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(Circulation. 2003;108:1474.)
© 2003 American Heart Association, Inc.

Clinical Investigation and Reports

Long-Term Survival After Surgical Treatment of Patients With Takayasu’s Arteritis

Tetsuro Miyata, MD; Osamu Sato, MD; Hiroyuki Koyama, MD; Hiroshi Shigematsu, MD; Yusuke Tada, MD

From the Division of Vascular Surgery, Department of Surgery, Graduate School of Medicine, The University of Tokyo, Japan. Dr Sato is presently at the Department of Surgery, Saitama Medical Center, Japan. Dr Tada is presently at the Second Department of Surgery, Yamanashi Medical University, Japan.

Correspondence to Dr T. Miyata, Division of Vascular Surgery, Department of Surgery, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. E-mail miyata-2su{at}h.u-tokyo.ac.jp

Received February 6, 2003; de novo received April 10, 2003; revision received July 11, 2003; accepted July 11, 2003.

	Abstract

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Background— Surgical interventions have been performed to ameliorate the complications of Takayasu’s arteritis. However, the efficacy of surgery to increase long-term survival has not been established.

Methods and Results— A retrospective review was performed on the survival of 106 consecutive patients with Takayasu’s arteritis who underwent surgical treatment during the past 40 years. Their ages ranged from 5 to 69 years (mean±SEM, 31.7±1.3 years). Survival was compared with the reported results of medically treated patients according to Ishikawa’s prognostic classification. There were 12 hospital deaths, and the remaining 94 patients were followed up from 8 months to 41.8 years (mean, 19.8 years). A serious long-term complication was anastomotic aneurysm, with a cumulative incidence at 20 years of 13.8%. Thirty-one late deaths were observed, and the major cause was congestive heart failure. The overall cumulative survival rate at 20 years was 73.5%. The prognostic classification by Ishikawa had little influence on the survival of surgically treated patients. For stage 3 patients, surgery seemed to increase survival; however, surgery-related complications conversely decreased the survival of stage 1 patients.

Conclusions— Surgery seems to increase the long-term survival of patients with stage 3 Takayasu’s arteritis, whereas conservative treatment is recommended for those with stage 1 or 2 disease. An anastomotic aneurysm may occur at any time after surgery, and regular follow-up using imaging modalities such as multi-detector CT, MRI, or ultrasonography at least once every several years for the rest of the patient’s life is mandatory for the early detection of anastomotic aneurysm.

Key Words: arteries • surgery • survival • peripheral vascular disease

	Introduction

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Takayasu’s arteritis is a chronic disease characterized by nonspecific inflammation of the aorta and its branches. This inflammation results in cardiac involvement, with occlusive or aneurysmal changes of the affected arteries producing symptoms of cerebral hypoperfusion, secondary hypertension, and aneurysm. Surgical interventions have been performed to ameliorate these complications that would adversely affect the life expectancy of patients.^1–5 However, the efficacy of surgical management has not yet been established, because the prevalence of this disease is low and the course and prognosis differ widely depending on the affected artery. In addition, long-term follow-up over 20 years is mandatory to reach a conclusion on whether surgical therapy has an impact on the natural history of this inflammatory arteriopathy.

Several authors have tried to document predictive factors for the outcome of the disease after medical treatment.^6–10 Among them, the grouping by Ishikawa revealed a good association with the life expectancy of patients and was adopted by others.⁹ Our retrospective study elucidated the role of surgery in patients with Takayasu’s arteritis by reviewing the long-term course of 106 consecutive patients treated surgically. We staged our patients according to Ishikawa’s criteria and compared their survival with the reported results of medically treated patients to better select patients for surgery.

	Methods

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Patients’ Background
Between January 1955 and March 1995, 106 patients with Takayasu’s arteritis underwent surgical treatment at the Second Department of Surgery, The University of Tokyo. Most patients were treated in the 1960s, with several cases a year encountered thereafter (Figure 1). They consisted of 87 women and 19 men whose age at operation ranged from 5 to 69 years with a mean±SEM of 31.7±1.3 years. The diagnosis of Takayasu’s arteritis was confirmed by the characteristic clinical and radiological findings.¹¹ Ninety-four patients were diagnosed at or before 40 years of age and 12 patients over 40 years.

View larger version (27K): [in this window] [in a new window]   Figure 1. Number of patients with Takayasu’s arteritis who underwent surgical treatment. The distribution of the prognostic classification by Ishikawa and Maetani10 was not significantly different between the early and late series of patients.

This study covers a long time frame, during which different therapeutic approaches and modalities existed. For the analysis, we classified these patients into the following 2 groups according to the time when the initial operation was performed: 78 patients operated on before 1980 (early series) and 28 operated on after 1981 (late series). The distribution of the prognostic classification by Ishikawa and Maetani¹⁰ was not significantly different between the early and late series of patients (Figure 1).

Treatment and Follow-Up
Overall, 155 vascular procedures were performed for the treatment of primary lesions of Takayasu’s arteritis. These procedures, together with the indications for surgery, are listed in Table 1.

View this table: [in this window] [in a new window]   TABLE 1. Indications for Surgery and Surgical Procedures Performed for the Treatment of Takayasu’s Arteritis

There were 12 hospital deaths, which all occurred in the early series. Causes of hospital death were acute renal failure in 4 cases, postoperative bleeding in 2, cerebrovascular accident in 2, multiple organ failure attributable to ruptured aneurysm in 2, congestive heart failure in 1, and other cause in 1. The numbers of deaths after surgical treatment, classified by the prognostic classification,¹⁰ are listed in Table 2. Consequently, 94 patients were followed up from 8 months to 41.8 years with a mean±SEM of 19.8±1.2 years, and their follow-up details provide the data for this study. The patients were examined after operation, 43 at our institution and 51 at other clinics according to where they lived. Follow-up data were obtained regularly. As a result, 89 patients were followed up either until death or until October 30, 2001. Five patients were lost to follow-up from 1.3 to 17 years after surgery (at 1.3, 6.3, 9.8, 15, and 17 years). The completeness of follow-up calculated according to the life table method was 95% at 10 years and 94% at both 20 and 30 years. Seventy-three patients (78%) were followed up over 10 years, 45 patients (48%) over 20 years, 22 patients (23%) over 30 years, and 3 patients (3%) over 40 years.

View this table: [in this window] [in a new window]   TABLE 2. Number of Deaths After Surgical Treatment of Takayasu’s Arteritis

Prognostic Classification
To clarify the factors that might influence the long-term survival of patients who undergo surgical treatment, the following 14 factors were analyzed in these patients: type of disease, sex, age at operation, period between the onset of disease and diagnosis, erythrocyte sedimentation rate (ESR), presence of major complication, retinal changes, blood pressure, severity of aortic regurgitation, presence of cardiac lesion, presence of aneurysmal lesion, clinical course, prognostic classification, and presence of anastomotic aneurysm. These factors were divided into 2 categories for analysis, except type of disease and prognostic classification (Table 3).

View this table: [in this window] [in a new window]   TABLE 3. Comparison of Survival Rates of Patients With Takayasu’s Arteritis by Clinical Variables

The patients were classified into 4 groups according to the type of surgery and the severity of disease using Ueno’s criteria.¹² Type I patients had cerebral hypoperfusion attributable to aortic arch lesions; type II patients had systemic hypertension attributable to aortic or renal vessel involvement; type III patients had both cerebral hypoperfusion and systemic hypertension attributable to combined extensive lesions of the aortic arch and thoracoabdominal aorta; and type IV patients had aneurysms. ESR was evaluated before corticosteroid therapy. Retinal findings was divided into 2 categories according to Uyama-Asayama’s classification,¹³ which represents the severity of circulatory disturbance of the brain. Stage 0 indicates normal retinal findings; stage 1, vascular dilatation; stage 2, microaneurysm formation; stage 3, arteriovenous communication; and stage 4, complicated retinal vascular lesions. Patients with stage 2, 3, or 4 retinal findings were classified into the group with severe retinal changes. Severe hypertension was defined as a brachial pressure of 200 mm Hg systolic or 110 mm Hg diastolic or, alternatively, a popliteal pressure of 230 mm Hg systolic or 110 mm Hg diastolic. Aortic regurgitation of grade 3 or 4 according to the aortographic classification was considered to be a severe lesion. Cardiac lesions consisted of aortic regurgitation, congestive heart failure, and ischemic heart disease. The clinical course was classified according to Ishikawa’s criteria,⁸ progressive course (crescendo symptom pattern C or D), and nonprogressive course (pattern A or B). In this classification, the presenting symptoms evaluated included easy fatigability of the limbs, dizziness, blurred vision, arthralgia, neck pain, general fatigue, dyspnea, syncopal attacks, headache, and fever.

These patients were divided into 3 prognostic groups according to the criteria by Ishikawa et al¹⁰ based on whether they had major complications, a progressive course, or low ESR. The criteria for major complications were the presence of at least 1 of the following conditions attributed to Takayasu’s arteritis¹⁰: microaneurysm formation (stage 2 retinopathy according to Uyama-Asayama’s classification), the presence of severe hypertension as described previously, grade 3 or 4 aortic regurgitation, and angiographic demonstration of an aortic or arterial aneurysm with a diameter more than twice normal. Patients with 2 or more of these complications were also classified into the major complication group, even if both of the complications were less severe than defined above.

Statistical Analysis
Comparison of the distribution of the prognostic classification between the early and late series of patients was performed using ² test. The Kaplan-Meier method was applied to evaluate survival after surgery and the incidence of anastomotic aneurysm. Comparison of the cumulative incidence curves between paired groups was carried out by univariate analysis using the log-rank test, and P<0.05 was considered to be significant. Multivariate Cox regression analysis was performed on the factors found to be significant or nearly significant by univariate analysis, using StatView version 5.0 (SAS Institute Inc) to identify independent influential factors that could not be replaced by other factors that influenced survival after operation.

	Results

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During the follow-up period, we encountered 18 early and 7 late graft failures, including occlusion of 3 carotid, 5 subclavian, 16 renal, and 1 mesenteric arterial bypass. Patency of carotid, subclavian, and aorto-aortic reconstruction was determined by physical examination with blood pressure measurement. The patency of renal and mesenteric arterial reconstruction was determined by angiography and for recent series by computed tomography. The overall primary 10-year cumulative patency rate of carotid, subclavian, aorto-aortic, renal, and mesenteric arterial reconstructions was 88%, 64%, 100%, 68%, and 67%, respectively.

In this series, 278 anastomoses were made in the surgical procedures. Thirty-one anastomotic aneurysms, which were detected incidentally except those in the recent series, were encountered in 19 patients after operation. Details of anastomotic aneurysms were reported previously.¹⁴ The cumulative incidence of anastomotic aneurysm as a whole at 20 years was 13.8% (Figure 2). Twenty-six of these anastomotic aneurysms occurred in 16 patients, including 6 cases of rupture that were treated surgically (ascending aorta, 2; descending aorta, 11; abdominal aorta, 6; carotid artery, 3; subclavian artery, 1; abdominal visceral artery, 2; and iliofemoral artery, 1). The procedures consisted of resection and grafting in 13 aneurysms, patch closure in 8, stent graft insertion in 4, and direct closure in 1. There were 3 operative deaths, including 2 cases of rupture. Three patients with 5 anastomotic aneurysms were not treated surgically; 2 died of rupture before diagnosis, and 1 was not treated because of difficulty in surgically repairing 3 anastomotic aneurysms at ascending aorta, subclavian, and carotid artery in 1964 because of their location.

View larger version (11K): [in this window] [in a new window]   Figure 2. Cumulative incidence of anastomotic aneurysms in surgically managed Takayasu’s arteritis. A total of 31 anastomotic aneurysms were encountered in 19 patients. The cumulative incidence of anastomotic aneurysms at 20 years was 13.8%.

Thirty-one late deaths were observed in 94 patients. The major cause of late death was congestive heart failure in 14 patients, followed by anastomotic aneurysm in 5 (rupture in 4, including 2 operative deaths at emergency operation and operative death in 1 at scheduled reoperation). Other causes of death consisted of rupture of a true aneurysm in 2 patients, intracranial hemorrhage in 3, cerebral infarction in 2, cancer in 1, and miscellaneous in 4 (retroperitoneal hemorrhage of unknown cause, massive hematemesis of unknown cause, anaphylactic shock, and suicide). Among the 14 patients who died of congestive heart failure (5 patients died in the 1970s, 6 in the 1980s, and 3 in the early 1990s), 5 had ischemic heart disease and 3 had aortic valve disease. The details of heart failure in the remaining 6 patients were not known. They all were treated conservatively, probably because cardiac surgery for Takayasu’s arteritis was not well established at the time. The causes of death classified according to the prognostic stage are listed in Table 2. In 57% of the patients with stage 1 disease, the causes of late death were related to surgical treatment. The overall survival rate of the 94 patients who survived the operation was 73.5% at 20 years after operation (Figure 3). The survival rate of the patients in the early series was not different from that in the late series (P=0.96).

View larger version (10K): [in this window] [in a new window]   Figure 3. Cumulative survival rate after surgical treatment in patients with Takayasu’s arteritis. A total of 31 late deaths were observed. Overall survival rate at 20 years after operation was 73.5%.

When the cumulative survival rates were compared with regard to the 14 factors analyzed, there were statistically significant differences in the type of disease (P=0.0142), age at operation (P=0.0052), and presence of an aneurysmal lesion (P=0.0106) in the early series. In the late series, only the type of disease influenced the long-term survival (P<0.0001). The prognostic classification by Ishikawa had little influence on the survival of surgically treated patients with Takayasu’s arteritis in both groups (Table 3). Cox regression analysis performed on the 3 factors that had a probability value of less than 0.1 by univariate analysis in the early series (ie, type of disease, age at operation, and presence of aneurysmal lesion) showed that only the age at operation was significantly associated with the survival after surgical treatment (P=0.0243). The group of patients who were older than 35 years at operation had a 2.74-fold higher risk of death than those aged 35 years or younger.

	Discussion

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Careful interpretation is essential in analyzing the results of surgical treatment performed several decades ago together with recent series. The mortality and morbidity of surgery have decreased dramatically due to the development of various paramedical technologies, such as hemodialysis for patients with acute renal failure and mechanical ventilation for those with acute respiratory failure. In addition, the development of preoperative evaluation and management of surgical risk of patients and learning and understanding the pathophysiology of arterial reconstruction in patients with Takayasu’s arteritis have also contributed markedly to decreasing the complications after surgery. Thus, we divided our series into 2 groups according to the time when the operation was performed to analyze the factors influencing survival. Although all of the operative deaths occurred in the early series, the survival after discharge did not differ significantly between the groups. So, to evaluate the effect of surgical treatment on the long-term survival, we analyzed the mortality of patients who survived the operation.

Only a few previous English-language articles have dealt with the natural course of Takayasu’s arteritis. Among them, Ishikawa performed prognostic analysis with the largest number of patients and the longest follow-up period.^6–8,10 He proposed a prognostic classification based on 2 clinical factors, the presence of complications and the clinical course. In a group of patients who had major complications together with a progressive course (stage 3), the 15-year survival rate was only 43%. He suggested that patients with stage 3 Takayasu’s arteritis might require surgical treatment. Ishikawa’s prognostic classification was supported by Subramanyan et al.⁹ In their analysis of 88 patients with Takayasu’s arteritis, they also found a poor prognosis in group 2B and group 3 patients of Ishikawa’s classification, together with severe hypertension, cardiac involvement, and severe functional disability. Subramanyan et al⁹ also recommended intervention including surgery for these patients with a poor prognosis.

In our series, the distribution of the prognostic classification was not significantly different between the early and late series of patients, and patients with stage 3 disease attained better survival in both series than in Ishikawa’s series. This may be explained by the effect of surgical treatment. On the contrary, the survival of the stage 1 group in our series was inferior to that in Ishikawa’s report, irrespective of the time when the operations were performed. So we additionally analyzed the cause of death of the patients with each stage and found that 57% of the causes of death in stage 1 patients were surgery-related.

In our series, 31 anastomotic aneurysms were encountered in 19 patients. Except in the recent series, most of the anastomotic aneurysms were detected incidentally. However, because the presence of an anastomotic aneurysm inevitably leads to a fatal condition, we consider that the incidence of anastomotic aneurysm in our series reflects the true occurrence. The details of these lesions, except several recent cases, were reported previously.¹⁴ An anastomotic aneurysm can occur at any time after operation, especially in patients who undergo operation for an aneurysmal lesion.¹⁴ However, we could not simply conclude that anastomotic aneurysms were a complication of aneurysmal lesions. In fact, although anastomotic aneurysm was a very important cause of morbidity in Ishikawa’s stage 1 group, they did not include patients with an aneurysmal lesion by definition. In stage 1 patients, the risk of surgery-related complications seems to surpass the benefit of surgery. We consider that the complication of anastomotic aneurysm is unavoidable as long as we implant a graft. Regular follow-up using imaging modalities such as multi-detector CT, MRI, or ultrasonography at least once every several years for the rest of the patient’s life is mandatory for the early detection of anastomotic aneurysm.

Congestive heart failure or arrhythmia induced by a cardiac lesion is the main cause of death in patients with Takayasu’s arteritis in Japan.¹⁵ In our series, in which none of the patients underwent cardiac surgery because their cardiac symptoms were not severe at the time of operation, the major long-term cause of death was also congestive heart failure. In Takayasu’s arteritis, aortic regurgitation is reported to be present in 13% to 44% of cases^16–18 and coronary arterial lesions in 10%.^19–21 These lesions should be managed properly for the long-term survival of patients. Recently, cardiac operations are performed frequently for patients with Takayasu’s arteritis. These include aortic valve replacement, sometimes together with repair of an ascending aortic aneurysm,^22–25 and coronary arterial reconstruction.²⁶ However, on the contrary, several complications such as valvular detachment, paravalvular leakage, and pseudoaneurysm formation are not infrequently reported,²² and we should wait for the long-term results to determine the indication for cardiac surgery.

In our statistical analysis, age at operation was an independent predictive factor for survival of patients with Takayasu’s arteritis who underwent surgical treatment before 1980. Instead, the type of disease was a predictive factor after 1981. Although the precise explanation for these results was not revealed in this analysis, we should bear in mind this result before recommending surgery to patients.

Conclusions
Surgical treatment for patients with Takayasu’s arteritis might increase the survival of those with stage 3 disease; however, surgical treatment produced surgery-related complications and conversely decreased the survival of patients with stage 1 disease. For patients with stage 1 or 2 Takayasu’s arteritis, conservative treatment is recommended, whereas for those with stage 3, surgical treatment seems to increase the long-term survival. An anastomotic aneurysm may occur at any time after surgery, and regular follow-up using imaging modalities such as multi-detector CT, MRI, or ultrasonography at least once every several years for the rest of the patient’s life is mandatory for the early detection of anastomotic aneurysm.

	References

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This Article Abstract Full Text (PDF) All Versions of this Article: 108/12/1474    most recent 01.CIR.0000089089.42153.5Ev1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Miyata, T. Articles by Tada, Y. Search for Related Content PubMed PubMed Citation Articles by Miyata, T. Articles by Tada, Y. Related Collections CV surgery: aortic and vascular disease