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Back to Journal »International Journal of Chronic Obstructive Pulmonary Disease» Volume 16

Correlation of pulmonary function and quality of life between the large airway lumen mucus score during severe acute exacerbation of COPD: a cross-sectional study

Authors: Yang C, Zeng Huahong, Du Yingjie, Huang Jie, Zhang Qiyuan, Lin Ke

Published on May 28, 2021, Volume 2021: 16 pages, 1449-1459 pages

DOI https://doi.org/10.2147/COPD.S311659

Single anonymous peer review

Editor who approved for publication: Dr. Richard Russell

Cheng Yang,1 Han-Hua Zeng,1 Yan-Jia Du,1 Juan Huang,1 Qian-Yun Zhang,1 Kun Lin2 1Department of Pulmonary Disease and Critical Care Medicine, Meizhou People's Hospital, Meizhou, 5143031, Guangdong, People's Republic of China; 2Department of Preventive Medicine, Shantou University School of Medicine, Shantou 515041, Guangdong 515041 Corresponding Author: Zhang Qianyun, No. 63 Huangtang Road, Meijiang District, Meizhou City 514031, No. 63 Huangtang Road, Meijiang District, Meizhou City, People's Republic of China Tel +86 07532202723 Fax +86 07532204840 Email [email protected] Department of Preventive Medicine, Kunlin, Shantou University Medical College, No. 22, Xinling Road, Jinping District, Shantou City 515041 People’s Republic of China Tel +86 075488900445 Fax +86 075482903637 E-mail [Email protected] Background and purpose: Small airway lumen mucus blockage It is related to decreased lung function and death in patients with chronic obstructive pulmonary disease (COPD). However, few people pay attention to the possible role of mucus in the large airways in acute exacerbation of COPD (AECOPD). Therefore, this study aims to explore the relationship between the large airway lumen mucus score and other physiological parameters of severe AECOPD. Participants and methods: A total of 74 AECOPD hospitalized patients participated in this cross-sectional study. All patients underwent pulmonary function test and bronchoscopy, and their lumen mucus was observed and scored by bronchoscopy. Four questionnaires, including St. George's Respiratory Questionnaire (SGRQ), Modified Medical Research Council Dyspnea Scale (mMRC), COPD Assessment Test (CAT) and Chronic Lung Disease Exacerbation Tool (EXACT), used to assess health-related quality of life (HRQoL). Results: The mucus score of the large airway lumen was significantly correlated with vital capacity parameters and HRQoL score. Both the mMRC grade and SGRQ score were significantly positively correlated with the lumen mucus score (ρ=0.527, P<0.001; ρ=0.441, P<0.001). FVC (FEF25%-75%) and FEV1% predicted 25% to 75% of the forced expiratory flow, as a functional measure reflecting small airway disease, and was significantly negatively correlated with the lumen mucus score (ρ=−0.518, P < 0.001; ρ=−0.498, respectively P <0.001). The stepwise multiple linear regression model showed that the mMRC classification and FEV1% prediction can predict the lumen mucus score (R2=0.348, F=18.960, P<0.001). Conclusion: For the severe acute exacerbation of COPD, the mucus in the lumen of the large airways detected by bronchoscopy is related to the decline of lung function and health-related quality of life. Keywords: chronic obstructive pulmonary disease, acute exacerbation, lumen, mucus, bronchoscopy

Mucus dysfunction is the main pathophysiological feature of chronic obstructive pulmonary disease (COPD), manifested by excessive mucus production and luminal occlusion. 1 Mucus exudation in the small airways is related to the decrease in lung function and the increase in mortality in COPD patients, which confirms the pathological examination of the isolated lung tissue. 2 In the large airways (diameter> 2 mm), CT shows that the obstruction of the lumen is related to airflow obstruction, poor health-related quality of life (HRQoL), and emphysema phenotype. 3 However, whether the lumen blockage determined by CT is caused by mucus remains to be confirmed by bronchoscopy.

Acute exacerbation of COPD (AECOPD) is characterized by dyspnea, increased sputum volume, and worsening of respiratory symptoms such as suppuration. It is the main cause of hospitalization and death of the disease. 4 However, few people have noticed the possible role of mucus in the large airways in exacerbations. It was found that the bronchitis index score determined by the secretion, erythema, edema and fragility of patients with chronic bronchitis through bronchoscopy was significantly higher than that of normal people. 5 Therefore, we assume that the lumen mucus of the large airways may also be closely related to the traditional AECOPD index.

The main purpose of this study is to explore the relationship between the LMS of inpatients with bronchoscopy and the functional parameters reflecting the severity of AECOPD, including lung function, HRQoL score and laboratory test results. 4 In addition, more easily measurable clinical indicators were tested to predict LMS in the large airways, because bronchoscopy is an invasive procedure.

The cross-sectional study was conducted at the People's Hospital of Meizhou City, Guangdong Province, China from May 2020 to January 2021. A total of 90 hospitalized patients who were clinically diagnosed with AECOPD were continuously screened, and 74 of them were included in the study. The selection process of participants is shown in Figure 1. Figure 1 Flow chart of participants' enrollment in the study. Abbreviations: AECOPD, acute exacerbation of chronic obstructive pulmonary disease; LFT, lung function test.

Figure 1 Flow chart of participants' enrollment in the study.

Abbreviations: AECOPD, acute exacerbation of chronic obstructive pulmonary disease; LFT, lung function test.

The inclusion criteria are as follows: (1) FEV1/FVC ratio after bronchodilator is less than 0.7; (2) The diagnosis of AECOPD is defined as: 6 Two main symptoms (dyspnea, increased sputum volume, or purulent sputum), or one main Symptoms, combined with at least one secondary symptom (wheezing, chills, fever, sore throat or cough); (3) Written informed consent obtained before participating in the study. The exclusion criteria are as follows: (1) There are contraindications in bronchoscopy or lung function test; (2) Patients with known respiratory diseases other than COPD, including sarcoidosis, active tuberculosis, pulmonary fibrosis, cyst Fibrosis or diseases that may significantly affect clinical evaluation according to the judgment of the investigator; (3) The diagnosis of lung cancer, including the current and recent 5 years of diagnosis; (4) There are neurological diseases that affect the ability to expectoration; (5) Lack of the ability to read and understand Mandarin.

Complete blood count, C-reactive protein (CRP), 4 items of blood coagulation (prothrombin time, activated partial thromboplastin time, thrombin time, fibrinogen), and electrocardiogram on the first day of admission. The HRQoL assessment, 7 including the modified Medical Research Council Dyspnea Scale (mMRC), St. George's Respiratory Questionnaire (SGRQ), COPD Assessment Test (CAT) and Chronic Lung Disease Exacerbation Tool (EXACT) questionnaire, was completed on the second day. Perform a bronchoscopy immediately after the HRQoL assessment, and perform a lung function test within 12 to 48 hours after the bronchoscopy. The research process did not interfere with patient management decisions. This study has been registered in the Chinese Clinical Trial Registry (Registration Number: ChiCTR2000033101).

The bronchoscopy was performed by Yang under the guidance of the Chinese Medical Association. 8 The entire examination under the bronchoscope was recorded by the video processor (CV-290 EVIS LUCERA ELITE, Olympus, Tokyo, Japan). All patients were examined using the same bronchoscope (BF-Q290, Olympus, Tokyo, Japan). Patients without contraindications were given intravenous midazolam for conscious sedation 10 minutes before surgery, with a total dose not exceeding 10 mg. Before the bronchoscope is introduced into the airway through the vocal cords, spray 2% lidocaine through the working channel with a total dose not exceeding 5 mg/kg. The mucus observed under the bronchoscope is removed. According to clinical needs, we performed lavage and/or biopsy, and collected specimens for microbiology and/or cytology. Monitor the patient's blood pressure, pulse oximetry, heart rate and respiratory rate as appropriate throughout the operation.

The video files are named with the corresponding subject number, not the patient's name or other information. Once ignorant of other clinical data of the patient, the luminal mucus was scored based on the video. Regarding the scoring system, Thompson et al.5 proposed a scoring system involving six parts, including five lobes and uvula. We used this scoring system and added four other central airways involved, including trachea, right main bronchus, left main bronchus, and right middle bronchus. The luminal mucus score is 0 to 3 points (0=normal, 3=severe abnormality), so the total LMS ranges from 0 to 30 points (Figure 2). Mucus is scored based on the most severe part of each lobe and tongue, and the most severe part of the central airway, regardless of the length of the airway involved. Figure 2 The results of bronchoscopy at the entrance to the bronchus of the right middle lobe and lower lobe show the luminal mucus score. (A) 0 points, normal; (B) 1 point, clear mucus strands; (C) 2 points, mucus balls; (D) 3 points, airway obstruction.

Figure 2 The results of bronchoscopy at the entrance to the bronchus of the right middle lobe and lower lobe show the luminal mucus score. (A) 0 points, normal; (B) 1 point, clear mucus strands; (C) 2 points, mucus balls; (D) 3 points, airway obstruction.

According to the guidelines issued by the American Thoracic Society and the European Respiratory Society, the lung function test was performed using an electronic spirometer (microQuark PFT, Cosmed, Rome, Italy). 9 After four to six quiet breaths, ask the patient to inhale as much air as possible to vital capacity (TLC), and then exhale with best effort for at least 6 seconds to residual capacity (RV); expiratory volume is the forced vital capacity (FVC) ). After inhaling 400 μg Ventolin, wait for 20 minutes and repeat the spirometry. Only the post-bronchodilator lung capacity parameters were used in this analysis.

Chronic bronchitis is defined as sputum expectoration during most of the day or night for at least 3 months of the year for ≥ 2 years. If the patient answers affirmatively to the following question, it is considered that there is chronic bronchitis: "Did you cough up sputum for at least 3 months each year (in most days or nights) during the past 2 years?" 10

The Health-Related Quality of Life (HRQoL) questionnaire is used to assess the quality of life. 7 We used a total of four different questionnaires, including mMRC, SGRQ, CAT and EXACT. The mMRC score is used to assess the degree of dyspnea in COPD patients, ranging from 0 to 4. 11 The SGRQ score ranges from 0 to 100 points and is widely used to evaluate airway diseases that cause a decrease in HRQoL. 12 CAT is a validated questionnaire that contains eight items to assess and quantify the impact of symptoms on the health of COPD patients. 4 EXACT is used to directly measure the acute exacerbation symptoms reported by the patient and conduct a standardized assessment of the patient's condition. 13 The subjects were asked to choose the description that best matched their symptoms, or their level of agreement with each statement. Yang can provide an explanation if necessary, but he did not give any suggestions or answers. For all four questionnaires, a higher grade or score indicates a poorer quality of life.

We estimated a sample of 72 participants based on the reported prevalence of 25% of lumen mucus embolism in the large airways, 3 with an accuracy of 10% (95% CI). We also estimate that 20% of patients will not be able to complete bronchoscopy or lung function tests, so we plan to recruit 90 subjects.

All results have descriptive data. The results are expressed as mean ± standard deviation or median (IQR 25-75). According to the data distribution, the parameter differences between patients are included and excluded by the t test or Wilcoxon rank sum test. Spearman rank correlation coefficient was used to evaluate the correlation between LMS and lung function parameters, HRQoL score, and laboratory test results; the correlation coefficient was expressed as ρ. In the subsequent multiple linear regression analysis, indicators showing significant correlation were used as potential covariates. The stepwise regression algorithm is used to perform multiple linear regression analysis to further test the relationship between the total LMS of the large airway and many other variables. Body mass index (BMI), partial pressure of carbon dioxide (PaCO2), FVC, FVC% predicted value, FEV1, FEV1% predicted value, FEV1/FVC, peak expiratory flow (PEF), forced expiratory flow is 25% to 75% FVC (FEF25%-75%), mMRC grade, SGRQ score, CAT score, and EXACT score are included as covariates in the model. A P value of less than 0.05 on both sides is considered statistically significant. In addition, in the correlation analysis, Bonferroni correction was applied to re-determine the α value. IBM SPSS Statistics 13.0 (IBM Corporation, Armonk, NY, USA) is used to process and analyze all data.

We conducted this study in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Meizhou People’s Hospital (approval number: 2020-C-07). Written informed consent was obtained from all participants.

The clinical characteristics of the patients are summarized in Table 1, showing that the difference between included and excluded patients was not statistically significant (P>0.05). Of the 74 patients included, 73 (98.7%) were men. The average age is 68.2±6.3 years. Bronchoalveolar lavage fluid (BALF) and/or sputum cultures were positive in 4 patients; two patients tested positive for Pseudomonas aeruginosa, while the remaining two patients tested positive for Klebsiella pneumoniae . The serum procalcitonin (PCT) levels of two patients were >0.25 μg/L. During the hospitalization, no patient died or received invasive mechanical ventilation, 1 patient was admitted to the ICU, and 5 patients received non-invasive positive pressure ventilation (NPPV). The median length of hospital stay was 5.0 (IQR 25-75, 5.0-7.0). Table 1 Comparison of included and excluded patients

Table 1 Comparison of included and excluded patients

The median total LMS was 15.0 (IQR 25-75, 12.0-21.0). In at least one site, 58 (78.4%) patients had mucus blockage in the lumen-the corresponding site scored 3. The results of lung function after bronchodilator are shown in Table 2. The predicted medians of FEF25%-75% and FEV1% reflecting small airway diseases were 0.42 L/sec (IQR 25-75, 0.30-0.62 L/sec) and 39.6 (IQR 25–75, 29.8–52.4), respectively . Table 2 Pulmonary function of 74 COPD patients after using bronchodilators

Table 2 Pulmonary function of 74 COPD patients after using bronchodilators

Table 3 shows the correlation analysis results of total LMS, lung function parameters and HRQoL scores (CAT, mMRC, EXACT, SGRQ). Among the demographic characteristics, BMI, length of hospital stay, and the presence of chronic bronchitis were weakly correlated with total LMS (ρ=-0.269, P=0.020; ρ=0.257, P=0.027; and ρ=0.300, P= 0.009), while there is no significant correlation between age and smoking volume and total LMS. Table 3 The relationship between the total lumen mucus score and other parameters

Table 3 The relationship between the total lumen mucus score and other parameters

The scores of the 4 questionnaires (CAT, mMRC, EXACT and SGRQ) were significantly positively correlated with the total LMS, and the correlation coefficient between the total LMS and the mMRC and SGRQ scores was relatively high (ρ=0.527, P<0.001; ρ=0.441, P< 0.001, respectively) (Figure 3). Pulmonary function parameters after bronchodilators were significantly negatively correlated with total LMS. The predicted FEF25%-75% and FEV1% were strongly correlated with total LMS (ρ=-0.518, P<0.001; ρ=-0.498, P< 0.001, respectively) (Figure 3). Among the results of these laboratory tests, only PaCO2 was weakly positively correlated with total LMS (ρ=0.273, P=0.018), while serum CRP levels and the counts of neutrophils, lymphocytes, and eosinophils were not correlated with total LMS sex. Figure 3 Correlation score of total lumen mucus and mMRC grade, SGRQ score, FEF25%–75% and FEV1% prediction. Note: The total lumen mucus score is significantly correlated with mMRC grade (A), SGRQ score (B), FEF25%-75% (C) and FEV1% prediction (D). Abbreviations: mMRC, Modified Medical Research Council Dyspnea Scale; SGRQ, St. George's Respiratory Questionnaire; PaCO2, FEF 25%–75%, mandatory expiratory flow is 25% to 75% of FVC.

Figure 3 Correlation between total lumen mucus score and mMRC grade, SGRQ score, FEF25%–75% and FEV1% prediction. Note: The total lumen mucus score is significantly correlated with mMRC grade (A), SGRQ score (B), FEF25%-75% (C) and FEV1% prediction (D).

Abbreviations: mMRC, Modified Medical Research Council Dyspnea Scale; SGRQ, St. George's Respiratory Questionnaire; PaCO2, FEF 25%–75%, mandatory expiratory flow is 25% to 75% of FVC.

In order to reduce the risk of type I errors in the multi-index correlation analysis, the Bonferroni correction was used to determine a more stringent α level of 0.0023 (0.05/22), which was used to reassess the correlation between the total LMS and other parameters. At the new test level, total LMS showed significant correlation with mMRC, EXACT, SGRQ and vital capacity parameters.

Table 4 shows the relationship between LMS and FEV1% predicted value and mMRC grading in each lobe. 9 lung lobes were examined, including right upper lobe bronchus (RULB), right middle lobe bronchus (RMLB), right lower lobe bronchus (RLLB), left upper lobe bronchus (LUDB), tongue bronchus, left lower lobe bronchus (LLLB), bilateral upper lobe Bronchus (RULB and LUDB), RMLB and tongue bronchus, bilateral lower lobe bronchus (RLLB and LLLB). Except for LMS in RLLB and RULB, LMS in all other lung lobes was significantly positively correlated with FEV1% predicted value. Regarding the mMRC grade, the LMS in all leaves except RLLB are significantly correlated with this grade. Under the more stringent α level 0.0027 (0.05/18) re-determined by Bonferroni correction, LMS in LUDB and bilateral ULB were significantly correlated with predicted FEV1%; RULB, RMLB, LUDB, tongue bronchus, RMLB and tongue bronchus And the LMS in the bilateral ULB is significantly related to the mMRC classification. Table 4 The relationship between luminal mucus scores of different lung lobes and FEV1% predicted value and mMRC grade

Table 4 The relationship between luminal mucus scores of different lung lobes and FEV1% predicted value and mMRC grade

Perform stepwise multiple linear regression to determine the factors that can be used to predict lumen mucus. In the final regression model, mMRC score and FEV1% prediction were significant factors (R2=0.348, F=18.960, P<0.001). The results of multiple linear regression are shown in Table 5. Table 5 Stepwise multiple linear regression analysis of Luminal Mucus Scorea

Table 5 Stepwise multiple linear regression analysis of Luminal Mucus Scorea

The current study examines the relationship between LMS in hospitalized patients determined by bronchoscopy and indicators that reflect the severity of AECOPD, including lung function, HRQoL assessment, and laboratory test results. Our results indicate that LMS is associated with decreased lung function and worsening HRQoL in patients with severe AECOPD. Therefore, this study provides a new perspective on the luminal mucus in the large airways of the disease.

Our research has several advantages. First, previous studies have focused on small airways rather than large airways. Second, previous studies focused more on the airway mucus of patients with stable COPD, while we focused on the acute exacerbation phase, which is characterized by a significant increase in sputum production. Third, it is generally believed that the CT signs of "lumen plug" reflect the "mucus plug" in the large airway, but it still needs to be confirmed. We used bronchoscopy to score luminal mucus and obtained direct evidence of this problem. Last but not least, many clinical parameters of AECOPD, such as lung function, four different HRQoL questionnaires and laboratory indicators, are included to obtain more representative and convincing data.

We found that 78.4% of AECOPD subjects had at least one mucus blockage, which was higher than that of stable COPD patients (25%), 3 or severe asthma patients (58-67%). 14,15 In addition, in patients with AECOPD, their airway mucus increases as their lung function decreases, which is consistent with the results of recent studies. In patients with stable COPD3 or severe asthma, the obstruction of the large airways (diameter> 2 mm) identified on 14 CT scans was associated with a lower FEV1% predicted value. It is well known that the accumulation of mucus in the small airways is closely related to the severity of COPD2. In fact, the mucus-producing glands are mainly distributed in the large airways 1, and the storage of mucus in the epithelium significantly increases the airway cells of smokers with restricted airflow. 16 In addition, some studies have shown that the mucus in some small airways contains relatively few cells. Therefore, this mucus may be produced in the large airways and be inhaled into the small airways. 17 COPD patients often experience skeletal muscle dysfunction, diaphragm dysfunction, and impaired cilia function, 18,19 these often worsen during acute exacerbations. Under the combined action of these factors, lumen mucus cannot be effectively cleared, and it stays in the large airways, which is a common channel for mucus to be discharged. These factors may partially explain the relationship between airway LMS and AECOPD airflow obstruction, but the exact mechanism remains to be elucidated.

Chronic cough and sputum production, also known as chronic bronchitis, are common symptoms and key components of COPD. 18 The research focused on the potential impact of chronic bronchitis on COPD, called "chronic mucus hypersecretion". 20,21 Our results indicate that chronic bronchitis is weakly positively correlated with total LMS. However, in the two previous studies, lumen blockage was not associated with chronic cough and sputum in stable COPD and severe asthma. 3,14 One possible explanation for these inconsistent results is that the larger airways that can be observed by bronchoscopy may have more cough receptors. twenty two

COPD patients with higher tract mucus scores have higher SGRQ scores, indicating poor HRQoL. 3 In our study, not only the SGRQ score, but also the CAT score, mMRC score and EXACT score were significantly correlated with the total score. LMS further proves the relationship between airway mucus and HRQoL.

The correlation analysis of LMS of each leaf with FEV1% predicted value and mMRC classification showed that the correlation of upper lobe bronchus LMS was greater than that of lower lobe bronchus (Table 4). Our study cannot explain the results because there are many factors and mechanisms that affect the regional distribution of lung ventilation and perfusion. 23 Well-designed studies are needed to explore the potential effects of luminal mucus in different lung lobes on lung function.

When the CRP level and white blood cell count in the sputum of patients with acute exacerbation are significantly higher than in the steady state, serum CRP and sputum white blood cell count are positively correlated, which indicates that AECOPD systemic inflammation is related to lower respiratory tract inflammation. 24 Nevertheless, our results show that the total LMS in the large airways has no significant correlation with the counts of neutrophils, lymphocytes, eosinophils, fibrinogen or CRP, which is puzzling. Therefore, in order to draw a clearer conclusion, it is necessary to further study the relationship between systemic inflammation, lower respiratory tract inflammation and large respiratory tract mucus in the future.

EXACT is widely used to clinically assess the severity and duration of AECOPD. 25 It is also a sensitive and reliable tool for measuring changes in deteriorating conditions during recovery. 26 Compared with the baseline, the CAT score at the time of deterioration increased significantly and reflected the severity of the deterioration, as determined by the lung function and the length of the deterioration, indicating that CAT provides a reliable score of the severity of the deterioration. 4 In our study, total LMS is significantly correlated with CAT score and EXACT score, which indicates that total LMS may partly reflect the severity of AECOPD.

Our results may have therapeutic implications. For patients with AECOPD27 who underwent tracheal intubation and children with acute asthma28 with respiratory failure, bronchoscopic sputum suction showed clinical benefit. In addition, for COPD patients with acute respiratory failure who are suitable for conventional mechanical ventilation due to hypercapnic encephalopathy and unable to clear a large amount of secretions, bronchoscopy suction combined with non-invasive positive pressure ventilation enables 80% (12/15) of patients to avoid tracheal intubation Tube. 29 We found that 78.4% of hospitalized patients have at least one mucus blockage in the lumen, and the total LMS is proportional to PaCO2, which indicates that early application of airway clearance techniques, including bronchoscopy, may be effective for AECOPD hospitalized patients.

Our research has some limitations. First, this is a cross-sectional study without follow-up; therefore, causality cannot be established, and changes in stable COPD parameters are unclear. Therefore, further cohort studies are needed. Secondly, all the subjects in this study are hospitalized patients in the “severe” category of GOLD 2021 acute exacerbation. 18 Therefore, the conclusions of this study still need to be verified at all levels of the disease. Finally, bronchoscopy is invasive, which limits its wide clinical use for luminal mucus scoring.

In AECOPD hospitalized patients, mucus often blocks the lumen of the large airway, and LMS is significantly associated with decreased lung function and poor HRQoL. If repeated, our results suggest that LMS may be a direct indicator of the severity of AECOPD.

COPD, chronic obstructive pulmonary disease; AECOPD, acute exacerbation of COPD; SGRQ, St. George's Respiratory Questionnaire; mMRC, modified Medical Research Council Dyspnea Scale; CAT, COPD assessment test; EXACT, chronic lung disease deterioration tool; HRQoL, related to health Quality of life; FEF 25%–75%, forced expiratory flow is 25% to 75% of FVC; FEV1, forced expiratory volume in 1 second; LMS, lumen mucus score; FVC, forced vital capacity; CRP, C-reactive protein ; LFT, lung function test; BMI, body mass index; PaCO2, partial pressure of carbon dioxide; PEF, peak expiratory flow; RULB, right upper lobe bronchus; RMLB, right middle lobe bronchus; RLLB, right lower lobe bronchus; LUDB, left upper bronchus; LLLB, left lower lobe bronchus; ULB, upper lobe bronchus; LLB, lower lobe bronchus.

The data set used and/or analyzed in this study can be obtained from the corresponding author (Zhang Qianyun) according to reasonable requirements.

The author would like to thank the participants and their families who participated in this study. Thanks to the staff of the Department of Pulmonary Intensive Medicine, Meizhou People's Hospital, for their strong support.

All authors have made significant contributions to the work of the report, whether in terms of concept, research design, execution, data acquisition, analysis and interpretation, or in all these areas; drafting or writing, or drastically revised or critically reviewed The article; has reached an agreement on the journal to which the article will be submitted; finally approved the version to be published; and agreed to be responsible for the content of the article.

During the study, Dr. Yang reported on funding from the Guangdong Provincial Health Commission. Dr. Yang announced that he was awarded the Medical Science Research Fund of Guangdong Province, China (No.A2021410). Other authors report no conflicts of interest in this work.

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