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* From the Department of Pulmonary, Critical Care, and Internal Medicine (Drs. Swanson and Prakash) and the Department of Radiology (Drs. Johnson, McKusick, Andrews, and Stanson), Mayo Medical School and Mayo Medical Center, Rochester, MN.
Correspondence to: Karen L. Swanson, DO, Mayo Medical Center, East-18, Mayo Building, 200 First St SW, Rochester, MN 55905; e-mail: swanson.karen{at}mayo.edu
| Abstract |
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Materials and methods: A review of clinical experience to evaluate the demographics, clinical presentation, radiographic studies, bronchoscopy, and complications of bronchial arteriography and BAE at Mayo Medical Center, Rochester, MN, from 1981 to 2000.
Results: Fifty-four patients underwent bronchial arteriography. There were 34 men and 20 women with a mean age of 53 years. Hemoptysis was the most common indication in 53 patients (98%). Hemoptysis was caused by bronchiectasis (9 patients), pulmonary hypertension (9 patients), malignancy (7 patients), mycetoma (7 patients), and other identified causes (14 patients). The cause could not be identified in eight patients. Bronchoscopy was performed in 49 patients (92%), and the results identified the bleeding lobe in 32 patients, lateralized the side of the bleeding in 5 patients, and were not helpful in 12 patients. Bronchial arteriography revealed hypervascularity (45 patients), bronchial artery hypertrophy (17 patients), hypervascularity with shunting (15 patients), dense soft tissue staining (8 patients), vascular abnormalities (7 patients), and extravasation of contrast (1 patient). BAE was attempted in 54 patients, completed in 51 patients, and was unsuccessful in 3 patients. Overall, 72 embolization sessions were performed with a total of 131 arteries embolized, and the average number of arteries embolized per patient was 2.5. Control of hemoptysis was observed in 46 patients (85%) at 1 month. Rebleeding occurred within 30 days in five patients. Eight patients had recurrent hemoptysis that occurred 30 days after the procedure. The complications of embolization included subintimal dissection of a bronchial artery (two patients), bronchial arterial perforation by a guidewire (one patient), and the reflux of embolic material into the aorta without adverse sequelae (one patient).
Conclusions: BAE is a useful therapy to control both acute and chronic hemoptysis. BAE may help to avoid surgery in patients who are not good surgical candidates. Should hemoptysis recur in these patients, repeat embolization can be performed safely.
Key Words: angiography arterial embolization bronchial artery bronchoscopy hemoptysis
| Introduction |
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Herein we describe our experience with 54 patients who underwent bronchial arteriography and bronchial artery embolization (BAE) at Mayo Clinic through 2000. Additionally, we review the demographic characteristics, clinical features, results of imaging techniques, complications related to BAE, and follow-up.
| Materials and Methods |
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| Results |
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The findings of chest roentgenograms, which were performed in all patients, were abnormal in 47 patients (87%). Chest roentgenograms were suggestive of the etiology of hemoptysis in only nine patients (17%). Seven patients had normal chest roentgenogram findings (13%). CT scanning was performed in 44 patients (81%), and the findings were abnormal in all patients. In 31 patients (70%), the findings of CT scans were suggestive of the etiology of hemoptysis, and in 9 patients (20%) they were suggestive of focal hemorrhage. Bronchoscopy was performed prior to angiography in 49 patients (91%). Bronchoscopy identified the bleeding lobe in 32 patients (65%), lateralized the side of bleeding but not the specific lobe in 5 patients (10%), and was not helpful in 12 patients (24%).
Bronchial arteriography was performed in all patients. The findings of angiography included hypervascularity in 45 patients (83%), bronchial artery hypertrophy in 17 patients (31%), hypervascularity with shunting in 15 patients (28%), dense soft tissue staining in 8 patients (15%), vascular abnormalities in 7 patients (13%), and extravasation of contrast into the bronchial lumen in 1 patient (2%). Examples of hypervascularity and hypertrophy of the bronchial arteries before and after coil embolization are shown in Figures 1 and 2 . All available bronchial arteriograms (which were performed in 44 patients) were re-reviewed, and a spinal artery was identified in 9 patients (20%). Five spinal arteries originated from the left side, and four originated from the right side.
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The following agents were used to embolize arteries in our patients: coils, 6 patients; polyvinyl alcohol, 12 patients; coils and polyvinyl alcohol, 25 patients; polyvinyl alcohol and gelatin sponge particles, 6 patients; gelatin sponge particles, 1 patient; and gelatin sponge particles and coils, 1 patient. There was no correlation between rebleeding and the use of any particular agent or the type of embolization performed (proximally with coils alone vs distally with polyvinyl alcohol and/or coils). Of the five patients who developed rebleeding within 30 days, two had been embolized with polyvinyl alcohol alone and three had been embolized with polyvinyl alcohol and coils.
The complications of BAE included subintimal dissection in two patients (4%), arterial perforation by a guidewire in one patient (2%), and reflux of embolic material into the aorta without adverse sequelae in one patient (2%). Pleuritic chest pain postprocedure occurred in two patients (4%), shoulder pain postprocedure in one patient (2%), and transient dysphagia in one patient (2%). One patient developed a groin hematoma at the puncture site.
BAE was successful in controlling hemoptysis immediately in 51 of 54 patients (94%) and at 1 month in 46 patients (85%). Five patients (11%) had recurrent hemoptysis within 1 month of undergoing BAE. Three of these patients died of massive hemoptysis (two patients with bronchogenic carcinoma died 1 and 3 days after undergoing embolization, and one patient with tuberculosis died 10 days after undergoing embolization). One patient with congenital heart disease underwent successful repeat embolization of the right bronchial artery after recanalization had occurred (as well as embolizing the right inferior phrenic and right intercostal arteries that were contributing to the blood supply) and one patient required surgery to remove a mycetoma secondary to massive hemoptysis 1 week after undergoing the BAE. In the three patients (5%) in whom an embolization procedure could not be performed, hemoptysis continued. Of these, one patient died 3 days after the attempted procedure due to massive hemorrhage (malignancy), and the other two patients required surgery (one for the repair of an aorta-to-bronchial fistula at the site of a previous aortic aneurysm repair, and the other for the removal of a mycetoma).
Eight patients had recurrent hemoptysis > 1 month after undergoing BAE. Hemoptysis in two of these patients resolved spontaneously, and in one patient it resolved with antimycobacterial therapy. Two patients developed extensive collateralization requiring embolization of a right bronchial artery and numerous nonbronchial systemic arteries (ie, internal mammary artery, internal phrenic artery, and a left gastric artery). These two patients had ongoing pulmonary inflammation, congenital heart disease, and fibrosing mediastinitis. Coils were used for BAE in one patient, and polyvinyl alcohol and coils were used in the other patient. Three other patients developed recanalization of previously embolized arteries as well as collateralization requiring repeat embolization and embolization of nonbronchial systemic arteries.
Seven patients (13%) underwent surgery, two patients in whom BAE could not be performed, two due to recurrent hemoptysis (one from a congenital hemangioma and one from a mycetoma), two for removal of mycetomas, and one due to a celiac plexus blood supply that could not be embolized.
The follow-up revealed that 17 patients (31%) had died, 4 from massive hemorrhage and the remainder as a result of their disease process. There was no follow-up information available on 19 patients (35%). The remaining 18 patients had follow-up periods ranging from 6 months to 6 years without evidence of recurrent hemoptysis.
| Discussion |
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Bronchial arteriography and embolization were well-tolerated by our patients. An immediate control of bleeding was achieved with embolization in 51 of 54 patients (94%). Our results are similar to those of a study by Mal et al,8 who reported that among 56 patients undergoing attempted embolization procedures for hemoptysis, the immediate control of bleeding was achieved in 43 of 56 patients (77%). Cremaschi et al9 evaluated 209 patients who had been embolized for hemoptysis and noted that immediate control was achieved after BAE in 205 (98%). Rabkin et al10 evaluated 306 patients and found that BAE controlled acute bleeding in 278 (91%). Our results and those of the foregoing studies have shown that BAE is an effective procedure with which to stabilize many patients and to definitively treat some patients with hemoptysis. Table 1 compares our results with those of other studies.
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Saluja et al14 have suggested that coils should not be used for BAE as they cause proximal occlusion and do not allow for repeat embolization if necessary. We agree that coils will prevent repeat embolization of the same artery. However, they do provide a safe, thorough, and proximal occlusion of the artery, which can be difficult to achieve with injectable particles alone. It is still possible to embolize feeding collaterals if rebleeding develops. Polyvinyl chloride and coils provide permanent occlusion, while gelatin sponge particles are considered to provide temporary occlusion.
Hayakawa et al11 have reported two peak times of bleeding recurrence. The first is from 1 to 2 months after the patient undergoes embolotherapy, which may reflect bleeding from nonbronchial systemic arteries that were not previously embolized. Others have noted the control of hemoptysis at 1 month in 51 to 85% of patients and control at > 1 month in 52 to 82% of patients (Table 1) . The second peak for recurrence of hemoptysis is from 1 to 2 years after the patient undergoes embolotherapy. This appears to reflect the recruitment of blood supply and revascularization by the underlying pulmonary inflammation or progression of the underlying disease. Only one of our patients with congenital heart disease developed rebleeding > 1 year after embolization and underwent successful repeat embolization. Recurrent bleeding after embolotherapy may indicate incomplete embolization of the bronchial arteries, the presence of nonbronchial systemic arteries, recanalization of embolized arteries, or collateralization due to continued pulmonary inflammation. In order to eliminate these types of recurrent hemorrhages, it is important to treat the underlying disease condition as well as to perform complete embolization, including the embolization of any systemic arteries that may be contributing to the blood supply.
It is well-documented that bronchial arteries vary significantly in their numbers and sites of origin. More than 70% of bronchial arteries arise from the descending aorta between the levels of the fifth and sixth thoracic vertebrae.15 Based on a study of 150 human cadavers in 1948, Cauldwell et al16 defined four types of anatomic variation. The most common type is that of a single right bronchial artery with two left bronchial arteries (41%). Up to 20% of bronchial arteries may have an aberrant origin (from other systemic arteries), and nearly 10% arise from the anterior surface of the aortic arch or the descending aorta. A spinal artery can originate from a bronchial artery in up to 5% of patients, with right side being more common than the left side. A spinal artery was identified in nine of our patients, with five occurring on the left side and four occurring on the right side.
Significant hemoptysis was the indication for bronchial arteriography in 53 of our patients (98%). Our patients with bronchogenic carcinomas were more likely to have recurrent hemoptysis. This finding is similar to that in the series reported by Hayakawa et al.11 Their 63 patients with neoplasm-induced hemoptysis showed the highest failure rate with the worst long-term results, followed by the inflammation group, the idiopathic group, and the bronchiectatic group. Hirshberg et al17 studied the etiology, evaluation, and outcome of 208 patients with hemoptysis in a tertiary referral hospital. They found that the most common causes of hemoptysis included bronchiectasis (20%), lung cancer (19%), bronchitis (18%), and pneumonia (16%). In contrast, older studies reported tuberculosis as the most common cause of significant hemoptysis. In the series by Remy et al,7 the etiologies of hemoptysis included tuberculosis (34%), bronchiectasis (26%), aspergilloma (18%), pneumoconiosis in coal miners (13%), and bronchogenic carcinoma (3%). Knott-Craig and colleagues18 retrospectively studied 120 patients with hemoptysis and found that the right lung was the source in 62% and the left lung in 38%, with the right upper lobe being the area that was most commonly affected. Our results were similar in that the right lung was the source of bleeding in 33 patients (61%), the left lung was the source in 17 patients (31%), and both lungs were the source in 4 patients (7%). The right upper lobe was also more commonly involved in our patients. Table 2 compares our findings with those of several other series.
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The complication rate for BAE has diminished gradually over the years. During the early phases of selective bronchial arteriography, several patients developed transverse myelitis as a result of the use of nonionic contrast agents, more neurotoxic materials, and the inadvertent embolization of the spinal arteries. To prevent such neurologic complications, superselective BAE is utilized. This refers to embolization of more terminal branches of the arterial tree, beyond the origin of the spinal arteries. In an effort to compare the safety and efficacy of superselective BAE with those of proximal non-superselective embolization, Tanaka and colleagues21 selected 47 patients with hemoptysis. Superselective embolotherapy was performed using a microcatheter inserted into the bronchial artery beyond the spinal or mediastinal branches in 22 patients. In the remaining 25 patients, non-superselective embolization was performed near the origin of the bronchial artery. There were no significant differences between the two groups in the initial or cumulative control of hemoptysis. There were no neurologic complications in the superselective group. One patient in the non-superselective group developed spinal hemiparalysis caused by spinal infarction. The authors concluded that by using superselective embolization distal to the spinal or mediastinal branches, neurologic complications could be avoided and that the embolization may be more effective. This is in contrast to the series by Mal et al,8 who observed the following three episodes of spinal cord complications: Brown-Séquards syndrome, which regressed after 4 months without sequelae; paraparesis with spontaneous regression after 2 weeks; and complete paraplegia without regression. These complications occurred despite good, selective catheterization of the bronchial artery. None of our patients experienced any neurologic sequelae. If a spinal artery arises from a bronchial artery, we will only embolize the bronchial artery if we can achieve a stable distal position well beyond the spinal artery origin.
The complications among our patients were predominantly catheter-related and included subintimal dissection, guidewire perforation, and reflux of embolic agents into the aorta without adverse effects. Transient dysphagia, pleuritic chest pain, shoulder pain, and a groin hematoma also occurred. Ramakantan et al12 evaluated the results of BAE in 140 patients with tuberculosis and documented postprocedure complications in 12 patients, including transient paraparesis in 2 patients, transient dysphagia in 1 patient, and transient left orbital/forehead pain in 9 patients. The patients who developed left orbital/forehead pain only experienced the pain during the injection of gelatin sponge embolic material into the left bronchial artery and did not experience this pain with the injection of saline solution or contrast medium. The authors hypothesized that this may have occurred as referred pain to the ophthalmic and maxillary divisions of the trigeminal nerve via autonomic afferents reacting to the acute distension of the left bronchial artery during the injection of the gelatin sponge. Chest pain lasting up to 36 h developed in 33 of their patients.
The follow-up of our patients revealed that 17 patients (31%) had died, 4 from massive hemorrhage and the remainder as a result of their disease process. There was no follow-up information available on 19 patients (35%), because they did not return after treatment. The remaining 18 patients (33%) had follow-up periods ranging from 6 months to 6 years without evidence of recurrent hemoptysis.
In summary, BAE is a useful therapy to control both acute and chronic hemoptysis. It is important to embolize nonbronchial systemic arteries at the same setting, if they are angiographically shown to be contributing to the blood supply. It is also important to treat the underlying pulmonary process to decrease vascularity and the development of vascular collaterals. BAE may help to avoid surgery in patients who are not good surgical candidates. Should hemoptysis recur in these patients, repeat embolization can be safely performed. If surgery is indicated, BAE can stabilize the patient prior to surgery. Embolization distal to the spinal artery may significantly decrease the number of complications and may allow a more thorough embolization. Bronchoscopy and CT scanning have important contributing roles in delineating the etiology and/or the source of hemoptysis prior to the patient undergoing bronchial artery arteriography. Further studies are needed to determine whether any of the various embolic materials currently available is superior in preventing rebleeding.
| Footnotes |
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Received for publication May 15, 2001. Accepted for publication September 5, 2001.
| References |
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