February 2011, VOLUME 196

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February 2011, Volume 196, Number 2

Vascular and Interventional Radiology

Original Research

Bronchial and Nonbronchial Systemic Artery Embolization in Patients With Major Hemoptysis: Safety and Efficacy of N-Butyl Cyanoacrylate

+ Affiliations:
1Department of Radiology, Seoul National University Bundang Hospital, 300, Gumi-dong, Bundang-Gu, Seongnam, Gyeonggi-do, 463-707 Bundang, Korea.

2Department of Radiology, University of North Carolina, Chapel Hill, NC.

3Department of Internal Medicine, Seoul National University Bundang Hospital, Bundang, Korea.

Citation: American Journal of Roentgenology. 2011;196: W199-W204. 10.2214/AJR.10.4763

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OBJECTIVE. The purpose of this study was to evaluate the safety and efficacy of N-butyl cyanoacrylate for bronchial and nonbronchial systemic artery embolization in the management of major hemoptysis.

MATERIALS AND METHODS. From March 2004 through March 2006, 108 patients with major hemoptysis underwent embolization with N-butyl cyanoacrylate. The common conditions causing hemoptysis were bronchiectasis (n = 34), sequelae of tuberculosis (n = 31), active tuberculosis (n = 18), lung cancer (n = 8), and aspergilloma (n = 6). A retrospective analysis of postprocedure outcomes, including immediate success, recurrence of hemoptysis, cause of recurrence, and complications, was performed.

RESULTS. Immediate success was achieved in 105 patients (97.2%). During the follow-up period (range, 5 days–63 months; median, 28.5 months), recurrent hemoptysis was found in 21 of the 105 patients (20%). Repeat angiograms (n = 14) revealed incomplete embolization during the initial procedure in seven patients with early recurrence (< 3 months) and revascularization of nonbronchial systemic collateral arteries in seven patients with late recurrence (> 3 months). No recanalization of embolized arteries was found on repeat angiograms or at follow-up CT. The cumulative nonrecurrence rates were 91.4% 1 month, 83.4% 1 year, 76.7% 3 years, and 56.8% 5 years after the initial procedure. The procedure-related complications included transient chest pain (n = 21) and denudation of the bronchial mucosa (n = 3), which was clinically silent but found at bronchoscopy.

CONCLUSION. N-butyl cyanoacrylate is a safe and effective agent for embolization in patients with major hemoptysis.

Keywords: bronchial artery, embolization, N-butyl cyanoacrylate

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Bronchial artery embolization (BAE) is the minimally invasive alternative considered the most effective nonsurgical treatment of patients with massive or recurrent hemoptysis [1, 2]. The embolic material for BAE has typically included polyvinyl alcohol (PVA) particles and gelatin sponge particles. Successful outcome with newer embolic materials, such as tris-acryl gelatin microspheres and thrombin, has been reported [3, 4]. Each embolic material has advantages and disadvantages, but the optimal embolic agent for BAE has not yet been determined [5].

N-butyl cyanoacrylate (NBCA) is a permanent liquid embolic material. Although initially approved for embolization of cerebral arteriovenous malformation, NBCA has been gaining attention among interventionalists for the control of bleeding from various peripheral vessels [68]. NBCA, as an embolic agent, has the following advantages over other materials: rapid and complete vessel occlusion, even in patients with coagulopathy; controlled embolization by adjustment of polymerization rate; and relatively short procedure time [79]. Owing to these advantages, NBCA may be a suitable embolic material for BAE. The use of NBCA for BAE has been reported [10, 11], but these studies of the evaluation of efficacy and safety of NBCA were hindered by small sample sizes and short follow-up periods. The purpose of our study is to retrospectively evaluate the efficacy and safety of BAE performed with NBCA in a large population undergoing long-term follow-up.

Materials and Methods
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Our institutional review board approved this retrospective study and waived the requirement for patient informed consent. From March 2004 through March 2006, 108 patients (66 men, 42 women; mean age, 56.2 years; range, 22–82 years) with major hemoptysis underwent BAE with NBCA. Major hemoptysis was defined as acute massive bleeding of greater than 240 mL/d (n = 66) or moderate hemoptysis in the form of recurrent bleeding of substantial volume (> 100 mL/d) for several days (n = 42) [12, 13]. Five patients had previously undergone multiple sessions of BAE with PVA particles, and one patient had undergone left pneumonectomy because of hemoptysis. The most common underlying pulmonary diseases causing hemoptysis were bronchiectasis (n = 34), sequelae of tuberculosis (n = 31), active tuberculosis (n = 18), lung cancer (n = 8), and aspergilloma (n = 6) followed by actinomycosis, nontuberculous mycobacterial infection, atypical adenomatous hyperplasia, and pulmonary sequestration in one patient each. In seven patients, the cause of hemoptysis was not determined. Before BAE, all patients underwent contrast-enhanced CT of the thorax (16-MDCT scanner, Mx 8000, Philips Healthcare) for identification of the cause of hemoptysis, localization of the bleeding focus, and prediction of culprit vessels. Twelve patients underwent bronchoscopy immediately before BAE, and a bleeding focus was identified in nine of these patients.

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Fig. 1A 60-year-old man with moderate hemoptysis caused by sequelae of tuberculosis. Selective arteriogram of intercostobronchial trunk shows engorged right bronchial artery (arrow).

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Fig. 1B 60-year-old man with moderate hemoptysis caused by sequelae of tuberculosis. Arteriogram obtained after embolization with N-butyl cyanoacrylate–iodized oil mixture (1:3 ratio) shows complete embolization of bronchial artery (black arrow) with sparing of intercostal artery (white arrow).

Bronchial Artery Embolization Procedures

All angiographic procedures were performed with a digital subtraction angiography unit (Integris Allura, Philips Healthcare). Iodixanol (Visipaque, GE Healthcare) at a concentration of 270 mg I/mL was used as the contrast medium. Aortography covering thoracic and upper abdominal aorta was performed through the right femoral arterial approach with a 5-French pigtail catheter. On the basis of the CT and aortographic findings, selective angiograms of the bronchial and nonbronchial collateral arteries were obtained with 5-French angiographic catheters (Torcon NB, Cook). On the selective angiograms, abnormal engorgement, parenchymal hypervascularity, bronchopulmonary shunt, and extravasation of the contrast agent were regarded as pathologic findings [1]. In nine patients with identifiable bleeding foci at bronchoscopy, the pathologic arteries supplying the contributory segment were embolized. For other patients, the decision about which vessels to embolize was based on CT and selective angiographic findings. When localization was deemed unfeasible on the basis of CT and angiographic findings, we embolized all possible culprit vessels.

A 3-French microcatheter (Ranegade, Boston Scientific) was introduced coaxially into the angiographic catheter and advanced through the pathologic arteries at the most distal point possible to avoid spinal feeders and reflux of injected NBCA into the aorta. Once the microcatheter was in place, NBCA (Histoacryl, B-Braun) was mixed with iodized oil (Lipiodol Ultra Fluide, Guerbet) in a ratio of 1:2–1:4 according to operator's decision. After the microcatheter was flushed with 5% dextrose solution, the mixture was injected under careful fluoroscopic monitoring (Figs. 1A and 1B). The rate of injection was adjusted on the basis of the flow of the mixture away from the microcatheter. When reflux of the mixture occurred, we stopped the injection. The volume of mixture varied depending on size of the embolized vessels, ranging from 0.5 to 2 mL. The microcatheter was quickly removed after the injection to avoid adhesion between catheter tip and vessel wall. Immediately after withdrawal, the microcatheter was flushed with 5% dextrose solution to be reused for embolization of other pathologic arteries in the same session.

In 13 patients in whom pathologic arteries issued from the proximal part of internal mammary artery, the main trunk of the internal mammary artery was embolized with metallic coils before injection of the NBCA mixture to prevent nontarget distal embolization (Figs. 2A, 2B, 2C, and 2D). After completion of embolization, aortography was performed to confirm that no more pathologic arteries were present.


All patients were closely observed for recurrent hemoptysis and early complications of BAE. After discharge, the patients were examined every 1–3 months on an outpatient basis. Forty-six patients underwent bronchoscopy 1–4 weeks after BAE. All patients underwent contrast-enhanced CT every 3–6 months for assessment of procedure-related complications and evaluation for progression of underlying disease. The end of follow-up period was defined as April 2009. For patients who were lost to follow-up or died, the end of the follow-up period was defined as the most recent date on which follow-up information was obtained or the date of death.


Medical records and images of the 108 patients were retrospectively reviewed with regard to embolized vessels, immediate success, recurrent hemoptysis, cause of recurrence, and complications. Immediate success was defined as no episode of hemoptysis within 24 hours after BAE [13]. The recurrence rates were compared among the underlying diseases by use of Fisher's exact test. The cumulative nonrecurrence rates were determined by Kaplan-Meier estimation. A major complication was defined as an event that led to a specific therapy, increased the level of care needed, prolonged hospitalization, or resulted in permanent adverse sequelae or death [14]. All other complications were considered minor.

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A total of 319 arteries were embolized: 169 bronchial arteries (101 right, 68 left) and 150 nonbronchial systemic collateral arteries for an average of 2.9 ± 2.0 (SD) arteries per patient. Thirty-one bronchial arteries had an aberrant origin from the aortic arch (n = 15), subclavian artery (n = 8), thyrocervical artery (n = 6), and internal mammary artery (n = 2). Nonbronchial collateral arteries embolized were intercostal (n = 87), internal mammary (n = 19), inferior phrenic (n = 17), thyrocervical (n = 15), lateral thoracic (n = 7), and costocervical (n = 5). Two of five patients who previously had undergone BAE with PVA particles had recanalization of previously embolized bronchial arteries (Figs. 3A, 3B, and 3C).

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Fig. 2A 64-year-old man with massive hemoptysis caused by aspergilloma in right upper lobe. Arteriogram of right bronchial artery shows hypervascular masslike lesion (black arrows) supplied by engorged right bronchial artery (white arrow). Bronchial artery was embolized with N-butyl cyanoacrylate (NBCA) mixture (not shown).

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Fig. 2B 64-year-old man with massive hemoptysis caused by aspergilloma in right upper lobe. Right subclavian arteriogram shows absence of nonbronchial systemic collateral artery (arrows). Hemoptysis was immediately controlled after embolization, and patient was uneventfully discharged.

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Fig. 2C 64-year-old man with massive hemoptysis caused by aspergilloma in right upper lobe. Selective internal mammary arteriogram obtained after repetition of bronchial artery embolization for recurrence of hemoptysis 8 months after B shows revascularization of systemic collateral artery from proximal part of internal mammary artery and multiple abnormal arteries (black arrows) supplying hypervascular lesion (white arrows).

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Fig. 2D 64-year-old man with massive hemoptysis caused by aspergilloma in right upper lobe. Fluoroscopic image after deployment of coils (black arrow) to prevent distal nontarget embolization shows proximal part of internal mammary artery embolized with NBCA mixture and coils (white arrows).

Immediate success was achieved in 105 patients (97.2%). BAE did not control hemoptysis in three patients. Two of these patients, one of whom had terminal pulmonary diseases (tuberculosis sequelae) and the other lung cancer, had persistent massive hemoptysis and died within 24 hours. The third patient, who had pulmonary sepsis secondary to tuberculous esophagobronchial fistula and features of disseminated intravascular coagulopathy, died 3 days after BAE.

The 105 patients with immediate success underwent follow-up for 5 days–63 months (mean, 27.3 ± 20.1 months; median, 28.5 months). During the follow-up period, recurrent hemoptysis was found in 21 patients (20%). Seven patients (33.3%) had rebleeding within 1 month of the procedure, three patients (14.3%) within 1–3 months, four patients (19.0%) within 3 months–1 year, and seven patients (33.3%) within 1–5 years. Therefore, in 10 of 21 cases (47.6%), bleeding recurred within 3 months, and in 14 (66.7%), within 1 year. The rate of recurrence based on underlying pulmonary disease was 66.7% (four of six) for aspergilloma, 25.0% (two of eight) for lung cancer, 22.6% (seven of 31) for tuberculosis sequela, 16.7% (three of 18) for active tuberculosis, and 8.8% (three of 34) for bronchiectasis. The recurrence rates among patients with aspergilloma and those with bronchiectasis differed significantly (p = 0.001). Twenty-four repeat embolizations were performed on 14 patients for recurrent hemoptysis: one repeat procedure in nine patients, two in two patients, three in two patients, and five in one patient. Two of the other seven patients (one with active tuberculosis, one with aspergilloma) underwent surgery. Three patients refused further intervention and survived with medical management. Two patients with lung cancer died soon after the recurrence of hemoptysis.

Angiography showed that the cause of recurrent hemoptysis varied according to recurrence time. In the seven patients with early recurrence (within 3 months of initial BAE), nonbronchial collateral arteries were identified that had been missed at the initial BAE. In the seven patients with late recurrence (more than 3 months after initial BAE), however, the bleeding was caused by revascularization of nonbronchial systemic collaterals (Figs. 2A, 2B, 2C, and 2D), but there was no recanalization of previously embolized arteries. A total of 48 bronchial (n = 4) and nonbronchial systemic collateral (n = 44) arteries were embolized in repeat procedures.

The cumulative nonrecurrence rates after initial BAE were 91.4% at 1 month, 88.3% at 3 months, 83.4% at 1 year, 80.5% at 2 years, 76.7% at 3 years, and 56.8% at 5 years (Fig. 4). The rates of repeat procedures were 85.1% at 1 month, 60.2% at 3 months–2 years, and 40.1% at 3 years. Five of the 84 patients without recurrence underwent elective surgery. Two of those patients had tuberculosis sequelae; one, aspergilloma; one, pulmonary sequestration; and one, bronchiectasis. Seven patients died of the underlying condition: four with progression of pulmonary disease, two with pulmonary sepsis secondary to acute pneumonia, and one with esophageal cancer.

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Fig. 3A 74-year-old man with massive hemoptysis caused by bronchiectasis. Embolization was performed with polyvinyl alcohol particles (355–500 μm). Fluoroscopic image after embolization shows bronchial artery (arrow) is opacified by stagnation of contrast medium.

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Fig. 3B 74-year-old man with massive hemoptysis caused by bronchiectasis. Embolization was performed with polyvinyl alcohol particles (355–500 μm). Selective arteriogram obtained when massive hemoptysis recurred 10 months after A shows recanalization of previously embolized right bronchial artery (arrows). Right bronchial artery and multiple intercostal arteries were embolized with N-butyl cyanoacrylate (NBCA) mixture (1:3 ratio).

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Fig. 3C 74-year-old man with massive hemoptysis caused by bronchiectasis. Embolization was performed with polyvinyl alcohol particles (355–500 μm). Follow-up chest CT obtained 10 months after B shows NBCA mixture casting right bronchial (arrow) and intercostal arteries (arrowheads). Patient had no recurrent hemoptysis at 2-year follow-up examination.

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Fig. 4 Graph shows cumulative nonrecurrence rates after initial bronchial artery embolization estimated by Kaplan-Meier method.

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Fig. 5A 22-year-old man with moderate hemoptysis caused by active tuberculosis. Arteriogram shows hypervascular parenchymal staining (black arrow) supplied by right bronchial artery (white arrows).

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Fig. 5B 22-year-old man with moderate hemoptysis caused by active tuberculosis. Fluoroscopic image shows N-butyl cyanoacrylate mixture (1:4 ratio) embolizing right bronchial artery (arrows).

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Fig. 5C 22-year-old man with moderate hemoptysis caused by active tuberculosis. Bronchoscopic image obtained 3 days after bronchial artery embolization to evaluate endobronchial lesion due to tuberculosis shows diffuse mucosal denudation (arrows) at right upper lobar bronchus, suggesting ischemic injury.

No major complication was identified in the study sample. The most common minor complication was transient chest or shoulder pain (n = 21, 20%), which resolved spontaneously or with oral analgesics. Three patients had urticaria attributable to hypersensitivity to the contrast medium. No lung parenchymal ischemia or airway abnormality was found at follow-up CT. All the embolized arteries were seen as linear areas of extremely high attenuation due to casting of the NBCA mixture in the arterial lumen. This finding persisted on all CT scans a maximum of 62 months after BAE. Follow-up bronchoscopy (n = 46) revealed diffuse denudation of the bronchial mucosa in three patients (6.5%) (Figs. 5A, 5B, and 5C). In those three patients the procedures were de novo embolizations. Otherwise, there was no significant common finding. One patient had undergone embolization of two right bronchial arteries and the right thyrocervical branch with 1:2 and 1:3 mixtures. Another underwent embolization of one right bronchial artery with a 1:4 mixture. The third patient underwent embolization of the right and left bronchial arteries with a 1:3 mixture. Only one patient reported transient mild chest pain, which resolved spontaneously without treatment.

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BAE is an established procedure widely used in the treatment of patients with moderate to massive hemoptysis [15], and PVA particles are the most widely used embolic material in BAE. Particulates, however, can clump in the lumens of delivery catheters and blood vessels, which can lead to incomplete embolization. Other limitations of the use of PVA particles are prolonged procedure time to achieve complete embolization and inability to optimally visualize the embolic load. In addition, although the occlusion is expected to be permanent, many investigators have reported recanalization after embolization with PVA particles [11, 16]. Attempts to perform BAE with other embolic materials therefore have been increasing [35].

Baltacioğlu et al. [10] conducted a retrospective study on BAE with NBCA. They achieved immediate success in all 25 patients, and hemoptysis recurred in 16% of the patients during a mean follow-up period of 14 months. In another study [11], in which use of PVA particles (36 procedures) was compared with use of NBCA (12 procedures) with respect to postprocedure outcome, fewer cases of hemoptysis recurred in the NBCA group (12 cases in 42 months vs two cases in 11.7 months). The results of these previous studies suggested that NBCA is an effective embolic agent for BAE but were limited by small study samples and short follow-up periods. Our results support those of the previous studies but with a larger study sample and longer follow-up period. Immediate control of hemoptysis was achieved in 97.2% of our patients, and the cumulative nonrecurrence rates were similar to the results of previous studies [1720] with other embolic materials (Table 1). In our study the underlying diseases frequently associated with recurrent hemoptysis were aspergilloma (four of six cases, 66.7%), lung cancer (two of eight, 25.0%), and tuberculosis sequelae (seven of 31, 22.6%), which are well-known predisposing factors for recurrent hemoptysis [17, 19, 20]. Early recurrence (< 3 months) was mainly caused by incomplete embolization at the initial procedure, whereas late recurrence (> 3 months) was caused by revascularization of nonbronchial collateral arteries.

TABLE 1: Comparison of Immediate Success Rate and Cumulative Nonrecurrence Rates in past Reports

Although BAE is known to be effective for immediate control of hemoptysis, the following factors limit the long-term durability of the results: incomplete embolization of the culprit vessels, recanalization of previously embolized vessels, revascularization of the collateral circulation, and progression of the underlying pulmonary disease [1, 21]. Recurrence due to revascularization or underlying disease progression is an inherent limitation of BAE because embolization only controls the symptoms and does not address the underlying condition.

Recurrent hemorrhage due to recanalization of previously embolized vessels can be avoided. Kato et al. [19] found that recanalization of the embolized artery is one of the major causes of recurrent hemoptysis within the first month after embolization. Razavi and Murphy [11] reported recurrent hemoptysis as a result of vessel recanalization in eight patients after 36 procedures in which PVA particles had been used as the embolic agent. We also found recanalization of the embolized artery in two of five patients who had undergone BAE with PVA particles. This problem can be avoided with use of a more durable embolic agent. In the current study, in none of the 319 arteries embolized with NBCA was recanalization found at repeat angiography or follow-up CT.

One concern about liquid embolic agents, including NBCA, is the high risk of severe complications such as tissue necrosis and nontarget embolization due to uncontrolled reflux or shunting [1, 5, 11]. Girard et al. [22] reported a case of bronchial stenosis that developed after BAE with isobutyl-2-cyanoacrylate. However, most previous studies of the use of NBCA as an embolic material have shown that the high viscosity and rapid polymerization of NBCA prevents it from penetrating to the capillary beds or into the vasa vasorum, something that can occur with small particles and absolute ethanol. The rate of polymerization can be altered to manipulate the degree of vessel penetration with NBCA, allowing the operator to achieve more controlled embolization of target vessels [23]. In previous studies [10, 11] a fixed concentration of NBCA was used for all patients (12.5% concentration) or for each patient (20–33.3% concentration). We chose, however, to adjust the concentration according to the characteristics of the vessels being embolized. In large vessels with rapid blood flow and those associated with a prominent bronchopulmonary shunt, we used a lower ratio of NBCA to iodized oil (1 part NBCA to 2 or 3 parts iodized oil) for faster polymerization. We used a 1:4 mixture to embolize small arteries with low blood flow for slower polymerization [68, 23]. Using this technique, we found no evidence of ischemic complications such as lung parenchymal infarction and airway abnormality at follow-up CT. We did find three cases of bronchial mucosal denudation, which can be a sign of ischemic injury, at follow-up bronchoscopy, but the patients continued to have no symptoms.

Chest and shoulder pain is a common complication of BAE, reported in 24–91% of cases, and presumably reflects chest wall ischemia due to embolization of nonbronchial systemic arteries, such as the intercostal, internal mammary, and inferior phrenic arteries [1]. We encountered this complication in 20% of our patients, and it resolved spontaneously or was easily controlled with oral analgesics. Although we were not able to quantitatively assess the severity of pain, it seems to be less severe than that described in earlier studies [22, 24], in which violent retrosternal burning pain was reported after BAE with isobutyl-2 cyanoacrylate. In 13 patients, we used NBCA in conjunction with coils when small difficult-to-select pathologic arteries originated from the proximal part of the internal mammary artery. By deploying coils before NBCA injection, we were able to avoid nontarget embolization of the mid to distal part of the internal mammary artery, which might have reduced chest wall ischemia.

The most feared serious complication of BAE is nontarget embolization of the anterior spinal artery or vertebral artery. None of our patients experienced this complication. However, reflux of polymerized NBCA around a microcatheter can adhere to its tip and can be detached when the microcatheter is withdrawn after NBCA injection [11]. This situation is especially risky during embolization of intercostal arteries, from which spinal arteries can arise, and of the internal mammary and thyrocervical arteries, which are close to the vertebral artery. Therefore, extreme care should be taken in embolization of those vessels to avoid reflux of the NBCA mixture.

Our study had several limitations. First, the study had no control group. Although our results suggest that NBCA is a safe and effective embolic agent for BAE, a comparative study is needed to confirm the potential advantages over other those of other embolic agents. Second, owing to the retrospective design of this study, important data such as procedure time were difficult to obtain. In addition, our study was performed with an inhomogeneous patient population. Underlying diseases and severity of hemoptysis were variable, which made it difficult to compare our results with those of previous studies.

We conclude that embolization of bronchial and nonbronchial systemic collateral arteries with NBCA is safe and effective treatment of patients with massive and moderate hemoptysis. Our results showed a high immediate success rate and a low recurrence rate. Repeat angiography and follow-up CT showed no recanalization of embolized arteries. There were no major complications, including ischemic injury to the airways and lung parenchyma. On the basis of these results, we recommend performance of a prospective, randomized study to compare NBCA with other more commonly used embolic agents for BAE.

Supported by grant from Seoul National University Hospital Research Fund (02-2007-003).

Address correspondence to C. J. Yoon ().


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