CLINICAL STUDY
Results of Bronchial Artery Embolization for the Treatment of Hemoptysis Caused by Neoplasm Ignasi Garcia-Olivé, MD, Jose Sanz-Santos, MD, Carmen Centeno, MD, Felipe Andreo, MD, Aida Muñoz-Ferrer, MD, Pere Serra, MD, Jaume Sampere, MD, Josep Maria Michavila, MD, Jordi Muchart, MD, and Juan Ruiz Manzano, MD
ABSTRACT Purpose: To describe experience with bronchial artery embolization (BAE) in a cohort of patients with cancer. Materials and Methods: All consecutive patients with cancer and at least one episode of hemoptysis that required BAE during a 14-year period were included in this observational retrospective review. The endpoints of the study were immediate success, recurrence of hemoptysis, mortality resulting from hemoptysis, and all-cause mortality. Results: Immediate control of bleeding was achieved in 31 of 40 patients (77.5%). Recurrence requiring BAE occurred in eight patients (20%). Cumulative hemoptysis control rate was 0.90 (95% confidence interval [CI], 0.80–1.0) at 1 month and 0.65 (95% CI, 0.44–0.86) at 6 months. Probability of survival was 0.75 (95% CI, 0.62–0.88) at 1 month, 0.42 (95% CI, 0.27–0.57) at 6 months, 0.36 (95% CI, 0.21–0.51) at 12 months, and 0.08 (95% CI, 0.0–0.18) at 3 years. Conclusions: BAE is an effective and safe technique in the treatment of hemoptysis in patients with cancer. Nevertheless, mortality resulting from hemoptysis and recurrence rate are high among these patients secondary to progression of the underlying disease.
ABBREVIATIONS BAE = bronchial artery embolization, CI = confidence interval, PVA = polyvinyl alcohol
Since its first description by Remy et al (1), bronchial artery embolization (BAE) has become an established procedure in the management of massive and recurrent hemoptysis. Its efficacy, safety, and utility have been established (2–12). Although the most common indication for BAE is hemoptysis resulting from benign lung diseases such as bronchiectasis, cystic fibrosis, or tuberculosis, embolization may also be effective in controlling hemoptysis in patients with cancer. Although From Respiratory Service (I.G.-O., J.S.-S., C.C., F.A., A.M.-F., P.S., J.R.M.) and Department of Radiology (J.S., J.M.M., J.M.), Hospital Universitari Germans Trias i Pujol, Carretera del Canyet sn, 08916, Badalona, Barcelona; Fundació Institut d’Investigació en Ciències de la Salut Germans Trias i Pujol (I.G.-O., J.S.-S., F.A., J.R.M.), Badalona, Barcelona; CibeRes–Ciber de Enfermedades Respiratorias (I.G.-O., F.A., J.R.M.), Bunyola, Bunyola, Mallorca; and Department of Medicine (J.R.M.), Universitat Autònoma de Barcelona, Bellaterra, Spain. Received May 6, 2013; final revision received September 26, 2013; accepted September 27, 2013. Address correspondence to I.G.-O.; E-mail: [email protected] None of the authors have identified a conflict of interest. & SIR, 2014 J Vasc Interv Radiol 2014; 25:221–228 http://dx.doi.org/10.1016/j.jvir.2013.09.017
BAE is routinely performed in patients with hemoptysis secondary to neoplasm, several studies have reported that BAE in patients with lung cancer is associated with a high failure rate (4,10) and increased mortality (13). Nevertheless, the few studies that have focused exclusively on patients with hemoptysis secondary to malignancy have reported better results (14–16). The aim of this study was to report our experience with BAE in a consecutive group of patients with cancer and hemoptysis that required BAE and to evaluate retrospectively the efficacy and safety of the technique.
MATERIALS AND METHODS Patient Population This observational retrospective study comprised patients presenting with life-threatening or persisting hemoptysis who underwent BAE at Hospital Universitari Germans Trias i Pujol, a tertiary-care hospital in Badalona, Spain. Life-threatening hemoptysis was defined as bleeding amounting to 200 mL during 24 hours, 100 mL daily during at least 3 days, or minor bleeding with hemodynamic instability. All consecutive patients with at least
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one episode of hemoptysis that required BAE during a 14-year period (January 1999 to December 2012) with a histologically confirmed diagnosis of either primary lung cancer or extrapulmonary cancer with pulmonary metastases were included. The clinical records were reviewed, and the following data were collected for analysis: age, sex, diagnosis, BAE findings, and time period between embolizations in case of recurrence. Written informed consent was obtained from patients before embolization. The research protocol was approved by the regional ethics committee (Ethics Committee for Clinical Research of the Hospital Universitari Germans Trias i Pujol).
BAE According to our institution protocol, platelet count, international normalized ratio, and activated partial thromboplastin time were reviewed before angiography, and any coagulation disorders were corrected before the procedure. No patient was coagulopathic at the time of angiography. No other therapeutic measures were attempted before BAE. All procedures were performed by one of two interventional radiologists with 4 10 years of experience. The choice of catheter, microcatheter, and embolization materials was made at the discretion of the operating physician. BAE was performed using the Seldinger technique via the femoral approach except in one patient in whom BAE was performed via a brachial approach owing to extreme tortuosity of the supraaortic trunks. A descending thoracic aortogram was obtained at the beginning of the procedure, followed by selective catheterization of bronchial arteries using various shaped 4-F (Cobra 2, Radiofocus Glidecath; Terumo, Somerset, New Jersey) and 5-F angiographic catheters (Pigtail, Imager II; Boston Scientific, Natick, Massachusetts; Amplatz Left 2 Performa; Merit Medical, South Jordan, Utah). If no abnormal bronchial arteries were identified, nonbronchial systemic arteries were selectively catheterized, depending on the known site of pulmonary disease (assessed by x-ray, computed tomography (CT) scan, or diagnostic bronchoscopy). Target vessels were superselectively catheterized using a 3-F coaxial microcatheter system (Progreat; Terumo) if stable cannulation could not be achieved or if more distal cannulation of the vessel was required to avoid important side branches, such as the anterior spinal artery. The embolic material used was nonspherical polyvinyl alcohol (PVA) particles (Contour; Boston Scientific) (years 1999–2008) or gelatin crosslinked acryl microspheres (Bead Block; Biocompatibles, Farnham, Surrey, United Kingdom) (years 2009–2012) for proximal vessels and metal coils (VortX 18 Diamond; Boston Scientific) for proximal and larger arteries (especially when pseudoaneurysms in the bronchial arteries or arteriovenous malformations were present, which occurred in two patients). Embolization was performed of all abnormal vessels supplying the area of interest if technically possible. If there was no detectable underlying
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pulmonary abnormality, embolization was performed of all bronchial arteries on the side of the tumor that could be catheterized. Embolization was performed to complete stasis. Contraindications to embolization were visualization of the anterior spinal branch (if it was not possible to advance the catheter beyond this point) and catheter instability. Pulmonary angiography was not routinely performed. No embolizations were performed by using coils alone. Of the 40 embolization procedures, 23 (57.5%) were performed by using PVA particles alone. The size of PVA particles ranged from 300–500 μm (n = 12) and 500– 700 μm (n = 11). Of the 40 embolization procedures, 16 (40%) were performed by using microspheres alone. The size of the microspheres ranged from 300–500 μm (n = 10) and 500–700 μm (n = 4). In two procedures, a combination of microspheres 300–500 μm and 500–700 μm was used. In one procedure, a combination of microspheres 300–500 μm and PVA particles 300–500 μm was used.
Data Analysis The endpoints of this study were immediate success of the procedure, recurrence of hemoptysis, mortality secondary to hemoptysis, and all-cause mortality. Immediate success was defined as cessation of hemoptysis during the same admission, whereas failure was indicated by continued or recurrent hemoptysis during the same admission. Recurrence was defined as an episode of life-threatening hemoptysis or persisting hemoptysis requiring BAE in a patient with a previous BAE performed. Indications for BAE in recurring hemoptysis were the same as for the initial bleeding event (bleeding of 200 mL during 24 hours, 100 mL daily during at least 3 days, or minor bleeding with hemodynamic instability). Patient status at the end of the follow-up period was thoroughly investigated, including a review of hospital and outpatient medical records, computerized databases, and telephone contact with the patient or family members or primary care physician when necessary. When a patient died, the date of death was obtained from hospital medical records, if he or she died in the hospital, or from official death certificates.
Statistical Analysis The statistical package SPSS, version 19.0 (SPSS, Inc, Chicago, Illinois), was used for statistical analysis. All data were tabulated as mean and standard deviation in the case of quantitative variables and as absolute numbers and percentages in the case of qualitative variables. Survival curves for the groups were constructed according to the Kaplan-Meier method. Survival curves were compared using the log-rank test.
RESULTS During the study period, 40 patients with life-threatening hemoptysis secondary to neoplastic disease were
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included. Characteristics of the patients are summarized in Table 1. Histology and staging of patients with primary lung cancer are summarized in Table 2. Results of complementary examinations are presented in Table 3. All patients underwent embolization. No major complications, according to the Society of Interventional Radiology (SIR) definitions, occurred (17). There were no complications such as spinal cord ischemia, transient pleurisy, or groin hematoma.
Histology Squamous cell carcinoma Adenocarcinoma
12 (35.3%) 10 (29.4%)
Non–small cell lung cancer
4 (11.8%)
Small cell carcinoma Poorly differentiated carcinoma
2 (5.9%) 2 (5.9%)
Large cell carcinoma Unknown Staging
Immediate Control of Hemoptysis Immediate arrest of hemoptysis was achieved in 31 (77.5%) of 40 patients who underwent BAE. BAE failed to control bleeding in nine (22.5%) patients. Seven of these patients died of hemoptysis within 4 weeks of the procedure, and two underwent successful repeat embolization. Table 1 . Characteristics of 40 Patients Included in the Study Age (y) Mean (SD)
Table 2 . Histology and Staging of 34 Patients with Primary Lung Cancer
1 (2.9) 3 (8.8%)
IA
1 (2.9%)
IIA IIB
4 (11.8%) 2 (5.9%)
IIIA
5 (14.7%)
IIIB IV
6 (17.6%) 13 (38.2%)
Unknown
3 (8.8%)
Values are number (percentage). Table 3 . Complementary Examinations
62.8 (11.7) Imaging
Sex Male Female
34 (85%) 6 (15%)
Smoker Never Former
9 (22.5%) 22 (55.0%)
Current
9 (22.5%)
Hemoptysis volume (mL) Mean (SD)
241 (162)
Lung Breast
34 (85%) 2 (5.0%)
Colon
1 (2.5%)
Choriocarcinoma Sarcoma
1 (2.5%) 1 (2.5%)
Hypernephroma
1 (2.5%)
Yes Radiotherapy dose (Gy) Mean (SD)
10 (25%)
CT scan None
24 (60.0%) 6 (15.0%)
Imaging findings Normal Pulmonary nodule Multiple pulmonary nodules
Primary cancer
Previous radiotherapy No
Chest x-ray
Pulmonary mass Ground glass None Great intrathoracic vessels affected CT No Yes Bronchoscopy No Yes
27 (67.5%) 13 (32.5%)
Bronchoscopy findings Blood Tumor
49.1 (18.4)
2 (5.0%) 4 (10.0%) 4 (10.0%) 23 (57.5%) 1 (2.5%) 6 (15.0%) 20 (83.3%) 4 (16.7%) 20 (50.0%) 20 (50.0%) 10 (50.0%) 10 (50.0%)
Values are number (percentage).
Recurrence No Yes 1 recurrence 2 recurrences Mortality from hemoptysis No Yes All-cause mortality
32 (80.0%) 8 (20.0%) 6 (15.0%) 2 (5.0%) 28 (70.0%) 12 (30.0%)
No
6 (15%)
Yes
34 (85%)
Values are number (percentage) unless otherwise indicated. SD ¼ standard deviation.
Recurrence and Angiographic Findings Cumulative survival free of recurrence is shown in Figure 1. Probability of surviving free of recurrence at 1 month was 0.90 (95% confidence interval [CI], 0.80–1.0). Probability of surviving free of recurrence at 6 months was 0.65 (95% CI, 0.44–0.86). Recurring hemoptysis that required further BAE occurred in eight patients. Characteristics of patients with hemoptysis recurrence after BAE and characteristics of the procedures are presented in Table 4. Two of these eight patients required more than one procedure to achieve control of the bleeding. Recurrence occurred within 1
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Figure 1. Cumulative hemoptysis control rate.
month after the first episode in six cases (75%). Four of the patients who underwent repeat embolization procedures had previous radiotherapy.
Mortality Secondary to Hemoptysis Death as a result of hemoptysis occurred in 12 (30%) patients. Eight (66.7%) patients died within the first month after the episode. Three of four (75%) patients with invasion of thoracic great vessels as visualized by CT scan died as a result of massive hemoptysis despite BAE (range, 2–21 days). Probability of not dying as a result of hemoptysis at 1 month and at 6 months was 0.77 (95% CI, 0.64–0.90) and 0.68 (95% CI, 0.52–0.85). No patient presented with fatal hemoptysis after 8 months of follow-up.
All-Cause Mortality There were 28 (70%) patients who died as a result of etiologies other than hemoptysis. There were 12 deaths attributed to progression of neoplastic disease, 4 attributed to pneumonia, 3 attributed to cerebral hemorrhage, and 3 attributed to myocardial infarction. The cause of death was unavailable for six (15%) patients. Cumulative survival is shown in Figure 2. Probability of surviving was 0.75 (95% CI, 0.62–0.88) at 1 month, 0.42 (95% CI, 0.27–0.57) at 6 months, 0.36 (95% CI, 0.21–0.51) at 12 months, and 0.08 (95% CI, 0.0–0.18) at 3 years. Survival curve for patients who had previously received radiation therapy was not statistically significant
compared with patients with no previous history of radiotherapy (P ¼ .67). For the 34 patients with primary lung cancer, the mean overall survival was 14.2 months (95% CI, 7.41–21.03); the mean overall survival for the 6 patients with extrapulmonary primary cancer was 10.1 months (95% CI, 3.25–17.01). Difference in survival between the two groups was not statistically significant (P ¼ .83).
Imaging Findings The vessels interrogated at diagnostic angiography included the bronchial arteries (n ¼ 48), various intercostal arteries (n ¼ 37), internal mammary arteries (n ¼ 4), and lateral thoracic artery (n ¼ 1). Angiographic findings (Figs 3, 4) included active extravasation (17.5%; 5 of 40 cases), tumor blush (90%; 36 of 40 cases), bronchial artery enlargement (62.5%; 25 of 40 cases), bronchial artery tortuosity (40%; 16 of 40 cases), and arteriovenous fistula (2.5%, 1 of 40 cases). Three (7.5%) of the cases manifested with a single abnormality: enlarged bronchial artery (n = 2) and arteriovenous fistula (n = 1). There were no differences in immediate success of BAE or mortality according to angiographic findings or arteries involved.
DISCUSSION Our data demonstrate that BAE is an effective and safe technique in the treatment of hemoptysis in patients with
1.1 5.4
1.0
6 7
8
AVF ¼ arteriovenous fistula, BAE ¼ bronchial artery embolization, BBT ¼ bibronchial trunk, LBA ¼ left bronchial artery, NSCLC ¼ non–small cell lung cancer, PVA ¼ polyvinyl alcohol, RBA ¼ right bronchial artery, RICBT ¼ right intercostobronchial trunk, RLTA ¼ right lateral thoracic artery, RT ¼ radiotherapy. n Fed by segmental artery. † Pulmonary artery involved.
None† BBT Yes Microspheres and coils Yes IIIB
7.7 5
Lung (squamous)
RLTA BBT
RBA LBA
RICBT, BBT AVF* Yes Yes
Yes Microspheres
Microspheres and coils Coils Yes No
Yes IV
IIA
5.6 1.4
Lung (squamous) Choriocarcinoma
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Lung (NSCLC)
BBT BBT RICBT, LBA LBA No No PVA PVA Yes No Unknown
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Lung (NSCLC) Breast
LBA
LBA LBA No PVA No IIA
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Sarcoma
Lung (squamous)
First BAE
BBT, RICBT No PVA
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0.9
Death Caused
by Hemoptysis Material Used at BAE Previous RT
Staging
(Lung Cancer) Diagnosis
Recurrence after
BAE (mo) Case No.
Table 4 . Cases of Hemoptysis Recurrence after BAE
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No
Second BAE
Number 2
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cancer. Immediate control of bleeding was achieved in most patients. Recurrence requiring BAE occurred in 20% of patients. Hemoptysis in patients with cancer generally occurs secondary to local necrosis and inflammation of blood vessels within the tumor bed, rather than direct tumor invasion of blood vessels (18). In these patients, the tumors feeding bronchial arteries are extended and enlarged (19). BAE has become a common first-line therapy for life-threatening hemoptysis. Although most previous studies have focused on patients with hemoptysis secondary to benign lung diseases, such as bronchiectasis, tuberculosis, and aspergilloma, some of these series included patients with lung cancer in their analysis (4,13). These studies showed that BAE in patients with lung cancer was associated with a high failure rate (4) and increased mortality (18), even though angiographic findings in tumor-related bleeding were not significantly different from findings in benign causes of hemoptysis (15,16). However, studies exclusively in patients with hemoptysis secondary to malignancy showed better results (14–16). Witt et al (14) described their experience with BAE using platinum coils in patients with tumorous pulmonary bleeding. They prospectively studied 30 patients with lung cancer who underwent BAE and compared their results with 15 patients with moderate hemoptysis secondary to lung cancer who had been treated conventionally. These authors found that the mean survival time was significantly lower in the control group than in the BAE group. Park et al (15) included in their analysis 19 patients with a diagnosis of primary lung cancer who underwent BAE. They concluded that BAE was an effective technique in the treatment of hemoptysis in patients with lung cancer. Wang et al (16) studied 30 patients with a diagnosis of either lung cancer or pulmonary metastases from extrathoracic disease. They concluded that BAE was safe and effective, especially in patients with cancer in which bleeding was secondary to a benign cause and not related to the tumor. To the best of our knowledge, our series is among the largest analyzing the results of BAE in patients with hemoptysis resulting solely from malignancy and shows results similar to previous studies. Immediate control of bleeding was achieved 77.5% of patients. Although immediate success is defined differently in each article, it ranges from 79%–100% (15,16). Recurrence occurred in 20% of patients in our series, whereas in previous studies it ranged from 26%–53% (14,16). In our series, the mean overall survival for the 34 patients with primary lung cancer was 14.2 months. Wang et al (16) described a median overall survival time of 5.5 months. In the study by Witt et al (14), the mean survival time of patients with BAE treatment was 139 days. In our series, survival rate was 0.75 at 1 month, 0.42 at 6 months, 0.36 at 12 months, and 0.08 at 3 years. In the series by Wang et al, survival rate was 0.70 at 1 month, 0.25 at
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Figure 2. Cumulative survival (all cause mortality).
12 months, and 0.087 at 3 years. In the series by Witt et al, survival rate was 0.71 at 15 days and 0.28 at 6 months. Our study, with a large number of patients and a long follow-up period, shows that BAE is useful in the management of hemoptysis related to malignancy. It is also the first study that differentiates mortality secondary to hemoptysis from all-cause mortality. Wang et al (16) analyzed the effect of previous radiotherapy on the outcome of the technique. They found that the survival of patients who had previously received radiation therapy was not statistically significant compared with patients with no prior history of radiation therapy. In our group, we did not find differences in survival between patients who had received radiotherapy and patients who had not. Also, Wang et al (16) compared the results of BAE performed for hemoptysis related to tumor and not related to tumor (16). In our series all patients had tumor-related hemoptysis, so we did not perform this analysis. Apart from BAE, other interventional procedures, such as bronchoscopic techniques or palliative thoracic radiotherapy, can also be used. Several bronchoscopic treatments have been described for the treatment of lifethreatening hemoptysis in patients with lung cancer. Endoscopic methods include cold saline lavage, instillation of topical vasoconstrictive agents or fibrinogenthrombin, balloon or stent tamponade, endobronchial airway blockade, laser therapy, argon plasma coagulation, and electrocautery (20). In our series, 10 patients had
Figure 3. Selective bibronchial trunk arteriography (arrow) of a 79-year-old man with a pulmonary mass in the left lower lobe and hemoptysis. Embolization with microspheres was successfully performed. The patient died 13 days after the procedure because of acute respiratory failure and pneumonia.
endobronchial lesions. Only 25% of our patients would have benefited from endoscopic treatment of hemoptysis. None of these bronchoscopic techniques were attempted in our patients. No patient received palliative thoracic radiotherapy in our series. Causes for recurrent bleeding include progression of underlying disease; recanalization or revascularization; incomplete embolization; and emergence of other blood
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Figure 4. (a, b) Selective catheterization of an intercostobronchial trunk with hypervascularity in the intercostal artery (a and b, arrow) and right bronchial artery (a, arrowhead) in a 53-year-old man with a right pulmonary mass and hemoptysis. Embolization with microspheres and one coil was successfully performed. The patient was alive 10 months after the procedure.
supply to the affected area, such as from systemic collaterals (21). Early rebleeding has been related to incomplete embolization, whereas late rebleeding is generally due to disease progression (2,4,7,9). GarciaOlivé et al (22) reported more recently that recurring hemoptysis secondary to recanalization was related to time to recurrence but not to use of coils, number of arteries that received embolization, or neoplastic etiology. More specifically, we found that the artery that received embolization in the first 80 weeks after the first procedure would be a different one in most cases (suggesting incomplete embolization), whereas the artery that received embolization after 80 weeks would be the same as in the previous procedure in most cases (suggesting recanalization) (22). Our series included hemoptysis secondary to many conditions, including benign and malignant conditions. In our study, the artery that received embolization in the second procedure was a different one in seven of the eight patients with recurring hemoptysis, which may suggest incomplete embolization or emergence of other supply to the affected area. The small size of the sample did not allow us to compare the results between different agents. Multidetector CT has a role in the identification of the bronchial and nonbronchial arteries causing hemoptysis and improves the results of BAE (23–25). In our series, 6 (15%) patients had no imaging before BAE, and only 60% had a CT scan performed before the procedure. All six patients with no imaging were included in the study before 2004. Since then, our institution protocol for the management of life-threatening hemoptysis has changed, and it is now mandatory to perform a CT scan before BAE except when there is hemodynamic instability or extremely rapid bleeding. We have not seen any severe treatment-related complications. Likewise, Witt et al (14) did not report any complications. However, Park et al (15) described two minor complications (one episode of transient chest pain
and one puncture site hematoma), and Wang et al (16) described two minor complications (two cases of vessel dissection) and one spinal cord infarction. There are several limitations to this study. First, the sample size is small. Second, this is a retrospective study, with embolization procedures performed by different operators using different tools and embolic agents. Finally, there is no control group with which compare the results. In conclusion, BAE is an effective and safe technique in the treatment of hemoptysis in patients with oncologic disease. Nevertheless, mortality secondary to hemoptysis and recurrence are high among these patients, most likely resulting from progression of the underlying disease.
REFERENCES 1. Remy J, Voisin C, Ribet M, et al. Treatment, by embolization, of severe or repeated hemoptysis associated with systemic hypervascularization. Nouv Presse Med 1973; 2:2060 [in French]. 2. Rabkin JE, Astafjev VI, Gothman LN, Grigorjev Y. Transcatheter embolization in the management of pulmonary haemorrhage. Radiology 1987; 163:361–365. 3. Katoh O, Kishikawa T, Yamada H, Matsumoto S, Kudo S. Recurrent bleeding alter arterial embolization in patients with hemoptysis. Chest 1990; 97:541–546. 4. Hayakawa K, Tanaka F, Torizuka T, et al. Bronchial artery embolization for hemoptysis: immediate and long-term results. Cardiovasc Intervent Radiol 1992; 15:154–159. 5. Ramakantan R, Bandekar VG, Gandhi MS, Aulakh BG, Deshmukh HL. Massive hemoptysis due to pulmonary tuberculosis: control with bronchial artery embolization. Radiology 1996; 200:691–694. 6. Brinson GM, Noone PG, Mauro MA, et al. Bronchial artery embolization for the treatment of hemoptysis in patients with cystic fibrosis. Am J Respir Crit Care Med 1998; 157:1951–1958. 7. Mal H, Rullon I, Mellot F, et al. Immediate and long-term results of bronchial artery embolization for life-threatening hemoptysis. Chest 1999; 115:996–1001. 8. Osaki S, Nakanishi Y, Wataya H, et al. Prognosis of bronchial artery embolization in the management of hemoptysis. Respiration 2000; 67: 412–416. 9. Kato A, Kudo S, Matsumoto K, et al. Bronchial artery embolization for hemoptysis due to benign diseases: immediate and long-term results. Cardiovasc Intervent Radiol 2000; 23:351–357. 10. Swanson KL, Johnson M, Prakash UBS, McKusick MA, Andrews JC, Stanson AW. Bronchial artery embolization. Experience with 54 patients. Chest 2002; 121:789–795.
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11. Kim YG, Yoon HK, Ko GY, Lim CM, Kim WD, Koh Y. Long-term effect of bronchial artery embolization in Korean patients with haemoptysis. Respirology 2006; 11:776–781. 12. Chun JY, Belli AM. Immediate and long-term outcomes of bronchial and non-bronchial systemic artery embolisation for the management of haemoptysis. Eur Radiol 2010; 20:558–565. 13. Fartoukh M, Khoshnood B, Parrot A, et al. Early prediction of in-hospital mortality of patients with hemoptysis: an approach to defining sever hemoptysis. Respiration 2012; 83:106–114. 14. Witt CH, Schmidt B, Geisler A, et al. Value of bronchial artery embolisation with platinum coils in tumorous pulmonary bleeding. Eur J Cancer 2000; 36:1949–1954. 15. Park HS, Kim YI, Kim HY, Zo JI, Lee JH, Lee JS. Bronchial artery and systemic artery embolization in the management of primary lung cancer in patients with hemoptysis. Cardiovasc Intervent Radiol 2007; 30: 638–643. 16. Wang GR, Ensor JE, Gupta S, Hicks ME, Tam AL. Bronchial artery embolization for the management of hemoptysis in oncology patients: utility and prognostic factors. J Vasc Interv Radiol 2009; 20:722–729. 17. Angle JF, Siddiqi NH, Wallace MJ, et al. Quality improvement guidelines for percutaneous transcatheter embolization. Society of Interventional Radiology standards of practice committee. J Vasc Interv Radiol 2010; 21:1479–1486.
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18. Winter SM, Ingbar DH. Massive hemoptysis: pathogenesis and management. J Intens Care Med 1988; 3:171–188. 19. Newton TH, Preger L. Selective bronchial arteriography. Radiology 1965; 84:1043–1051. 20. Gompelmann D, Eberhardt R, Herth FJF. Advanced malignant lung disease: what the specialist can offer. Respiration 2011; 82:111–123. 21. Yoon W, Kyu Kim J, Hyun Kim Y, Woong Chung T, Keun Kang H. Bronchial and nonbronchial systemic artery embolization for life threatening hemoptysis: a comprehensive review. Radiographics 2002; 22:1395–1409. 22. Garcia-Olivé I, Sanz-Santos J, Centeno C, et al. Predictors of recanalization in patients with life-threatening hemoptysis requiring artery embolization. Arch Bronconeumol 2013; pii: S0300-2896(13)00188-9. 23. Yoon YC, Lee KS, Jeong YJ, Shin SW, Chung MJ, Kwon OJ. Hemoptysis: bronchial and nonbronchial systemic arteries at 16-detector row CT. Radiology 2005; 234:292–298. 24. Mori H, Ohno Y, Tsuge Y, et al. Use of multidetector row CT to evaluate the need for bronchial arterial embolization in hemoptysis patients. Respiration 2010; 80:24–31. 25. Hayes D Jr, Winkler MA, Kirkby S, Capasso P, Mansour HM, Attili AK. Preprocedural planning with prospectively triggered multidetector row CT angiography prior to bronchial artery embolization in cystic fibrosis patients with massive hemoptysis. Lung 2012; 190:221–225.
Results of Bronchial Artery Embolization for the Treatment of Hemoptysis Caused by Neoplasm Ignasi Garcia-Olivé, MD, Jose Sanz-Santos, MD, Carmen Centeno, MD, Felipe Andreo, MD, Aida Muñoz-Ferrer, MD, Pere Serra, MD, Jaume Sampere, MD, Josep Maria Michavila, MD, Jordi Muchart, MD, and Juan Ruiz Manzano, MD
ABSTRACT Purpose: To describe experience with bronchial artery embolization (BAE) in a cohort of patients with cancer. Materials and Methods: All consecutive patients with cancer and at least one episode of hemoptysis that required BAE during a 14-year period were included in this observational retrospective review. The endpoints of the study were immediate success, recurrence of hemoptysis, mortality resulting from hemoptysis, and all-cause mortality. Results: Immediate control of bleeding was achieved in 31 of 40 patients (77.5%). Recurrence requiring BAE occurred in eight patients (20%). Cumulative hemoptysis control rate was 0.90 (95% confidence interval [CI], 0.80–1.0) at 1 month and 0.65 (95% CI, 0.44–0.86) at 6 months. Probability of survival was 0.75 (95% CI, 0.62–0.88) at 1 month, 0.42 (95% CI, 0.27–0.57) at 6 months, 0.36 (95% CI, 0.21–0.51) at 12 months, and 0.08 (95% CI, 0.0–0.18) at 3 years. Conclusions: BAE is an effective and safe technique in the treatment of hemoptysis in patients with cancer. Nevertheless, mortality resulting from hemoptysis and recurrence rate are high among these patients secondary to progression of the underlying disease.
ABBREVIATIONS BAE = bronchial artery embolization, CI = confidence interval, PVA = polyvinyl alcohol
Since its first description by Remy et al (1), bronchial artery embolization (BAE) has become an established procedure in the management of massive and recurrent hemoptysis. Its efficacy, safety, and utility have been established (2–12). Although the most common indication for BAE is hemoptysis resulting from benign lung diseases such as bronchiectasis, cystic fibrosis, or tuberculosis, embolization may also be effective in controlling hemoptysis in patients with cancer. Although From Respiratory Service (I.G.-O., J.S.-S., C.C., F.A., A.M.-F., P.S., J.R.M.) and Department of Radiology (J.S., J.M.M., J.M.), Hospital Universitari Germans Trias i Pujol, Carretera del Canyet sn, 08916, Badalona, Barcelona; Fundació Institut d’Investigació en Ciències de la Salut Germans Trias i Pujol (I.G.-O., J.S.-S., F.A., J.R.M.), Badalona, Barcelona; CibeRes–Ciber de Enfermedades Respiratorias (I.G.-O., F.A., J.R.M.), Bunyola, Bunyola, Mallorca; and Department of Medicine (J.R.M.), Universitat Autònoma de Barcelona, Bellaterra, Spain. Received May 6, 2013; final revision received September 26, 2013; accepted September 27, 2013. Address correspondence to I.G.-O.; E-mail: [email protected] None of the authors have identified a conflict of interest. & SIR, 2014 J Vasc Interv Radiol 2014; 25:221–228 http://dx.doi.org/10.1016/j.jvir.2013.09.017
BAE is routinely performed in patients with hemoptysis secondary to neoplasm, several studies have reported that BAE in patients with lung cancer is associated with a high failure rate (4,10) and increased mortality (13). Nevertheless, the few studies that have focused exclusively on patients with hemoptysis secondary to malignancy have reported better results (14–16). The aim of this study was to report our experience with BAE in a consecutive group of patients with cancer and hemoptysis that required BAE and to evaluate retrospectively the efficacy and safety of the technique.
MATERIALS AND METHODS Patient Population This observational retrospective study comprised patients presenting with life-threatening or persisting hemoptysis who underwent BAE at Hospital Universitari Germans Trias i Pujol, a tertiary-care hospital in Badalona, Spain. Life-threatening hemoptysis was defined as bleeding amounting to 200 mL during 24 hours, 100 mL daily during at least 3 days, or minor bleeding with hemodynamic instability. All consecutive patients with at least
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one episode of hemoptysis that required BAE during a 14-year period (January 1999 to December 2012) with a histologically confirmed diagnosis of either primary lung cancer or extrapulmonary cancer with pulmonary metastases were included. The clinical records were reviewed, and the following data were collected for analysis: age, sex, diagnosis, BAE findings, and time period between embolizations in case of recurrence. Written informed consent was obtained from patients before embolization. The research protocol was approved by the regional ethics committee (Ethics Committee for Clinical Research of the Hospital Universitari Germans Trias i Pujol).
BAE According to our institution protocol, platelet count, international normalized ratio, and activated partial thromboplastin time were reviewed before angiography, and any coagulation disorders were corrected before the procedure. No patient was coagulopathic at the time of angiography. No other therapeutic measures were attempted before BAE. All procedures were performed by one of two interventional radiologists with 4 10 years of experience. The choice of catheter, microcatheter, and embolization materials was made at the discretion of the operating physician. BAE was performed using the Seldinger technique via the femoral approach except in one patient in whom BAE was performed via a brachial approach owing to extreme tortuosity of the supraaortic trunks. A descending thoracic aortogram was obtained at the beginning of the procedure, followed by selective catheterization of bronchial arteries using various shaped 4-F (Cobra 2, Radiofocus Glidecath; Terumo, Somerset, New Jersey) and 5-F angiographic catheters (Pigtail, Imager II; Boston Scientific, Natick, Massachusetts; Amplatz Left 2 Performa; Merit Medical, South Jordan, Utah). If no abnormal bronchial arteries were identified, nonbronchial systemic arteries were selectively catheterized, depending on the known site of pulmonary disease (assessed by x-ray, computed tomography (CT) scan, or diagnostic bronchoscopy). Target vessels were superselectively catheterized using a 3-F coaxial microcatheter system (Progreat; Terumo) if stable cannulation could not be achieved or if more distal cannulation of the vessel was required to avoid important side branches, such as the anterior spinal artery. The embolic material used was nonspherical polyvinyl alcohol (PVA) particles (Contour; Boston Scientific) (years 1999–2008) or gelatin crosslinked acryl microspheres (Bead Block; Biocompatibles, Farnham, Surrey, United Kingdom) (years 2009–2012) for proximal vessels and metal coils (VortX 18 Diamond; Boston Scientific) for proximal and larger arteries (especially when pseudoaneurysms in the bronchial arteries or arteriovenous malformations were present, which occurred in two patients). Embolization was performed of all abnormal vessels supplying the area of interest if technically possible. If there was no detectable underlying
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pulmonary abnormality, embolization was performed of all bronchial arteries on the side of the tumor that could be catheterized. Embolization was performed to complete stasis. Contraindications to embolization were visualization of the anterior spinal branch (if it was not possible to advance the catheter beyond this point) and catheter instability. Pulmonary angiography was not routinely performed. No embolizations were performed by using coils alone. Of the 40 embolization procedures, 23 (57.5%) were performed by using PVA particles alone. The size of PVA particles ranged from 300–500 μm (n = 12) and 500– 700 μm (n = 11). Of the 40 embolization procedures, 16 (40%) were performed by using microspheres alone. The size of the microspheres ranged from 300–500 μm (n = 10) and 500–700 μm (n = 4). In two procedures, a combination of microspheres 300–500 μm and 500–700 μm was used. In one procedure, a combination of microspheres 300–500 μm and PVA particles 300–500 μm was used.
Data Analysis The endpoints of this study were immediate success of the procedure, recurrence of hemoptysis, mortality secondary to hemoptysis, and all-cause mortality. Immediate success was defined as cessation of hemoptysis during the same admission, whereas failure was indicated by continued or recurrent hemoptysis during the same admission. Recurrence was defined as an episode of life-threatening hemoptysis or persisting hemoptysis requiring BAE in a patient with a previous BAE performed. Indications for BAE in recurring hemoptysis were the same as for the initial bleeding event (bleeding of 200 mL during 24 hours, 100 mL daily during at least 3 days, or minor bleeding with hemodynamic instability). Patient status at the end of the follow-up period was thoroughly investigated, including a review of hospital and outpatient medical records, computerized databases, and telephone contact with the patient or family members or primary care physician when necessary. When a patient died, the date of death was obtained from hospital medical records, if he or she died in the hospital, or from official death certificates.
Statistical Analysis The statistical package SPSS, version 19.0 (SPSS, Inc, Chicago, Illinois), was used for statistical analysis. All data were tabulated as mean and standard deviation in the case of quantitative variables and as absolute numbers and percentages in the case of qualitative variables. Survival curves for the groups were constructed according to the Kaplan-Meier method. Survival curves were compared using the log-rank test.
RESULTS During the study period, 40 patients with life-threatening hemoptysis secondary to neoplastic disease were
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included. Characteristics of the patients are summarized in Table 1. Histology and staging of patients with primary lung cancer are summarized in Table 2. Results of complementary examinations are presented in Table 3. All patients underwent embolization. No major complications, according to the Society of Interventional Radiology (SIR) definitions, occurred (17). There were no complications such as spinal cord ischemia, transient pleurisy, or groin hematoma.
Histology Squamous cell carcinoma Adenocarcinoma
12 (35.3%) 10 (29.4%)
Non–small cell lung cancer
4 (11.8%)
Small cell carcinoma Poorly differentiated carcinoma
2 (5.9%) 2 (5.9%)
Large cell carcinoma Unknown Staging
Immediate Control of Hemoptysis Immediate arrest of hemoptysis was achieved in 31 (77.5%) of 40 patients who underwent BAE. BAE failed to control bleeding in nine (22.5%) patients. Seven of these patients died of hemoptysis within 4 weeks of the procedure, and two underwent successful repeat embolization. Table 1 . Characteristics of 40 Patients Included in the Study Age (y) Mean (SD)
Table 2 . Histology and Staging of 34 Patients with Primary Lung Cancer
1 (2.9) 3 (8.8%)
IA
1 (2.9%)
IIA IIB
4 (11.8%) 2 (5.9%)
IIIA
5 (14.7%)
IIIB IV
6 (17.6%) 13 (38.2%)
Unknown
3 (8.8%)
Values are number (percentage). Table 3 . Complementary Examinations
62.8 (11.7) Imaging
Sex Male Female
34 (85%) 6 (15%)
Smoker Never Former
9 (22.5%) 22 (55.0%)
Current
9 (22.5%)
Hemoptysis volume (mL) Mean (SD)
241 (162)
Lung Breast
34 (85%) 2 (5.0%)
Colon
1 (2.5%)
Choriocarcinoma Sarcoma
1 (2.5%) 1 (2.5%)
Hypernephroma
1 (2.5%)
Yes Radiotherapy dose (Gy) Mean (SD)
10 (25%)
CT scan None
24 (60.0%) 6 (15.0%)
Imaging findings Normal Pulmonary nodule Multiple pulmonary nodules
Primary cancer
Previous radiotherapy No
Chest x-ray
Pulmonary mass Ground glass None Great intrathoracic vessels affected CT No Yes Bronchoscopy No Yes
27 (67.5%) 13 (32.5%)
Bronchoscopy findings Blood Tumor
49.1 (18.4)
2 (5.0%) 4 (10.0%) 4 (10.0%) 23 (57.5%) 1 (2.5%) 6 (15.0%) 20 (83.3%) 4 (16.7%) 20 (50.0%) 20 (50.0%) 10 (50.0%) 10 (50.0%)
Values are number (percentage).
Recurrence No Yes 1 recurrence 2 recurrences Mortality from hemoptysis No Yes All-cause mortality
32 (80.0%) 8 (20.0%) 6 (15.0%) 2 (5.0%) 28 (70.0%) 12 (30.0%)
No
6 (15%)
Yes
34 (85%)
Values are number (percentage) unless otherwise indicated. SD ¼ standard deviation.
Recurrence and Angiographic Findings Cumulative survival free of recurrence is shown in Figure 1. Probability of surviving free of recurrence at 1 month was 0.90 (95% confidence interval [CI], 0.80–1.0). Probability of surviving free of recurrence at 6 months was 0.65 (95% CI, 0.44–0.86). Recurring hemoptysis that required further BAE occurred in eight patients. Characteristics of patients with hemoptysis recurrence after BAE and characteristics of the procedures are presented in Table 4. Two of these eight patients required more than one procedure to achieve control of the bleeding. Recurrence occurred within 1
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Figure 1. Cumulative hemoptysis control rate.
month after the first episode in six cases (75%). Four of the patients who underwent repeat embolization procedures had previous radiotherapy.
Mortality Secondary to Hemoptysis Death as a result of hemoptysis occurred in 12 (30%) patients. Eight (66.7%) patients died within the first month after the episode. Three of four (75%) patients with invasion of thoracic great vessels as visualized by CT scan died as a result of massive hemoptysis despite BAE (range, 2–21 days). Probability of not dying as a result of hemoptysis at 1 month and at 6 months was 0.77 (95% CI, 0.64–0.90) and 0.68 (95% CI, 0.52–0.85). No patient presented with fatal hemoptysis after 8 months of follow-up.
All-Cause Mortality There were 28 (70%) patients who died as a result of etiologies other than hemoptysis. There were 12 deaths attributed to progression of neoplastic disease, 4 attributed to pneumonia, 3 attributed to cerebral hemorrhage, and 3 attributed to myocardial infarction. The cause of death was unavailable for six (15%) patients. Cumulative survival is shown in Figure 2. Probability of surviving was 0.75 (95% CI, 0.62–0.88) at 1 month, 0.42 (95% CI, 0.27–0.57) at 6 months, 0.36 (95% CI, 0.21–0.51) at 12 months, and 0.08 (95% CI, 0.0–0.18) at 3 years. Survival curve for patients who had previously received radiation therapy was not statistically significant
compared with patients with no previous history of radiotherapy (P ¼ .67). For the 34 patients with primary lung cancer, the mean overall survival was 14.2 months (95% CI, 7.41–21.03); the mean overall survival for the 6 patients with extrapulmonary primary cancer was 10.1 months (95% CI, 3.25–17.01). Difference in survival between the two groups was not statistically significant (P ¼ .83).
Imaging Findings The vessels interrogated at diagnostic angiography included the bronchial arteries (n ¼ 48), various intercostal arteries (n ¼ 37), internal mammary arteries (n ¼ 4), and lateral thoracic artery (n ¼ 1). Angiographic findings (Figs 3, 4) included active extravasation (17.5%; 5 of 40 cases), tumor blush (90%; 36 of 40 cases), bronchial artery enlargement (62.5%; 25 of 40 cases), bronchial artery tortuosity (40%; 16 of 40 cases), and arteriovenous fistula (2.5%, 1 of 40 cases). Three (7.5%) of the cases manifested with a single abnormality: enlarged bronchial artery (n = 2) and arteriovenous fistula (n = 1). There were no differences in immediate success of BAE or mortality according to angiographic findings or arteries involved.
DISCUSSION Our data demonstrate that BAE is an effective and safe technique in the treatment of hemoptysis in patients with
1.1 5.4
1.0
6 7
8
AVF ¼ arteriovenous fistula, BAE ¼ bronchial artery embolization, BBT ¼ bibronchial trunk, LBA ¼ left bronchial artery, NSCLC ¼ non–small cell lung cancer, PVA ¼ polyvinyl alcohol, RBA ¼ right bronchial artery, RICBT ¼ right intercostobronchial trunk, RLTA ¼ right lateral thoracic artery, RT ¼ radiotherapy. n Fed by segmental artery. † Pulmonary artery involved.
None† BBT Yes Microspheres and coils Yes IIIB
7.7 5
Lung (squamous)
RLTA BBT
RBA LBA
RICBT, BBT AVF* Yes Yes
Yes Microspheres
Microspheres and coils Coils Yes No
Yes IV
IIA
5.6 1.4
Lung (squamous) Choriocarcinoma
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Lung (NSCLC)
BBT BBT RICBT, LBA LBA No No PVA PVA Yes No Unknown
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Lung (NSCLC) Breast
LBA
LBA LBA No PVA No IIA
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Sarcoma
Lung (squamous)
First BAE
BBT, RICBT No PVA
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0.9
Death Caused
by Hemoptysis Material Used at BAE Previous RT
Staging
(Lung Cancer) Diagnosis
Recurrence after
BAE (mo) Case No.
Table 4 . Cases of Hemoptysis Recurrence after BAE
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No
Second BAE
Number 2
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cancer. Immediate control of bleeding was achieved in most patients. Recurrence requiring BAE occurred in 20% of patients. Hemoptysis in patients with cancer generally occurs secondary to local necrosis and inflammation of blood vessels within the tumor bed, rather than direct tumor invasion of blood vessels (18). In these patients, the tumors feeding bronchial arteries are extended and enlarged (19). BAE has become a common first-line therapy for life-threatening hemoptysis. Although most previous studies have focused on patients with hemoptysis secondary to benign lung diseases, such as bronchiectasis, tuberculosis, and aspergilloma, some of these series included patients with lung cancer in their analysis (4,13). These studies showed that BAE in patients with lung cancer was associated with a high failure rate (4) and increased mortality (18), even though angiographic findings in tumor-related bleeding were not significantly different from findings in benign causes of hemoptysis (15,16). However, studies exclusively in patients with hemoptysis secondary to malignancy showed better results (14–16). Witt et al (14) described their experience with BAE using platinum coils in patients with tumorous pulmonary bleeding. They prospectively studied 30 patients with lung cancer who underwent BAE and compared their results with 15 patients with moderate hemoptysis secondary to lung cancer who had been treated conventionally. These authors found that the mean survival time was significantly lower in the control group than in the BAE group. Park et al (15) included in their analysis 19 patients with a diagnosis of primary lung cancer who underwent BAE. They concluded that BAE was an effective technique in the treatment of hemoptysis in patients with lung cancer. Wang et al (16) studied 30 patients with a diagnosis of either lung cancer or pulmonary metastases from extrathoracic disease. They concluded that BAE was safe and effective, especially in patients with cancer in which bleeding was secondary to a benign cause and not related to the tumor. To the best of our knowledge, our series is among the largest analyzing the results of BAE in patients with hemoptysis resulting solely from malignancy and shows results similar to previous studies. Immediate control of bleeding was achieved 77.5% of patients. Although immediate success is defined differently in each article, it ranges from 79%–100% (15,16). Recurrence occurred in 20% of patients in our series, whereas in previous studies it ranged from 26%–53% (14,16). In our series, the mean overall survival for the 34 patients with primary lung cancer was 14.2 months. Wang et al (16) described a median overall survival time of 5.5 months. In the study by Witt et al (14), the mean survival time of patients with BAE treatment was 139 days. In our series, survival rate was 0.75 at 1 month, 0.42 at 6 months, 0.36 at 12 months, and 0.08 at 3 years. In the series by Wang et al, survival rate was 0.70 at 1 month, 0.25 at
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Figure 2. Cumulative survival (all cause mortality).
12 months, and 0.087 at 3 years. In the series by Witt et al, survival rate was 0.71 at 15 days and 0.28 at 6 months. Our study, with a large number of patients and a long follow-up period, shows that BAE is useful in the management of hemoptysis related to malignancy. It is also the first study that differentiates mortality secondary to hemoptysis from all-cause mortality. Wang et al (16) analyzed the effect of previous radiotherapy on the outcome of the technique. They found that the survival of patients who had previously received radiation therapy was not statistically significant compared with patients with no prior history of radiation therapy. In our group, we did not find differences in survival between patients who had received radiotherapy and patients who had not. Also, Wang et al (16) compared the results of BAE performed for hemoptysis related to tumor and not related to tumor (16). In our series all patients had tumor-related hemoptysis, so we did not perform this analysis. Apart from BAE, other interventional procedures, such as bronchoscopic techniques or palliative thoracic radiotherapy, can also be used. Several bronchoscopic treatments have been described for the treatment of lifethreatening hemoptysis in patients with lung cancer. Endoscopic methods include cold saline lavage, instillation of topical vasoconstrictive agents or fibrinogenthrombin, balloon or stent tamponade, endobronchial airway blockade, laser therapy, argon plasma coagulation, and electrocautery (20). In our series, 10 patients had
Figure 3. Selective bibronchial trunk arteriography (arrow) of a 79-year-old man with a pulmonary mass in the left lower lobe and hemoptysis. Embolization with microspheres was successfully performed. The patient died 13 days after the procedure because of acute respiratory failure and pneumonia.
endobronchial lesions. Only 25% of our patients would have benefited from endoscopic treatment of hemoptysis. None of these bronchoscopic techniques were attempted in our patients. No patient received palliative thoracic radiotherapy in our series. Causes for recurrent bleeding include progression of underlying disease; recanalization or revascularization; incomplete embolization; and emergence of other blood
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Figure 4. (a, b) Selective catheterization of an intercostobronchial trunk with hypervascularity in the intercostal artery (a and b, arrow) and right bronchial artery (a, arrowhead) in a 53-year-old man with a right pulmonary mass and hemoptysis. Embolization with microspheres and one coil was successfully performed. The patient was alive 10 months after the procedure.
supply to the affected area, such as from systemic collaterals (21). Early rebleeding has been related to incomplete embolization, whereas late rebleeding is generally due to disease progression (2,4,7,9). GarciaOlivé et al (22) reported more recently that recurring hemoptysis secondary to recanalization was related to time to recurrence but not to use of coils, number of arteries that received embolization, or neoplastic etiology. More specifically, we found that the artery that received embolization in the first 80 weeks after the first procedure would be a different one in most cases (suggesting incomplete embolization), whereas the artery that received embolization after 80 weeks would be the same as in the previous procedure in most cases (suggesting recanalization) (22). Our series included hemoptysis secondary to many conditions, including benign and malignant conditions. In our study, the artery that received embolization in the second procedure was a different one in seven of the eight patients with recurring hemoptysis, which may suggest incomplete embolization or emergence of other supply to the affected area. The small size of the sample did not allow us to compare the results between different agents. Multidetector CT has a role in the identification of the bronchial and nonbronchial arteries causing hemoptysis and improves the results of BAE (23–25). In our series, 6 (15%) patients had no imaging before BAE, and only 60% had a CT scan performed before the procedure. All six patients with no imaging were included in the study before 2004. Since then, our institution protocol for the management of life-threatening hemoptysis has changed, and it is now mandatory to perform a CT scan before BAE except when there is hemodynamic instability or extremely rapid bleeding. We have not seen any severe treatment-related complications. Likewise, Witt et al (14) did not report any complications. However, Park et al (15) described two minor complications (one episode of transient chest pain
and one puncture site hematoma), and Wang et al (16) described two minor complications (two cases of vessel dissection) and one spinal cord infarction. There are several limitations to this study. First, the sample size is small. Second, this is a retrospective study, with embolization procedures performed by different operators using different tools and embolic agents. Finally, there is no control group with which compare the results. In conclusion, BAE is an effective and safe technique in the treatment of hemoptysis in patients with oncologic disease. Nevertheless, mortality secondary to hemoptysis and recurrence are high among these patients, most likely resulting from progression of the underlying disease.
REFERENCES 1. Remy J, Voisin C, Ribet M, et al. Treatment, by embolization, of severe or repeated hemoptysis associated with systemic hypervascularization. Nouv Presse Med 1973; 2:2060 [in French]. 2. Rabkin JE, Astafjev VI, Gothman LN, Grigorjev Y. Transcatheter embolization in the management of pulmonary haemorrhage. Radiology 1987; 163:361–365. 3. Katoh O, Kishikawa T, Yamada H, Matsumoto S, Kudo S. Recurrent bleeding alter arterial embolization in patients with hemoptysis. Chest 1990; 97:541–546. 4. Hayakawa K, Tanaka F, Torizuka T, et al. Bronchial artery embolization for hemoptysis: immediate and long-term results. Cardiovasc Intervent Radiol 1992; 15:154–159. 5. Ramakantan R, Bandekar VG, Gandhi MS, Aulakh BG, Deshmukh HL. Massive hemoptysis due to pulmonary tuberculosis: control with bronchial artery embolization. Radiology 1996; 200:691–694. 6. Brinson GM, Noone PG, Mauro MA, et al. Bronchial artery embolization for the treatment of hemoptysis in patients with cystic fibrosis. Am J Respir Crit Care Med 1998; 157:1951–1958. 7. Mal H, Rullon I, Mellot F, et al. Immediate and long-term results of bronchial artery embolization for life-threatening hemoptysis. Chest 1999; 115:996–1001. 8. Osaki S, Nakanishi Y, Wataya H, et al. Prognosis of bronchial artery embolization in the management of hemoptysis. Respiration 2000; 67: 412–416. 9. Kato A, Kudo S, Matsumoto K, et al. Bronchial artery embolization for hemoptysis due to benign diseases: immediate and long-term results. Cardiovasc Intervent Radiol 2000; 23:351–357. 10. Swanson KL, Johnson M, Prakash UBS, McKusick MA, Andrews JC, Stanson AW. Bronchial artery embolization. Experience with 54 patients. Chest 2002; 121:789–795.
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11. Kim YG, Yoon HK, Ko GY, Lim CM, Kim WD, Koh Y. Long-term effect of bronchial artery embolization in Korean patients with haemoptysis. Respirology 2006; 11:776–781. 12. Chun JY, Belli AM. Immediate and long-term outcomes of bronchial and non-bronchial systemic artery embolisation for the management of haemoptysis. Eur Radiol 2010; 20:558–565. 13. Fartoukh M, Khoshnood B, Parrot A, et al. Early prediction of in-hospital mortality of patients with hemoptysis: an approach to defining sever hemoptysis. Respiration 2012; 83:106–114. 14. Witt CH, Schmidt B, Geisler A, et al. Value of bronchial artery embolisation with platinum coils in tumorous pulmonary bleeding. Eur J Cancer 2000; 36:1949–1954. 15. Park HS, Kim YI, Kim HY, Zo JI, Lee JH, Lee JS. Bronchial artery and systemic artery embolization in the management of primary lung cancer in patients with hemoptysis. Cardiovasc Intervent Radiol 2007; 30: 638–643. 16. Wang GR, Ensor JE, Gupta S, Hicks ME, Tam AL. Bronchial artery embolization for the management of hemoptysis in oncology patients: utility and prognostic factors. J Vasc Interv Radiol 2009; 20:722–729. 17. Angle JF, Siddiqi NH, Wallace MJ, et al. Quality improvement guidelines for percutaneous transcatheter embolization. Society of Interventional Radiology standards of practice committee. J Vasc Interv Radiol 2010; 21:1479–1486.
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18. Winter SM, Ingbar DH. Massive hemoptysis: pathogenesis and management. J Intens Care Med 1988; 3:171–188. 19. Newton TH, Preger L. Selective bronchial arteriography. Radiology 1965; 84:1043–1051. 20. Gompelmann D, Eberhardt R, Herth FJF. Advanced malignant lung disease: what the specialist can offer. Respiration 2011; 82:111–123. 21. Yoon W, Kyu Kim J, Hyun Kim Y, Woong Chung T, Keun Kang H. Bronchial and nonbronchial systemic artery embolization for life threatening hemoptysis: a comprehensive review. Radiographics 2002; 22:1395–1409. 22. Garcia-Olivé I, Sanz-Santos J, Centeno C, et al. Predictors of recanalization in patients with life-threatening hemoptysis requiring artery embolization. Arch Bronconeumol 2013; pii: S0300-2896(13)00188-9. 23. Yoon YC, Lee KS, Jeong YJ, Shin SW, Chung MJ, Kwon OJ. Hemoptysis: bronchial and nonbronchial systemic arteries at 16-detector row CT. Radiology 2005; 234:292–298. 24. Mori H, Ohno Y, Tsuge Y, et al. Use of multidetector row CT to evaluate the need for bronchial arterial embolization in hemoptysis patients. Respiration 2010; 80:24–31. 25. Hayes D Jr, Winkler MA, Kirkby S, Capasso P, Mansour HM, Attili AK. Preprocedural planning with prospectively triggered multidetector row CT angiography prior to bronchial artery embolization in cystic fibrosis patients with massive hemoptysis. Lung 2012; 190:221–225.
