Bronchiectasis complicated by pulmonary aspergillosis: a multicenter study on prognosis and risk factors
Highlight box
Key findings
• Pulmonary aspergillosis (PA) is frequent in bronchiectasis and associated with a poorer prognosis. Cavities and prior pulmonary tuberculosis are significant risk factors for PA in these patients.
What is known and what is new?
• Infection plays an important role in the pathogenesis of bronchiectasis. Pseudomonas aeruginosa, Haemophilus influenzae, and Staphylococcus aureus are the most prevalent bacteria detected in bronchiectasis.
• Due to the destruction of lung tissue in patients with bronchiectasis and the lack of sensitive diagnostic methods, diagnosing bronchiectasis combined with aspergillosis is challenging. Data on clinical characteristics of patients with bronchiectasis with PA are scarce. The present study investigated the clinical significance of aspergillosis among patients with bronchiectasis.
What is the implication, and what should change now?
• Bronchiectasis combined with PA indicates a worse prognosis. It is very important to diagnose aspergillosis and carry out antifungal treatment as early as possible in patients with bronchiectasis.
Introduction
Background
Bronchiectasis is a chronic respiratory disease characterized by permanent dilation of the airways caused by multiple factors (1-3). Infection plays an important role in the pathogenesis of bronchiectasis. Diverse inciting factors result in impaired mucociliary clearance mechanism, which is essential for eliminating pathogens from the airways, thereby sustaining persistent inflammation. This, in turn, triggers an inflammatory response that damages the airways and induces abnormal remodeling, ultimately culminating in bronchiectasis (4,5). Pseudomonas aeruginosa, Haemophilus influenzae, and Staphylococcus aureus are the most prevalent bacteria detected in bronchiectasis (6-9).
Rationale and knowledge gap
Over the past decade, there has been an increasing recognition of the pathogenic role of Aspergillus in bronchiectasis. Aspergillus can cause a range of pulmonary diseases in patients with bronchiectasis (7,10-12), including invasive pulmonary aspergillosis (IPA), chronic pulmonary aspergillosis (CPA), and allergic bronchopulmonary aspergillosis (ABPA) (13,14). However, due to the destruction of lung tissue in patients with bronchiectasis and the lack of sensitive diagnostic methods, diagnosing bronchiectasis combined with aspergillosis is challenging. Data on clinical characteristics of patients with bronchiectasis with pulmonary aspergillosis (PA) are scarce.
Objective
The objective of this study was to assess both the prevalence and characteristics of PA in patients with bronchiectasis and identify potential factors associated with bronchiectasis complicated by aspergillosis. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1139/rc).
Methods
Study population
We retrospectively reviewed the medical records of bronchiectasis patients from four tertiary hospitals (Yijishan Hospital of Wannan Medical College, The Second Affiliated Hospital of Wannan Medical College, Nanjing Drum Tower Hospital, Anhui Chest Hospital) between February 2023 and April 2024. After excluding patients with coexisting conditions such as ABPA, lung cancer, interstitial lung disease (ILD), active pulmonary tuberculosis (TB), hematologic malignancy, or a history of lung transplantation, a total of 899 bronchiectasis patients were included in the study. Among these, 303 cases underwent screening for PA, and 62 cases were diagnosed with PA. The diagnosis of IPA was based on European Organization for Research and Treatment of Cancer/Mycoses Study Group Education and Research Consortium (EORTC/MSGERC) Definitions of Invasive Fungal Diseases: Summary of Activities of the Intensive Care Unit Working Group (15). CPA was diagnosed according to the European Society for Clinical Microbiology and Infectious Diseases and European Respiratory Society guidelines (16). All patients should have their respiratory samples [sputum, bronchoalveolar lavage fluid (BALF), or pulmonary biopsy] tested for Aspergillus. Clinical data, including the cause of bronchiectasis, clinical manifestations, comorbidities, microbiological isolation, chest imaging, treatment, and outcomes, were recorded. Patients were followed-up for 1 year. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Drum Tower Hospital (No. 2023-579). All participating hospitals were informed and agreed to the study.
Statistical analysis
Statistical analysis was performed using SPSS (version 25). The Kolmogorov-Smirnov test was used to assess the normality of data distribution. Quantitative variables are presented as mean ± standard deviation (SD) for normally distributed data or as median with interquartile range (IQR) for non-normally distributed data. Group comparisons for normally distributed quantitative variables were performed using Student’s t-test, while the Mann-Whitney U-tests were applied for non-normally distributed data. Qualitative variables were expressed as absolute numbers and percentages. Comparisons of proportions for qualitative variables were performed using the χ2 test or Fisher’s exact test. The time to first hospitalizations for each group was analyzed using the Kaplan-Meier (KM) method and compared with the log-rank test. KM curves were generated with R (version 4.2.1). Logistic regression analysis was used to assess the risk factors for PA. A P value <0.05 was considered statistically significant.
Results
Study population and Aspergillus detection results
Among 899 patients with bronchiectasis admitted to the four hospitals between February 2023 and April 2024, 303 were screened for PA (Figure S1). Aspergillus spp. was isolated from sputum, BALF, or pulmonary biopsy in 68 patients. Considering clinical manifestations of infection and other supporting evidence, 62 cases were finial diagnosed with PA, including IPA (n=11) and CPA (n=51). An additional 241 patients without Aspergillosis infection evidence were included in the non-PA group.
Among the 68 positive Aspergillus detection results, 51 cases were identified as patients with PA, while the remaining 17 cases were categorized as non-PA patients and considered to represent colonization. The most frequently isolated species was Aspergillus fumigatus (38/68, 34 in PA patients and 4 in non-PA patients), followed by Aspergillus flavus (15/68, 12 in PA patients and 3 in non-PA patients), Aspergillus niger (4/68, 2 in PA patients and 2 in non-PA patients), Aspergillus oryzae (1/68, in PA patients), and unclassified Aspergillus species (15/68, 7 in PA patients and 8 in non-PA patients) (Figure 1). Notably, five PA patients had two species of Aspergillus isolated [Aspergillus fumigatus + Aspergillus flavus (n=3), Aspergillus flavus + Aspergillus niger (n=1), and Aspergillus flavus + Aspergillus oryzae (n=1)].
Characteristics of PA and non-PA patients
A detailed summary and comparison of clinical characteristics between the PA and non-PA groups are presented in Table 1. No significant differences were observed between the two groups in terms of age and etiology. However, the PA group included a higher proportion of males (69.4% in the PA and 37.8% in the non-PA) and smokers (25.8% in the PA and 8.7% in the non-PA) compared to the non-PA. Additionally, the PA group exhibited a lower mean body mass index (BMI) (20.2 kg/m2 in the PA and 21.8 kg/m2 in the non-PA), a higher prevalence of connective tissue diseases (CTDs) (9.7% in the PA and 2.1% in the non-PA), and a history of TB (58.1% in the PA and 12.9% in the non-PA). There were no significant differences between the groups in terms of the use of bronchodilators, macrolides, or inhaled corticosteroids (ICSs). Notably, the PA group had a higher proportion of immunosuppressive therapy (3 cases in the PA and none in the non-PA).
Table 1
| Variables | PA (n=62) | Non-PA (n=241) | P value |
|---|---|---|---|
| Male | 43 (69.4) | 91 (37.8) | 0.001 |
| Age (years) | 61 [55–69] | 65 [56–72] | 0.17 |
| Etiology | 0.06 | ||
| Idiopathic | 17 (27.4) | 102 (42.3) | |
| Postinfection | 36 (58.1) | 102 (42.3) | |
| Other | 9 (14.5) | 37 (15.4) | |
| Comorbidities | |||
| Previous TB | 36 (58.1) | 31 (12.9) | 0.001 |
| COPD | 11 (17.7) | 29 (12.0) | 0.24 |
| Asthma | 1 (1.6) | 13 (5.4) | 0.21 |
| Cardiovascular | 19 (30.6) | 104 (43.2) | 0.07 |
| Diabetes | 8 (12.9) | 32 (13.3) | 0.94 |
| CTD | 6 (9.7) | 5 (2.1) | 0.01 |
| Smoking status | |||
| Current or ex-smoker | 16 (25.8) | 21 (8.7) | 0.001 |
| Never | 46 (74.2) | 220 (91.3) | 0.001 |
| BMI (kg/m2) | 20.2 [17.2–22.0] | 21.8 [19.5–24.3] | 0.001 |
| mMRC score | 1 [1–3] | 1 [0–2] | 0.001 |
| Symptoms | |||
| Cough/expectorant | 52 (83.9) | 156 (64.7) | 0.004 |
| Hemoptysis | 31 (50.1) | 68 (28.2) | 0.001 |
| Fever | 15 (24.2) | 29 (12.0) | 0.02 |
| Dyspnea | 19 (30.6) | 106 (44.0) | 0.057 |
| Chest pain | 3 (4.8) | 7 (2.9) | 0.45 |
| Respiratory failure | 6 (9.7) | 21 (8.7) | 0.81 |
| Exacerbation during last year (number) | 1 [1–3] | 1 [1–2] | 0.001 |
| Hospital admission during last year (number) | 1 [1–3] | 1 [1–2] | 0.001 |
| Pseudomonas colonization | 9 (14.5) | 54 (23.2) | 0.14 |
| Long-term treatment | |||
| Bronchodilator | 9 (14.5) | 45 (18.7) | 0.45 |
| Antibiotics | 2 (3.2) | 12 (5.0) | 0.56 |
| ICSs | 4 (6.5) | 13 (5.4) | 0.75 |
| Immunosuppressive therapy | 3 (4.8) | 0 (0.0) | 0.001 |
Data are presented as n (%) or median [IQR]. BMI, body mass index; COPD, chronic obstructive pulmonary disease; CTD, connective tissue disease; ICS, inhaled corticosteroid; IQR, interquartile range; mMRC, modified Medical Research Council; PA, pulmonary aspergillosis; TB, tuberculosis.
Symptoms such as cough/expectorant, hemoptysis, and fever were more prevalent in the PA group, and the PA group also showed higher modified Medical Research Council (mMRC) scores than the non-PA group. No significant differences were observed between the two groups in clinical manifestations such as shortness of breath, chest pain, or respiratory failure, and the positive rate of Pseudomonas aeruginosa also did not differ significantly.
Notably, during the preceding year, the PA group experienced more frequent exacerbations and hospitalizations compared to the non-PA group (P=0.001).
Laboratory and chest imaging results of bronchiectasis patients with PA and non-PA group
Laboratory findings and chest imaging results are detailed in Table S1. No significant differences were observed between the two groups in leukocyte count, neutrophil count, hemoglobin (Hb), lactate dehydrogenase (LDH), C-reactive protein (CRP), procalcitonin (PCT), and albumin (ALB). However, lymphocyte count levels were lower in the PA group, while platelet (PLT) counts were higher in the PA group compared to the non-PA group.
As biomarkers commonly used in diagnosing PA, BALF galactomannan (GM) demonstrated significantly higher sensitivity than serum GM sensitivity (91.3% vs. 26.8%, P<0.001) (Figure S2).
Chest high-resolution computed tomography (HRCT) scans revealed that cavities were more frequently observed in the PA group. Nodules and pleural thickening were also more prevalent in the PA group than in the non-PA group.
Analysis of prognosis and risk factors associated with PA in bronchiectasis
In the PA group, 53 patients received antifungal therapy, including 7 who underwent lobectomy combined with antifungal treatment. Lobectomy was performed for hemoptysis in 4 patients and localized disease with persistent symptoms in 3 patients. Voriconazole was the most commonly used antifungal agent (n=49), with 7 cases discontinued or switched to other medications due to side effects or lack of effectiveness. Itraconazole, isavuconazole, and amphotericin B were administered to 2, 1, and 1 patient, respectively. Nine CPA patients did not receive antifungal therapy, and 2 of these patients died during the 12-month follow-up. The in-hospital mortality rate in the PA group was higher than that in the non-PA group (4.8% vs. 0.4%, P=0.03). During the 6- and 12-month follow-ups, the PA group experienced more frequent hospitalizations compared to the non-PA group (P=0.001). At 12 months after discharge, the mortality rate was higher in the PA group (11.3% vs. 3.5%, P=0.02). Detailed treatment regimens and outcomes are presented in Table 2.
Table 2
| Variables | PA (n=62) | Non-PA (n=241) | P value |
|---|---|---|---|
| Antifungal therapy | – | ||
| Voriconazole | 43 (69.4) | – | |
| Posaconazole | 2 (3.2) | – | |
| Itraconazole | 4 (6.5) | – | |
| Isavuconazole | 2 (3.2) | – | |
| Lobectomy | 7 (11.3) | 0 (0.0) | 0.001 |
| In-hospital mortality | 3 (4.8) | 1 (0.4) | 0.03 |
| 6-month follow-up | |||
| Hospitalizations | 1 [0–2] | 0 [0–1] | 0.001 |
| 12-month follow-up | |||
| Hospitalizations | 1 [1–4] | 0 [0–1] | 0.001 |
| Mortality | 7 (11.3) | 8 (3.5) | 0.02 |
Data are presented as n (%) or median [IQR]. IQR, interquartile range; PA, pulmonary aspergillosis.
As illustrated in Figure 2, during the 12-month follow-up period, the non-PA group had a significantly longer mean time to first hospitalizations [267 days; 95% confidence interval (CI): 251–285] compared to the PA group (109 days; 95% CI: 79–140; log-rank P=0.001).
To identify the factors associated with PA in patients with bronchiectasis, we performed a multivariate logistic regression analysis. Our findings indicate that cavities on HRCT [odds ratio (OR): 13.547; 95% CI: 5.304–34.596; P=0.001] and prior pulmonary TB (OR: 3.611; 95% CI: 1.588–8.210; P=0.002) were independently associated with PA in bronchiectasis (Table 3).
Table 3
| Variables | Univariable analysis | Multivariable analysis | |||
|---|---|---|---|---|---|
| OR (95% CI) | P value | OR (95% CI) | P value | ||
| BMI <18.5 kg/m2 | 1.412 (0.787–2.535) | 0.25 | |||
| Lymphocyte count <1.0×109/L | 2.201 (1.186–4.085) | 0.01 | 1.800 (0.796–4.072) | 0.16 | |
| ≥ Two exacerbations in previous year | 2.723 (1.489–4.981) | 0.001 | 1.242 (0.580–2.663) | 0.58 | |
| With cavities | 29.037 (12.94–65.161) | 0.001 | 13.547 (5.304–34.596) | 0.001 | |
| Previous TB | 9.38 (4.996–17.008) | 0.001 | 3.611 (1.588–8.210) | 0.002 | |
BMI, body mass index; CI, confidence interval; OR, odds ratio; PA, pulmonary aspergillosis; TB, tuberculosis.
Discussion
Key findings
The present study investigated the clinical significance of aspergillosis among patients with bronchiectasis. Aspergillus spp. were isolated from sputum, BALF, or pulmonary biopsy in 68 patients. There were 62 cases that were finally diagnosed with PA, and the majority of them were CPA (n=51). Patients with PA exhibited a poorer prognosis than those without PA, a higher in-hospital mortality rate, more frequent hospitalizations at 6 months and 1 year after discharge, and a higher mortality rate 1 year after discharge.
Comparison with similar research
The prevalence of Aspergillus spp. isolation in our study is similar to previous reports (7,10,17). The most prevalent species isolated was A. fumigatus. Among the 68 patients with positive Aspergillus isolation, 51 were eventually diagnosed with PA, which was significantly higher than that in previous studies. This might be because the included patients in this study were in-patients with severe bronchiectasis. This also suggests that the isolation of Aspergillus from hospitalized patients with bronchiectasis requires vigilance against the possibility of aspergillosis.
Patients with PA had some different demographic characteristics from the non-PA group. Patients with PA included a higher proportion of males and smokers compared to the non-PA group, and patients in the PA group also exhibited a lower BMI than in the non-PA group. This is consistent with a previous study (18). Low BMI and underweight are commonly described in patients with PA.
Explanations of findings
The underlying diseases differed between the two groups. Patients with PA had a higher prevalence of CTDs, a higher proportion of immunosuppressive therapy, and a history of TB. This might be that the immunosuppressive drugs used by CTD patients are significantly associated with the risk of PA, and the history of TB itself is also an important risk factor for PA (19-22). The proportions of patients who used inhaled corticosteroids (ICSs) or bronchodilators were not higher in the group of diagnosed PA. This may be for the proportion of bronchiectasis patients receiving ICS treatment was relatively low. Lymphocytes are lower in patients with PA, possibly because lymphocytes are an important part of Aspergillus immunity; decreased lymphocytes are an important risk factor for aspergillosis (23,24).
In the diagnosis of bronchiectasis combined with aspergillosis, the BALF GM test had a relatively high sensitivity, but the serum GM test had a relatively poor sensitivity in our study.
There were 85.5% of our PA patients who underwent antifungal therapy, including 7 who underwent lobectomy combined with antifungal treatment. Lobectomy was performed for hemoptysis in 4 patients and localized disease with persistent symptoms in 3 patients. The in-hospital mortality rate in the PA group was higher than that in the non-PA group. During the 6- and 12-month follow-ups, the PA group experienced more frequent hospitalizations compared to the non-PA group. At 12 months after discharge, the mortality rate was higher in the PA group. Nine CPA patients did not receive antifungal therapy, and 2 of these patients died during the 12-month follow-up. This suggests that the prognosis may be worse if antifungal treatment is not carried out after the diagnosis of PA. However, due to the small number of cases, further research is needed.
Multivariate analysis identified the presence of cavities on chest HRCT and a previous history of pulmonary TB as independent risk factors for the development of PA. This might be because the cavities in the lungs provide a favorable environment for the growth of Aspergillus, but chronic Aspergillus infection can also cause pulmonary cavities. Therefore, the presence of cavities on chest HRCT in patients with bronchiectasis requires vigilance against the possibility of PA.
Strengths and limitations
This study represents a real-life setting of Aspergillus spp. isolation in clinical practice and diagnosis of bronchiectasis combined with PA. This study provides information on the prevalence of Aspergillus spp. isolation and significance of PA in patients with bronchiectasis. This may assist in overcoming clinician’s difficulty of interpreting the meaning of a positive isolation of Aspergillus spp. and enhance their understanding of bronchiectasis combined with PA. This study also highlights the need to increase awareness of PA in patients with bronchiectasis and implement timely diagnosis and treatment.
There are also several limitations of this study. The principal limitation is the difficulty of diagnosing PA in patients with bronchiectasis. The positive rates of Aspergillus culture and serological tests are low, and some patients had severe lung damage, which brings challenges to diagnosis, and some patients may be missed in diagnosis, the actual incidence of bronchiectasis combined with aspergillosis may be higher than reported. Second, due to the limited number of cases in our study, a small subset of variables could not be included in the multivariate model, which may have constrained the comprehensiveness of our prognostic analysis. Additionally, given the retrospective nature of this study, residual confounding from unmeasured or unrecorded variables cannot be fully excluded, which may affect the interpretability of our findings to some extent.
Conclusions
In conclusion, isolation of Aspergillus is frequent in patients with bronchiectasis and highly indicates PA. Bronchiectasis combined with PA indicates a worse prognosis. It is very important to diagnose aspergillosis and carry out antifungal treatment as early as possible in patients with bronchiectasis.
Acknowledgments
We would like to express our sincere gratitude to all the participants in this study for their valuable time and cooperation. We also wish to acknowledge the dedicated efforts of the clinicians and researchers involved in medical record collection and data management. Their contributions were essential to the success of this study.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1139/rc
Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1139/dss
Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1139/prf
Funding: This work was supported by
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1139/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Drum Tower Hospital (No. 2023-579). All participating hospitals were informed and agreed to the study. Informed consent was taken from all the patients.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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