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The characteristics and prognosis of bronchiectasis patients with airflow limitation: a prospective longitudinal study

BMC Pulmonary Medicine volume 24, Article number: 599 (2024) Cite this article

Abstract

Background

As bronchiectasis progresses, increasing degrees of airflow limitation can occur.

Objectives

This study aimed to investigate whether concomitant airflow limitation was associated with poor prognosis in patients with bronchiectasis and to identify the characteristics of patients with airflow limitation in bronchiectasis.

Design

A prospective longitudinal study was conducted to determine the characteristics and prognosis of bronchiectasis patients with airflow limitation.

Methods

We conducted a prospective longitudinal study. Patients who failed to complete the follow-up were withdrawn from the trial. High-resolution computed tomography (HRCT) was used for diagnosing bronchiectasis, whereas postbronchodilator forced expiratory volume in one second of the predicted value (post-FEV1%) was employed for grading airflow limitation. The main variables included questionnaires, anthropometric measurements, pulmonary function tests, laboratory tests, and CT findings. The primary outcome was frequent exacerbations. Differences among the groups were evaluated via two-tailed Student’s t test or ANOVA for continuous variables if the data were normally distributed. In the case of a nonnormal distribution, the Mann–Whitney U test and Kruskal–Wallis test were used. The chi-square test or Fisher’s exact test was used for categorical variables. Binary logistic regression analyses were used to identify factors and calculate the odds ratio (OR) for frequent exacerbations.

Results

A total of 189 subjects with bronchiectasis were enrolled in the study, including 97 patients with airflow limitation and 92 patients without airway obstruction. Patients with airflow limitation had greater numbers of exacerbations (1.46 ± 0.83 vs. 1.76 ± 1.10 times, P = 0.013) at 12 months after enrolment and greater numbers of hospitalizations (1.10 ± 0.30 vs. 1.36 ± 0.67 times, P = 0.0016) at 24 months after enrolment. In addition, acute exacerbations lasted longer (8.69 ± 3.78 vs. 13.11 ± 14.03 days, P = 0.0171), and the total number of hospitalizations was greater (1.34 ± 0.77 vs. 1.80 ± 1.67 times, P = 0.0421) for patients with a mean follow-up duration of 32 months (Table 3). Bronchiectasis patients with airflow limitation exhibit more severe manifestations of bronchiectasis both clinically and functionally. Furthermore, the cohort of bronchiectasis patients with airflow limitation had a significantly greater infection rate than did the BE group (P = 0.0244), with a notable disparity observed in the incidence of P. aeruginosa infection (P < 0.0001).

Conclusion

The results of our study suggest that patients with airflow limitation are more likely to experience acute exacerbations and hospitalizations than are those without airflow limitation. Patients with bronchiectasis concomitant with airflow limitation should be identified as early as possible, and individualized treatment methods should be formulated.

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Introduction

Background

Bronchiectasis (BE) is a chronic respiratory disease. Although it has long been neglected in China, recent epidemiological studies have shown that its incidence is trending upwards with the ageing of the population [1]. The most common aetiologies are idiopathic, accounting for 5-82% of cases [2].

The main characteristic of BE is irreversible dilatation and thickening of the bronchial tree due to a vicious spiral involving inflammation, infection, and repair of the bronchial mucosa [3]. The gold standard for the diagnosis of bronchiectasis is high-resolution CT (HRCT) [4]. The dramatic increase in the number of cases in the past decade has placed an enormous burden on the global economy and healthcare system [5].

Airflow limitation often coexists with bronchiectasis (BE). It not only debilitates lung function but also significantly compromises quality of life and can lead to premature death [6, 7]. Currently, there is no research indicating the combined impact of airflow limitation on bronchiectasis and its prognosis. There is an exigent demand for further research to mitigate the constraints of airflow limitation. Therefore, we aimedto investigate the impact of airflow limitation on patients with bronchiectasis.

As a key event in the natural history of bronchiectasis, the exacerbation of bronchiectasis exerts an important influence on the prognosis of the disease and impairs quality of life [8]. Frequent exacerbations, defined as either two or more exacerbations per year or one hospitalization per year, offers the highest predictive value for mortality independent of the initial severity of bronchiectasis. Patients who experience frequent exacerbations represent a distinct subgroup with a more severe disease course and greater healthcare needs. Emphasizing the clinical importance of identifying and targeting this high-risk group is of great significance [9,10,11]. Therefore, we sought to study whether and how concomitant airflow limitation affects the frequency of bronchiectasis exacerbation.

Objectives

This study was performed to investigate whether concomitant airflow limitation was associated with poor prognosis in patients with bronchiectasis and to identify the characteristics of patients with airflow limitation in bronchiectasis [12].

Methods

Study design

We conducted a prospective longitudinal study.

Setting

The subjects in the study were patients with bronchiectasis at the Department of Respiratory and Critical Medicine at The First Affiliated Hospital of Ningbo University from 2018 to 2021. Researchers contacted patients or caregivers by telephone and reviewed their medical records to collect data about exacerbations and hospitalizations every year. Patients who failed to complete the follow-up were withdrawn from the trial.

Diagnostic criteria of disease

High-resolution computed tomography (HRCT) is the diagnostic modality of choice to definitively ascertain or exclude bronchiectasis in patients presenting with suggestive clinical features. According to the expert consensus on the Diagnosis and Treatment of Adult Bronchiectasis in China, the diagnosis of bronchiectasis depends on HRCT. Bronchiectasis is diagnosed if one or more of the following criteria are present in one or more of the lung lobes: (a) airway dilation (much greater airway lumen diameter compared with adjacent pulmonary vessels), (b) gradual thinning of the abnormal airway of any degree (no change in the airway cavity diameter from the proximal to distal airway), or (c) bronchi within 1 cm of the pleura [13].

Disease severity was evaluated via the Bronchiectasis Severity Index (BSI). The score included 8 indicators, such as age, body mass index (BMI), prebronchodilator forced expiratory volume in one second of the predicted value (pre-FEV1%), the number of hospital admissions in the previous 2 years, the number of acute exacerbations in the previous 12 months, the modified Medical Research Council (mMRC) dyspnoea scale, and the presence of Pseudomonas aeruginosa and other microbial colonization and imaging findings. A total score of 0–4 was classified as mild, 5–8 was classified as moderate, and ≥ 9 was classified as severe [14, 15].

Airflow limitation was defined as an FEV1/FVC ratio < 0.7, and all patients were classified into three classes according to the postbronchodilator FEV1% [16]. The postbronchodilator FEV1% under mild-to-moderate airflow limitation was greater than 50%; under severe airflow limitation, it was less than 50%. The MRC dyspnoea scale can be used to assess perceived breathlessness during daily activities [17, 18]. An acute exacerbation of bronchiectasis was defined as patients with bronchiectasis meeting three or more of the following key symptoms for at least 48 h: cough; sputum volume and/or consistency; sputum purulence; breathlessness and/or exercise tolerance; fatigue and/or malaise; and haemoptysis, with determination by a clinician that a change in bronchiectasis treatment was needed [19]. Frequent exacerbations are defined as having either two or more acute exacerbations per year or at least one hospitalization annually.

Selection criteria

The inclusion criteria for patients were as follows: presentation with imaging evidence of bronchiectasis on high-resolution computed tomography (HRCT) and clinical signs consistent with the patient’s condition, where bronchiectasis was identified as the primary or major respiratory diagnosis.

Exclusion criteria were as follows: individuals younger than 18 years of age and those who had received a lung transplant.

Questionnaires and anthropometric measurements

All data collection was performed by the clinical physicians involved in this research according to a standardized protocol. The data collected included general conditions, clinical symptoms, radiographic manifestations, pulmonary function indices, modified Medical Research Council (mMRC) scores, and acute exacerbations over the past year (particularly hospitalizations). The subjects completed pulmonary function tests, including spirometry and bronchial reversibility tests, via short-acting bronchodilators. Spirometric measurements were performed while patients were in a clinically stable condition and refrained from smoking and consuming heavy meals with a Vyaire spirometer (Leibnizstrasse 7,97204 Hoechberg, Germany). Patients were encouraged to exert maximal effort during each manoeuvre to obtain reliable and reproducible results.

Spirometry of prebronchodilators included FVC%, FEV1%, FEV1/FVC%, MEF50%, MEF25%, MEF75/25%, DLCO SB% and DLCO/VA%, whereas postbronchodilator spirometry was measured before and 15 min after the administration of ventolin via inhalation, including FVC%, FEV1%, FEV1/FVC%, MEF50%, MEF25% and MMEF75/25%. Laboratory tests were mainly based on sputum culture to determine whether there were infections. The CT findings were evaluated by a professional radiologist. We recorded the number of lobes affected and the pattern of bronchiectasis (cylindrical, cystic, and varicose) for the subsequent analyses.

Outcomes

The primary outcome was frequent exacerbations. The secondary outcomes were the number of acute exacerbations 12 months after enrolment, the number of hospitalizations 24 months after enrolment, the total number of hospitalizations until the end of follow-up, exacerbation duration (persistence of symptoms until return to daily symptoms) and death.

Statistical analysis

All the statistical analyses were performed via GraphPad Prism 9.0 (GraphPad Software, La Jolla, CA, USA) and SPSS Statistics 26 (IBM). We first categorized all enrolled patients into male and female groups and then compiled baseline data. We then divided the bronchiectasis patients into two groups on the basis of whether their FEV1/FVC ratio was less than 70%. Additionally, the group with airflow limitation (FEV1/FVC less than 70%) was further divided into two groups on the basis of the post-FEV1% value. Differences among the groups were evaluated via two-tailed Student’s t test or ANOVA for continuous variables if the data were normally distributed. In the case of a nonnormal distribution, the Mann–Whitney U test and Kruskal–Wallis test were used. The chi-square test or Fisher’s exact test was used for categorical variables. The selection of statistical analysis models depends on the data types of the dependent and independent variables. The primary outcome of the study was frequent exacerbations. A binary logistic regression analysis was conducted to assess the associations between airflow limitation, the number of acute exacerbations in the previous 12 months, and the outcome. Odds ratios (ORs) and 95% confidence intervals (CIs) were estimated for each variable to evaluate their influence on the likelihood of frequent exacerbations. Variables are presented as numbers (percentages), means (SDs), or medians (interquartile ranges [IQRs]) as appropriate. For all analyses, the differences were considered statistically significant if the P value was less than 0.05.

Results

Study cohort

A total of 189 subjects were included in the study cohort, including 97 patients with airflow limitation and 92 patients without airway obstruction. Among them, 49 patients were in the mild-to-moderate airflow limitation group, and 43 were in the severe airflow limitation group. The mean (SD) age was 62.57 (12.42) years, and 50.26% (95) of the patients were male. Twenty-two patients failed to return questionnaires after two unanswered telephone reminders (Fig. 1).

Fig. 1
figure 1

Flowchart of the study participants. FEV1%=The ratio of forced expiratory volume in 1 s percentage to the predicted value; FEV1/FVC = Forced expiratory volume in 1 s percent/Forced vital capacity to the predicted value

Full size image

Among the patients with bronchiectasis, males had a greater average BMI (P = 0.008) and were more likely to be smokers than females were (P < 0.0001). Moreover, males had worse pulmonary function, as demonstrated by lower FVC% (P = 0.0003), FEV1% (P = 0.0084), and FEV1/FVC (%) (P = 0.0112) values. After the bronchodilation test, there was a significant difference in the FVC% (P = 0.0002), FEV1% (P = 0.004), and FEV1/FVC (%) (P = 0.0021). However, females had a greater prevalence of haemoptysis (P = 0.0049) and more hospitalizations. Otherwise, there was no difference between males and females (Supplemental Table 1).

Baseline characteristics of bronchiectasis patients with airflow limitation

Among the 189 subjects, 97 (51.32%) had no airflow limitation, 49 had mild-to-moderate airflow limitation (post-FEV1%≥50%), and 43 had severe airflow limitation (Table 1). The subjects with airflow limitation were more likely to be male (P = 0.0045), to be smokers (P = 0.046), and to have coronary atherosclerotic heart disease (P = 0.0033), and they were more prone to having a longer history of respiratory disease (P = 0.0014) than were the other subjects. However, the two groups did not differ in terms of age, BMI, or history of hypertension or diabetes (Table 1).

Table 1 Baseline characteristics of the study population stratified by the severity of COPD as well as those who were lost to follow-up
Full size table

Clinical manifestations of bronchiectasis in patients with airflow limitation

Bronchiectasis patients with airflow limitation presented a more severe form of bronchiectasis in clinical and functional terms. Supplemental Table 2 shows that the more severe the combined airflow limitation was, the lower the pulmonary function indices were, including FVC%, FEV1/FVC%, MEF50%, MEF25%, MEF75/25%, DLCO SB%, and DLCO/VA%, both prebronchodilator and postbronchodilator (Supplemental Table 2). Compared with patients in the no airflow limitation group, those in the airflow limitation group were more prone to cough (P = 0.0324) and dyspnoea (P = 0.0073). However, the two groups did not show significant differences in expectoration or haemoptysis. Patients with airflow limitation had a greater number and greater severity of exacerbations, which were reflected in the number of hospitalizations over 2 years (P = 0.0064) and the number of acute exacerbations over 12 months (P = 0.0008). Moreover, patients in the airflow limitation group had a greater infection rate than did those in the BE group (P = 0.0244), and there was a significant difference in Pseudomonas aeruginosa infection (P < 0.0001) (Table 2).

Table 2 Clinical manifestations of the study population divided by the severity of airflow limitation as well as those who were lost to follow-up
Full size table

Although a more severe airflow limitation might suggest more severe bronchiectasis, the evidence supporting this relationship is insufficient

Patients were divided into 2 grades according to the post-FEV1% to distinguish airflow limitation severity. As mentioned above, the severity of bronchiectasis was reflected in the BSI score. As shown in Fig. 2A, B, in patients with bronchiectasis, more severe airflow restriction might be associated with more severe bronchiectasis. As the severity of airflow limitation increased, the proportion of patients with mild bronchiectasis gradually decreased, and the proportion of patients with severe bronchiectasis gradually increased.

Fig. 2
figure 2

(A) shows that the exact value of the BSI is used for the analysis among multiple groups, whereas (B) shows that BSI scores are divided into three intervals for analysis. (C) shows the number of patients with different mMRC scores in each group

Full size image

The severity of airflow limitation is positively correlated with the BSI, as illustrated in the graph. Analysis across three groups yielded a significant p value of < 0.0001. However, post hoc analysis revealed no statistically significant differences between the two groups with different degrees of airway limitations. Hence, while an overall trend may exist, further validation with larger sample sizes may be needed to ascertain specific intergroup differences.

Prognosis of bronchiectasis patients with airflow limitation

Among the 189 subjects, 167 completed the follow-up. There were 83 patients without airflow limitation and 84 patients with airflow limitation available for the two-group analysis. Among them, 47 patients were in the mild-to-moderate airflow limitation group, and 43 were in the severe airflow limitation group. No differences were found in mortality between the no airflow limitation and airflow limitation groups. However, patients with airflow limitation had a greater number of exacerbations (1.46 ± 0.83 vs. 1.76 ± 1.10, P = 0.013) 12 months after enrolment and a greater number of hospitalizations (1.10 ± 0.30 vs. 1.36 ± 0.67, P = 0.0016) 24 months after enrolment. In addition, these patients exhibited longer duration of acute exacerbations (8.69 ± 3.78 vs. 13.11 ± 14.03, P = 0.0171) and a greater total number of hospitalizations within a mean follow-up duration of 32 months (1.34 ± 0.77 vs. 1.80 ± 1.67, P = 0.0421). Moreover, the number of acute exacerbations 12 months after enrolment and the number of hospitalizations were significantly different among the three groups. Patients with severe airflow limitation had more acute exacerbations 12 months after enrolment and more hospitalizations 24 months after enrolment than those with mild-to-moderate airflow limitation or without airflow limitation (Table 3).

Table 3 Prognosis of bronchiectasis patients with airway limitations
Full size table

Binary logistic regression analyses were used to identify possible independent risk factors associated with frequent exacerbations. Frequent exacerbations were predicted in patients with airflow limitation and more previous exacerbations. The results revealed that individuals with airflow limitation are 3.095 times more likely to experience frequent exacerbations than are those without airflow limitation (95%CI: 1.584–6.046). This finding suggested that for each additional acute exacerbation, the likelihood of experiencing frequent exacerbations increased by a factor of 1.532(CI: 1.130–2.075) (Table 4).

Table 4 Regression analysis of predictors for frequent exacerbations
Full size table

Discussion

This was a prospective longitudinal study aimed at determining whether the clinical characteristics of patients with airflow limitation among bronchiectasis patients are different from those of patients with bronchiectasis alone and the impact on the prognosis of patients with bronchiectasis airflow limitation. The main findings of this study were that (1) bronchiectasis patients with no airflow limitation and airflow limitation differ in terms of demographics, symptoms, lung function, imaging, and microbial infection, and (2) patients with airflow limitation experience more frequent exacerbations and hospitalizations than BE patients do, but their mortality is not greater.

Patients with bronchiectasis often exhibit symptoms of airflow limitation. Currently, there is no research indicating the comprehensive impact of airflow limitation on bronchiectasis and its prognosis. We found that patients with airflow limitation had worse prognosis and experienced greater numbers of exacerbations (1.46 ± 0.83 vs. 1.76 ± 1.10, P = 0.013) at 12 months after enrolment and more hospitalizations (1.10 ± 0.30 vs. 1.36 ± 0.67, P = 0.0016) at 24 months after enrolment. In addition, acute exacerbations lasted longer (8.69 ± 3.78 vs. 13.11 ± 14.03 days, P = 0.0171), and the total number of hospitalizations was greater (1.34 ± 0.77 vs. 1.80 ± 1.67 times, P = 0.0421) for patients with a mean follow-up duration of 32 months (Table 3). Therefore, we need to be aware of the impact of airway limitations on bronchiectasis. Despite the clear trend observed in Fig. 2A and B, no significant differences were observed between the mild to moderate and severe airflow limitation groups, possibly because of the small sample sizes. An oversight exists regarding a significant limitation when comparing airflow limitation groups using the BSI. Given that FEV1 is a component of the BSI calculation, it inherently implies that individuals with lower lung function will exhibit greater severity. The current effects are speculative; therefore, additional research is needed to substantiate the relationship between the severity of bronchiectasis and the severity of coexisting airflow limitation. In terms of demographics, male patients, smokers, and patients with coronary heart disease and a long history of respiratory disease were more prone to concurrent airflow limitation. These patients had worse lung function, exhibited more coughing and difficulty breathing and were more susceptible to microbial infections [20]. Similar to previous studies [21, 22], our study revealed a higher rate of infection in airflow-limited patients (P = 0.0244), especially those with with Pseudomonas aeruginosa infection (P < 0.0001). Furthermore, airflow limitation aggravated the condition of patients with bronchiectasis. Therefore, patients with these characteristics require more attention to prevent their condition from worsening [23].

Studies have shown that the mortality rate of BCO is much higher than that of COPD alone [23]. However, in our study, the presence or absence of airflow limitation was not associated with the mortality of bronchiectasis patients. This may be partly because 22 patients were lost to follow-up. They could not be contacted via phone, and their living status could not be obtained. Another possibility is that the number of patients included in the study was insufficient for the statistical power required to capture the predictive power of mortality.

However, patients with airflow limitation were significantly more likely to experience acute exacerbations (including the number and duration of acute exacerbations) and hospitalization than were those without airflow limitation, which is consistent with previous research [24]. Moreover, we observed that the occurrence of frequent exacerbations was significantly correlated with airflow limitation and the previous number of exacerbations. In patients with bronchiectasis, the comorbidity of airflow limitation can be used to predict exacerbations.

In addition, our study has the following limitations. First, it is difficult to determine whether a patient has primary airflow limitation with secondary bronchiectasis or primary bronchiectasis with secondary airflow limitation. Second, the sample size was limited, and the sample was not multicentric. Third, our research did not elaborate on the effects of relevant treatments on different groups. Further research is needed to formulate individualized treatments for brochiectasis patients with airflow limitation.

The airflow limitation associated with bronchiectasis should be diagnosed as early as possible, allowing the specialized management of these patients to greatly reduce their financial and health burdens [25, 26].

Conclusions

Our study provides the basis for more scientific patient management. Patients with airflow limitation in bronchiectasis have a more severe clinical presentation, including increased cough, dyspnoea, and exacerbation, and higher infection rates, particularly with Pseudomonas aeruginosa. In the bronchiectasis patient population, patients with airflow limitation are more likely to experience acute exacerbation and hospitalization. Patients with bronchiectasis should receive more attention to identify those with concomitant airflow limitation and to formulate individualized treatment methods.

Data availability

The datasets used and analysed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank Aimee Talarski from AJE for her help in polishing the language. The cost was paid by the Department of Respiratory and Critical Medicine, Ningbo First Hospital. We thank Taotao Zhou for his guidance in statistics. We thank all staff members at Ningbo First Hospital. Finally, we would like to express our gratitude to the patients and their families for their active cooperation.

Funding

This work was supported by the Zhejiang Province cobuilds key medical disciplines (2022-S01). The funder of the study had no role in the study design, analysis, interpretation of the data, or writing of the report.

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Authors and Affiliations

  1. The First Affiliated Hospital of Ningbo University, Ningbo, China

    Yuanting Cai, Linbin Xv, Zili Zhu, Shiyi He & Chao Cao

  2. Ningbo University, Ningbo, China

    Yuanting Cai, Linbin Xv & Tianyu Sun

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  1. Yuanting Cai
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Contributions

CC developed the study idea and provided key advice. YC conducted the literature search. YC, TS and LX collected and verified the data. ZZ, a radiologist with four years of experience in diagnostic imaging, evaluated the CT findings. YC performed the data analysis. SH proposedput forward suggestions for modification. YC drafted the manuscript. CC and YC reviewed the final manuscript. CC is the guarantor. All the authors approved the final version of the manuscript. All the authors have access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding author

Correspondence to Chao Cao.

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Ethics approval and consent to participate

All methods were carried out in accordance with relevant guidelines and regulations. This study was approved by the Ethics Commission of Ningbo First Hospital (2021 - R062). Consent was obtained from the participants prior to their participation in the study.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Cai, Y., Xv, L., Zhu, Z. et al. The characteristics and prognosis of bronchiectasis patients with airflow limitation: a prospective longitudinal study. BMC Pulm Med 24, 599 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03422-x

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03422-x

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BMC Pulmonary Medicine

ISSN: 1471-2466

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