Percutaneous Bronchial Artery Embolization in the Management of Massive Hemoptysis in Chronic Lung Diseases. Immediate and Long- Term Outcomes

By Serasli, E Kalpakidis, V; Iatrou, K; Tsara, V; Siopi, D; Christaki, P

Aim. Bronchial artery embolization (BAE) is a well-established, non-surgical procedure in the emergency treatment of massive hemoptysis. This study aims to evaluate the immediate and long-term prognosis of BAE for the management of massive hemoptysis in our center. Methods. Twenty consecutive patients (mean age: 59+-14 years) with massive hemoptysis, underwent BAE with microspheres (Embospheres BioSphere Medical SA, Paris, France), polyvinyl alcohol particles (PVA, Ivalon, Cathmed Science; Paris, France) or/and steel coils (Cook, Denmark) after thoracic aortography and diagnostic selective and superselective catheterization of bronchial arteries and systemic collateral vessels in the bleeding lung area. Hemoptysis was due to bronchiectasis (55%), non-operable aspergillomas (15%), active tuberculosis (15%), malignancy (10%) and cystic fibrosls (5%). Mean duration of follow-up was 29+-18 months. The recurrent-free time was calculated with Kaplan-Meier analysis.

Results. Immediate control of bleeding was achieved in all patients. Recurrent cases of hemoptysis were observed in 6/20 patients (30%) within 3 years and 4 of them (66.6%) occurred early in the first 3 months. Recurrent-free time was 9 months (standard error: 4) (95% confidence interval: 0-17). Repeated interventions were required in all early recurrences, due to either recanalization of the occluded arteries or non-bronchial systemic artery supply. Combined use of PVA and coils was proved effective in these cases. No serious complications were observed.

Conclusion. BAE is an effective and safe intervention in cases of massive hemoptysis. However, recurrences are common and long-term follow-up is considered important with a view to perform repeated interventions with combination of embolic materials.

[Int Angiol 2008;27:319-28]

Key words: Hemoptysis – Embolization, therapeutic – Bronchial arteries – Angiography, digital subtraction – Catheterization – Lung diseases.

Massive hemoptysis, also known as life-threatening hemoptysis, represents a critical, high-risk, clinical condition and it is quite common among patients with chronic lung disease, since it is estimated that 28% of chest physicians experience mortality associated to hemoptysis annually.1

Treatment options in such cases are hampered by the need for swift diagnosis of the underlying disease and mostly by the urgency for effective and safe therapeutic interventions. Surgical management in the acute phase is accompanied by high operative mortality (30-40%), taking into consideration that these patients are often poor surgical candidates, due to bilateral pulmonary involvement and/or concomitant respiratory failure.2

Percutaneous bronchial artery embolization (BAE) has been considered an alternative, nonsurgical therapeutic approach and it was introduced by Remy et al.3 The initial report was followed by the widespread use of the technique and BAE was rapidly established as an effective, interventional radiological approach for managing active hemoptysis, achieving an immediate control in 75-90% of patients.4 However, rebleeding rates higher than 20% are reported during follow-up and few reports have previously investigated the long-term results.5

The aim of our study was to analyze the experience of BAE for managing massive hemoptysis in patients with chronic lung disease in our center and explore the immediate and long-term prognosis, according to an established prospective protocol.

Materials and methods

A prospective, descriptive study was undertaken, including patients with chronic lung diseases, representing with life- threatening hemoptysis, who underwent percutaneous BAE at G. Papanikolaou General Hospital, a tertiary-care hospital in Thessaloniki, Greece. In May 2001, 2nd Chest Clinic and the Interventional Radiology Department of our hospital developed a common protocol for the diagnostic and therapeutic management of life-threatening hemoptysis. Life-threatening hemoptysis was defined as: 1) expectoration of at least 250 mL of blood in 24 h; 2) requirement for blood transfusion in cases of a significant decrease in hemoglobin level or 3) failure or inadequacy of conservative management of the hemoptysis, either because of ongoing hemoptysis or because the hemoptysis posed a serious threat to life in patients with significant respiratory impairment.

According to the protocol, all patients who were clinically and hemodynamically stable underwent chest radiography and computed tomography (CT), as well as diagnostic flexible bronchoscopy, in order to identify the cause and the location of the bleeding. Biochemical and coagulation analyses were also routinely performed in all patients, as part of the diagnostic work-up.

From May 2001 to August 2006, BAE was performed after these standard procedures in 20 consecutive patients with chronic lung disease, who were referred with a history of life-threatening hemoptysis on the day of their hospital admission to the Clinic. All patients had previously signed an informed consent form, whereas contraindications were not considered in the study.

In the study population of 20 patients (17 male and 3 female), ranging in age from 25 to 80 years (mean age: 59.8+-13.9 years), the following underlying lung diseases were identified: bronchiectasis in 11 patients (55%), which were tuberculosis sequelae in 5/11 patients (45.4%), aspergillomas in 3 patients (15%), active tuberculosis in 3 (15%), lung malignancy in 2 (10%) and cystic fibrosis in one patient (5%). Demographic and also clinical characteristics of the patients, in terms with their respiratory function, are demonstrated in Table I.

In all cases, the patients were deemed unsuitable for surgical interventions, due to significant bilateral pulmonary disease (active tuberculosis in 3 patients, cystic fibrosis in 1 patient), poor lung function (8 patients), non-operable lung malignancy (2 patients) or refusal to surgery (6 patients).

Diagnostic angiography and BAE were performed using a high- resolution, digital subtraction angiography unit (Philips Integris 500) at the Interventional Radiology Department with provision of adequate monitoring and life support equipment. All patients were treated by the same radiologist (V. K.); another trained radiologist was actively involved in the procedure. None of the patients required mechanical ventilation during or after the embolization. Initially, diagnostic thoracic aortography was performed via percutaneous cannulation of the femoral artery in all patients, using 5F pigtail catheters (Cook, Denmark). According to the protocol applied in the unit, the number, location and degree of pathologic enlargement of the bronchial arteries, as well as the presence of non-bronchial systemic collateral vessels (in particular intercostal, subclavian and internal mammary arteries) were evaluated in all patients. Selective catheterization of all arteries responsible for hemoptysis was performed using 4F to 5F, C2 or Simmons catheters (Cordis, Miami, FL, USA). Ultravist 300 (Schering, Berlin, Germany) was the contrast agent used. Arteries were considered pathologic, when we observed predefined direct signs, such as extravasation and aneurysm or indirect signs, such as irregularity, increased caliber, vascular tufts and arteriovenous or arterio-arterial shunting. Super-selective microcatheterization was performed in 10 cases of unstable catheter position and small vessel caliber, by the coaxial insertion of 2- to 3-Fr microcatheters (Terrumo SP, Japan) through guiding C2 catheters. Thorough attempts were made in all cases to identify the medullary arteries; according to the protocol, their presence was considered a contraindication to embolization.

BAE was performed using 300 to 500 [mu]m polyvinyl alcohol particles (PVA, Ivalon, Cathmed Science; Paris, France) in 12 cases or nonabsorbable particles of microspheres (Embospheres; BioSphere Medical SA, Paris, France) in 20 cases. Detachable steel coils (Cook, Denmark) were used in 3 cases of aspergillomas. More than one types of embolization material were used in 8 cases. The objective of the embolotherapy was the occlusion of all diseased arteries and this was defined as technical success, whereas clinical success was defined as cessation of bleeding for at least 1 month.

Recurrence during follow-up was defined as the presence of hemorrhage of 50 mL or more in 24 h, excluding thus all cases of minor hemosputum. Follow-up appointments were scheduled for 1 month, 3 months, 6 months and 12 months, followed by annual appointments. They included physical examination, chest radiograph and CT scan, when necessary.

Analysis of outcome

All clinical records included in the protocol were reviewed and the following data and images were collected for analysis: age, sex, clinical features, chest radiograph, CT scan, bronchoscopy, bronchial arteriography, BAE, and results, complications and follow- up. The end of follow-up was defined as December 2006. Cumulative hemoptysis control rate was calculated by the Kaplan-Meier method.

Results

The findings of chest radiographs, performed upon admission, were abnormal in 16 patients and were suggestive of the site of hemoptysis in 7 cases. According to the protocol, all patients also underwent chest CT scan and the findings were abnormal and suggestive of the underlying chronic lung disease in every case. However, only in 10 patients the findings were indicative of the location of the bleeding, whereas diagnostic bronchoscopy that was performed prior to BAE and had identified the bleeding side in 15 patients. Pleural disease, defined as thickening of the pleura adjacent to the radiologically abnormal lung area, was identified in 5 patients on the chest CT scans and this finding was accompanied by non-bronchial systemic arteries supply of the bleeding area in all patients. The arterial sources of bleeding were satisfactorily identified during angiography and the affected arteries were embolized in all patients. Direct signs of hemorrhage (extravasation of contrast into the bronchial lumen and/or aneurysm) were present in one patient (5%). Angiographie findings included indirect signs, such as hypertrophie and tortuous bronchial arteries in 15 patients, neovascularity in 14 patients, hypervascularity in 18 patients, and shunting into pulmonary artery in 3 patients (Table II and Figures 1- 3).

The embolized arteries were in their vast majority bronchial, with the exception of 5 cases, in which systemic collateral arteries supplied the abnormal vascular network. In these cases, the occluded arteries were the internal mammary (4 patients), intercostal arteries (3 patients), branch from the subclavian artery (1 patient).

Hemoptyses were controlled during the first 24 h in 18 patients (90%) and in 48 h in the remaining 2 patients. Immediate clinical control of bleeding for 1 month was achieved in 19 patients (95%).

The complications of BAE included pleuritic chest pain that occurred in 6 patients (30%) and transient paraparesis in 1 patient (5%), who subsequently recovered fully.

Follow-up

Mean follow-up time for all patients was 29.4+-16.3 months (ranging from 6 to 70 months). During this period, recurrence of hemoptysis occurred in 6 patients (30%). According to Kaplan-Meier analysis the recurrence-free time was 9 months (standard error: 4) (95% confidence interval: 0-17) (Figure 4).

One of them, suffering from active tuberculosis under antimycobacterial therapy, relapsed early within the next month. He underwent successful repeat embolization of the right bronchial artery that had been occluded in the first session by PVA. Recanalization of the vessel was the main cause of the relapse and it was embolized again, using combination of PVA and embospheres.

Three patients with intracavity pulmonary aspergillomas were readmitted to our clinic with episodes of massive hemoptysis and repeat intravascular interventions were required within the first 3 months.

Two of them, with concurrent chronic obstructive pulmonary disease (COPD) and chronic respiratory failure that precluded any surgical intervention, had developed extensive collateralisation, recanalization of the previously occluded vessels. In these cases, embolization of non-bronchial systemic arteries was performed using embospheres and coils (Figure 3). They both relapsed again with episodes of hemoptysis within the next year and they underwent repeat embolization of the involved arteries one more time.

Another patient with necrotic invasive aspergillosis on a ground of previous lobectomy, who refused surgical treatment, experienced the first relapse also 1 month after the first BAE. She underwent a repeat endovascular procedure, which included the occlusion of the right internal mammary, intercostal arteries and of a systemic-to- pulmonary shunt in the bleeding lung area (Figure 2). During the long-term follow-up period of 70 months, she had recurrent, less severe, episodes of hemoptysis and embolization was repeated three times, with combination of embospheres and coils at the last session.

Two patients with lung cancer relapsed later in the course of the disease and during this period they were under chemotherapy and radiotherapy for the underlying disease. In these cases, recurrences occurred after 15 and 27 months, respectively. The second relapse was fatal in the first patient, whereas in the other case, the bleeding resolved with conservative therapy, due to denial of the patient to proceed to any intervention.

Discussion

It is well established that in life-threatening hemoptysis, massive bleeding originates mostly from pathologic bronchial arteries or less frequently from non-bronchial systemic collateral vessels. Consequently, the control of hemorrhage by BAE is considered a logical therapeutic intervention.4, 5 Remy et al. introduced the method in 1973, whereas the first radiographie visualization of bronchial arteries had already been demonstrated in the early 1960s, using nonselective aortography,3,6 In 1977, Remy et al. published the results of the intervention on a large series of 104 patients with a success rate of 84%.7 Subsequently, BAE was widely used in controlling massive hemoptysis and its efficacy and safety have been well documented in many reports, reaching high clinical success rates (80-92%).8-12

Bronchial arteriography and embolization were well tolerated by our patients and an immediate control of hemorrhage was achieved in 18 of them in 24 h (90%) and in the remaining 2 in 48 h, providing a overall immediate clinical success rate of 100%. Cremaschi et al also reported 98% of the cases in his study to be controlled by embolization in the first 24 h, whereas 2% in the following 48 h.13

The immediate success rates have been increased lately and this may be attributed to the introduction of superselective embolization and the refinement of embolie agents and techniques. Superselective catheterization of the vascular network allows optimal catheter stability and safety, avoiding reflux of embolization materials and furthermore preventing the occlusion of spinal artery.14-16 The technique was successfully employed in 8 cases in our study, in order to overcome technical difficulties and it was helpful even for the embolization of non-bronchial arteries of small caliber, providing maximal effectiveness. The high immediate clinical success rate of our study may also be due to the prospective design of the study that allowed early and effective diagnostic interventions and prompt therapeutic approach in all cases of massive hemoptysis, according to a prospective, specific protocol.

It is quite interesting that the success rate of BAE varies significantly in the literature as well as the definition of massive hemoptysis in terms with the amount of the expectorated blood (300 to 600 mL in 24 h).17 This lack of consensus and also the retrospective design of most of the studies, seem to account for these conflicting results. In our study, we used the term to denote any case of severe hemoptysis that posed a threat on the patients’ life, as suggested by Jougon et al. and defined by Wong et al.18, 19

In order to guide the interventional radiologist by determining the site and the vascular source of bleeding, specific diagnostic procedures are employed and they are routinely performed in all published reports. However, the cause of hemoptysis cannot be determined in 20-30% of cases.20 According to the results of our study, the location of hemorrhage was diagnosed in 35%, 50%, and 75% of the patients based on chest radiography, bronchoscopy and chest CT-scan findings, respectively. These procedures were thus proved to be valuable modalities, as they minimized the time-consuming need to explore the vascular network, in search of abnormalities and contributed to the swift targeting and occlusion of the involved arteries.

In regards to technical aspects of BAE, it is obvious that working knowledge of the bronchial artery anatomy and its common variations is most important. In most of the patients’ angiographies, the bronchial arteries arise from the aorta or the intercostal arteries. However, Unflackerei al. identified as many as 10 different patterns in a group of 72 patients, who underwent BAE.5 Furthermore, it is well established that the source of massive hemoptysis is usually the bronchial circulation (90% of cases) rather than the pulmonary circulation (5% of cases).4 As far as the pathology of hemoptysis is concerned, in many acute and chronic lung diseases, hypoxic vasoconstriction, intravascular thrombosis and vasculitis of the pulmonary circulation are common pathophysiologic features. As a result, bronchial arteries proliferate and enlarge and may be ruptured, due to erosion by bacterial agents or due to elevated region blood flow, at the area of parenchymal inflammation.21,22

It is of note that the involvement of the parietal pleura, representing as pleural thickening on chest CT-scans, was indicative of non-bronchial systemic artery supply in the hypervascular area in 5 cases, including the 3 cases of aspergillomas. Bibliographic data support the view that nonbronchial arteries should be explored as possible contributors to the origin of hemoptysis in cases where there is associated pleural disease.23

From another point of view, the etiology of massive hemoptysis in various countries may reflect the socioeconomic development of the geographic location and tuberculosis and its sequelae are proved to be the main causes in the developing countries. These patients frequently have bilateral disease and significantly compromised pulmonary function.24 Although bronchiectasis were the most common diagnosis in the patients of our study, it was proved that they were post-tuberculous in origin in 45.4% of patients, whereas colonization of old tuberculous cavities by Aspergillus was involved in 3 cases. Taking also into consideration the three cases with active tuberculosis, it seems that the disease process participates directly or indirectly in the majority of cases in the study.

Chronic inflammation was the common pathophysiologic feature in the patients of our study, as there was evidence of parenchymal disease on CT-scan in all of them. Consequently, our angiographie findings such as hypertrophie and tortuous bronchial arteries, hypervascularity and neovascularity were not specific. Interestingly, systemic-to-pulmonary shunts were only visualized in the patients with aspergillomas and these cases required more than one therapeutic intervention with the combined use of embolic materials. Specific angiographic findings of hemorrhage, reported in the literature, such as extravasation and aneurysm, were not common among our patients, in accordance with literature data.4 The choice of the embolizing agent depends upon the anatomic features of the affected arteries. Currently, distal embolization is recommended using PVA or microspheres, and proximal embolization using coils.25 To our knowledge, there are no comparative studies evaluating the embolie materials and their specific indications in terms with the immediate and long-term outcomes. Nevertheless, it is widely accepted that enormous bronchial arteries with high flow and large systemic-to-pulmonary shunts require the use of coil for safe and adequate occlusion.26 However, this type of proximal occlusion is generally reserved in recurrent cases of massive hemoptysis. According to our experience, the use of coils in combination with microspheres was proved effective in the management of recurrent massive hemoptysis, due to non-operable aspergillomas. In these three cases, angiography revealed the involvement of systemic arteries and the development of shunts and led to the decision of repeated embolizations.

Successful management of massive hemoptysis in aspergillomas has been recently reported by Corr in 11/12 patients (91.6%) as a temporizing measure and only one of his patients subsequently required lobectomy, although in a series by Katoh et al., the majority of patients (75%) with aspergilloma experienced recurrence.27- 2S However, surgical intervention is often precluded from the beginning, as in our study, suggesting that BAE may be the treatment of choice in such cases.

Recurrences after BAE are rather common, according to the few reports that have investigated the long-term outcomes of BAE. Garcia- Medina et al. analyzed the long-term prognosis in their series and Kaplan-Meier curves proved that 18% of recurrences occurred within 7 days, 24% within 1 month, 33% within 6 months and 38% in 1 year. No further recurrences occurred 1 to 2 years after embolization.29 Osaki et al. also applied KaplanMeier test and found that 75% of the recurrent cases occurred within 1.5 years and no case recurred more than 3 years after the first BAE.30 Long-term recurrence rates have been reported to be 10% to 52% with a mean follow-up period ranging from 1 to 46 months.30-32

Recurrent bleeding may be caused by recanalization of embolized vessels, incomplete embolization, revascularization by the collateral circulation, non-bronchial artery supply (short-term recurrence) or by inadequate treatment of the underlying disease and inflammatory progression (long-term recurrence).28,33 Specifically, hemoptysis may recur after successful BAE, if the dis ease process is not well-controlled with drug therapy or surgery, bearing in mind that embolization does not address the underlying chronic lung disease, but rather controls the symptom in an acute phase. In this sense, BAE is considered a palliative procedure, the potential for hemoptysis is not precluded and repeat BAE may be required.2,28

Regarding the factors predisposing to relapse, apart from technical reasons, the underlying pathology seems to play a major role and patients with tuberculosis, aspergilloma and lung cancer are more prone to recurrent hemorrhage.11, 28 In a 6-year follow-up study of 134 patients by Goh et al., repeat embolization was required in 15.5% of cases, that were all due to chronic tuberculosis.34 Mossi et al. also analyzed predictors of failed arterial embolization in a retrospective study of 88 patients treated for hemoptysis and concluded that tuberculosis, aspergilloma and systemic-to- pulmonary shunts are associated with a high risk of recurrence.35

Unlike Osaki et al. who recognized that bronchiectatic changes on the chest CT-scan are risk factors for recurrence,30 our findings in patients with bronchiectasis were not predictors of relapse, since all these cases were recurrentfree during long-term follow-up. On the other hand, the presence of systemic-to-pulmonary artery shunt was accompanied by relapse of hemorrhage in each of our 3 cases.

Our study results demonstrated a high recurrent-free time of 9 months, estimated with KaplanMeier test, during a 5-year follow-up period. Furthermore, in accordance to literature, the relapsed cases were all patients with aspergillomas, lung cancer and tuberculosis and they all underwent successful repeat embolization at least once with well-established techniques and combination use of embolie agents. Especially, in two cases with lung malignancy, BAE was effective and patients experienced no relapses for over 1 year. Even the patient with cystic fibrosis had been stable without any episode of hemoptysis for almost 2 years. According to literature, BAE is effective in patients with cystic fibrosis, providing high long- term success rate.36

The complication rates after BAE have been diminished gradually over the years, due to the introduction of superselective technical aspects and the use of non-absorbable embolie agents. Chest pain is the most common complication with a reported prevalence of 24-91%; it is usually, transient and is related to ischemia.4, 8 It occurred in 15% of patients in our study and it subsided spontaneously.

Other reported complications are spinal cord syndromes, bronchial stenosis, bronchoesophageal fistula infraction of a bronchus and transient cortical blindness.19 Spinal cord complications, such as Brown-Sequard syndrome, paraparesis, paraplegia were reported by Mal et al. and they are attributed to spinal ischemia, caused by accidental occlusion of spinal arteries.8 It is of interest that the anterior spinal artery was not demonstrated to arise from a bronchial artery or an intercostobronchial trunk in any of the 75 patients in a series by Unflacker.5 On the contrary, Cohen et al. found a spinal artery branching from a vessel that supplied the bronchial artery circulation in as many as 55% of 20 patients with cystic fibrosis.37 In view of these conflicting data, many authors suggest that identification of the anterior spinal artery or spinal radicular arteries arising from the bronchial arteries is an absolute contraindication to proceed with BAE, although others do not.5,19,38 It is noteworthy that cases in which spinal cord injury followed embolotherapy, branches to the spinal cord were not identified at angiography.8 39 Among our group of patients, only one (5%) experienced transient paraparesis with spontaneous regression. Neither in this patient with clinical symptoms, nor in any other patient was the anterior spinal artery visualized in angiography.

Conclusions

BAE may be considered a safe, non-surgical procedure for the management of massive hemoptysis in patients with chronic lung diseases. However, long-term clinical follow-up is considered important, especially in cases of non-operable aspergillomas, due to frequent relapses of hemoptysis that require both management of the underlying clinical pathology of the disease and repeated interventions with technical difficulties. New technical aspects that are recently introduced, such as the employment of selective techniques and combined use of embolie materials, can provide high success rates and may be proved life saving.

The study has also been accepted as poster presentation at the European Respiratory Society Congress, was held in Stockholm in September 2007.

Received on May 24, 2007; acknowledged on June 1, 2007; accepted for publication on November 1, 2007.

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E. SERASLI 1, V. KALPAKIDIS 2, K. IATROU 2, V. TSARA 1, D. SIOPI 1, P. CHRISTAKI 1

1 2nd Chest Department, G. Papanikolaou General Hospital, Thessaloniki, Greece

2 Interventional Radiology Department, G. Papanikolaou General Hospital, Thessaloniki, Greece

Address reprint requests to: E Serasli, MD PhD, 2nd Chest Dept. G. Papanikolaou General Hospital, Exohi, Thessaloniki, Greece. E- mail: serasli@patsialas.gr

Copyright Edizioni Minerva Medica Aug 2008

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