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AJR 2003; 180:1577-1581
© American Roentgen Ray Society


Added Benefit of Thoracic Aortography After Transarterial Embolization in Patients with Hemoptysis

Ho Jong Chun1, Jae Young Byun1, Seung-Schik Yoo2 and Byung Gil Choi1

1 Department of Radiology, Kangnam St. Mary's Hospital, College of Medicine, The Catholic University of Korea, 505 Banpo-Dong, Seocho-Ku, Seoul 137-040, Korea.
2 Present address: Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, 75 Francis St., Boston, MA 02115.

Received September 10, 2002; accepted after revision November 12, 2002.

 
Address correspondence to B. G. Choi.


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of this study was to examine the usefulness of thoracic aortography performed after transarterial embolization in identifying additional arteries responsible for causing hemoptysis.

SUBJECTS AND METHODS. Between March 2000 and November 2001, we prospectively performed thoracic aortography after transarterial embolization in 76 patients with hemoptysis. Underlying diseases included tuberculosis (n = 34), bronchiectasis (n = 30), emphysema (n = 4), bronchitis (n = 4), aspergillosis (n = 3), and lung cancer (n = 1). Initially, angiography of bronchial and other systemic arteries possibly contributing to hemoptysis was performed with embolization. After completion of the embolization, thoracic aortography was performed, with the tip of the catheter located just distal to the origin of the left subclavian artery.

RESULTS. A total of 200 arteries (52 right bronchial, 40 left bronchial, six common bronchial, 76 intercostal, 11 inferior phrenic, six thoracodorsal, eight internal mammary, and one thyrocervical) were identified either at the initial embolization or on thoracic aortography as being responsible for causing hemoptysis. Among them, 29 arteries (14.5%) that were not included on the initial selection for embolization were later identified on postembolization thoracic aortography. There were two right bronchial, three left bronchial, eight inferior phrenic, and 16 intercostal arteries.

CONCLUSION. The inferior phrenic and intercostal arteries were often missed on routine transarterial embolization in patients with hemoptysis. Postembolization thoracic aortography is useful for monitoring the effectiveness of embolization and for improving the detection of arteries contributing to hemoptysis.


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Hemoptysis is a relatively common symptom in patients with a variety of pulmonary diseases; in severe cases it leads to death [1]. With the development of angiographic techniques, microcatheters, and embolic materials, transarterial embolization has become widely used and is often preferred to surgery as a treatment of hemoptysis. Transarterial embolization, when applied to recurrent cases of minor hemoptysis, may prevent the further deterioration of this condition [2, 3, 4, 5, 6, 7].

The variations of bronchial arteries and the presence of nonbronchial systemic collateral arteries are well recognized as factors contributing to inadequate embolization of these arteries [7, 8]. Other researchers have reported that thoracic aortography might be useful in identifying bronchial arteries of anomalous origin or the nonbronchial systemic collateral arteries that cause hemoptysis [9, 10]. However, to our knowledge, no prospective studies have been published on this topic. We were therefore motivated to perform thoracic aortography after transarterial embolization in patients with hemoptysis to assess the utility of thoracic aortography.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
We performed transarterial embolization in 76 consecutive patients (48 men and 28 women; age range, 24–80 years; mean age, 54 years) who were admitted to our institution between March 2000 and November 2001 with various degrees of hemoptysis. The underlying diseases in these patients included tuberculosis (n = 34), bronchiectasis (n = 30), emphysema (n = 4), bronchitis (n = 4), aspergillosis (n = 3), and lung cancer (n = 1). All angiography procedures were performed using a digital subtraction angiography unit (Multistar, Siemens, Erlangen, Germany) and iopromide (Ul-travist, Schering, Berlin, Germany) contrast medium at a concentration of 300 mg I/mL. Informed consent was obtained from all patients, and the study protocol was approved by our institutional review board.

Initially, the bronchial arteries were selected using 5-French bronchial catheters (Bronchial, Jungsung, Seoul, Korea) that were introduced in all patients via cannulation of the common femoral artery. If the bronchial arteries were thought to cause hemoptysis after the selective angiographies, they were catheterized using coaxial 3-French microcatheters (Leggiero, Terumo, Tokyo, Japan) and then embolized with 355- to 500-µm polyvinyl alcohol particles (Contour, Boston Scientific, Cork, Ireland), gelatin sponge particles (Gelfoam, Pharmacia and Upjohn, Kalamazoo, MI), or microcoils (Tornado, Cook, Bloomington, IN). The subclavian arteries were also selected in all patients using the same 5-French bronchial catheters, and selective arteriograms were then obtained. Any nonbronchial collateral arteries responsible for hemoptysis, such as the intercostal and inferior phrenic arteries and branches of the subclavian arteries (internal mammary, thyrocervical, lateral thoracic, and thoracodorsal), were also selected using the microcatheters and were embolized. The criteria for defining the arteries associated with hemoptysis included tortuous hypertrophy (compared with the size of adjacent normal intercostal arteries), bronchopulmonary shunt, extravasation of the contrast material, and peribronchial hypervascularity on the selective arteriograms. Pulmonary angiography was not performed in any patient.

After the completion of all possible embolizations by two interventional radiologists, thoracic aortography was consequently performed in all patients. An anteroposterior projection and a 5-French pigtail catheter (Pig, Cook) with its tip located just distal to the origin of the left subclavian artery were used, and an injection of 40 mL of contrast medium was administered at a rate of 20 mL/sec. The representative procedure is shown in Figures 1A, 1B, 1C. When the arteries possibly associated with hemoptysis were found unembolized on thoracic aortograms, they were subsequently selected and embolized.



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Fig. 1A. 53-year-old man with pulmonary tuberculosis. Bronchial arteriogram shows left bronchial artery to be hypertrophied with abnormal parenchymal stain (arrows) in left upper lobe.

 


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Fig. 1B. 53-year-old man with pulmonary tuberculosis. After embolization of left bronchial artery using Gelfoam ([gelatin sponge particles], Pharmacia and Upjohn, Kalamazoo, MI) and microcoils, thoracic aortogram shows no remaining opacification of left bronchial artery or abnormal parenchymal stain in left upper lobe.

 


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Fig. 1C. 53-year-old man with pulmonary tuberculosis. Late phase thoracic aortogram shows 5-French pigtail catheter (arrow) (Pig, Cook, Bloomington, IN) located distal to origin of left subclavian artery. Note microcoils (arrowhead) (Tornado, Cook) from initial embolization.

 


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
A total of 200 arteries (52 right bronchial, 40 left bronchial, six common bronchial, 76 intercostal, 11 inferior phrenic, six thoracodorsal, eight internal mammary, and one thyrocervical) were found and considered to be the origin of hemoptysis in 76 patients (Table 1). In 38 patients, embolization was limited to the bronchial arteries. In the other patients, systemic collateral arteries of nonbronchial origin were found and considered responsible for the hemoptysis.


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TABLE 1 Number of Arteries Embolized Before and After Thoracic Aortography

 

Twenty-nine arteries (14.5%) that were not included on the initial embolization were later found via postembolization thoracic aortography. They were mainly nonbronchial systemic collateral arteries, such as eight inferior phrenic (4.0% of the total number of arteries; 72.7% of the identified phrenic arteries) and 16 intercostal arteries (8.0% of the total number of arteries; 21.1% of the identified intercostal arteries). In addition, two right bronchial and three left bronchial arteries were also included. Additional embolizations resulting from thoracic aortography included the left bronchial artery (Figs. 2A, 2B, 2C) and the left intercostal and inferior phrenic arteries (Figs. 3A, 3B, 3C, 3D). The arteries identified on thoracic aortography were also embolized, except for six arteries (3.0%) that could not be catheterized or embolized because of their tortuous course, proximal stenosis, arterial injury during selection, or presence of a spinal artery.



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Fig. 2A. 35-year-old man with pulmonary tuberculosis. Bronchial arteriogram shows left bronchial artery to be hypertrophied along with abnormal parenchymal stain and systemic pulmonary shunt (arrow) in left upper lobe. Left bronchial artery was selected and embolized with polyvinyl alcohol particles (Contour, Boston Scientific, Cork, Ireland).

 


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Fig. 2B. 35-year-old man with pulmonary tuberculosis. Postembolization aortogram shows abnormal hypervascular stain (arrows) in left perihilar lung.

 


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Fig. 2C. 35-year-old man with pulmonary tuberculosis. After additional left bronchial artery was selected with 5-French bronchial catheter (Bronchial, Jungsung, Seoul, Korea), selective arteriogram shows tortuous hypertrophy with parenchymal stain.

 


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Fig. 3A. 57-year-old woman with pulmonary tuberculosis and cystic bronchiectasis. After embolization of both bronchial arteries, thoracic aortogram shows hypertrophy with suspicious parenchymal stains (arrows) involving left highest and fifth intercostal arteries and inferior phrenic arteries.

 


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Fig. 3B. 57-year-old woman with pulmonary tuberculosis and cystic bronchiectasis. Selective arteriograms show tortuous hypertrophy of left highest (arrow, B) and fifth intercostal arteries (arrow, C) and inferior phrenic arteries (arrow, D) associated with parenchymal stains and arteriovenous shunts.

 


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Fig. 3C. 57-year-old woman with pulmonary tuberculosis and cystic bronchiectasis. Selective arteriograms show tortuous hypertrophy of left highest (arrow, B) and fifth intercostal arteries (arrow, C) and inferior phrenic arteries (arrow, D) associated with parenchymal stains and arteriovenous shunts.

 


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Fig. 3D. 57-year-old woman with pulmonary tuberculosis and cystic bronchiectasis. Selective arteriograms show tortuous hypertrophy of left highest (arrow, B) and fifth intercostal arteries (arrow, C) and inferior phrenic arteries (arrow, D) associated with parenchymal stains and arteriovenous shunts.

 

No significant complications developed related to embolization. The hospital stay after completion of transarterial embolization was 3–15 days (mean, 4.3 days), and clinical short-term follow-up was performed during admission. All patients were discharged without significant recurrence of hemoptysis during the hospital stay after completion of transarterial embolization.


Discussion
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
In patients with hemoptysis, systemic circulation—mainly the bronchial arteries—is a primary source of bleeding. Reduced pulmonary circulation in the lesions of inflammatory lung diseases leads to systemic pulmonary anastomosis accompanied by a compensatory increase in systemic circulation, resulting in the rupture of systemic arteries [11]. In addition to the bronchial arteries, many systemic arteries constitute various nonbronchial systemic collaterals that also contribute to hemoptysis [7, 8, 12, 13, 14, 15, 16].

In general, bronchial arteries arise from the thoracic aorta between the lower margin of T4 and the upper margin of T6 adjacent to the major bronchi. However, the anomalous bronchial arteries may arise from arteries other than the thoracic aorta, including the subclavian, internal mammary, brachiocephalic, pericardia-cophrenic, inferior phrenic, and thyrocervical trunk arteries and the abdominal aorta [9, 17]. Nonbronchial systemic collateral arteries are different from anomalous bronchial arteries in that they are not congenital and are developed during various pulmonary disease processes. Morphologically, their courses are not parallel to those of bronchi, and they may pass through the pulmonary ligaments or adherent pleura. Systemic collateral arteries may include a wide spectrum of arteries within or near the thorax, such as the intercostal [13], thyrocervical [14], internal mammary [15, 16], thoracodorsal, and lateral thoracic arteries and other branches of the subclavian artery [8]. Even intraabdominal arteries, including the inferior phrenic arteries, may also provide nonbronchial collateral supplies for the lung lesions that cause hemoptysis [10, 12].

The nonbronchial systemic collateral arteries are known to be common in the presence of pleural thickening and adhesion in chronic inflammatory lung disease or lung malignancies, thereby facilitating transpleural systemic pulmonary anastomosis. These nonbronchial collateral arteries are assumed to proliferate via thickened pleura and consequently to reduce the therapeutic effect of embolization. Tamura et al. [18] found that the incidence of rebleeding after bronchial arterial embolization was higher in the presence of pleural thickening.

Therefore, it is important to recognize the presence of anomalous bronchial arteries and nonbronchial systemic collateral arteries during transarterial embolization in patients with hemoptysis. Although the morphologic features on CT or unenhanced radiography may be useful in identifying the presence and location of anomalous bronchial arteries or nonbronchial systemic collaterals [18], identification of these arteries associated with hemoptysis would require a time-consuming and exhaustive search. In particular, identifying and selecting collateral arteries originating below the diaphragm is difficult except in cases confined to the basal regions of the lungs.

We used thoracic aortography only occasionally in patients in whom the causal arteries could not be detected using the blind technique in spite of the presence of substantial bleeding or lung lesions causing hemoptysis. During this process, the arteries found on thoracic aortography were mostly anomalous bronchial or nonbronchial systemic collateral arteries that were often situated in unexpected locations. These experiences have led us to believe that the completion of transarterial embolization without thoracic aortography may fail to detect arteries causing hemoptysis and may result in the recurrence of hemoptysis.

Our results suggest that intercostal and inferior phrenic arteries are frequently missed in routine transarterial embolization. The intercostal arteries are in pairs of 12 and have variable origins and long tortuous courses. These factors often lead to difficulty in properly associating these arteries to various intrathoracic lesions. The inferior phrenic arteries, as with the extrathoracic arteries, are not readily associated with hemoptysis.

As we have described, the tip of the pigtail catheter was placed just distal to the origin of the left subclavian artery during thoracic aortography. Therefore, the regions supplied by the subclavian arteries were not adequately visualized in this study. Additional subclavian arteriography could thus be easily performed without the use of additional catheters. Simultaneous visualization of the subclavian arteries in thoracic aortography is undesirable because the flow pattern and the amount of injected contrast medium are suboptimal to opacify all the arteries of interest.

Our study does not include long-term results of transarterial embolization. Instead, we performed immediate clinical follow-up during the patient admission. Although this might be a limitation to our study, thoracic aortography would still be helpful for when performed with transarterial embolization in patients with hemoptysis. Performing thoracic aortography after transarterial embolization may help to successfully complete the procedure by evaluating the effectiveness of prior embolization and detecting the missed arteries causing hemoptysis. Therefore, thoracic aortography may provide a supplementary method to help the interventional radiologist finish the procedure when no additional hypervascular stain or abnormally hypertrophied artery is found on the thoracic aortogram. In practice, the final criteria required to complete thoracic aortography are not yet established, although clinical improvement of hemoptysis might be helpful. In this aspect, thoracic aortography performed after transarterial embolization would be preferable to preliminary thoracic aortography. Preliminary thoracic aortography performed before transarterial embolization in patients with hemoptysis may have limitations.

Thoracic aortography may help interventional radiologists identify the arteries responsible for hemoptysis before performing selective arteriography. However, several arteries may overlap, or their courses and origins from the thoracic aorta may be misinterpreted, particularly in severe cases of hemoptysis with many collateral arteries. Moreover, the arteries with arteriovenous shunting or highly vascular lesions may consume most of the contrast material from the opacified thoracic aorta, which may preclude adequate opacification of smaller adjacent arteries that are also responsible for hemoptysis. An artery that is initially normal but recruited as an immediate collateral causing hemoptysis after embolization of an adjacent artery might be missed in a search for the arteries responsible for hemoptysis in the preliminary thoracic aortography. In addition, whether long-term follow-up can reflect the technical success of a transarterial embolization procedure is still questionable because it is only a conservative treatment for hemoptysis, and newly hypertrophied arteries may contribute to recurrent hemoptysis during long-term follow-up.

In conclusion, the inferior phrenic and intercostal arteries were often missed during routine transarterial embolization in patients with hemoptysis. Postembolization thoracic aortography is useful for improving the detection of arteries that contribute to hemoptysis.


Acknowledgments
 
We thank Bonnie Hami, Department of Radiology, University Hospitals Health System, Cleveland, OH, for her editorial assistance in the preparation of this manuscript.


References
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

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