ORIGINAL ARTICLE


https://doi.org/10.5005/jp-journals-11010-1083
Indian Journal of Respiratory Care
Volume 12 | Issue 4 | Year 2023

Investigation of the Pulmonary Function of Patients with Asthma and Chronic Obstructive Pulmonary Disease Following COVID-19 Infection


Azita Tangestaninezhad1, Alireza Jafarinezhad2, Shaghayegh Hoseindoust3, Habib Islami4

1–4Inflammatory Lung Diseases Research Center, Department of Internal Medicine, School of Medicine, Razi Hospital, Guilan University of Medical Sciences, Rasht, Iran

Corresponding Author: Alireza Jafarinezhad, Inflammatory Lung Diseases Research Center, Department of Internal Medicine, School of Medicine, Razi Hospital, Guilan University of Medical Sciences, Rasht, Iran, Phone: +989368829763, e-mail: alireza.jafarinezhad.md@gmail.com

Received: 17 July 2023; Accepted: 14 December 2023; Published on: 18 January 2024

ABSTRACT

Aims and background: In this present study, we aimed to investigate the pulmonary function of patients with asthma and chronic obstructive pulmonary disease (COPD) following coronavirus disease of 2019 (COVID-19) infection.

Materials and methods: All data of 266 COVID-19 patients with and without a history of asthma/COPD who were referred to the Razi Hospital, Rasht, Iran, from 2021 to 2022 were collected. Patient self-assessment of the impact of COVID-19 on health using the COPD assessment test (CAT) score criterion in both study groups, asthma control test (ACT) in asthma patients, and modified Medical Research Council (mMRC) in COPD patients were evaluated. All data were analyzed using Statistical Package for the Social Sciences (SPSS) version 26 with a significant level of <0.05.

Result: According to our results, the mean age of patients was 51.7 ± 14.1 years old; 51% of them were female, and most of the patients were obese. Hypertension and diabetes were the most common comorbidities. The frequency of 6-minute walking test (6MWT) was higher in patients with asthma/COPD at the time of discharge. From the first to second and third follow-ups, forced expiratory volume in 1 second (FEV1) increased in asthma/COPD groups, and FEV1/forced vital capacity (FVC) decreased in the control group. Also, the CAT score in the first and second follow-ups was worse in asthma/COPD groups compared to the control group. In both studied groups, the self-evaluation of patients using all three questionnaires shows a significant improvement process.

Conclusion: A significant improvement in shortness of breath and self-assessment tests was observed in patients with asthma/COPD. However, the results of the 6MWT and self-assessment tests at the time of discharge in these patients were more concerning compared to the control group.

Clinical significance: Patients with asthma/COPD were at a similar risk of COVID-19 infection compared to the general population. Females and obese individuals were the majority of the patients. FEV1 in asthma/COPD groups showed improvement in long-term follow-up.

How to cite this article: Tangestaninezhad A, Jafarinezhad A, Hoseindoust S, et al. Investigation of the Pulmonary Function of Patients with Asthma and Chronic Obstructive Pulmonary Disease Following COVID-19 Infection. Indian J Respir Care 2023;12(4):339–344.

Source of support: Nil

Conflict of interest: None

Keywords: 6-minute walk test, Asthma, Chronic obstructive pulmonary disease, Coronavirus disease of 2019

INTRODUCTION

The coronavirus disease of 2019 (COVID-19) pandemic caused by acute respiratory syndrome severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has so far affected millions of people in the world, and despite the vaccination of people to reduce the deaths caused by COVID-19, this disease is still treating lives. COVID-19 affects the lungs more than other organs. SARS-CoV-2 primarily attacks lung alveolar epithelial cells.1,2 Although most SARS-CoV-2 infections are thought to be subclinical or associated with mild symptoms, this infection may lead to acute respiratory distress syndrome (ARDS) and sometimes organ failure.3 Virus particles are transmitted through large respiratory droplets by a symptomatic patient or an asymptomatic carrier when coughing and sneezing.4 It has been reported that SARS-CoV-2 uses angiotensin-converting enzyme 2 (ACE-2) as a cell receptor to enter the cell. It has been found that SARS-CoV-2 also uses the same enzyme as a receptor to enter the cell.5 ACE-2 is present in the cells of the lung alveolar epithelium and enterocytes of the small intestine, and it is the place where the virus enters the cell. This enzyme breaks down angiotensin 2, which is an inflammatory factor in the lungs. Therefore, inhibition of the receptor of this enzyme by the coronavirus has been suggested as another factor in lung damage.6

Also, SARS-CoV-2, with direct damage to ACE-2 enzyme receptors and disruption of the immune system, leads to cardiovascular complications such as myocarditis, acute myocardial infarction (MI), heart failure, dysrhythmias, and cardiac thrombolytic. Disruption of the immune system with the increase of inflammatory cytokines leads to an increase in metabolic demand and coagulation activities in the form of instability of vascular plaques. These injuries increase the lethality of the disease and affect the quality of life of patients who have recovered from COVID-19.7,10 Asthma and chronic obstructive pulmonary disease (COPD) are very common inflammatory diseases of the airways. Also, the prevalence of these two diseases is increasing, and they impose a lot of costs on society. Pulmonary function tests are necessary to diagnose and evaluate the severity of respiratory diseases and are useful in tracking their progress.11,12 Due to the lack of complete understanding of the characteristics of COVID-19, the effect of underlying respiratory diseases, such as the presence of COPD on clinical manifestations and the course of SARS-CoV-2 infection, is not clear.5

In some studies, it has been reported that the risk of contracting COVID-19 in patients with asthma is significantly lower. It may be due to a decrease in the expression of the ACE-2 enzyme receptor in these patients compared to the control group and COPD patients. Meanwhile, the expression of this receptor is more prominent in older age.13 On the other hand, viruses that infect the respiratory system are considered a risk factor for the exacerbation of asthma, and early respiratory viral infections may even lead to the development of asthma.14 In addition, the similarity of symptoms of exacerbation in asthma/COPD, including cough and shortness of breath, with the symptoms of COVID-19 makes the diagnosis of COVID-19 in these patients so challenging.15 Also, COPD increases the risk of morbidity and mortality in comorbidities with other respiratory diseases. Moreover, lung damage caused by COVID-19 pneumonia can lead to impaired lung function and continue for months and years.2

The obstructive pattern of lung function, which is associated with an increased risk of life-threatening comorbidities, has been seen in patients who survived COVID-19 pneumonia. Considering the changing nature of this disease, it’s important to pay more attention to the respiratory function of patients with asthma, COPD, and lung injuries caused by COVID-19. In this regard, we aimed to determine the pulmonary function of asthma/COPD patients after COVID-19 using spirometry and evaluating forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC), FE1/FVC, and TLC, 6-minute walking test (6MWT), and also evaluating the severity and number of asthma/COPD attacks via CAT, modified Medical Research Council (mMRC), and asthma control test (ACT) scores.

MATERIALS AND METHODS

Study Design

This retrospective study involved the selection of 266 recovered patients with COVID-19. The patients were selected using a convenience sampling method from those referred to Razi Hospital in Rasht, Iran, between 2021 and 2022. The diagnosis of COVID-19 was confirmed through a positive result on a nasopharyngeal polymerase chain reaction (PCR) test, while asthma or COPD diagnoses were made based on the national protocol by a specialist. The patients were divided into two groups: the case group (n = 54) consisted of COVID-19 patients with asthma or COPD, and the control group (n = 212) comprised COVID-19 patients without any underlying lung disease. Inclusion criteria required patients to have undergone at least two spirometry or 6MWT tests after COVID-19 infection and to have undergone follow-up. Patients who died during hospitalization and those with incomplete data were excluded from the study. The study received ethical approval from the ethical committee at the Guilan University of Medical Sciences, Rasht, Iran [IR.GUMS.REC.1400.278].

Variables

Demographic data and clinical characteristics of the patients were collected from their medical records. This included information such as age, gender, place of residence, body mass index (BMI) categorized as low weight (BMI < 18.5 kg/m2), normal weight (BMI = 18.5–24.99 kg/m2), overweight (BMI = 25–29.9 kg/m2), and obese (BMI ≥ 30 kg/m2), smoking history, comorbidities, time interval from hospital discharge to referral, spirometry test values including FEV1, FVC, FEV1/FVC ratio, 6-minute walk test (6MWT) results, and walking distance. The impact of the disease on patients’ daily life expectancy was assessed using the CAT score questionnaire. The number of asthma and COPD attacks, as well as the severity of these conditions after contracting COVID-19, were evaluated using the ACT and mMRC questionnaires, respectively. Follow-up assessments were conducted at the time of clinical improvement or discharge, as well as 3 and 6 months after discharge. In spirometry, normal values for FEV1 and FVC are expected to be >80% of the predicted normal, while FEV1/FVC should be >70%. In cases of obstructive pulmonary dysfunction, FVC decreases, and in cases of restrictive dysfunction, both FEV1 and FEV1/FVC are lower than normal.

The main criterion for assessing the functional status of the patients was the distance they were able to walk, which was measured in meters. An increase in walked distance or a decrease in symptoms after walking the same distance indicated an improvement in the patient’s performance. During the 6MWT, if any symptoms such as chest pain, shortness of breath, unbearable fatigue, leg cramps, dizziness, diaphoresis (sweating), pale appearance, or cyanosis occurred, the test was paused, and the patient’s oxygen saturation was checked.16 If the oxygen saturation decreased >3% from the baseline or if it was below 94% at the end of the 6MWT, the result was considered positive.17,18

Statistical Analysis

Descriptive statistics were used to summarize the data. Mean and standard deviations were used to describe quantitative variables with a normal distribution, while median and interquartile ranges were used for variables with an abnormal distribution. Qualitative variables were described using counts and percentages. To compare quantitative parametric variables, the t-test was employed, whereas the Mann–Whitney U test was used for nonparametric variables. The Chi-squared test was utilized to analyze qualitative variables. Changes in spirometry indices and CAT scores were tracked using the ANOVA statistical method. For comparing qualitative variables between two groups at different measurement times, the Chi-squared test and Fisher’s exact test were employed. The significance level for all tests in this study was set at <0.05. All data analyses were performed using Statistical Package for the Social Sciences (SPSS) version 26 software.

RESULTS

Out of 266 patients, 212 patients had no history of primary lung disease (control). Out of 54 patients, 44 patients (81.5%) had asthma, and 10 patients (18.5%) had COPD. The frequency of demographical data and clinical characteristics of patients are illustrated in Table 1. Due to our results, the frequency of patients in the two groups was similar in terms of age, gender, habitat, BMI, and type of underlying diseases. About 57.9% of the patients were in the age group above 50 years (with an average age of 51.7 ± 14.1; the youngest age was 18, and the oldest was 85 years). The frequency of males and females with COVID-19 was similar. About 51% of the patients were female, and about 49% were male. The majority of patients (84.2%) were rural residents. Most of the patients were overweight and obese.

Table 1: Demographical data and clinical characteristics of patients with COVID-19 with and without asthma and COPD
Variables Patients with COVID-19, n (%) p-value
With COPD or asthma, n = 54 Without COPD or asthma, n = 212 Total, n = 226
Age (year) <40 16 (29.6) 38 (17.9) 54 (20.3) 0.100
40–49 13 (24.1) 45 (21.2) 58 (21.8)
50–59 9 (16.7) 66 (31.1) 75 (28.2)
60< 16 (29.6) 63 (29.7) 79 (29.7)
Sex Male 22 (40.7) 109 (51.4) 131 (49.2) 0.161
Female 32 (59.3) 103 (48.6) 135 (50.8)
Hospitalized status ICU 1 (1.9) 4 (1.9) 5 (1.9) 0.010
Other units 40 (74.1) 189 (89.20) 229 (86.1)
Outpatient 13 (24.1) 19 (9.0) 32 (12.0)
Habitat Urban 44 (81.5) 180 (84.9) 224 (84.2) 0.538
Rural 10 (18.5) 32 (15.1) 42 (915.8)
History of smoking No 40 (74.1) 200 (94.3) 240 (90.2) <0.001
Yes 14 (25.9) 12 (5.7) 26 (9.8)
BMI <20 3 (5.6) 3 (1.4) 6 (2.3) 0.296
20 < BMI < 25 15 (27.8) 53 (25.0) 68 (25.6)
25 < BMI < 30 19 (35.2) 84 (39.6) 103 (38.7)
30< 17 (31.5) 729 (34.0) 89 (33.5)
Diabetes mellitus No 43 (79.6) 151 (71.2) 194 (72.9) 0.215
Yes 11 (20.4) 61 (28.8) 72 (27.1)
Hypertension No 39 (72.20) 152 (71.7) 191 (71.8) 0.939
Yes 15 (27.8) 60 (28.3) 75 (28.2)
CVD No 53 (98.1) 193 (91.0) 246 (92.5) 0.077
Yes 1 (1.9) 19 (9.0) 20 (7.50
Hyperlipidemia No 48 (88.9) 172 (81.1) 220 (82.7) 0.178
Yes 6 (11.1) 40 (18.9) 46 (17.3)
Cerebrovascular disease No 53 (98.1) 207 (97.6) 260 (97.7) 0.050
Yes 1 (1.9) 5 (2.4) 6 (2.3)

The most frequent underlying diseases were hypertension, diabetes mellitus, hyperlipidemia, and cardiovascular disease (CVD), 28.2, 27.1, 17.3, and 7.55%, respectively. The majority of the patients had no history of smoking, and the frequency of smokers in the asthma/COPD group (25.9%) compared to the control group (5.7%), p < 0.05. The frequency of hospitalization in the two study groups was significantly different among patients (p < 005) and was 15% higher in the control group compared to asthma/COPD groups.

In general, 152 patients participated in the second follow-up at a time interval of 3.22 ± 0.971 months from the first visit (minimum of 1 month and maximum of 8 months later), of which 102 patients were in the control group, and 50 patients were in asthma/COPD group. Also, 53 patients (27 patients from the control group and 26 patients from the asthma/COPD group) participated in the third follow-up at a time interval of 6.74 ± 2.56 months from the time of discharge (minimum 3 and maximum 13 months later). There is no significant difference between the two studied groups in terms of the follow-up time intervals (p > 0.05).

According to the result of pulmonary function tests, a significant improvement in FEV1 of asthma/COPD groups was observed in the second and third follow-ups compared to the first follow-up (p1–3 = 0.043, p1–2 = 0.033). In the FEV1/FVC ratio in the control group, there was a significant decrease in the second and third follow-ups compared to the first follow-up (p1–2 and p1–3 < 0.001). To compare both groups, the amount of FVC in the second follow-up and the FEV1/FVC ratio in the first follow-up was significantly lower in asthma/COPD groups than in the control group (p1 = 0.036 and p2 = 0.002, respectively) (Table 2).

Table 2: Spirometric indices among two study groups during the follow-up periods of the patients
Scores Patients with COVID-19 p-value
With COPD or asthma, mean ± SD Without COPD or asthma, mean ± SD Total, mean ± SD
CAT I 13.49 ± 5.07 8.10 ± 3.62 10.52 ± 5.08 <0.001
CAT II 5.22 ± 3.11 3.68 ± 3.21 4.34 ± 3.25 0.009
CAT III 2.29 ± 1.92 1.79 ± 3.17 2.42 ± 2.11 0.145
FEV1 I 78.08 ± 19.89 96.89 ± 18.88 89.71 ± 21.20 0.002
FEV1 II 85.03 ± 17.45 98.44 ± 14.99 95.55 ± 15.87 <0.001
FEV1 III 80.06 ± 9.39 98.94 ± 17.67 94.65 ± 17.90 0.014
FVC I 87.67 ± 16.66 9420 ± 17.38 91.71 ± 17.25 0.194
FVC II 86.98 ± 14.59 93.65 ± 14.98 92.21 ± 15.09 0.036
FVC III 87.90 ± 10.61 96.86 ± 20.15 94.82 ± 18.59 0.183
FEV1/FVC I 83.33 ± 15.79 97.20 ± 13.94 92.06 ± 15.96 0.002
FEV1/FVC II 85.26 ± 11.41 87.70 ± 4.85 87.17 ± 6.84 0.185
FEV1/FVC III 89.90 ± 4.13 87.36 ± 8.00 87.94 ± 7.30 0.256

In the self-evaluation of patients with COVID-19, the mean and median CAT score in asthma and COPD group in the first (p < 0.001) and second follow-up (p = 0.009) was worse than the control group (13/49 vs 8/10 at the time of discharge). Also, this score had a significant decrease in both groups (p < 0.001), and the recovery frequency was higher in asthma/COPD groups compared to the control group (p = 0.009). This course of recovery was also evident in the examination of each group of patients with asthma (based on the ACT questionnaire) and COPD patients (based on mMRC).

According to Table 3, the results of 6MWT revealed that the prevalence of patients with a positive 6MWT in the first follow-up among the asthma/COPD group was higher than the control group (37.5 vs 12.6%, p < 0.001). The walking distance in the first follow-up was significantly less in the asthma/COPD group compared to the control group (average of 358.70 vs 411.43 m, p = 0.010). The differences in walked distance only in the first visit were significant between the two groups (p = 0.010). The changes in the walked distance from the first to the second follow-up in the control group (p = 0.196) and also in the asthma/COPD group (p = 0.464) were not statistically significant.

Table 3: The results of the 6MWT during the follow-up times
Scores Patients with COVID-19 p-value with COPD or asthma, n (%)
With COPD or asthma, n (%) Without COPD or asthma, n (%) Total, n (%)
6MWT follow-up I 12 (37.5) 23 (12.6) 35 (16.4) <0.001
20 (62.5) 159 (87.4) 179 (83.6)
6MWT follow-up II 0 (0.0) 12 (15.8) 12 (13.8) 0.176
11 (100.0) 64 (84.2) 75 (86.2)
6MWT follow-up III 0 (0.0) 0 (0.0) 0 (0.0)
1 (100.0) 5 (100.0) 6 (100.0)

Based on the results of this study, in the 6MWT, in the first, second, and third follow-ups, 2.5, 3.3, and 0.0% of the patients had a baseline oxygen saturation of <94%. The prevalence of patients with O2 saturation of <94% in the control group from the first to the third follow-up was 2, 3.8, and 0.0%, respectively, and in asthma/COPD, was 5.6% in the first follow-up and 0.0% in the second and third follow-ups. Also, after performing this test, arterial oxygen saturation in 4.4, 1.1, and 0.0% of the patients was >3% in the first to third follow-ups, respectively. The frequency of patients with O2 saturation decreased by >3% from the baseline at the end of this test in the control group from the first to the third follow-ups, 4.1, 1.3, and 0%, respectively, and in the asthma and COPD group, 5.9% in the first follow-up and 0.0% in the other two follow-ups, which represented no statistically significant difference among groups (p > 0.05).

It was found that 10.6% of the patients stopped in the first round of this test, and this rate was 10.1 and 14.3% in the second and third follow-ups, respectively. In the control group, the prevalence of patients who stopped the test before six minutes due to reasons such as musculoskeletal pain, chest pain, fatigue, and shortness of breath from 8.1% the first time increased to 11.5 and 16.7% in the second and third follow-up, respectively, and in asthma/COPD group, it decreased from 25% in the first time to 0.0% in the other two times. The frequency of cessation in asthma/COPD patients in the first follow-up was significantly higher compared to the control group (25 vs 8.1%, p = 0.004).

DISCUSSION

Despite the high prevalence of COVID-19 disease, asthma, and COPD all around the world, many studies are still required to be conducted in the field of outcomes for patients with asthma and COPD who engage with COVID-19 diseases. Therefore, this study investigated the lung function tests, including spirometry, 6MWT, and self-evaluation of patients with primary asthma/COPD after recovery from COVID-19, using the well-known CAT score criteria to compare with recovered COVID-19 patients without any history of lung diseases. Our results demonstrated that the average age of participants was 51.7 ± 14.1 years; 51% of the participants were female, and 72.2% were overweight and obese. Hypertension, diabetes, CVD, and dyslipidemia were the most frequently reported comorbidities. We found significant differences between asthma/COPD and control groups in the CAT score measures on the first and second follow-ups. The improvement was found in mMRC test results among COPD patients and ACT in asthma patients. There were more positive results in 6MWT and stopping before 6 minutes in the asthma/COPD group on the first follow-up than in the control group with less average distance. Spirometry results showed no statistically significant changes during the follow-ups of the patients in this study; however, there was a significant trend toward improvement in FEV1 among patients with asthma/COPD and a significant decrease in the FEV1/ FVC among the control group.

Based on the spirometry findings in the study of Frija-Masson et al., the average FEV1 was 93 (83–100), FVC was 93 (85–99), and FEV1/FVC was 0.81 (0.87–75) L. They reported that 46% of patients had a normal pattern in pulmonary function tests. The frequency of pulmonary disorders was diffusion capacity disorder (26%), restrictive pattern with diffusion disorder (16%), and restrictive pattern alone (12%), respectively.19 In Huang’s study, the mean of FEV1 was 97.89, FVC was 100.96, and FEV1/FVC was 81.22. The severity of FVC disorder was expressed in 8.7% of cases with mild conditions and 1.8% of patients with moderate conditions. Also, the severity of FEV1/FVC disorder was mild in 43.9% of patients.20

In various studies, restrictive lung pattern has been mentioned as one of the most common disorders in pulmonary function tests. This can be related to the neuromuscular weakness caused by the disease, the decrease of the lung’s ability, and the strong reaction of the airways to infection and long-term smoking.21,22 The mean of FEV1, FVC, and ratio of FEV1/FVC were 92.7 ± 11.57, 93.59 ± 12.25, and 80.70 ± 5.81%, respectively, were reported in Mo et al.’s study. Also, FEV1 and FVC were <80% in 15 and 10% of patients, respectively, and the ratio of FEV1/FVC was <70% in 5% of patients, and the restrictive pattern was the most common spirometric complications among these patients.2

A study by Fumagali et al. demonstrated that the limiting pattern was seen in 10 of the 13 patients, and six weeks after discharge from the intensive care unit (ICU), despite the improvement of these patients’ pulmonary function, the pattern was still present.23 Sibila et al.’s study demonstrated that the median of FEV1, FVC, and FEV1/FVC was 94 (80–105), 90 (80–100), 90, and 0.8 (0.75–0.84) L, respectively, and the most common lung diseases were FEV1 (in 25% of patients) and FVC (in 24%).24 Their results were in line with the spirometric findings of our study.

In Huang et al.’s study, 11.6% of the studied patients were unable to complete the 6MWT in 30 days after discharge from the hospital. A higher frequency of positive 6MWT in patients hospitalized in ICU or with a longer hospitalization period, shortness of breath, a respiratory rate >30 times per minute, arterial oxygen saturation <93%, and mechanical ventilation (p = 0.011).20

Due to the results of the current study, mean CAT scores in asthma and COPD groups were higher (worse) in the first and second follow-ups, while in the third follow-up, the scores were more similar in the two groups (p > 0.05). In the study of Daynes et al. on 131 hospitalized patients diagnosed with COVID-19, asthma and COPD were present in 25.2% of the studied patients. Also, in the patients of this study, the symptoms related to the airways were similar to the normal population, whereas the score related to the symptoms of shortness of breath, decreased energy, sleep disorders, and activity were concerning.25

The mMRC criterion patients with COPD patients decreased and improved from the first to the second follow-up and also from the second to the third follow-up So that the intensity of shortness of breath in the patients who were unable to leave the house in the first follow-up or had shortness of breath while getting dressed, reached zero in the subsequent follow-ups, and the maximum amount of shortness of breath was after intense exercise. In Xiaojun et al.’s study on 83 patients with COVID-19 without any underlying disease or a history of smoking, after three months of discharge, this criterion was at least 1 in 81% of patients and at least 2 in 6%. This criterion improved rapidly after 12 months of discharge, and severe shortness of breath persisted in only 5% of patients.26

Limitation

The retrospective nature of the study is one of its limitations. Also, it has been suggested that a larger sample size be investigated in future studies.

CONCLUSION

As noted, patients with asthma/COPD were not at a higher risk than the general population in terms of exacerbation of lung function tests and activity capacity after COVID-19 infection, and there was a significant improvement in shortness of breath and self-assessment tests of patients. As a result, it is recommended to evaluate these patients in terms of the need for pulmonary rehabilitation and respiratory physiotherapy to prevent irreversible pulmonary complications such as pulmonary fibrosis.

Clinical Significance

  • Patients with asthma/COPD were not at a higher risk than the general population after COVID-19 infection.

  • The frequency of females and obesity was higher among patients.

  • A significant improvement in FEV1 of asthma/COPD groups was observed in long-term follow-up.

REFERENCES

1. Morawska L, Cao J. Airborne transmission of SARS-CoV-2: the world should face the reality. Environ Int 2020;139:105730. DOI: 10.1016/j.envint.2020.105730

2. Mo X, Jian W, Su Z, et al. Abnormal pulmonary function in COVID-19 patients at time of hospital discharge. Eur Respir J 2020;55(6):2001217. DOI: 10.1183/13993003.01217-2020

3. Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382(18):1708–1720. DOI: 10.1056/NEJMoa2002032

4. Zou L, Ruan F, Huang M, et al. SARS-CoV-2 viral load in upper respiratory specimens of infected patients. N Engl J Med 2020;382(12):1177–1179. DOI: 10.1056/NEJMc2001737

5. Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020;579(7798):270–273. DOI: 10.1038/s41586-020-2012-7

6. Ni W, Yang X, Yang D, et al. Role of angiotensin-converting enzyme 2(ACE2) in COVID-19. Crit Care 2020;24(1):422. DOI: 10.1186/s13054-020-03120-0

7. Li J, Wang Y, Zeng Y, et al. Critically ill pregnant patient with COVID-19 and neonatal death within two hours of birth. Int J Gynaecol Obstet 2020;150(1):126–128. DOI: 10.1002/ijgo.13189

8. Zeinali T, Faraji N, Joukar F, et al. Gut bacteria, bacteriophages, and probiotics: tripartite mutualism to quench the SARS-CoV2 storm. Microb Pathog 2022;170:105704. DOI: 10.1016/j.micpath.2022

9. Halaji M, Heiat M, Faraji N, et al. Epidemiology of COVID-19: an updated review. J Res Med Sci 2021;26:82. DOI: 10.4103/jrms.JRMS_506_20

10. Yaghubi T, Shakoori V, Nasiri S, et al. Clinical characteristics and outcomes of COVID-19 patients with a history of cardiovascular disease. J Curr Biomed Reports 2022;3(1): 2022. DOI: 10.52547/jcbior.3.1.36

11. Silverman EK, Crapo JD, Make BJ. Harrison’s Principles of Internal Medicine, 21st edition. New York: McGraw-Hill Education; 2022.

12. Israel E. Asthma. Harrison’s Principles of Internal Medicine, 21st edition. New York: McGraw-Hill Education; 2022.

13. Sunjaya AP, Allida SM, Di Tanna GL, et al. Asthma and COVID-19 risk: a systematic review and meta-analysis. Eur Respir J 2022;59(3).2101209. DOI: 10.1183/13993003.01209-2021

14. Dong X, Cao YY, Lu XX, et al. Eleven faces of coronavirus disease 2019. Allergy 2020;75(7):1699–1709. DOI: 10.1111/all.14289

15. Shchikota AM, Pogonchenkova IV, Turova EA, et al. Chronic obstructive pulmonary disease and COVID-19: topical issues. Pul’monologiya 2020;30(5):599–608. DOI: 10.18093/0869-0189-2020-30-5-599-608

16. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002;166(1):111–117. DOI: 10.1164/ajrccm.166.1.at1102

17. Halabchi F, Mazaheri R. Six min walk test as a criterion for going to the hospital in suspected COVID-19 patients; is it practical, safe and scientifically justified? Front Emerg Med 2020;4(3):e67–e67.

18. Pandit R, Vaity C, Mulakavalupil B, et al. Unmasking hypoxia in COVID 19-six minute walk test. J Assoc Physicians India 2020;68(9):50–51.

19. Frija-Masson J, Debray MP, Gilbert M, et al. Functional characteristics of patients with SARS-CoV-2 pneumonia at 30 days post-infection. Eur Respir J 2020;56(2):2001754. DOI: 10.1183/13993003.01754-2020

20. Huang Y, Tan C, Wu J, et al. Impact of coronavirus disease 2019 on pulmonary function in early convalescence phase. Respir Res 2020;21(1):163. DOI: 10.1186/s12931-020-01429-6

21. Ranu H, Wilde M, Madden B. Pulmonary function tests. Ulster Med J 2011;80(2):84–90.

22. Chiang J, Mehta K, Amin R. Respiratory diagnostic tools in neuromuscular disease. Children (Basel) 2018;5(6):78. DOI: 10.3390/children5060078

23. Fumagalli A, Misuraca C, Bianchi A, et al. Pulmonary function in patients surviving to COVID-19 pneumonia. Infection 2021;49(1):153–157. DOI: 10.1007/s15010-020-01474-9

24. Sibila O, Albacar N, Perea L, et al. Lung function sequelae in COVID-19 patients 3 months after hospital discharge. Arch Bronconeumol 2021;57:59–61. DOI: 10.1016/j.arbres.2021.01.036

25. Daynes E, Gerlis C, Briggs-Price S, et al. COPD assessment test for the evaluation of COVID-19 symptoms. Thorax 2021;76(2):185–187. DOI: 10.1136/thoraxjnl-2020-215916

26. Wu X, Liu X, Zhou Y, et al. 3-month, 6-month, 9-month, and 12-month respiratory outcomes in patients following COVID-19-related hospitalisation: a prospective study. Lancet Respir Med 2021;9(7):747–754. DOI: 10.1016/S2213-2600(21)00174-0

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