Abstract
Recent bronchiectasis studies from large-scale multinational, multicentre registries have demonstrated that the characteristics of the disease vary according to geographic region. However, most perspectives on bronchiectasis are dominated by data from Western countries. This review intends to provide an Asian perspective on the disease, focusing on the established registries in India, Korea and China. Asian patients with bronchiectasis are less likely to show female predominance and experience exacerbations, are more likely to be younger, have milder disease, and have fewer options for guideline-recommended treatment than those living in other global regions. Furthermore, Asian bronchiectasis patients demonstrate different comorbidities, microbiological profiles and unique endophenotypes, including post-tuberculosis and dry bronchiectasis. Notably, each Asian region reveals further geographic variations and inter-patient differences. Future studies are warranted to better characterise Asian patients with bronchiectasis.
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Asian patients with bronchiectasis exhibit unique characteristics, including different comorbidities, microbiological profiles and endophenotypes, compared with those living on other continents. https://bit.ly/3YBg3JJ
Introduction
Heterogeneity is the fundamental aspect of bronchiectasis because the disease represents the final common pathway of several infectious, genetic, autoimmune and allergic disorders [1, 2]. Furthermore, epidemiological studies from large-scale multicentre registries have recognised bronchiectasis as heterogeneous in geographic regions [3–11]. Asian patients with bronchiectasis demonstrate different characteristics from those living in other regions, including Europe, the USA and Australia (figure 1).
However, perspectives on bronchiectasis are often dominated by data from Europe and the USA. This review aimed to provide an Asian perspective on the disease while reviewing the clinical characteristics, aetiologies, microbiology, treatment, environmental factors and endophenotypes of Asian bronchiectasis. To this end, we compared characteristics between Asian patients in bronchiectasis registries, including those from Korea, India, Australia and Europe [3, 6, 7, 10] (table 1). Furthermore, each Asian country has different characteristics of bronchiectasis, which were compared between Korean, Indian and Chinese patients (table 2).
Search strategy
The authors searched the PubMed, Google Scholar and Embase databases between January 1990 and April 2024 using the search terms “bronchiectasis” and “Asian countries”. H. Choi , J-F. Xu and R. Dhar assessed eligibility.
Demographics
Bronchiectasis is a common condition in Asia. The overall prevalence of bronchiectasis is 464 cases per 100 000 people in Korea [12] and 1200 per 100 000 individuals aged ≥40 years in China [13]. These figures are higher compared to Western countries, where the prevalence is 67 and 138 cases per 100 000 individuals in Germany and the USA, respectively [14, 15]. Although data from China and Korea consistently indicate a female predominance of bronchiectasis, in line with the epidemiology of other continents [3, 6, 7], Indian bronchiectasis registry data demonstrate a male predominance, possibly correlated with the high prevalence of tuberculosis (TB) [16, 17]. Additionally, compared with Australian and European patients with bronchiectasis, Asian patients show a generally lower body mass index (BMI) (approximately 21.5 kg·m−2 of median), likely influenced by chronic disease-related metabolic demands and potentially further hampered by TB-destroyed lungs [17]. Although China and India have high smoking rates, smokers constitute only a modest proportion (approximately 26%) of the Asian bronchiectasis population [18–21]. The economic burden of bronchiectasis among Asian patients is noteworthy [12], with epidemiological data from China indicating an annual per capita cost of $7697 for patients with bronchiectasis [16].
Comorbidities
Comorbidity patterns in Asian patients showed intercontinental variability and intercountry variation within the continent. In Korea and India, patients with bronchiectasis exhibit a higher proportion of comorbid asthma and COPD (both >20%) compared to those in China (approximately 10%), possibly because of delayed diagnosis and underdiagnosis of these conditions in China [19, 21–24]. The prevalence of comorbid gastro-oesophageal reflux disease is relatively common in Asian bronchiectasis populations (approximately 16%), whereas stroke is exceptionally rare (approximately 1%) [19, 22, 24]. The rate of osteoporosis was significantly lower in Korean and Indian patients with bronchiectasis (7%) than in both Australian (23%) and European (13%) patients, which may be associated with the younger age of Asian patients (table 1). The proportion of diabetes mellitus is lower among Chinese patients with bronchiectasis (approximately 7%) compared to Korea (12%) and India (14%), whereas coronary heart disease is more prevalent in Indian patients (16.2%) than in Chinese (8%) and Korean (5%) patients [19, 21–24].
Radiological status
Cystic bronchiectasis constitutes approximately 50–60% of chest computed tomography findings in Asian patients with bronchiectasis and the left lower lobe is the most commonly affected at approximately 60% [17, 25–27]. The Reiff score, which serves as an imaging index for assessing disease severity, has a median of 6 (interquartile range (IQR) 3–9) [19]. Although cystic bronchiectasis is common, the Reiff scores suggest mild to moderate severity of imaging findings in Asian patients, possibly due to the lower involvement of the lung lobes in the entire study population.
Disease severity
Respiratory distress and exacerbation significantly affect the prognosis and quality of life of patients with bronchiectasis. Compared to patients with bronchiectasis in other geographic regions, Asian patients with bronchiectasis seemed to experience more severe dyspnoea and showed relatively less disease severity, which was not in agreement with the hospitalisation rate. The modified Medical Research Council (mMRC) dyspnoea scale was higher in Asian patients with bronchiectasis than in those living in Australia and Europe. A higher mMRC score would have been driven more by Indian registry data than Korean data [8, 10]. In line with this, Chinese patients with bronchiectasis had a median mMRC dyspnoea score of 1.5 (IQR 0.7–2.4) [17]. The frequency of exacerbations in the previous year was relatively low among Asian populations with bronchiectasis, with a median of approximately 1 (IQR 0–2) [19]. The proportion of patients hospitalised at least once in the previous year varies significantly among Korea, India and China, ranging from 18 to 60%, possibly influenced by healthcare policies, physician treatment strategies and patient preferences in each country [22]. As hospitalisation significantly affects the Bronchiectasis Severity Index (BSI), BSI score risk classification considerably differs among countries. For instance, in a single-centre study in China, 60% of patients were classified as having a “severe” BSI score, whereas in Korea, the proportion was only 27% [27, 28]. Overall, the median BSI score among Asian patients with bronchiectasis was approximately 7, which was similar to the BSI of European data (median=7) but lower than Australian data (median=9). In addition, approximately 40% of patients were classified as having “severe” bronchiectasis in Asia (table 1). In summary, bronchiectasis severity in Asian patients typically ranges from mild to moderate. From an Asian perspective, as recurrent hospitalisations potentially increase the risk of drug-resistant bacterial infections, particularly in the context of antibiotic overuse, region-specific short-course antibiotic treatment protocols should be explored.
Microbiology–bacteriome in Asia
The expectoration of sputum is far less common in Asia than elsewhere. According to multicentre registry data, approximately 60 and 40% of the Indian and Korean populations, respectively, do not produce sputum everyday [8, 10]. At least one sputum sample was collected from 59% of the Indian population and 73% of the Korean population. Single-centre studies from China, however, show a higher amount of daily sputum production at approximately 81%.
Pseudomonas (P.) aeruginosa was the most common bacteria isolated in most Asian studies and in the Korean and Indian registries. Haemophilus (H.) influenzae, Moraxella (M.) catarrhalis and Staphylococcus aureus are common in Europe but rarely isolated in Asia. In contrast, Enterobacteriaceae is grown on culture in 1 out of 10 patients from India and seems rare in other parts of Asia. Klebsiella is the most common bacteria in this category and its isolation is associated with greater mortality [9]. A study from Singapore that examined the microbiome of bronchiectasis identified Neisseria as a significant component. Neisseria species commonly represent commensals; however, a Singapore-based research group used a combination of human cohorts, next-generation sequencing, systems biology and animal models to demonstrate that the presence of Neisseria species indicates a poor prognosis, including an increased risk of exacerbations [29]. Nontuberculous mycobacteria (NTM), commonly cultured in the US population [3], varies across the Asian sub-continent and is uncommon in parts of Asia and rare in India [8, 30–34]. This phenomenon could have been influenced by the structure and organisation of data collection and research; for instance, the Korean bronchiectasis research group originally focused on airway disease, although sputum mycobacterial culture was performed in all patients enrolled in the Korean and Indian bronchiectasis registries. Additionally, the authors highlight that significant laboratory variations, where the cultures are processed across Asia, should also be considered when interpreting microbiologic profiles in Asian patients with bronchiectasis. The laboratory variations include specimen transport, processing protocols, etc.
Hence, the microbiology in Asia shows a greater preponderance of Gram-negative bacteria with a lower incidence of Gram-positive bacteria and atypical organisms. There is also heterogeneity within the continent; therefore, it is important to understand the local microbiological milieu. The microbiomes of bronchiectasis, especially post-TB bronchiectasis, allergic bronchopulmonary aspergillosis (ABPA) and bronchiectasis-COPD overlap, need to be better defined from an Asian perspective.
Lung function
Spirometry in bronchiectasis varies across continents. In Korean bronchiectasis registry data, the majority of patients (54%) had an obstructive ventilatory defect [10] (table 2). This observation may have resulted from comorbid COPD and asthma in Korean patients with bronchiectasis. However, European patients with bronchiectasis showed a relatively lower rate of obstructive ventilatory defect (35%), even though comorbid COPD and asthma were also common in this population [7] (table 1). In this regard, it was hypothesised that this is because patients with post-TB bronchiectasis often develop airflow obstruction along with bronchiectasis [35]. However, Indian bronchiectasis registry data demonstrated that patients with post-TB bronchiectasis had low lung function (low forced vital capacity (FVC)) and a predominantly restrictive ventilatory defect [8]. Bronchiectasis seemed to have the greatest impact on lung function in the Asian population compared with the rest of the world. Low lung function could be related to the underdiagnosis of coexisting chronic lung diseases. These data indicate the need for better characterisation of patients with post-TB bronchiectasis. This, in turn, would also help develop guidelines to follow-up with patients even after seemingly recovering from TB.
Aetiology
Idiopathic and post-infective bronchiectasis were the leading aetiologies in all international bronchiectasis cohorts; however, post-TB bronchiectasis was more common in the Korean and Indian registries than in the Australian and European ones. In addition to these three aetiologies, asthma and NTM pulmonary disease were included in the top five aetiologies in the Korean registry and ABPA and COPD were included in the Indian registry (table 1). COPD and asthma were common in Taiwan [36] and immunodeficiency was a common aetiology in a single-centre Chinese study [37].
Notably, post-TB bronchiectasis is currently the leading cause of bronchiectasis in Asia [8, 10, 36, 37], which is a natural phenomenon considering the high TB burden in this region [38]. Post-TB bronchiectasis is discussed later as a phenotype of Asian bronchiectasis. However, the change in TB epidemiology may be followed by a reduction in the proportion of post-TB bronchiectasis cases in Asia. For example, in Korea, government-led TB control programmes have decreased the incidence of TB, consequently changing the country's status from a high to an intermediate TB burden [39, 40]. Similarly, the proportion of post-TB bronchiectasis has continuously decreased among the aetiologies of Chinese paediatric bronchiectasis [13]. In this regard, TB control could contribute to reducing the disease burden of bronchiectasis in Asia and potentially change the common aetiologies of bronchiectasis.
Another important issue needs highlighting, specifically that identifying a patient with bronchiectasis who has a history of TB does not necessarily imply that the patient has post-TB bronchiectasis. This is especially true for TB-endemic countries such as India. Hence, these patients should undergo a comprehensive workup to define the aetiology of bronchiectasis.
Common aetiologies of bronchiectasis are also linked to standardised testing of the disease; therefore, testing protocols may need to be optimised according to geographic regions. For example, the European Respiratory Society (ERS) bronchiectasis guidelines recommend testing for ABPA in adult patients with bronchiectasis [41]. This recommendation also seems reasonable for the Indian population, as ABPA is a common cause of bronchiectasis. Only 18% of the Indian registry patients were screened for ABPA and 50% of them were found to have the disease [2]. This underlines the importance of ABPA screening in all Indian patients with bronchiectasis. However, the low prevalence of ABPA has led Korean experts to recommend ABPA testing in patients with bronchiectasis and history of asthma [42]. As such, the aetiologies of bronchiectasis would significantly differ among Asian countries because there are huge differences in healthcare systems and the effects of the environment, such as air quality and exposure to biomass fuels. Established Asian bronchiectasis cohorts and future registries will help acquire a true picture of bronchiectasis aetiologies and develop optimised guidelines and strategies for investigation in the region [8, 11, 43].
Asian environment
Ambient air pollution is recognised as a leading contributor to disability-adjusted life-years [44]. Furthermore, rapid economic growth in the last century has particularly worsened air pollution in Asian countries [45, 46]. Environment plays a considerable role in bronchiectasis because air pollution increases the risk of bronchiectasis exacerbation, a significant event in the natural course of the disease [47–49]. Notably, a UK study demonstrated that large fluctuations in the air quality index were associated with an increased risk of exacerbation [47].
These findings were replicated in studies conducted in Asian countries. A study performed in Southern China collected the daily concentrations of ambient air pollutants and examined their association with hospital admissions for bronchiectasis [50]. This study demonstrated that acute fluctuations in air pollution were potential risk factors for hospitalisation in patients with bronchiectasis; moreover, this phenomenon was more evident in older age groups and females [50]. A study conducted in Seoul also showed that increased concentrations of particulate matter smaller than 10 nm in diameter, nitrogen dioxide, sulphur dioxide and carbon monoxide seemed to increase healthcare utilisation in patients with bronchiectasis [51]. However, considering that air pollution is more severe in Asian countries than in Western countries, further studies are warranted to elucidate this issue in Asian patients with bronchiectasis.
Treatment
The largest lacunae appear to be involved in the treatment of this disease. No drugs are licenced globally for the treatment of patients with bronchiectasis. However, there is an evidence-based treatment for the use of long-term macrolides (mainly azithromycin), inhaled antibiotics and mucolytics [52–55]. All of these agents are used in a low proportion of patients with bronchiectasis in Asia. Nebulised antibiotics, which are unavailable in most Asian countries, were the least used. For example, the Korean National Health System does not permit the use of inhaled antibiotics because of reimbursement issues. Furthermore, the cost precludes the regular use of this important drug in countries such as India, where it is available. The use of agents such as inhaled hypertonic saline and mannitol is also scarce in some Asian countries [56]. The disease is treated similarly to other airway diseases involving inhaled bronchodilators and corticosteroids. This occurs in the absence of overlapping COPD, asthma or obstructive ventilatory defects. The indiscriminate use of inhaled steroids also likely increases the risk of pneumonia and mycobacterial infections in patients with bronchiectasis, for whom there is no indication. This is an extrapolation from COPD literature [57, 58]. However, there is evidence from European cohorts that approximately 20% of patients with bronchiectasis have eosinophilic disease [59] and, hence, would benefit from inhaled corticosteroids if used appropriately [50]. Experts believe that the incidence of eosinophilic bronchiectasis is likely to be even lower in the Indian population. Physicians should be educated to ensure that bronchiectasis-specific guidelines are followed. Uniformity in terms of access to drugs and a governmental focus on their costs as well as concerns about antimicrobial resistance in Asia seem to be relevant areas of focus for the region.
The use of chest physiotherapy is generally poor; however, there is some variability. In India, chest physiotherapy is prescribed to approximately 40% of patients, which is on par with that of the European Registry [8]. However, the prescribed physiotherapy was mainly in the form of postural drainage and an active cycle of breathing. The Korean registry and Chinese studies have even fewer prescriptions for chest physiotherapy [10]. Modern positive expiratory pressure and oscillatory positive expiratory pressure techniques are rarely used in certain sections of Asia [56].
Hence, in most parts of Asia, there are opportunities to improve evidence-based treatments for bronchiectasis, such as low-dose macrolides, inhaled antibiotics and chest physiotherapy.
Endophenotypes of Asian bronchiectasis
Post-TB bronchiectasis
Post-TB bronchiectasis, a typical phenotype of Asian bronchiectasis, is usually characterised by male predominance, lower BMI, more upper lobe involvement (even though the Indian cohort for post-TB bronchiectasis has no lobar predilection) and more severe radiological extent than bronchiectasis caused by other aetiologies [8, 25]. Lung function in the Indian population with post-TB bronchiectasis showed low FVC or a restrictive ventilatory defect. A smaller proportion of patients with post-TB bronchiectasis also have post-TB obstructive airway disease, which is an obstructive ventilatory defect. This contrasts with the Korean registry data. Despite the unique characteristics of post-TB bronchiectasis, it remains largely unknown whether post-TB bronchiectasis differs in its natural history, clinical course and therapeutic approach from bronchiectasis arising from other aetiologies, which is an important area for future work.
Bronchodilators may be useful for treating this phenotype of bronchiectasis, although they have been less investigated in patients with bronchiectasis. As TB history has been a well-recognised risk factor for airflow obstruction in intermediate-to-high TB burden countries [60, 61], approximately 66% of patients with post-TB bronchiectasis showed obstructive ventilatory defect with a median 57.6 of FEV1 % pred (IQR 43.0–74.2) in the Korean bronchiectasis registry [25]. Although the ERS bronchiectasis guidelines recommend offering long-acting bronchodilators to patients with bronchiectasis with significant breathlessness on an individual basis [41], the authors suggest using bronchodilators more proactively in post-TB bronchiectasis, considering that obstructive ventilatory defects are common in the Korean population (less common in the Indian population) and that breathlessness itself is a strong predictor of mortality [62, 63].
A different aspect of post-TB bronchiectasis that needs to be considered is the long-term TB effect of persisting host–mycobacterium interactions even after microbiological cure [64, 65]. Consequently, TB survivors showed a significantly higher risk of ischaemic stroke and heart diseases than those without TB infection, even after adjusting for various confounders [66, 67]. As such comorbidities also negatively affect the long-term prognosis of patients with bronchiectasis [68], lifestyle modifications such as smoking cessation and periodic health screening exams need to be emphasised more in post-TB bronchiectasis than in bronchiectasis arising from other aetiologies.
Dry bronchiectasis
Dry bronchiectasis, characterised by no or a minimal amount of sputum, is frequently encountered in Asian clinics, even with a significant radiological presence of bronchiectasis. In a European study including 1145 patients with bronchiectasis, one of the four identified clusters was dry bronchiectasis, showing the least severe radiological and functional impairment, again in contrast with the dry bronchiectasis observed in Asian patients [69]. A subset of Asian patients with bronchiectasis lacks purulent sputum despite significant lung destruction due to previous respiratory infections, including pneumonia and measles. 58% of patients in the Indian registry were made up of individuals who do not produce sputum every day [8].
New molecular techniques have been developed to measure inflammatory markers that correlate with the disease activity and long-term prognosis of bronchiectasis [55, 70, 71]. Based on our advanced knowledge of bronchiectasis, dry bronchiectasis may represent high disease severity (severely destroyed lungs) but low disease activity (low inflammation), which is usually not a target for bronchiectasis management such as anti-inflammatory and suppressive long-term inhaled antibiotic treatments. Although increased radiological involvement and reduced lung function were related to increased bronchiectasis-related mortality in validated BSI and FACED (FEV1 % pred; Age, presence of chronic Colonisation by P. aeruginosa, radiological Extension and Dyspnoea) tools [63, 72], the natural history and therapeutic aspects of this phenotype warrant future studies in Asian populations.
Exacerbations, hospitalisations and prognosis
The number of exacerbations in the previous year was higher in the European bronchiectasis cohort than in the Asian and Australian cohorts. However, interestingly, the number of hospitalisations was higher in the Asian bronchiectasis cohort than in other regions [7, 8, 10] (table 1). This phenomenon might reflect more severe exacerbations in the Asian cohort but might equally indicate different healthcare systems that are potentially more accessible to hospitalisations in Asian settings.
The Indian bronchiectasis registry study revealed that factors associated with frequent exacerbations (≥3 per year) included a history of pulmonary TB, male sex, P. aeruginosa infection, dyspnoea score, daily sputum production and radiological severity of disease [8]. Furthermore, a Chinese multicentre study showed that depression was independently associated with an increased risk of exacerbation and hospitalisation and reduced time to the first exacerbation in bronchiectasis [73], which was also replicated in the Korean bronchiectasis registry study [74].
Regarding the long-term prognosis of bronchiectasis, a Korean nationwide study showed an approximately 1.2-fold greater mortality risk in the bronchiectasis cohort than in the matched cohort and the risk was the greatest among older adult patients and males and was more evident in the subset of patients with respiratory comorbidities, including asthma, COPD, lung cancer and cardiovascular diseases [75]. Similar results were also observed in a Korean single-centre study and a Taiwanese multicentre study [76, 77].
Furthermore, a prospective cohort study from the Indian registry provided details on the factors related to long-term prognosis. Mortality was independently associated with increasing age and comorbidities such as COPD, cardiovascular disease, dyspnoea, cigarette smoking and frequent exacerbations [9]. Although most factors related to the long-term prognosis of bronchiectasis were similar to those reported in previous studies, there was a notable finding regarding Klebsiella (K.) pneumoniae, a prevalent Gram-negative pathogen prevalent in Asia [78]. Infection with K. pneumoniae was well correlated with exacerbations and mortality in the Indian bronchiectasis registry, whereas P. aeruginosa was only correlated with exacerbations [9]. The incidence of multidrug-resistant Enterobacteriaceae is another source of concern. The BSI and FACED tools were developed in European populations [63, 72]; therefore, future studies are warranted to develop a tool for the Asian population that incorporates factors such as cigarette smoking and chronic K. pneumoniae infection, as well as those identified in future Asian bronchiectasis registry studies.
Challenges in Asia
1) The two published registry datasets from India and Korea show that approximately 80% of patients have a label of idiopathic, post-TB or post-infective bronchiectasis, which indicates the limited understanding of this disease in Asia.
2) The heterogeneity of the disease extends not only between continents but also within Asia, making it difficult to design clinical trials and develop clinical guidelines that can be generalised across continents.
3) There is an urgent need for national registry data from other countries in Asia to understand and embrace the heterogeneity of the disease and develop more generalisable recommendations across Asia. To address this, the China Bronchiectasis Registry and Research Collaboration (BE-China) was established in January 2020 [43, 79]. Currently, BE-China enrols more than 10 000 patients from 111 hospitals across the country. Publication of these data in the latter half of 2024 will deepen our understanding of bronchiectasis in Asia. However, Asia is a very large and diverse continent. The two most populous nations, China and India, plus Korea, now have registries, but others are yet to identify and develop bronchiectasis management and research to the same extent. Therefore, the authors have tried to highlight the challenges posed by the absence of bronchiectasis data for the majority of Asian countries.
4) The microbiology and microbiome are also very different across continents and within Asia. We need to understand whether the relatively low incidence of organisms such as H. influenzae and M. catarrhalis (very common in Northern Europe and the UK) is because they are truly absent in this geographical territory or because they are fastidious organisms that are difficult to grow in culture. Indeed, reports have shown that since the advent of molecular platforms in India, many more organisms have been recognised. Heterogeneity within the continent is also profound, with Enterobacteriaceae occurring in one in ten individuals in India, which also predicts a higher risk of mortality.
5) Although the guidelines for bronchiectasis come mostly from the Western world, the disease burden seems to be greatest in countries where TB is an endemic. This presents challenges for patients, physicians and healthcare systems with regard to trained physiotherapists, microbiologists and access to evidence-based treatments such as inhaled antibiotics. In countries such as India, much of the treatment comes from the private sector, where patients do not have insurance; hence, quality healthcare is deemed very expensive.
6) While this review discusses the challenges of Asian bronchiectasis, it also highlights opportunities for collaboration and teamwork [80–82]. However, the need to generate more data across Asia is unambiguous. This will help develop guidelines focused on Asian patients. The importance of greater focus on aetiological diagnosis has also been well established. There is much to do, but there seems to be light at the end of the tunnel.
Footnotes
Provenance: Commissioned article, peer reviewed.
Number 5 in the Series “World Bronchiectasis Conference 2024” Edited by James D. Chalmers, Felix C. Ringshausen and Pieter C. Goeminne
This article has an editorial commentary: https://doi.org/10.1183/16000617.0124-2024
Previous articles in this series: No. 1: Perea L, Faner R, Chalmers JD, et al. Pathophysiology and genomics of bronchiectasis. Eur Respir Rev 2024; 33: 240055. No. 2: Mac Aogáin M, Dicker AJ, Mertsch P, et al. Infection and the microbiome in bronchiectasis. Eur Respir Rev 2024; 33: 240038. No. 3: Van Braeckel E, Bosteels C. Growing from common ground: nontuberculous mycobacteria and bronchiectasis. Eur Respir Rev 2024; 33: 240058. No. 4: De Angelis A, Johnson ED, Sutharsan S, et al. Exacerbations of bronchiectasis. Eur Respir Rev 2024; 33: 240085.
Conflict of interest: H. Choi reports grant from the Basic Science Research Program of the Korean Ministry of Education (grant no. 2021R1I1A3052416); and consulting and lecture fees from Boryung Pharmaceutical Co., Ltd. and Kolon Pharma. J-F. Xu reports leadership or fiduciary roles in other boards, societies, committees, or advocacy groups (unpaid) with the Shanghai Medical Association, Chinese Thoracic Society, and Chinese Association of Chest Physicians. S.H. Chotirmall has served on advisory boards for CSL Behring, Pneumagen Ltd and Boehringer Ingelheim, on data monitoring boards for Inovio Pharmaceuticals and Imam Abdulrahman Bin Faisal University, and has received personal fees from AstraZeneca and Chiesi Farmaceutici, all unrelated to this work J.D. Chalmers reports grants or contracts from AstraZeneca, Boehringer Ingelheim, Genentech, Gilead Sciences, GlaxoSmithKline, Grifols, Insmed, LifeArc and Novartis; and consulting fees from AstraZeneca, Chiesi, GlaxoSmithKline, Insmed, Grifols, Novartis, Boehringer Ingelheim, Pfizer, Janssen, Antabio and Zambon. L.C. Morgan reports payment or honoraria for speakers’ bureau from Boehringer Ingelheim, AstraZeneca and Insmed, and educational events from GSK Pharmaceutical and AstraZeneca, all unrelated to this work. In addition, L.C. Morgan reports a leadership or fiduciary role in other boards, societies, committees, or advocacy groups (unpaid) as Chair of the Lung Foundation Australia. R. Dhar reports grants from GSK Pharmaceutical and Glenmark and Thorasis; and lecture fees from Cipla Ltd., Lupin Respira, Glenmark, Abbott, Sanofi and AstraZeneca.
- Received May 2, 2024.
- Accepted July 31, 2024.
- Copyright ©The authors 2024
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