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EDUCATION EXHIBIT 1395

RadioGraphics
Bronchial and Nonbron-
chial Systemic Artery
Embolization for Life-
threatening Hemop-
tysis: A Comprehensive
Review1
Woong Yoon, MD ● Jae Kyu Kim, MD ● Yun Hyun Kim, MD
ONLINE-ONLY
CME Tae Woong Chung, MD ● Heoung Keun Kang, MD
See www.rsna
.org/education
/rg_cme.html. Massive hemoptysis is one of the most dreaded of all respiratory emer-
gencies and can have a variety of underlying causes. In 90% of cases,
the source of massive hemoptysis is the bronchial circulation. Diagnos-
LEARNING
OBJECTIVES tic studies for massive hemoptysis include radiography, bronchoscopy,
After reading this
and computed tomography (CT) of the chest. Bronchoscopy and chest
article and taking radiography have been considered the primary methods for the diagno-
the test, the reader
will be able to: sis and localization of hemoptysis. Many researchers currently suggest
䡲 List the most com- that CT should be performed prior to bronchoscopy in all cases of
mon causes of mas-
sive hemoptysis. massive hemoptysis. Bronchial artery embolization (BAE) is a safe and
䡲 Discuss the roles of effective nonsurgical treatment for patients with massive hemoptysis.
CT and bronchos- However, nonbronchial systemic arteries can be a significant source of
copy in the diagnosis
of massive hemopty- massive hemoptysis and a cause of recurrence after successful BAE.
sis. Knowledge of the bronchial artery anatomy, together with an under-
䡲 Describe the tech- standing of the pathophysiologic features of massive hemoptysis, are
niques, embolic ma-
terials, results, and essential for planning and performing BAE in affected patients. In ad-
complications associ- dition, interventional radiologists should be familiar with the tech-
ated with BAE for
massive hemoptysis. niques, results, and possible complications of BAE and with the char-
acteristics of the various embolic agents used in the procedure.
©
RSNA, 2002

Abbreviations: BAE ⫽ bronchial artery embolization, FOB ⫽ fiberoptic bronchoscopy, ICBT ⫽ intercostobronchial trunk

Index terms: Arteries, bronchial, 943.1264, 943.92 ● Arteries, therapeutic embolization, 943.1264 ● Bronchi, anatomy, 671.92 ● Bronchi, interven-
tional procedures ● Lung, CT, 60.1211, ● Lung, hemorrhage ● Pulmonary angiography, 60.124

RadioGraphics 2002; 22:1395–1409 ● Published online 10.1148/rg.226015180


1From the Department of Diagnostic Radiology, Chonnam National University Hospital, Chonnam National University Medical School, 8 Hak-1-
dong, Dong-gu, Gwangju 501-757, South Korea. Recipient of a Certificate of Merit award for an education exhibit at the 2001 RSNA scientific as-
sembly. Received December 19, 2001; revision requested April 23, 2002; final revision received July 26; accepted August 1. Address correspon-
dence to W.Y. (e-mail: radyoon@cnuh.com).
©
RSNA, 2002
1396 November-December 2002 RG f Volume 22 ● Number 6

RadioGraphics Introduction riod of 24 hours, and the most widely used crite-
Life-threatening hemoptysis is one of the most rion is the production of 300 – 600 mL per day
challenging conditions encountered in critical (2– 4,15). However, depending on the ability of
care and requires a thorough and timely investiga- the patient to maintain a patent airway, a life-
tion. Despite advances in medical and intensive threatening condition may be caused by a rather
care unit management, massive hemoptysis re- small amount of hemorrhage. Thus, a more func-
mains a serious threat. According to recently pub- tional definition of “massive” as an amount suffi-
lished data, 28% of chest clinicians had experi- cient to cause a life-threatening condition should
enced a patient’s death from massive hemoptysis be used in deciding whether to undertake inter-
during a previous 1-year period (1). Conservative ventional management (15,16).
management of massive hemoptysis carries a Massive hemoptysis may result from various
mortality rate of 50%–100% (2). The cause of causes, and the frequency with which these causes
death is usually asphyxiation, not exsanguination occur differs greatly between the Western and the
(3). The reported mortality rates for surgery per- non-Western world. In the non-Western world,
formed for massive hemoptysis range from 7.1% pulmonary tuberculosis, including tuberculosis
to 18.2% (4). However, the mortality rate in- bronchiectasis, is the most common underlying
creases significantly, up to about 40%, when the cause of massive hemoptysis. Bronchogenic carci-
surgery is undertaken as an emergency proced- noma and chronic inflammatory lung diseases
ure (4). due to bronchiectasis, cystic fibrosis, or aspergil-
Bronchial artery embolization (BAE) has be- losis are the more prevalent causes of hemoptysis
come an established procedure in the manage- in Western countries (2,3,15). Other causes in-
ment of massive and recurrent hemoptysis; its use clude lung abscess, pneumonia, chronic bronchi-
was first reported in 1973 by Remy et al (5). The tis, pulmonary interstitial fibrosis, pneumoconio-
efficacy, safety, and utility of BAE in controlling sis, pulmonary artery aneurysm (Rasmussen
massive hemoptysis have been well documented aneurysm), congenital cardiac or pulmonary vas-
in many subsequent reports (6 –14). Because of cular anomalies, aortobronchial fistula, ruptured
poor pulmonary reserve and other medical co- aortic aneurysm, and ruptured bronchial artery
morbid conditions, most patients with massive aneurysm.
hemoptysis are not surgical candidates (2,3). Bronchial artery aneurysm or pseudoaneurysm
However, surgery remains the procedure of is a rare entity, and the term aneurysm is used in-
choice in the treatment of massive hemoptysis terchangeably with pseudoaneurysm in the litera-
caused by specific conditions, such as hydatid ture (17–22). The cause of bronchial artery aneu-
cyst, thoracic vascular injury, bronchial adenoma, rysm is unknown, although bronchiectasis or re-
and aspergilloma that is resistant to other thera- current bronchopulmonary inflammation, a
pies (15). Even in surgical candidates, BAE is mycotic origin, trauma, and Rendu-Osler-Weber
effective in preparing the patient for elective syndrome are often associated with an aneurysm
rather than high-risk emergency surgery (4). (21). Bronchial artery aneurysms can be charac-
In this article, we describe the definition and terized as either mediastinal (juxtaaortic) or in-
causes, pathophysiologic features, and diagnosis trapulmonary. The treatment options for bron-
of massive hemoptysis and review the angio- chial artery aneurysm include transcatheter em-
graphic and computed tomographic (CT) anat- bolization, placement of a covered stent, and
omy of the bronchial circulation. We also discuss surgery (21,22).
the technique, embolic materials, results, and
complications associated with BAE. In addition, Pathophysiologic Features
we describe the role of nonbronchial systemic The source of massive hemoptysis is usually the
artery embolization and present CT findings that bronchial circulation (90% of cases) rather than
are useful in predicting the existence of nonbron- the pulmonary circulation (5%) (23). In a minor-
chial systemic arterial supply in patients with ity of cases (5%), massive hemoptysis may origi-
massive hemoptysis. nate with the aorta (eg, aortobronchial fistula,
ruptured aortic aneurysm) or the systemic arterial
Massive Hemoptysis supply to the lungs (24 –26). In many acute and
chronic lung diseases, pulmonary circulation is
Definition and Causes reduced or occluded at the level of the pulmonary
Massive hemoptysis has been described as the arterioles because of hypoxic vasoconstriction,
expectoration of an amount of blood ranging intravascular thrombosis, and vasculitis (27). As a
from 100 mL to more than 1,000 mL over a pe- result, bronchial arteries proliferate and enlarge to
replace the pulmonary circulation. The enlarged
bronchial vessels, which exist in an area of active
or chronic inflammation, may be ruptured due to
RG f Volume 22 ● Number 6 Yoon et al 1397

RadioGraphics erosion by a bacterial agent or due to elevated of massive hemoptysis (15). The risks of FOB
regional blood pressure. The arterial blood under include possible airway compromise from seda-
systemic arterial pressure subsequently extrava- tion, delay in definitive treatment, hypoxemia,
sates into the respiratory tree, resulting in massive and high cost.
hemoptysis (27,28). The role of CT in the evaluation of patients
with hemoptysis has been validated (30,32,38).
Diagnosis CT has proved to be of considerable value in di-
Diagnostic studies for massive hemoptysis include agnosing bronchiectasis, bronchogenic carci-
radiography, bronchoscopy, and CT of the chest noma, and aspergilloma in patients with massive
(15,16,29,30). In patients with massive hemopty- hemoptysis (31,39). CT may demonstrate lesions
sis, the diagnostic work-up is usually performed that may not be visible on conventional radio-
both to find the cause of the bleeding and to lo- graphs, and contrast material– enhanced CT may
calize the pulmonary lobes in which bleeding is help detect vascular lesions that cause massive
suspected. Localization of the bleeding site prior hemoptysis. CT findings can suggest a specific
to BAE is very important if the procedure is to be diagnosis in 50% of patients in whom FOB find-
performed in a focused and efficient manner. ings are nondiagnostic and in 39%– 88% of pa-
Conventional radiography is a basic study and tients in whom chest radiographs are nondiagnos-
is readily available even under emergency condi- tic (29,30,32,39). CT can also help localize the
tions. It may be helpful in diagnosing and localiz- site of bleeding in 63%–100% of patients with
ing pneumonia, acute or chronic pulmonary tu- hemoptysis, a rate that is higher than that for
berculosis, bronchogenic cancer, or lung abscess FOB (16,33). It has been stated that CT and
(29). However, radiographic findings are normal FOB are not competitive but complementary
or nonlocalizing in 17%– 81% of patients with tools for assessing patients with hemoptysis, and
hemoptysis (16,29 –33). In a retrospective evalua- indeed, the combined use of FOB and CT does
tion of 208 patients with hemoptysis, Hirshberg yield the best results in evaluating hemoptysis
et al (31) found that radiography was considered (33). However, many researchers are currently
to be diagnostic in only 50% of cases. suggesting that CT should be performed prior to
Bronchoscopy has long been considered by bronchoscopy in all patients with hemoptysis
chest clinicians to be the primary method for di- (15,30,32,38). State-of-the-art CT allows rapid
agnosis and localization of hemoptysis (34,35). scanning, making timely examination feasible in
Fiberoptic bronchoscopy (FOB) has proved effi- critically ill patients. In addition, bronchial and non-
cacious in evaluating central bronchial lesions. A bronchial systemic feeder vessels can be detected at
vasoactive drug can be infused locally during contrast-enhanced CT. In a prospective study of
bronchoscopy to control bleeding (15). 40 patients with massive hemoptysis, 27 patients
It has been reported that FOB can help localize (67.5%) had a nonbronchial systemic arterial sup-
bleeding to one side or the other in 49%–92.9% ply, and CT had an overall accuracy of 84% in
of patients with hemoptysis (16,31,33). The role identifying this finding (unpublished data).
of FOB in the evaluation of patients who present
with hemoptysis is still controversial, especially in Anatomy of the Bronchial Artery
cases in which chest radiographic findings are Interventional radiologists who perform BAE
normal or nonlocalizing (29). The diagnostic ac- should have a thorough knowledge of bronchial
curacy of FOB in patients with hemoptysis and artery anatomy. The bronchial arteries have vari-
normal chest radiographs is low, ranging from 0% able anatomy in terms of origin, branching pat-
to 31% (29,31,32,36,37). The overall diagnostic tern, and course (40). The bronchial arteries
accuracy of FOB in evaluating patients with he- originate directly from the descending thoracic
moptysis is reported to be 10%– 43% (29 –33). In aorta, most commonly between the levels of the
a recent article, Hsiao et al (16) documented that T5 and T6 vertebrae (3). Cauldwell et al (41)
FOB prior to BAE is unnecessary in patients with reported four classic bronchial artery branching
hemoptysis of known cause if the site of bleeding patterns: two on the left and one on the right that
can be determined on conventional radiographs. presents as an intercostobronchial trunk (ICBT)
FOB has some disadvantages in the diagnosis and (40% of cases); one on the left and one ICBT on
localization of massive, active hemoptysis. It is the right (21%); two on the left and two on the
difficult to localize the bleeding site with FOB in right (one ICBT and one bronchial artery)
patients with massive hemoptysis because of ex- (20%); and one on the left and two on the right
cessive blood in the bronchi. Moreover, endo-
bronchial therapies are not effective in most cases
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Figure 1. Diagrams illustrate the types of bronchial arterial supply: Type I, two bronchial arteries on the left and
one on the right that manifests as an ICBT (40.6% of cases); Type II, one on the left and one ICBT on the right
(21.3%); Type III, two on the left and two on the right (one ICBT and one bronchial artery) (20.6%); and Type IV,
one on the left and two on the right (one ICBT and one bronchial artery) (9.7%).

Figure 2. Right intercostobronchial artery. On a se- Figure 3. Common bronchial trunk. On a selective
lective right ICBT angiogram, an intercostal branch bronchial angiogram, the right intercostobronchial ar-
(solid arrows) and the right bronchial artery (open ar- tery (black arrow) and a pathologic left bronchial artery
rows) are seen to arise from a common trunk. (white arrow) are seen to arise from a common trunk
and supply hypervascular lesions in the left lower lobe.

(one ICBT and one bronchial artery) (9.7%) (Fig


1). The right ICBT is the most consistently seen Bronchial arteries that originate outside the
vessel at angiography (80% of individuals) (Fig area between the T5 and T6 vertebrae at the level
2). The right ICBT usually arises from the right of the major bronchi are considered to be anoma-
posterolateral aspect of the thoracic aorta and the lous (41,42). The reported prevalence of bron-
normal right and left bronchial arteries from the chial arteries with an anomalous origin ranges
anterolateral aspect of the aorta. Right and left from 8.3% to 35% (42,43). These aberrant bron-
bronchial arteries that arise from the aorta as a chial arteries may originate from the aortic arch,
common trunk are not uncommon at angiogra- internal mammary artery (Fig 4), thyrocervical
phy (Fig 3). The true prevalence of a common trunk (Fig 5), subclavian artery, costocervical
bronchial artery trunk is unknown. trunk, brachiocephalic artery, pericardiaco-
The bronchial arteries supply the trachea, ex- phrenic artery, inferior phrenic artery, or abdomi-
tra- and intrapulmonary airways, bronchovascular nal aorta. Aberrant bronchial arteries can be dis-
bundles, nerves, supporting structures, regional tinguished anatomically and angiographically
lymph nodes, visceral pleura, and esophagus as from nonbronchial systemic collateral vessels in
well as the vasa vasorum of the aorta, pulmonary that they extend along the course of the major
artery, and pulmonary vein (27). bronchi. In contrast, nonbronchial systemic col-
lateral vessels enter the pulmonary parenchyma
RG f Volume 22 ● Number 6 Yoon et al 1399

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Figure 5. Aberrant bronchial artery. (a) Thoracic aortogram shows a hypertrophic right bronchial artery (arrow)
and intercostal arteries that supply hypervascular lesions in both upper lobes. There is no evidence of hypervascular-
ity in the right middle lobe or the lower lobes despite the visualization of significant parenchymal lesions at chest radi-
ography. (b) Image obtained after selective injection of an aberrant bronchial artery that arises from the left thyrocer-
vical trunk shows hypertrophic arteries that supply hypervascular lesions in the right lower and left upper lobes. Un-
like systemic collateral vessels, the aberrant bronchial arteries extend along the course of the primary bronchi.

through the adherent pleura or via the pulmonary


ligament, and their course is not parallel to that
of the bronchi (42). The majority of aberrant
bronchial arteries originate from the aortic arch
(41,42). The prevalence of bronchial arteries with
origins outside the aorta is unknown. Interven-
tional radiologists should be aware of the possible
presence of aberrant bronchial arteries, especially
when a significant bronchial arterial supply to ar-
eas of abnormal pulmonary parenchyma is not
demonstrated during a catheter search or at de-
scending thoracic aortography (44). In addition,
bronchial arteries of anomalous origin should be
suspected and investigated angiographically in
patients who present with recurrent hemoptysis
despite successful embolization and in those in
whom the source of bleeding has not been de-
tected (42).
Figure 4. Aberrant bronchial artery in a 46-year-old Two kinds of spinal arteries may be seen at
man who presented with massive hemoptysis. Thoracic bronchial and intercostal angiography during
aortography and a catheter search demonstrated only hy- BAE. Dorsal and ventral radicular arteries (Fig 6)
pertrophic intercostal arteries with no identification of the are small vessels that arise from segmental spinal
right bronchial artery. Despite the embolization of mul- arteries and supply the dorsal and ventral roots.
tiple pathologic intercostal arteries, massive hemoptysis An average of eight anterior medullary arteries
recurred after 1 day, and the patient underwent repeat
reinforce the anterior spinal artery, which is the
angiography. Selective right internal mammary angio-
gram shows an aberrant right bronchial artery (arrows) major independent source of spinal cord perfu-
that originates from the proximal portion of the right in- sion. The artery of Adamkiewicz, or greater ante-
ternal mammary artery. This aberrant bronchial artery rior medullary artery, reinforces the circulation of
was embolized, and the massive hemoptysis did not recur
during a follow-up period of 1 year.
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Figure 6. Radicular arteries. Left intercostal angio- Figure 7. Anterior medullary artery. Selective left sev-
gram shows two radicular arteries (arrows) that arise enth intercostal angiogram shows an anterior medullary
from the proximal portion of intercostal arteries. artery with the typical hairpin configuration (arrows).

Figures 8, 9. Bronchial artery. (8) Contrast-enhanced CT scan shows a pathologic right bronchial artery (arrow)
that originates from the anteromedial aspect of the thoracic aorta and a hypertrophic left bronchial artery in the aor-
topulmonary window (arrowheads). (9) Contrast-enhanced CT scan shows a pathologic left bronchial artery (arrow)
that originates from the anterior wall of the descending thoracic aorta.

lumbar enlargement of the spinal cord. This uni- with embolization. It has been suggested that spi-
lateral vessel has been observed to arise between nal arteries will arise from the intercostal branch
T9 and T12 in 75% of cases (45). Anterior med- of the right ICBT in 5%–10% of cases, but it is
ullary arteries have a characteristic “hairpin” con- generally believed that the true prevalence is con-
figuration at angiography (Fig 7). Radicular arter- siderably lower (3).
ies are often visualized during BAE. In our experi- In adults, normal bronchial arteries measure
ence, unintentional embolization of radicular less than 1.5 mm in diameter at their origin and
arteries does not cause clinical problems like spi- 0.5 mm at their point of entry into a bronchopul-
nal cord ischemia. It has been stated that the monary segment (27). A bronchial artery larger
presence of radicular arteries is not considered to than 2 mm at CT is most likely abnormal (46).
be a contraindication for BAE (8,9,43). Anterior Hypertrophic bronchial arteries are easily visual-
medullary arteries are rarely observed, but em- ized as enhancing nodular or tubular structures
bolization and repeat angiography should be within the mediastinum and around the central
avoided because spinal cord ischemia may occur airway on contrast-enhanced CT scans (47) (Figs
8, 9). The primary locations of enlarged bronchial
arteries at CT are the retroesophageal area, retro-
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Figure 10. Value of preliminary thoracic aortography. (a) Descending thoracic aortogram demonstrates two hyper-
trophic bronchial arteries (solid arrows) and one intervening intercostal artery (open arrow) that supply a hypervas-
cular lesion in the right upper lobe. (b) On a selective upper bronchial angiogram, the bronchial artery that supplies
the large hypervascular lesion is seen to have an anomalous origin from the inferior aspect of the aortic arch. Marked
bronchopulmonary shunting is also noted. (c) Selective lower bronchial angiogram shows a hypertrophic artery that
supplies the hypervascular lesion, along with marked bronchopulmonary shunting. (d) Selective intercostal angio-
gram shows a hypertrophic artery that supplies the hypervascular lesion, along with bronchopulmonary shunting.
The two bronchial arteries and the intervening intercostal artery were selectively embolized with polyvinyl alcohol
particles. Postembolization angiograms (not shown) demonstrated occlusion of each vessel, with no opacification of
the hypervascular lesion and no pulmonary arterial shunting.

tracheal area, retrobronchial area, posterior wall fully evaluated to determine the optimal angio-
of the main bronchus, and aortopulmonary win- graphic approach. This can be accomplished with
dow. Mediastinal lymph nodes, the azygos vein, a preliminary descending thoracic aortogram. Ab-
and an enhancing esophageal wall can mimic the normal bronchial arteries are visualized on an ini-
bronchial arteries at CT (48). tial thoracic aortogram in the majority of affected
patients (Fig 10). A descending thoracic aorto-
Bronchial Artery Embolization gram is also useful in the detection of nonbron-
chial systemic arteries that supply parenchymal
Technique
Prior to BAE, the number and origin sites of
bronchial arteries from the aorta should be care-
1402 November-December 2002 RG f Volume 22 ● Number 6

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Figure 11. Value of preliminary thoracic aortography. (a) Descending thoracic aortogram shows a tortuous
branch of the right inferior phrenic artery (arrows) that supplies a hypervascular lesion in the right lower lobe.
(b) Selective right inferior phrenic angiogram shows a nonbronchial systemic artery that supplies the hypervas-
cular lesion (arrows) in the right lower lobe. Filling of the pulmonary artery is also seen.

Figure 12. Superselective embolization with a microcatheter. (a) Selective intercostal angiogram shows hy-
pervascular areas and a small amount of pulmonary arterial shunting (open arrow) at the periphery of the left
lower lung field. Note the small radicular artery (solid arrow) that arises from the proximal portion of the inter-
costal artery. (b) Postembolization angiogram shows a microcatheter (arrows) that has been advanced into the
intercostal artery beyond the origin of the radicular artery.

lesions (Fig 11) (49). Although cobra-type curved types of catheters (eg, Simmons-1, headhunter,
catheters are most commonly used for catheter- Yashiro-type) should be prepared for optimal se-
ization of the bronchial artery, several different lection of bronchial arteries. The usefulness of a
microcatheter for selective BAE has been empha-
RG f Volume 22 ● Number 6 Yoon et al 1403

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Figures 13, 14. (13) Systemic artery–pulmonary artery shunt. Right bronchial angiogram demonstrates an en-
larged bronchial artery that supplies a hypervascular lesion in the right upper lobe. There is massive bronchopulmo-
nary shunting with visualization of the branches of the right upper lobar pulmonary arteries (arrows). (14) Systemic
artery–pulmonary vein shunt. Right ICBT angiogram shows a hypervascular staining lesion in the right lower lung as
well as shunting with branches of the right inferior pulmonary vein (arrows).

artery and safe positioning in the bronchial circu-


lation beyond the origin of spinal cord branches,
which prevents severe complications (Fig 12).
After catheterization of the bronchial artery,
bronchial angiography is performed with manual
injection of contrast medium.
Angiographic findings in massive hemoptysis
include hypertrophic and tortuous bronchial ar-
teries, neovascularity, hypervascularity (Figs 3, 5,
10), shunting into the pulmonary artery or vein
(Figs 13, 14), extravasation of contrast medium
(Fig 15), and bronchial artery aneurysm (Fig 16).
Although extravasation of contrast medium is
considered a specific sign of bronchial bleeding,
this finding is rarely seen, and its reported preva-
lence ranges from 3.6% to 10.7% (12,16). Thus,
Figure 15. Contrast material extravasation. Right the determination of which arteries are to be em-
bronchial angiogram shows multifocal hypervascular bolized should be based on a combination of CT,
lesions in the right lung and extravasation of contrast
material into the right lower lobe bronchus (arrow).
bronchoscopic, and angiographic findings with
clinical correlation. All angiograms, including
intercostal arteriograms, must be carefully scruti-
sized in many recent articles (2,3,50,51). This nized for opacification of spinal arteries to avoid
superselective catheterization permits stabiliza- inadvertent embolization.
tion of the catheter position within the bronchial
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Figure 16. Bronchial artery aneurysm. (a) Selective left bronchial angiogram demonstrates a large, hypervascular
lesion in the left upper lobe with an aneurysm (arrow). (b) On an angiogram obtained after embolization with polyvi-
nyl alcohol particles, neither the hypervascular lesion nor the aneurysm is visualized.

Embolic Materials cluded, possibly leading to disastrous complica-


A variety of embolic materials are used for BAE. tions (eg, bronchial, esophageal, pulmonary arte-
Absorbable gelatin sponge is widely used because rial, or aortic wall necrosis) (3). To avoid the
it is inexpensive, easy to handle, and has a con- complications indicated earlier, we recommend
trollable embolic size. However, disadvantages of the use of polyvinyl alcohol particles with a diam-
absorbable gelatin sponge are its resolvability and eter of 350 –500 ␮m for BAE.
lack of radiopacity. Its use may lead to recanaliza- Bronchopulmonary fistula is a common finding
tion of the embolized artery and may sometimes at bronchial angiography in patients with massive
be responsible for recurrent bleeding (50). Polyvi- hemoptysis. Regardless of whether a bronchopul-
nyl alcohol particles are nonabsorbable embolic monary fistula is demonstrated at bronchial an-
materials, and particles 350 –500 ␮m in diameter giography, we perform BAE with the same tech-
are the most frequently used worldwide (51). nique and the same size of embolic materials
Their use may prevent the early recurrence of he- (polyvinyl alcohol particles over 350 ␮m in diam-
moptysis due to recanalization of the embolized eter or absorbable gelatin sponge), and we have
artery, as might be anticipated with absorbable not encountered any clinical problems related to
gelatin sponge. pulmonary infarction or systemic embolization.
It is essential to avoid the use of embolic mate- Thus, we recommend the use of the same strategy
rials that can pass through the bronchopulmonary even when a bronchopulmonary fistula is visual-
anastomosis. Experimental study has demon- ized at bronchial angiography.
strated a bronchopulmonary anastomosis of 325 Liquid embolic agents (eg, isobutyl-2 cyanoac-
␮m in the human lung (52). Pulmonary infarc- rylate, absolute ethanol) are not currently used
tion via bronchial artery–pulmonary artery shunts because of the high risk of severe complications
or systemic artery embolization via bronchial ar- such as tissue necrosis. Stainless steel platinum
tery–pulmonary vein shunts may occur when em- coils are generally not used for BAE because they
bolic agents less than 325 ␮m in diameter are tend to occlude more proximal vessels and may
used. In addition, it is important to avoid using preclude repeat embolization if hemoptysis re-
embolic agents that produce distal occlusion to curs. However, they may be used to occlude a
such an extent that normal peripheral branches pulmonary artery aneurysm and may occasionally
that supply the bronchi, esophagus, or vasa vaso- be used in the internal mammary artery to pre-
rum of the pulmonary artery or aorta become oc- vent embolization of a normal vascular territory
and development of collateral vessels (Fig 17)
(3,53).
RG f Volume 22 ● Number 6 Yoon et al 1405

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Figure 17. Coil embolization. (a) Selective right internal mammary angiogram shows small branches that supply a
hypervascular staining lesion in the right upper lobe, as well as a pseudoaneurysm (arrow). (b) On a postembolization
angiogram obtained after deposition of two coils (arrows) at both the proximal and distal portions of the origin site of
the small branches and use of additional polyvinyl alcohol particles, neither the hypervascular lesion nor the pseudo-
aneurysm is visualized.

Results 103 patients who underwent BAE, 16 patients


Previous studies have shown that BAE is very ef- (15.5%) required repeat embolization; all 16 had
fective in controlling acute massive hemoptysis. hemoptysis due to chronic tuberculosis (56). It is
The initial nonrecurrence rates for BAE have believed that this was due mainly to hypertrophy
been reported to be 73%–98%, with a mean fol- of the collateral nonbronchial systemic arteries. In
low-up period ranging from 1 day to 1 month (7– a series by Katoh et al (55), 75% of patients with
14,54). Immediate success rates have increased aspergilloma experienced recurrence of hemopty-
recently because of the introduction of superse- sis after undergoing initial embolization. Haya-
lective embolization and the refinement of em- kawa et al (11) reported that BAE failed within 1
bolic agents and techniques. However, the long- month in 42% of patients with neoplasm. A neo-
term success rate of BAE in hemoptysis is unfa- plasm receives its blood supply from multiple
vorable. Long-term recurrence rates have been feeder vessels other than the bronchial artery and
reported to be 10%–52%, with a mean follow-up invades the vascular structure aggressively.
period ranging from 1 to 46 months (2,3,55).
However, the long-term success rate can be im- Complications
proved with repeat BAE. Hemoptysis may recur Several complications of BAE have been reported
after successful BAE if the disease process is not in the literature. Chest pain is the most common
controlled with drug therapy or surgery because complication, with a reported prevalence of 24%–
embolization does not address the underlying dis- 91% (12,43,57). Chest pain is likely related to an
ease but rather treats the symptom. In this sense, ischemic phenomenon caused by embolization
BAE is a palliative procedure that prepares the and is usually transient. In addition, dysphagia
patient for elective surgery for localized disease or due to embolization of esophageal branches may
continued antimicrobial therapy (51). be encountered, with a reported prevalence of
Recurrent bleeding may be caused by recan- 0.7%–18.2% (12,57). Dysphagia also regresses
alization of embolized vessels, incomplete em- spontaneously. Subintimal dissection of the aorta
bolization, revascularization by the collateral cir- or the bronchial artery during BAE is the other
culation, inadequate treatment of the underlying minor complication, with a reported prevalence of
disease, progression of basic lung disease, or non- 1%– 6.3% (8,9,11,13,14). There are usually no
bronchial systemic arterial supply (2,3,51,55). symptoms or problems related to the subintimal
Recurrence rate may also be influenced by the dissection.
cause of the hemoptysis. Recurrent bleeding is
more common in patients with chronic tuberculo-
sis, aspergilloma, or neoplasm. In one study of
1406 November-December 2002 RG f Volume 22 ● Number 6

RadioGraphics

Figure 18. Nonbronchial systemic artery. Right sub- Figure 19. Nonbronchial systemic artery. Selective
clavian angiogram shows an enlarged superior thoracic left thyrocervical angiogram shows tortuous branches
artery, lateral thoracic artery, and subscapular artery that supply a hypervascular lesion in the left upper
and numerous small branches from the subclavian and lung, with a pseudoaneurysm (solid arrow) and sys-
axillary arteries that supply a hypervascular lesion in temic artery–pulmonary artery shunting (open arrow).
the right upper lobe, along with systemic artery–pulmo-
nary artery shunting (arrows).

The most disastrous complication of BAE is


spinal cord ischemia due to the inadvertent occlu-
sion of spinal arteries. The prevalence of spinal
cord ischemia after BAE is reported to be 1.4%–
6.5% (12,13,50,58). As discussed earlier, the vi-
sualization of radicular branches on bronchial or
intercostal angiograms is not an absolute contra-
indication for BAE. However, when the anterior
medullary artery (artery of Adamkiewicz) is visu-
alized at angiography, embolization should not be
performed.
Other rare complications that have been re-
ported in the literature include aortic and bron-
chial necrosis, bronchoesophageal fistula, non–
target organ embolization (eg, ischemic colitis),
pulmonary infarction, referred pain to the ipsilat-
eral forehead and orbit, and transient cortical Figure 20. Nonbronchial systemic artery. Selective
blindness (59 – 64). It is hypothesized that cortical right lateral thoracic angiogram shows a hypervascular
blindness develops because of embolism to the lesion with systemic artery–pulmonary artery shunting
occipital cortex, either via a bronchial artery–pul- (arrows) in the periphery of the right upper lobe.
monary vein shunt or via collateral vessels be-
tween the bronchial and vertebral arteries (64). tion of the bronchial artery. Many investigators
have documented that a concerted search for
Nonbronchial nonbronchial systemic arterial supply should be
Systemic Arterial Supply made (3,10,53,56,58). In the presence of pleural
Nonbronchial systemic arteries can be a signifi- thickening, nonbronchial systemic feeder vessels
cant source of massive hemoptysis, especially in that originate from various arteries (eg, intercostal
patients with pleural involvement caused by an artery [Figs 10, 12], branches of the subclavian
underlying disease. Missing the nonbronchial sys- and axillary arteries [Figs 18 –20], internal mam-
temic arteries at initial angiography may result in mary artery [Fig 21], inferior phrenic artery [Fig
early recurrent bleeding after successful emboliza- 11]) (3,10,47,53,55) may develop along the pleu-
ral surface and become enlarged as a result of the
inflammatory process. Pleural thickening that is
RG f Volume 22 ● Number 6 Yoon et al 1407

RadioGraphics

Figure 21. Prediction of nonbronchial systemic arterial supply. (a) Contrast-enhanced CT scan shows irregular
pleural thickening at the left apical thorax with tortuous vascular structures within a hypertrophic extrapleural layer of
fat (arrows). (b) On a left subclavian angiogram, a tortuous, enlarged internal mammary artery (solid arrows) and its
branches are seen to supply a hypervascular lesion in left upper lobe. A hypertrophic lateral thoracic artery (open ar-
rows) also supplies the hypervascular lesion.

Figure 22. Prediction of nonbronchial systemic arterial supply. (a) Contrast-enhanced CT scan demonstrates dif-
fuse pleural thickening at the upper thorax (solid arrows) and tortuous, enhancing vascular structures within a hyper-
trophic extrapleural layer of fat (open arrows). Hypertrophic bronchial arteries are also seen in the aortopulmonary
window. (b) Selective intercostal angiogram shows tortuous hypertrophic vessels with systemic artery–pulmonary
artery shunting (arrows).

noted at chest radiography negatively influences tortuous enhancing vascular structures within
the long-term success rate of BAE (65). CT may hypertrophic extrapleural fat seen at contrast-
help predict the presence of nonbronchial sys- enhanced CT are signs of nonbronchial systemic
temic collateral vessels as a source of bleeding in arterial supply in patients with massive hemopty-
patients with massive hemoptysis. In our experi- sis (Figs 21, 22) (unpublished data). Use of CT
ence, pleural thickening of more than 3 mm and
1408 November-December 2002 RG f Volume 22 ● Number 6

RadioGraphics to predict the presence of nonbronchial systemic 12. Ramakantan R, Bandekar VG, Gandhi MS, Aulakh
vessels that supply a parenchymal lesion is impor- BG, Deshmukh HL. Massive hemoptysis due to pul-
monary tuberculosis: control with bronchial artery
tant prior to BAE because it helps in localizing embolization. Radiology 1996; 200:691– 694.
the site of bleeding and in selecting systemic ves- 13. Mal H, Rullon I, Mellot F, et al. Immediate and long-
sels for the interventional approach. term results of bronchial artery embolization for life-
threatening hemoptysis. Chest 1999; 115:996 –1001.
Conclusions 14. Kato A, Kudo S, Matsumoto K, et al. Bronchial ar-
tery embolization for hemoptysis due to benign dis-
Massive hemoptysis constitutes a significant and eases: immediate and long-term results. Cardiovasc
often life-threatening respiratory emergency. Intervent Radiol 2000; 23:351–357.
Bronchial and nonbronchial systemic artery 15. Jean-Baptiste E. Clinical assessment and manage-
ment of massive hemoptysis. Crit Care Med 2000;
embolization is a safe and effective nonsurgical 28:1642–1647.
treatment for patients with massive hemoptysis. 16. Hsiao EI, Kirsch CM, Kagawa FT, Wehner JH,
Knowledge of bronchial artery anatomy, together Jensen WA, Baxter RB. Utility of fiberoptic bron-
with an understanding of the pathophysiologic choscopy before bronchial artery embolization for
massive hemoptysis. AJR Am J Roentgenol 2001;
features of massive hemoptysis, are essential for 177:861– 867.
performing BAE. The pulmonary artery can be 17. Servois V, Denys A, Silbert A. Mycotic aneurysm of
the source of massive hemoptysis in a minority of the bronchial artery: a rare cause of hemoptysis (let-
cases, and pulmonary arterial disease should be ter). AJR Am J Roentgenol 1992; 159:428.
18. Cearlock JR, Fontaine AB, Urbaneja A, Spigos DG.
considered in cases of recurrent hemoptysis. CT Endovascular treatment of a posttraumatic bronchial
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M. Bronchial artery aneurysm. Ann Thorac Surg
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