Pseudomonas aeruginosa isolation is an important predictor for recurrent hemoptysis after bronchial artery embolization in patients with idiopathic bronchiectasis: a multicenter cohort study
Respiratory Research volume 24, Article number: 84 (2023)
Nearly half of bronchiectasis patients receiving bronchial artery embolization (BAE) still have recurrent hemoptysis, which may be life-threatening. Worse still, the underlying risk factors of recurrence remain unknown.
A retrospective cohort was conducted of patients with idiopathic bronchiectasis who received BAE from 2015 to 2019 at eight centers. Patients were followed up for at least 24 months post BAE. Based on the outcomes of recurrent hemoptysis and recurrent severe hemoptysis, a Cox regression model was used to identify risk factors for recurrence.
A total of 588 individuals were included. The median follow-up period was 34.0 months (interquartile range: 24.3–53.3 months). The 1-month, 1-year, 2-year, and 5-year cumulative recurrent hemoptysis-free rates were 87.2%, 67.5%, 57.6%, and 49.4%, respectively. The following factors were relative to recurrent hemoptysis: 24-h sputum volume (hazard ratio [HR] = 1.99 [95% confidence interval [95% CI]: 1.25–3.15, p = 0.015]), isolation of Pseudomonas aeruginosa (HR = 1.50 [95% CI: 1.13–2.00, p = 0.003]), extensive bronchiectasis (HR = 2.00 [95% CI: 1.29–3.09, p = 0.002]), and aberrant bronchial arteries (AbBAs) (HR = 1.45 [95% CI: 1.09–1.93, p = 0.014]). The area under the receiver operating characteristic curve of the nomogram was 0.728 [95% CI: 0.688–0.769].
Isolation of Pseudomonas aeruginosa is an important independent predictor of recurrent hemoptysis. The clearance of Pseudomonas aeruginosa might effectively reduce the hemoptysis recurrence rate.
Bronchiectasis, a permanent and progressive bronchial deformation due to fibrosis of the bronchial wall muscles and destruction of elastic tissue, presents with chronic cough, purulent sputum, and recurrent hemoptysis [1, 2]. Aetiologies include congenital, idiopathic, post-infection, immunodeficiency, chronic obstructive pulmonary disease, connective tissue disease, ciliary dysfunction, and allergic bronchopulmonary aspergillosis [2, 3], with idiopathic bronchiectasis the most common in China [4, 5].
The United States Bronchiectasis Research Registry reported that 23% of patients with bronchiectasis had a history of hemoptysis . The hemoptysis volume was larger than other diseases with more cases leading to recurrence . In-hospital death rates due to hemoptysis among adults with bronchiectasis occurred in approximately 4.5–9.2% of hospitalizations [7, 8]. Bleeding arteries of patients with idiopathic bronchiectasis included bronchial arteries (BAs) and non-bronchial systemic arteries (NBSAs) . BAs are systemic arteries running through the hilum around the main bronchus that enter the lung, including BAs directly from the descending thoracic aorta, and aberrant BAs (AbBAs) from outside this area .
Bronchial arterial embolization (BAE) has become the first-line treatment for hemoptysis . However, nearly one-third of patients experience recurrent hemoptysis one year after BAE, and one-fifth of patients after BAE still require repeated embolization [12, 13]. A few clinical studies suggest that recurrent severe hemoptysis after BAE was associated with hemoptysis history, age, bronchial-pulmonary shunt, and NBSAs [2, 12]. However, these studies have overlooked other clinical indicators including pathogenic microorganisms and computed tomography (CT) imaging. In addition, few studies have specifically investigated the risk factors associated with recurrent hemoptysis with idiopathic bronchiectasis.
Therefore, this multicenter retrospective cohort study aimed to report the prevalence of the recurrence of hemoptysis in patients with idiopathic bronchiectasis who received BAE. Furthermore, we aimed to identify the independent risk factors of recurrence comprehensively including medical histories, pathogens, CT imaging, and responsible arteries.
A total of 667 patients with idiopathic bronchiectasis treated with BAE for hemoptysis between January 1, 2015, and December 31, 2019, from eight centers were enrolled in this multicenter, retrospective, observational cohort study. The study was approved by the institutional ethics review board of eight centers. The inclusion criteria were as follows: (1) age ≥ 18 years, (2) patients were diagnosed with idiopathic bronchiectasis according to the British Thoracic Society’s guideline for bronchiectasis in 2019  and the expert consensus of Chinese bronchiectasis in 2021 , and (3) patients underwent BAE to control hemoptysis. BAE was performed on patients with life-threatening hemoptysis, which manifested as a hemoptysis volume > 100 mL/d, abnormal gas exchange or airway obstruction, hemodynamic instability , or repeated hemoptysis that did not respond to medical treatment. The exclusion criteria were as follow: (1) missing CT angiography (CTA) (n = 39), (2) bronchiectasis combined with invasive pulmonary aspergillosis (n = 10), (3) technical failure (n = 1), and (4) lost to follow-up (n = 29). Based on these criteria, data from 588 patients were analyzed. A flowchart of the enrolled patients is shown in Fig. 1.
Study design and data collection
The baseline was defined as the time of BAE. Demographic characteristics (age, sex, smoking status, and duration of bronchiectasis), clinical data (symptoms on admission, comorbidities, pathogen findings, and CT and CTA findings), and treatment regimens were collected at baseline in detail from the electronic medical records of enrolled patients. CT findings included the number of broncniectatic lobes, bronchoarterial ratio, bronchiectatic type, and the presence of atelectasis and emphysema. CTA findings included the name and number of abnormal arteries. To minimize information bias, the imaging data were evaluated by two radiologists, and the results were averaged.
Patients were followed up via telephone interviews that covered their general conditions, recurrence status, recurrence time, and management in detail. The end of follow-up was December 2021. Recurrent hemoptysis was defined as the expectoration of blood alone without mucus from the airways or lung parenchyma after BAE . Recurrent severe hemoptysis was defined as hemoptysis requiring repeated BAE, lobectomy, or death from hemoptysis after BAE . Recurrence-free time was calculated from the date of BAE to the date of recurrence, death, or last follow-up.
Bronchial arterial angiography and embolization
BAE was performed by trained interventional doctors at all eight centers. All doctors received the same treatment procedure training  by designated radiologists of Shanghai Pulmonary Hospital, the special pulmonary vascular interventional center in China that experience with about 10,000 cases with BAE and more than 1000 cases per year. First, CTA (slice thickness, 0.625 or 1 mm; slice gap, 0.625 or 1 mm) was performed prior to BAE to assess lung lesions and possible relevant arteries . Second, angiography was performed through various types of 4F or 5F catheters based on the CTA findings through the femoral artery to confirm relevant arteries. Abnormal angiographic signs were vascular proliferation and distortion with extravasation of contrast medium in lung lesions, or systemic arterial-pulmonary circulation shunts. Lastly, all confirmed relevant arteries underwent super-selective catheterization and embolization with a coaxial microcatheter system. The embolic materials were 300–700 µm polyvinyl alcohol particles. Successful embolization was defined as no obvious distal vascular signs during the second angiography.
Continuous variables, if conforming to a normal distribution, were expressed as the mean ± standard deviation (SD), and if not conforming to a normal distribution, were expressed as median (interquartile range). Categorical variables were presented as numbers (percentages). To compare the difference between groups, we used the t-test for normal distribution continuous variables, the Mann–Whitney U test for non-normal distribution continuous variables, and the χ2 and Fisher exact test for categorical variables. Survival curves were plotted by the Kaplan–Meier method and compared by the log-rank test. Factors with a p-value < 0.05 of univariate regression and clinical relevance were included in the multivariate regression model. Significant predictors in multivariate Cox regression were used to construct a nomogram model. The model discrimination ability was evaluated by calculating the area under the receiver operating characteristic curve (AUC), while the calibration plot was used to graphically assess the calibration. A p-value < 0.05 was considered statistically significant. All of the analyses were conducted using SPSS (version 25), R software (version 4.1.0), and GraphPad Prism (version 8.3.0).
The features of all 588 patients are summarized in Table 1. The mean age was 59.9 years (range, 18–93), and 276 patients (46.9%) were female. No severe procedure-related complications occurred. Minor complications included chest tightness (n = 36), chest pain (n = 33), hematoma at the puncture site (n = 11), fever (n = 7), and dysphagia (n = 5) (Table 1). All symptoms were relieved spontaneously or after appropriate treatment (Additional file 2: Fig. S2).
The median duration of bronchiectasis before BAE was 10 years (interquartile range [IQR], 5–20 years), while the median duration of hemoptysis before BAE was 7 years (IQR, 2–20 years). Hypertension was present in 130 patients (22.1%). The pathogen with the highest isolation rate in sputum was Pseudomonas aeruginosa (P. aeruginosa), accounting for 140 patients (23.8%). Other bacteria isolated from sputum included Klebsiella pneumoniae, Haemophilus, Acinetobacter baumannii, and Stenotrophomonas maltophilia. The bronchoarterial ratio was more than three times in 217 patients (36.9%). Three or more bronchiectatic lobes were presented in 427 patients (72.6%), and 336 patients (57.1%) had mixed bronchiectasis (Table 1).
Outcomes of post-BAE
The median follow-up period of recurrent hemoptysis was 34.0 months (IQR, 24.3–53.3 months; range, 0.1–81.1 months). Hemoptysis occurred in 267 patients (45.4%) after BAE. The 1-month, 1-year, 2-year, and 5-year cumulative recurrent hemoptysis-free rates were 87.2%, 67.5%, 57.6%, and 49.4%, respectively. A total of 114 patients (19.4%) experienced recurrent severe hemoptysis, including 6 cases of pulmonary lobectomy, and 9 cases of death. The 1-year, 2-year, and 5-year cumulative recurrent severe hemoptysis-free rates were 91.4%, 84.9%, and 74.8%, respectively (Fig. 2).
Massive sputum quantities (18.4% [21/114] vs. 9.3% [44/474]; p < 0.001), isolation of P. aeruginosa (49.1% [56/114] vs. 17.7% [84/474]; p < 0.001), three or more lobes affected (86.0% [98/114] vs. 69.4% [329/474]; p = 0.001), more than two times the bronchoarterial ratio (54.4% [62/114] vs. 32.7% [155/474]; p < 0.001), mixed bronchiectatic type (72.8% [83/114] vs. 53.4% [253/474]; p < 0.001) (Table 1), and abnormal AbBAs (31.8% [35/114] vs. 18.6% [89/474]; p = 0.002) were more prevalent in the recurrent severe hemoptysis group (Table 2).
Independent predictors of recurrent hemoptysis
The results of the univariate Cox regression analysis are shown (Additional file 4: Tables S1 and S2). The independent predictors of recurrent hemoptysis were 24-h sputum volume (hazard ratio [HR], 1.99; 95% CI, 1.25–3.15), isolation of P. aeruginosa (HR, 1.50; 95% CI, 1.13–2.00), extensive bronchiectasis (HR, 2.00; 95% CI, 1.29–3.09), and abnormal AbBAs (HR, 1.45; 95% CI, 1.09–1.93) (Fig. 3A) The independent factors associated with recurrent severe hemoptysis were age (HR,1.02; 95% CI, 1.00–1.04), the isolation of P. aeruginosa (HR, 2.87; 95% CI, 1.89–4.36), and AbBAs (HR, 1.59; 95% CI, 1.05–2.41) (Fig. 3B). Recurrent hemoptysis was present in 96 of 140 patients (68.6%) in the isolation of P. aeruginosa group, 75 of 124 patients (60.5%) in the AbBAs group, 231 of 427 patients (54.1%) in the three or more lobes affected group, and 44 of 65 patients (67.7%) with massive sputum production. The impact of predictors on recurrence was confirmed by Kaplan–Meier curve analysis. The hemoptysis control rates were significantly lower in the isolation of P. aeruginosa group (p < 0.001), AbBAs group (p < 0.001), three or more lobes affected group (p < 0.001), and massive 24-h sputum production group (p < 0.001) (Additional file 1: Figure S1).
Based on the above independent significant predictors identified by multivariate Cox regression, two nomograms were established to predict the recurrent hemoptysis rate and recurrent severe hemoptysis rate of patients after BAE at 1-year, 3-year, and 6-year time points, respectively (Fig. 4A, B). AUC evaluated the discriminatory performance, which was 0.728 (95% CI, 0.688–0.769) in the recurrent hemoptysis group, and 0.709 (95% CI, 0.653–0.765) in the recurrent severe hemoptysis group (Fig. 4C). Finally, the calibration plot of the nomograms was performed at 2-year timepoint using 1000 bootstrap resamples, which showed good calibration (Fig. 4D).
Characteristics of abnormal arteries
Abnormal arteries were found on CTA images of all patients, and almost every patient had abnormal BA. Abnormal left inferior phrenic arteries, the most common abnormal NBSAs, were identified in 208 patients. Abnormal AbBAs on CTA were found in 124 patients (Additional file 3: Figure S3). Half of the abnormal arteries were anatomically normal bronchial arteries, of which 5.29% were abnormal AbBAs on CTA. The other 44.82% were NBSAs. All arteries showed thickening, some showed exudation and vascular network formation, and a few formed systemic-pulmonary artery shunts. Representative images before BAE were shown in Fig. 5.
To further explore the relationship between AbBAs and recurrence, the origination of abnormal AbBAs on CTA was analyzed in detail. AbBAs originating from the subclavian arteries and their branches were the most found in 41 patients (32%). The recurrence rate of hemoptysis patients with abnormal arteries was about 58% (72/124), and the recurrence rate of severe hemoptysis was more than 30% (38/124). Recurrent hemoptysis was found in all patients with AbBAs originating from the proper esophageal artery. More than half of patients with AbBAs originating from the left gastric artery recurred with severe hemoptysis. Patients with AbBAs originating from the left common carotid arteries accounted for only 1.57% (n = 2) of abnormal AbBAs, and no recurrence was observed (Additional file 3: Figure S3).
In this multicenter retrospective cohort study, the presence of recurrent hemoptysis was high in patients with idiopathic bronchiectasis after BAE affecting almost half of patients, while one-quarter of patients needed a second BAE or lobectomy. Recurrent hemoptysis correlated with P. aeruginosa infection, massive sputum production, abnormal AbBAs, and extensive bronchiectasis. Furthermore, recurrent severe hemoptysis was associated with P. aeruginosa infection, abnormal AbBAs, and age.
Several studies have investigated the recurrence of severe hemoptysis among different aetiologies of bronchiectasis. All 588 patients in this study were idiopathic bronchiectasis patients, and this is the first study to our knowledge assessing a single aetiology on BAE and hemoptysis recurrence. The cumulative recurrent severe hemoptysis rates in this study were similar to previous studies [12, 13, 18]. The recurrence rate of hemoptysis in patients with bronchiectasis was lower than in patients with mycobacterium, fungal infection, or a post-tuberculous phenotype of bronchiectasis [20, 21]. A previous retrospective study of 106 bronchiectasis patients revealed that neither the bacteria, presence of NBSAs, nor the number of bronchiectatic lobes correlated with hemoptysis control . Notably, this previous study  did not focus on P. aeruginosa, and the number of bronchiectatic lobes was less than that in our study. Another study showed lung destruction, sex, and systemic arterial-pulmonary circulation shunts could be used to predict recurrence . Instead of lung destruction, this study classified and described the CT findings of patients in detail .
Patients with P. aeruginosa had more severe radiological findings, worse lung function, and more stubborn disease [23,24,25]. P. aeruginosa, as a risk factor for exacerbated bronchiectasis , has attracted attention in bronchiectasis because of its high drug resistance, easy colonization, and repeated exacerbation [27,28,29]. Multiple mutations exist in the genotype of P. aeruginosa isolated from patients with bronchiectasis . We have reported that virulence genes exoU or pldA of P. aeruginosa led to a higher incidence of exacerbation in patients with idiopathic bronchiectasis . A vicious cycle of inflammation and infection can perpetuate symptoms and further airway damage. Guidelines recommend that patients with first isolation P. aeruginosa should be treated with eradication antibiotics , while long-term inhaled antibiotic or oral macrolides are recommended for patients with three or more repeated exacerbations per year [14, 32]. Whether long-term antimicrobial prophylaxis (such as macrolide) can reduce the risk of recurrent hemoptysis needs to be confirmed in prospective studies. Furthermore, this study showed that severe recurrent hemoptysis in patients with isolated P. aeruginosa was 2.87 times higher than that in patients without P. aeruginosa. Bronchiectasis patients with hemoptysis may be treated with antibiotics guided by routine sputum examination and antibiotic susceptibility results. More prospective or even randomized controlled trials are needed to explore management strategies for patients with bronchiectasis with P. aeruginosa infection to further optimize treatment guidelines.
Considering that patients with P. aeruginosa infection manifested more purulent sputum , this study specifically excluded the possibility of collinearity between P. aeruginosa and 24-h sputum volume so that sputum volume was an independent predictor of recurrent hemoptysis. Although recommended for bronchiectasis , airway clearance techniques might aggravate hemoptysis. Therefore, it is necessary to select appropriate airway clearance techniques or use expectorants regularly to discharge sputum.
In general, the severity of bronchiectasis should be associated with a recurrence incidence of hemoptysis. Therefore, we evaluated the severity of bronchiectasis with the bronchoarterial ratio, the number of bronchiectatic lobes, and bronchiectatic type on CT scans, and explored the correlation of bronchiectasis severity with recurrence. The multiple Cox regression analysis showed that recurrent hemoptysis was positively correlated with the number of bronchiectatic lobes. A Korean study showed that the number of bronchiectatic lobes was positively related to the in‑hospital mortality, and negatively related to the survival rate . Efforts should be made to delay the progression of bronchiectatic lobes, especially in patients with hemoptysis.
Abnormal arteries manifested as dilatation, exudation, vasoganglion formation, aneurysms, and arterial-pulmonary circulation shunts on CTA or digital subtraction angiography. Proper esophageal arteries accounted for 17.7% (n = 183) of NBSAs in this study. We have reported that proper esophageal arteries can be involved in hemoptysis, especially when the basal segment of the lobe is involved , which was confirmed in South Korea . The pulmonary plexus originates from the dorsal aorta during embryonic development. Once connected to the pulmonary arteries, the primitive BAs begin to degenerate, which results in only some branches formed in adults . The proportion of AbBAs originating from the subclavian and its branches were the largest, indicating more persistence of primitive branches of high origin . According to embryonic development, AbBAs are also probably potential in the general population; however, these arteries are too thin to be discerned on CTA. Chronic infection may induce vascular thickening, making them easier to identify. Compared to patients without abnormal AbBAs on CTA, patients with abnormal AbBAs had an increased incidence of recurrent severe hemoptysis in this study, supporting the idea that the pulmonary vascular system developed before the tracheal system and the development of BAs was due to some stimulus . As the lung developed, some blood vessels degenerated, but arteries of incomplete degeneration may thicken during infection. Therefore, more attention should be paid to abnormal AbBAs.
One strength of our study is that this was a multicenter study with the largest cohort of patients with idiopathic bronchiectasis. Endovascular treatments of hemoptysis were performed in more than 1000 cases per year in our hospital, and the operators of BAE in the eight centers were trained uniformly, which provided reassurance for this research. The second strength is that specific abnormal arteries were identified. The Third strength is that this study indicated the significance of P. aeruginosa in the recurrence of hemoptysis and suggested the importance of P. aeruginosa clearance therapy.
This study has some limitations as well. First, there is recall bias and reporting bias. Second, some unspecified and unquantifiable factors, such as environmental exposures, climatic variation, lifestyle, and psychosocial factors, also affect the outcomes of bronchiectasis  and require a more thorough investigation. We hope to improve these data in the future by conducting a prospective trial.
In summary, factors associated with relapse of hemoptysis after BAE in patients with idiopathic bronchiectasis are P. aeruginosa infection, massive sputum production, abnormal AbBAs, and extensive bronchiectasis. Recurrent severe hemoptysis correlated with age, P. aeruginosa infection, and abnormal AbBAs. In view of we could not change the responsible vascular malformation and the degree of bronchiectasis. Therefore, the isolation of P. aeruginosa from patients requires further attention, and the appropriate airway clearance techniques should be individually applied after BAE.
Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Aberrant bronchial arteries
Area under the receiver operating characteristic curve
Bronchial artery embolization
Non-bronchial systemic arteries
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We acknowledge all the patients involved in this study.
This work was supported by the National Natural Science Foundation of China (81925001); the Innovation Program of Shanghai Municipal Education Commission (202101070007-E00097); Program of Shanghai Municipal Science and Technology Commission (21DZ2201800); Bethune Charitable Foundation (BJ-RW2020001J); Innovative research team of high-level local universities in Shanghai and Innovative team of Shanghai Pulmonary Hospital.
Ethics approval and consent to participate
The study protocol was approved by the Institutional Review Board of The Shanghai Pulmonary Hospital (K21-297), Jiangxi Chest Hospital (2022), The Second People’s Hospital of Jingdezhen (HZKYXM2021001), The Second Affiliated Hospital of Hengyang Medical School (2021k03-042), People’s Hospital of Yichun (2021), Affiliated Hospital of Jiujiang University (2022), Jingzhou Hospital Affiliated to Yangtze University (20210803-1), Affiliated Hospital of Jianghan University (WHSHIRB-K-2022003). The anonymous nature of the data allowed the requirement for informed consent from the patients to be waived.
Consent for publication
The authors declare that they have no competing interests.
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The cumulative rates of patients with recurrent hemoptysis-free or recurrent severe hemoptysis-free with Pseudomonas aeruginosa, abnormal AbBAs on CTA, extensive bronchiectasis, and high 24-h sputum volume.
Distribution characteristics of abnormal arteries in 588 patients. BAs, bronchial arteries; NBSAs, non-bronchial system arteries.
Specific origination, the recurrence rate, and the severe recurrence rate of abnormal AbBAs on CTA. (A) The proportion of certain abnormal AbBAs on CTA to all abnormal AbBAs on CTA. (B) Ratio of recurrent hemoptysis group to all patients per abnormal AbBAs on CTA. (C) Ratio of recurrent severe hemoptysis group to all patients per abnormal AbBAs on CTA.
Univariate Cox regression and multivariate Cox regression analysis of the factors associated with recurrent hemoptysis of patients with idiopathic bronchiectasis after BAE. Table S2. Univariate Cox regression and multivariate Cox regression analysis of the factors associated with recurrent severe hemoptysis of patients with idiopathic bronchiectasis after BAE.
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Wang, LL., Lu, HW., Li, LL. et al. Pseudomonas aeruginosa isolation is an important predictor for recurrent hemoptysis after bronchial artery embolization in patients with idiopathic bronchiectasis: a multicenter cohort study. Respir Res 24, 84 (2023). https://doi.org/10.1186/s12931-023-02391-9