l arteries Renal artery occlusion or stenosis was present in 28 patients (74%), 17 of them bilaterally. The lesion involved a short segment of the proximal part of the renal artery in all cases, usually with abrupt tapering, except for a few case which showed elongated narrowing of the longer segment of the main artery. Poststenotic ditatation and aneurysm were demonstrated in 11 cases (Fig. 6). In 6 cases, aortic aneurysm was continuous with prestenotic di|atation of the renal arteries and manifested themselves by a characteristic "funnel-shape" or triangular configuration, as previously reported [6]. Ample collateral circulation was observed in almost all cases of complete or almost complete obstructive lesions of renal arteries Most of the 37 patients with hypertension demonstrated obstructive lesion of renal arteries, with a few cases of renal artery stenosis being normotensive.
Fig. 2. Thoracic aortogram shows an area of narrowing involving a short segment of mid-part of the descending thoracic aorta (arrowhead). The rest of the thoracic aorta appears normal
in 13 cases with 1 case of saccular aneurysm (Figs. 3 - 6 , 8) and stenotic lesion in 12 cases (Fig. 4). Complete occlusion of the abdomina| aorta with extensive collateral circulation was found in one case (Fig. 5). B r a c h i o c e p h a l i c arteries One or more branches of the brachiocephalic arteries were involved in 30 cases (79%) (Fig. 7). The subclavian arteries were the most commonly involved and more than half of the cases were bilateral. The |esions were mainly obstructive, but fusiform aneurysm and saccular aneurysm occurred in approximately one third of the cases. Most of the subclavian obstructive lesions developed at or just distal to the origin of the vertebral artery. A long segmental narrowing of the subclavian artery extension into the axil|ary artery was seen in a few cases. Vertebral arteries were the next commonly involved. All vertebral arterial lesions were the obstructive type, either stenosis or occlusive
Iliac and f e m o r a l arteries Because arteriographic studies of the femoral artery were not included for most of the cases, the true incidence of femoral artery involvement was not assessable. Internal iliac involvement was more common than the common iliac or external iliac arteries. In severe cases, multiple lesion sites were seen. Obstructive lesions occurred in 11 cases, (Fig. 9) while fusiform and saccular aneurysm were seen in 3 cases; each involving the common iliac and femoral arteries.
Discussion A diagnosis of Takayasu arteritis may be suspected on clinical grounds alone, particularly with presence of pulse weakness or deficits and especially in young female patients. However, a more definitive diagnosis is established on the basis of angiographic findings. The study should include the entire aorta and proximal branches [4, 5]. Intravenous digital subtraction angiography is very helpful in depicting the changes and is the preferred investigation in view of its safety. How-
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
63
Fig. 3. A saccular aneurysm is seen in this abdominal aortogram, located just below the origin of the celiac artery. The right renal artery is occluded. Note a stenotic lesion of the proximal part of the left renal artery (arrowhead)
Fig. 4. Abdominal aortogram reveals a long segment of stenotic lesion at its proximal and distal parts (arrowheads) with occlusion of the celiac and superior mesenteric arteries. Note dilated intercostal and lumbar arteries as well as many small vessels originating from the aorta serving collateral pathways. The proximal part of the right renal artery appears stenosed
ever, its use is limited in patients with congestive cardiac failure and the uncooperative patient. Mild involvement of the descending aorta in the region of the diaphragm could not be assessed. Intra-arterial digital subtraction angiography should be the better method for specific areas and details. Computed tomography is another method used for diagnosis and follow-up studies of Takayasu arteritis following steroid therapy [13, 14]. Aortic wall thickening may be demonstrated by CT and the thickening may be partly or largely due to periaortic infiltration. However, the measurement of the thickness of the wall is not always possible because of the limited spatial resolution of CT and the marked variations in caliber of the aorta during the cardiac cycle. Aneurysm
and related hematoma indicating prior aortic rupture or vascular rupture are also well demonstrated on CT scan [15, 16]. Presently, alternative imaging, such as magnetic resonance imaging (MRI) is not yet widely used for one reason, its high cost. Miller et al. [17] have evaluated the ability of MRI to detect vascular abnormalities in 10 patients with Takayasu arteritis, comparing it to angiography in 1985. Adequate MR visualization was consistently achieved only in the aorta, the common iliac arteries, and the inmominate artery. MRI also provided superior information about pulmonary artery patency [18]. With current equipment and technology, MRI may be even more useful as a screening examination, especially the technique of magnetic resonance angiography.
64
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
Fig. 5. a Abdominal aortogram shows a relatively long segment of an aneurysmal dilatation of the proximal abdominal aorta. Complete occlusion of the aorta below the origin of the renal artery is evident. Note dilatation of the gastroduodenal and meandering mesenteric arteries, b Late arterial phase demonstrates ample collateral circulation with retrograde filling of the distal part of the aorta to the level of occlusion (0). There is narrowing of the distal aortic segment just above the aortic bifurcation
Fig. 6. Abdominal aortogram demonstrates a large fusiform aneurysm of its proximal part. There is a complete occlusion of left renal artery near the origin. A stenotic lesion of the right renal artery is seen approximately 0.5cm from the origin
Doppler ultrasonography is another tool that could be useful in diagnosis of vascular abnormalities, but may be timited to certain areas [19-21]. It may be very useful in detection of aortic regurgitation.
Fig. 7. Arch aortogram reveals multiple stenotic lesions of the brachiocephalic arteries with a relatively long segmental involvement (arrowheads). Note occlusion of the right subclavian artery It is weil known that Takayasu arteritis affects females more than male. However, the sex incidence has geographic variations. The committee report in 1975 revealed that 2,148 patients in Japan had Takayasu disease and that 89% were women [8]. On the other hand, the sex incidence is a lesser feature in reports from Africa and Northern European countries [23]. In our series a 1.88:1 female to male ratio is noted.
C. Piyachon and N. Suwanwela: Takayasu arteritis in Thailand
65
Fig. 8. Abdominal aortogram shows aneurysmal dilation of the proximal part. There is occlusion of all visceral branches. Stenosis of the renal arteries is seen with collateral circulation
In the present study, most cases show diffuse anatomical distribution of the lesions. However, the abdominal aorta, particularly its proximal and midsegments is more frequently involved than the thoracie aorta or distal aortic segment. In certain countries such as India, the descending thoracic aorta is the most commonly affected and the ascending aorta is free from disease [24]. Similarly, in China the ascending aorta is rarely involved [25]. In our series, dilatation of the ascending aorta being commonly observed is in agreement with that reported by others [4, 5]. While reports from Midand West African countries show a high incidence of distal aortic involvement [1, 26]. Of the branch arteries, the brachiocephalic arteries are found to be the most frequently involved in most geographic areas [4, 6, 27]. In our series, 79% of the cases were so involved. Obstructive lesions of the renal arteries in the present series, as well as reports from this part of the world appear to be higher than in other geographie areas [2-7]. In out experience, Takayasu arteritis is the most common cause of renal vascular hypertension in patients under 40 years of age. This is in agreement with a report from India [28]. Ample collateral circulation is well known in Takayasu arteritis. This is weil depicted in most cases of renal artery occlusion, as well as occlusion of the other arteries. Vascular lesion type is found to vary geographically. It has been stated that occlusive lesions are common in Japan, Europe, and the United States where aneurysms are rare. In India, Thailand, and Africa aneurysms are common [1, 3, 6]. In a clinicopathologic autopsy study
Fig. 9. Abdominal aortogram shows a complete occlusion of the right common iliac artery at its origin. Note the irregular contour of the aorta
of 8 cases report from Thailand, aneurysm was common in the ascending aorta [3]. Since these aneurysms were small and found at autopsy they would have undoubtedly escaped angiographic detection. Most of these aneurysms are saccular in nature. However, in out series with arteriographic studies, fusiform aneurysms were more common. When destruction of the aortic wall is extensive, there is disruption of the elastic fibres, the weakened aortic wall then balloons out, producing aneurysmal dilation [2, 3]. Such aneurysm may be fusiform or saccular. Diffuse dilatation of the aorta may due to pre- or post-stenosis as weil as due to destruction of the aortic wall. When the abdominal aorta is more than 2cm in diameter, a fusiform aneurysm may be diagnosed, otherwise the term dilatation is applied. On the contrary, saccular aneurysm, if seen on arteriographic studies, is not difficult to diagnose. It is evident from the present series that stenotic and occlusive lesions commonly
66 occur in branch arteries, the brachiocephalic, renal, visceral and iliac arteries, while aneurysm and stenosis affect the aorta with almost equal frequency. Dilatation of the branch vessels encountered in these cases mainly represents increased blood flow secondary to a collateral pathway. However, diseases involving their wall may play some role in producing the dilatation in some cases. In our series, renal artery stenosis occurring in combination with abdominal aortic aneurysm in the region were commonly encountered. Observation of the "funnel-shaped" configuration resulting from this combined occurrence was not rare. This configuration is characteristic of the Takayasu arteritis occurring in out geographic area [6]. The earliest detectable change at arteriographic studies in Takayasu arteritis has been stated to be localized narrowing or irregularity of the aortic wall [9]. A long narrowing was frequently found in out cases. Although it occurred infrequently in this study, the "flame-shaped" termination of a brachiocephalic obstruction may be characteristic of Takayasu arteritis [29]. The lesion occurs predominantly at the proximal part of the brachiocephalic arteries. It has been noted that pulmonary artery involvement in Takayasu arteritis is not u n c o m m o n [25]. In our series, neither pulmonary arteriography not puimonary scintigraphy was performed. These studies are very helpful in demonstrating pulmonary artery lesions. However, aortographic studies, dilatation of the bronchial arteries with prompt visualization of the pulmonary artery branches in out 2 cases, indirectly indicated the presence of a pulmonary stenotic lesion. We believe that the incidence of pulmonary involvement has been underestimated [4, 30]. Involvement of the coronary artery was seen in one case in out series following aortography. The true incidence of coronary artery involvement could not be estimated, since coronary arteriography was not usually performance in these patients. Most of our cases had advanced lesions as depicted by extensive arterial involvement. This is supported by the evidence of lumbar and intercostal arterial obstruction. Iliac and femoral artery occlusions are also higher than the previous reports [4, 5]. This may partly be due to no arteriographic studies of these arteries having been performed.
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