Bronchial artery embolization for hemoptysis in adult patients with cystic fibrosis: a single-center retrospective study

Abstract

Background

Hemoptysis is a severe complication of cystic fibrosis (CF) for which bronchial artery embolization (BAE) is an efficient primary therapeutic option. However, recurrence is more frequent than for other etiologies of hemoptysis.

Purpose

To assess the safety and efficacy of BAE in patients with CF and hemoptysis and predictive factors for recurrent hemoptysis

Material and Methods

This retrospective study reviewed all adult patients with CF treated by BAE for hemoptysis in our center from 2004 to 2021. The primary endpoint was the recurrence of hemoptysis after bronchial artery embolization. Secondary endpoints were overall survival and complications. We introduced the vascular burden (VB) defined as the sum of all bronchial artery diameters measured on pre-procedural enhanced computed tomography (CT) scans.

Results

A total of 48 BAE were performed in 31 patients. A total of 19 recurrences occurred with a median recurrence-free survival of 3.9 years. In univariate analyzes, percentage of unembolized VB (%UVB) (hazard ratio [HR] = 1.034, 95% confidence interval [CI=1.016–1.052; P < 0.001) and %UVB vascularizing the suspected bleeding lung (%UVB-lat) (HR = 1.024, 95% CI=1.012–1.037; P < 0.001) were associated with recurrence. In multivariate analyzes, only %UVB-lat remained significantly associated with recurrence (HR = 1.020, 95% CI=1.002–1.038; P = 0.030). One patient died during follow-up. No complication of grade 3 or higher was reported according to the CIRSE classification system for complications.

Conclusion

When possible, unilateral BAE seems sufficient in patients with CF with hemoptysis even in such a diffuse disease involving both lungs. The efficiency of BAE could be improved by thoroughly targeting all arteries vascularizing the bleeding lung.

Keywords

Cystic fibrosis hemoptysis bronchial artery embolization

Introduction

Cystic fibrosis (CF) is an autosomal recessive genetic disorder affecting one in 4000 newborns. The prognosis of the disease mainly depends on the progressive worsening of the respiratory function, leading to premature death in 90% of cases (1). Alteration of pulmonary mucus induces chronic diffuse inflammation, promotes infection, and irreversibly damages the bronchial tree resulting in bronchiectasis. Chronic bronchial ischemia and inflammation lead to enlarged and tortuous bronchial arteries and the recruitment of systemic collateral vessels. Therefore, hemoptysis, a life-threatening complication, is one of the serious respiratory complications of CF along with exacerbations and pneumothoraces. In the French CF registry in 2019, hemoptysis occurred in 5.7% of patients, with an incidence increasing with age (2). However, thanks to new therapies, the occurrence of hemoptysis may decrease in patients with CF even when life expectancy is improving (3,4). Treatment of hemoptysis is mainly based on bronchial artery embolization (BAE), a safe and effective treatment modality performed for many years (5). Other therapies available include airway protection with mechanical ventilation, if necessary, correction of coagulation dysfunction, bronchoscopy with local instillation of hemostatic solutions (ice-cold saline, dilutions of epinephrine), and surgery when bleeding persists despite BAE, while the systemic injection of vasoconstrictor (terlipressin) is debated (6,7). As shown by Cornalba et al., recurrence of bleeding remains more frequent in patients with CF than in other etiologies (38% vs. 21%) (8). The aim of the present study was to assess the safety and efficacy of BAE in patients with CF and hemoptysis and predictive factors for recurrent hemoptysis.

Material and Methods

Data collection

The study was approved by our institutional ethics committee (No. IRB00012437). We retrospectively reviewed all BAE performed in our single institution during 2004–2021.

Patient records were reviewed for patient demographics, the volume of hemoptysis, time to recurrence, and patient outcome. Follow-up ended when the patient either died, had lung transplantation, pneumonectomy, or was lost to follow-up. Hemoptysis was defined as massive or non-massive with a cutoff volume of 100 mL of expectorated blood volume in 24 h (9).

Contrast-enhanced chest computed tomography (CT) scans before the embolization were reviewed by a senior radiologist with >5 years of expertise in vascular imaging to identify the side that was suspected to be at the origin of the bleeding and to highlight the maximal diameter of all bronchial arteries, their ostial localization, and their side destination. Bronchial arteries emerging from the descending aorta were referred to as orthotopic and atypical arteries (10). Any other location was defined as ectopic or collateral. The measurements of arteries diameter were carried out at the site of the largest caliber of the branch with an exclusive bronchial destination (Figs. 1 and 2).

To depict the weight of bronchial vascularization before each BAE, we defined the patient bronchial vascular burden (VB) as the sum of all bronchial artery (orthotopic, atypical, ectopic, and collateral) diameters (in millimeters), measured on pre-procedural enhanced CT scans. For example, a patient with two orthotopic bronchial arteries of 3 and 2 mm in the largest diameter and a collateral bronchial artery of 1 mm in the largest diameter had a VB of 6 mm. Procedure reports and arteriographic images were also reviewed for identification of embolized arteries and to obtain the embolized VB. The embolized VB was calculated by summation of all embolized bronchial and/or collateral arteries’ maximum diameters as measured on the pre-procedural CT scan. The unembolized VB (UVB) was obtained by subtracting embolized VB from the initial VB. When an artery was embolized but was not visible on the pre-embolization CT scan, the minimum score of 1 was attributed in both initial VB and embolized VB. If the same artery was re-embolized within 24 h, it was considered non-embolized during the prior session and 0 was attributed to this artery in the embolized VB score.

The percentage of UVB (%UVB) was calculated as follows: %UVB = (initial VB – embolized VB) / initial VB × 100.

The VB lateralized to the suspected side of bleeding (VB-lat) only included arteries vascularizing this suspected bleeding side when identifiable. When the side of bleeding was undefined, both sides were suspected of being the source of the bleeding. The bleeding side was determined based on the pre-procedural CT scan images and/or bronchoscopic and/or clinical data such as “gurgling,” discomfort, unusual feeling, or localized warmth in a specific area of the thorax (11 –13). The percentage of UVB lateralized to the suspected bleeding lung (%UVB-lat) was calculated as follows: %UVB-lat = (initial VB-lat – embolized VB-lat) / initial VB-lat × 100.

Selection criteria

Pre-specified inclusion criteria were as follows: (i) BAE for the treatment of hemoptysis; (2) adult patients (aged >18 years); and (iii) proven CF.

Exclusion criteria were as follows: (i) the lack of embolization report; (ii) embolization after lung transplantation; and (iii) unavailability of the contrast-enhanced pre-BAE CT scan.

Procedures

A multidisciplinary agreement between pulmonologists and/or intensive care physicians and interventional radiologists was obtained before each procedure and was based on the volume of hemoptysis, the existence of repeated bleeding, the deterioration of the respiratory status, and the existence of bronchial arteries unembolized during a previous procedure. BAE were performed by a senior interventional radiologist with >5 years of expertise in performing interventional radiology procedures under fluoroscopic guidance, under local or general anesthesia based on the patient's clinical condition. For each procedure, the interventional radiologist relied on the pre-procedural CT scan to identify bronchial arteries, and no aortography was performed before BAE. Control angiograms were performed after embolizations. The equipment used was a 4- or 5-Fr catheter, supplemented with a 2.4- or 2.7-Fr micro-catheter at the discretion of the interventional radiologist The angiographic endpoint was reached with the appearance of stasis in the targeted vessels

Endpoints

The primary endpoint of this study was the recurrence of hemoptysis after BAE in adult patients with CF. Recurrence was defined as hemoptysis leading to death or requiring embolization, pneumonectomy, or lung transplantation. If one patient had more than one BAE, the subsequent procedures were considered recurrences of the previous BAE.

The secondary endpoints were overall survival and complications of BAE. Complications were reported using the CIRSE classification system for complications (14).

Statistical analysis

Statistical analyses were performed by using EZR software (v 1.52) (15). Recurrence-free survival was generated according to the Kaplan–Meier method. The impact of patient features (age, sex, body mass index), disease characteristics (number of ectopic and collateral arteries, initial VB, massive hemoptysis), and procedure specificities (micro-catheterization, use of spherical particles sized <700 µm, %UVB, and %UVB-lat) on hemoptysis recurrence after BAE was studied with a survival analysis using a Cox model. We tested all the variables in univariate analysis. Stepwise Cox regression was used to determine risk factors associated with recurrence of hemoptysis and the AIC was used to set a limit on the total number of variables included in the final model. A P value <0.05 was considered significant.

Results

Patients

A total of 646 BAE were performed in this center from January 2004 to June 2021. Of those procedures, 60 involved patients diagnosed with CF. Twelve procedures were excluded, one due to the lack of BAE report, five due to the unavailability of the pre-BAE chest CT scan, and six because it was performed after lung transplantation. Therefore, a total of 48 procedures were performed on 31 patients (12 women, 19 men; mean age = 27.9 years; age range = 20–58 years) and included in the analysis. Patient and procedure characteristics for each intervention are listed in Tables 1 and 2, respectively. Hemoptysis was described as massive before 22 (45.8%) procedures. A bleeding side was suspected before 36 (75%) BAE. Median initial VB and initial VB-lat were 7 (range = 2–27) and 6 (range = 1–27). Bronchial arteries were orthotopic and atypical arteries for 56.3% and ectopic and recruited collateral arteries for 43.7%.

Table 1.

Patient characteristics.

Characteristics
Total No. of patients	31
Age (years)	27.9 (20–58)
Sex
Female	12 (38.7)
Male	19 (61.3)
BMI (kg/m²)	20.0 (15.6–30.1)
BAE for hemoptysis	48
Hemoptysis” abundance
Massive	22 (45.8)
Non-massive	26 (54.2)
Suspected side of bleeding
Bilateral	12 (25.0)
Left	17 (35.4)
Right	19 (39.6)

Values are given as n (%) or mean (range).

BAE, bronchial artery embolization; BMI, body mass index.

Table 2.

Procedure characteristics.

Characteristics
Total No. of procedures	48
Micro-catheterization
Yes	39 (81.2)
No	9 (18.8)
Embolization agent
Spherical particles 300–700 µm	11 (22.9)
Spherical particles 700–1200 µm	16 (33.3)
Spherical particles 300–1200 µm	20 (41.7)
Gelatin foam	1 (2.1)
Vascular burden
Initial VB	7 (2–27)
UVB	3 (0–19)
%UVB	36.7 (0–100)
UVB-lat	2 (0–19)
%UVB-lat	22.5 (0–100)

Values are given as n (%) or median (range).

%UVB, percentage of unembolized vascular burden; %UVB-lat, percentage of unembolized vascular burden on the suspected bleeding side; VB, vascular burden; UVB, unembolized vascular burden; UVB-lat, unembolized vascular burden on the suspected bleeding side.

Table 3.

Predictive factors of recurrence after bronchial artery embolization.

Variables	Hazard ratio (95% CI)	P value
Univariate
Age	1.001 (0.967–1.059)	0.964
Sex	1.187 (0.467–3.017)	0.719
BMI	0.973 (0.840–1.128)	0.719
Massive hemoptysis	1.038 (0.422–2.558)	0.935
Number of ectopic and collateral arteries	1.232 (0.926–1.638)	0.153
Micro-catheterization	0.625 (0.224–1.751)	0.372
Spherical particles size <700 µm	0.589 (0.239–1.452)	0.250
Initial VB	1.054 (0.981–1.131)	0.150
%UVB	1.034 (1.016–1.052)	<0.001
%UVB-lat	1.024 (1.012–1.037)	<0.001
Multivariate
Spherical particles size <700 µm	0.429 (0.162–1.337)	0.089
%UVB	1.019 (0.996–1.042)	0.115
%UVB-lat	1.020 (1.002–1.038)	0.030

%UVB, percentage of unembolized vascular burden; %UVB-lat, percentage of unembolized vascular burden on the suspected bleeding side; BMI, body mass index; CI, confidence interval; VB, vascular burden.

Procedures

Embolization agents were always spherical particles (except for one phrenic artery treated with gelatin foam), with diameters in the range of 300–700 µm in 11 (22.9%) procedures, 700–1200 µm in 16 (33.3%) procedures, and 300–1200 µm in 20 (41.7%) procedures. Micro-catheterization was used in 39 (81.2%) procedures. A mean of 2.6 arteries (median = 2, range = 1–8) were embolized during each procedure, with a median embolized VB of 4 mm (range = 1–13 mm) and a median UVB of 3 mm (range = 0–19 mm). The median embolized VB-lat was 3 mm (range = 0–13 mm) and the median UVB-lat was 2 mm (range = 0–19 mm). Median %UVB and %UVB-lat were 36.7% (range = 0–100%) and 22.5% (range = 0–100%), respectively.

Risk factor of recurrence (Table 3)

A total of 19 recurrences occurred in nine patients with a median recurrence-free survival of 3.9 years. Among the recurrences, 18 were treated by BAE and one was treated by lung transplantation. The Kaplan–Meier estimate is shown in Fig. 3. In univariate analysis, age, sex, massive hemoptysis, micro-catheterization, use of particles sized < 700 µM, number of ectopic and collateral arteries, and initial VB were not significantly associated with recurrence.

In univariate analysis, the %UVB (hazard ratio [HR] = 1.034, 95% confidence interval [CI] = 1.016–1.052; P < 0.001) and the %UVB-lat (HR = 1.024, 95% CI = 1.012–1.037; P < 0.001) were significantly associated with recurrence.

In the multivariate analysis, only the %UVB-lat remained significantly associated with recurrence (HR = 1.020, 95% CI = 1.002–1.038; P = 0.030).

Overall survival

Overall, 30 patients were alive after a mean follow-up time of 2.1 years and one patient died of respiratory failure before lung transplantation could be performed due to CF disease progression.

Complications

Six complications occurred, five grade 1 and one grade 2 according to the CIRSE classification system for complications: one hematoma at the arterial puncture site with no additional treatment required, one asymptomatic vertebral artery dissection, three chest pains, and one bronchial infection treated by antibiotics. No complications of grade 3 or higher were reported.

Discussion

The value of pre-procedural CT-scans in hemoptysis management is now well established in the literature (16,17). In studies with variable etiologies, the sensitivity for bronchial artery detection on CT scans was estimated to be in the range of 62%–100% (18), and 70%–92.5% for the detection of the bleeding site (19,20). Due to the diffuse bronchial architectural abnormalities and often bilateral infectious lesions in CF, identification of the bleeding site is more challenging. However, as previously shown, the patient's report of clinical sensations such as “gurgling,” discomfort, unusual feeling, or localized warmth in a specific area of the thorax is a reliable method to localize the area of the bleeding (11 –13). In our series, when the bleeding side could not be highlighted, both lungs were suspected as being the source of the bleeding, consistent with daily practice resulting in bilateral embolization.

In the present study, the patient's %UVB-lat was the only factor associated with recurrence of hemoptysis after BAE in patients with CF suggesting that embolization of the lung suspected of being the source of the bleeding is sufficient and that the other arteries, also pathological in this diffuse disease, have less influence on clinical success. While many authors advocate bilateral embolization of all bronchial arteries (21 –24), our findings support a selective approach with embolization directed toward the lung suspected of being the source of the bleeding as previously proposed by others (12,13). UVB was evaluated in percentage rather than in absolute value as the initial VB range was wide, in the range of 2–27 mm.

Some authors evoked a responsibility of BAE in the CF patients’ respiratory function deterioration by disruption of CO₂ exchanges that can become significant through the enlarged bronchial arterial network developing throughout the disease (25,26). These hypotheses emphasize the need for optimization of BAE in patients with CF by avoiding systematic embolization of all bronchial arteries when the bleeding site can be highlighted. Careful selection of arteries to be embolized can reduce procedure duration, X-ray exposure, amount of contrast agent delivered, and potentially spare long-term respiratory function.

The complication rate of 12.5% with no major adverse event reported, was consistent with the literature, confirming the safety of BAE even in patients with CF with numerous collateral arteries frequently arising from the supra-aortic trunks (27,28).

The embolization agent was almost always spherical particles of trisacryl gelatin. Their physical behavior is more homogeneous than historically used uncalibrated PVA particles (29). They allow a theoretically more distal embolization by avoiding aggregation while protecting the microscopic systemic-pulmonary anastomoses. Their use coupled with micro-catheterization minimizes the risk of non-target artery embolization. No liquid embolization agent was used in our cohort. Some suggest it could maximize technical and clinical success with a more definitive occlusion of the targeted vessels (30).

We report a prevalence of ectopic and collateral arteries of 43.7%, consistent with the study by Martin et al. (31) on patients with CF, and two times higher than in the series with multiple etiologies by Hartman et al. (19), illustrating the major vascular recruitment in CF. Orthotopic bronchial arteries are admitted in the literature as embryological arteries arising from the aorta at levels T5–T6, while arteries originating outside the T5–T6 level or from another artery than the aorta are referred to as ectopic. Strictly speaking, they are distinct from collateral arteries that are acquired neo-vessels, recruited during pathological processes. Ectopic arteries arising from the descending aorta are also sometimes referred to as atypical rather than ectopic arteries. The frequency of atypical bronchial arteries is high, present in approximately 40% of patients (10,19), making the distinction between orthotopic and atypical arteries debatable. Therefore, following Carette et al. (10), we chose not to differentiate orthotopic and atypical arteries, especially because the distinction is useless for the interventional radiologist while they do not imply any difficulty or technical challenge during BAE, unlike ectopic and collateral arteries. In addition, we chose not to differentiate between ectopic and collateral arteries, not implying any therapeutic distinction in daily practice.

The study by Vidal et al. (21) suggested that the number of collateral arteries was associated with a higher risk of recurrence after BAE. However, in our cohort, the number of collateral arteries was not associated with a higher risk of recurrence. In the study by Vidal et al., no mention is made of performing a pre-BAE contrast-enhanced CT scan in order to visualize all bronchial arteries while identification of bronchial and collateral arteries was made by angiography of the descending thoracic aorta and intercostal and subclavian arteries. However, with angiography being less reliable than contrast-enhanced CT to depict all bronchial arteries (17), a higher number of collateral arteries having been embolized may have meant a higher total of collateral arteries missed by angiography.

The present study has some limitations. First, its retrospective nature led to some missing data as six BAE were excluded from the analysis due to five missing pre-BAE CT scans and one missing BAE report. Second, 17 years elapsed between the first and the last BAE. Over this period, many factors have evolved, such as hardware, software, operators, and practices that may invoke some selection and outcomes bias. However, BAE has not considerably evolved since 2004 and all procedures were performed using spherical particles while microcatheters were used in the majority of procedures. Third, the impact of other noteworthy elements of the clinical history, such as pulmonary function, pulmonary hypertension, liver cirrhosis, portal hypertension, genotypes, bacteriologic colonization with Pseudomonas or Staphylococcus aureus, or associated co-morbidities were not studied here. Fourth, the patient population and the procedural details were heterogeneous with half (54.2%) of the patients having non-massive hemoptysis and with various particles' sizes being used during BAE. Finally, although being one of the largest studies reporting BAE for hemoptysis in patients with CF, the study included a relatively small number of patients.

In conclusion, our experience suggests that the percentage of UVB on the suspected bleeding side is associated with the recurrence of hemoptysis after BAE in patients with CF and that an exhaustive embolization of all bronchial arteries vascularizing the lung that is suspected to be the source of the bleeding may be sufficient. Even in such a disease involving both lungs, unilateral BAE may be performed when hemoptysis originates from a single lung.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Guillaume Gravel

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