Lung function at three months after hospitalization due to COVID‑19 pneumonia: Comparison of alpha, delta and omicron variant predominance periods
- Authors:
- Published online on: January 5, 2024 https://doi.org/10.3892/etm.2024.12372
- Article Number: 83
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Copyright: © Georgakopoulou et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Over 700 million individuals have been affected by the coronavirus disease 2019 (COVID-19), which has already resulted in over 6.5 million deaths (1). The majority of COVID-19 patients have no or minor symptoms, while ~20% of them experience significant symptoms that necessitate hospitalization (2). The most frequent effects of COVID-19 include abnormalities of the respiratory system, although other organs may also be affected (3-7). The host's features, viral dynamics during acute infection and the host immune response have all been reported to correlate with disease severity (8,9). A severe COVID-19 course and greater mortality have been linked to older age, a high body mass index and a variety of comorbidities, including cardiovascular illnesses, diabetes, or types of cancer (10-13).
‘Long-COVID’ refers to some of the recovered patients who have experienced persistent impairments (14-16). In a retrospective analysis involving 193,113 participants, it was discovered that there is an elevated risk for several clinical outcomes, such as respiratory impairment, after COVID-19 disease (17). Another study found that >20% of COVID-19 survivors had pulmonary function impairment after 6 months. In addition, it has been reported that there had been no significant change in lung function impairment after 2 years in one of the largest research projects, with 349 and 230 subjects who had pulmonary function testing, respectively, 6 months and 2 years after discharge (18,19). In the present study, compared with their counterparts who were matched for age, sex and chronic pulmonary disease after two years, survivors with a critical illness had a greater risk of diffusion capacity for carbon monoxide (DLCO) impairment, lower residual volume (RV) and lower total lung capacity (TLC) (18).
The most prevalent manifestation, DLCO, has been related to critical courses during acute illness in a number of studies (20-22). The variability of study designs and settings across studies, however, makes it challenging to reach definitive conclusions. Moreover, most of the studies refer to the first waves of the pandemic (23,24).
Several studies have reported a significantly reduced risk of hospitalization, admission to the intensive care unit, requirement for oxygenation and mortality rate in omicron-infected patients compared with those infected with other variants (25-27).
In addition, it has been reported that there is a reduction in the risk of developing the long COVID-19 syndrome with the omicron variant compared with the delta variant (28). However, knowledge about lung function after hospitalization during the omicron variant predominance period is still scarce. The purpose of the present study was to describe the pulmonary function at three months after hospitalization due to COVID-19 pneumonia and to make a comparison of alpha, delta and omicron variant predominance periods.
Materials and methods
Study population and data collection
This retrospective study included consecutive, ambulatory patients who visited the post-COVID-19 Outpatient Clinic of Laiko General Hospital (Athens, Greece) for respiratory function evaluation 3 months after their hospitalization for COVID-19 pneumonia. The period of their hospitalization was between February 15, 2021 and May 15, 2022, covering all the periods of predominance of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Inclusion criteria were: i) The ability to perform pulmonary function tests (PFTs) satisfactorily; and ii) a stable clinical and physical condition (vital signs, such as their heart rate, blood pressure and body temperature, were steady and within normal limits. Also, the patients were conscious (aware) and comfortable for at least 4 weeks before evaluation. Exclusion criteria were: i) History of congestive heart failure; ii) primary lung disease such as asthma, chronic obstructive pulmonary disease (COPD), or lung fibrosis; iii) neuromuscular diseases; iv) collagen vascular diseases; and v) occupational exposure that could probably affect lung function. In addition, none of the patients had reported a lung infection 2 weeks before the evaluation.
The patients were subjected to the recording of their age, sex, medical history, smoking history, height, weight and body mass index (BMI). The patients were classified into four groups according to the levels of oxygen required during hospitalization: Group A, no oxygen requirement; group B, delivery of oxygen ≤60%; group C, need for delivery of oxygen 60-100% or high flow nasal cannula or non-invasive mechanical ventilation; group D, need for mechanical ventilation.
The retrospective design of the present study could lead to bias from missing data and this was addressed by obtaining only complete data.
The Institutional Review Board of Laiko General Hospital in Athens, Greece, approved the present study (protocol number 765/12-2021). The present study was in accordance with the Declaration of Helsinki of 1995 (as revised in Edinburgh, 2000). All subjects gave written informed consent for enrollment in the present study.
Assessment of lung function
PFTs included spirometry, body plethysmography and the measurement of DLCO. The Powercube Body+, a new generation body box (GANSHORN Medizin Electronic GmbH), was used to perform PFTs. For spirometry, maximal expiratory flow volume estimation was conducted while participants were seated and wearing nose clips. An automated spirometer connected to the body box was used for the measurement of forced expiratory volume in 1 sec (FEV1) and the measurement of forced vital capacity (FVC). Up to three trials were performed and the average of two technically acceptable tests was recorded. The predicted values were those of the European Respiratory Society (29).
DLCO is the volume of CO that diffuses across the alveolo-capillary membrane in one unit of time (1 min) with a certain pressure gradient (1 mmHg) (30). The DLCO was measured with the single breath holding technique using CH4 and CO as tracer gases. Corrections were made for the arterial hemoglobin concentration. Up to four trials were performed and the average of two technically acceptable trials was recorded. The predicted values were those of the European Respiratory Society (31).
TLC is the volume of air in the lungs upon the maximum effort of inspiration (30). The measurement of TLC was performed using the body plethysmography technique. Breathing at rest and the shutter maneuver, which uses transient occlusion to purposefully block the airflow, come first in the estimation of lung function by body plethysmography. After the opening of the shutter, an expiratory reserve volume (ERV) effort and an inspiratory vital capacity (IVC) effort were performed, allowing the computation of TLC. During measurement, the box is closed with an airtight seal, with the exception of a small, controlled used for the stabilization of the internal pressure. One pressure transducer measures the pressure inside the body box relative to ambient pressure, while another is placed close to the mouth for monitoring mouth pressure during the shutter maneuver. Up to three trials were performed and the average (mean) of two technically acceptable measurements was recorded. The predicted values were those of the European Respiratory Society (29). Abnormal values of FEV1, FVC, DLCO and TLC were considered values <80% of the predicted (29). A summary of the present study scheme is illustrated in Fig. 1.
Statistical analysis
The assessment of the normal distribution of variables was performed with the Kolmogorov-Smirnov test. The mean ± standard deviation (normally distributed) is used to present continuous variables. Categorical variables are displayed as frequencies or percentages. Comparisons of variables between groups were performed using the unpaired t-test or one-way ANOVA for continuous variables and the Chi-squared test or Fischer's exact test for categorical variables. The Bonferroni test for multiple comparisons was also used after one-way ANOVA for continuous variables. Statistical analysis was conducted using IBM SPSS-Statistics version 29.0 (IBM Corp.). P<0.05 was considered to indicate a statistically significant difference.
Results
Baseline characteristics
A total of 116 (82 male and 34 female) patients with a mean age of 57.77±11.45 years (range 19-84) were finally included in the present study. A total of 83 (71.6%) patients were hospitalized in the period of alpha variant predominance, 16 (13.8%) in the period of delta variant predominance and 17 (14.6%) in the omicron variant predominance period. Of note, the majority of the patients were unvaccinated (103 patients, 88.8%). Abnormal values of FEV1% predicted (pred) were observed in 9 (7.8%) patients, abnormal values of FVC% pred were observed in 8 (6.9%) patients, abnormal values of DLCO% pred were observed in 33 patients (28.4%) and abnormal values of TLC% pred were observed in 24 (20.7%) patients. Baseline characteristics of the present study populations are displayed in Table I.
Characteristics of the study population in relation to the variant
In the cohort of the present study, there was no statistically significant difference in age, BMI, smoking status, sex, or need for oxygen during hospitalization among the patients infected with SARS-CoV-2 in different variant periods. However, there was a statistically significant difference in vaccination status, with the largest percentage of unvaccinated patients observed during the period of alpha variant predominance (P=0.001) (Table II).
PFTs results in the different categories of variants, smoking status, vaccination status, sex and need for oxygen during hospitalization
In addition, the mean values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred were compared in the different categories of variants, smoking status, vaccination status, sex and need for oxygen during hospitalization. A statistically significant difference was observed in the mean value of DLCO% pred among the patients infected with different variants, with higher values of DLCO% pred observed in patients infected during the omicron variant predominance period (P=0.028). In addition, there was a statistically significant difference in the mean values of FVC% pred, DLCO% pred and TLC% pred among the patients with different needs for oxygen during their hospitalization, with higher values observed in patients of groups A and B (P=0.001, P=0.007 and P=0.001, respectively). Moreover, there was a statistically significant difference in the mean values of DLCO% pred and TLC% pred between vaccinated and unvaccinated patients, with greater values observed among vaccinated patients (P=0.029 and P=0.034, respectively; Table III; Fig. 2).
 | Table IIIMean values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred in the different categories of variants, smoking status, vaccination status, sex and need for oxygen during hospitalization. |
Regarding the abnormal values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred, higher rates of impaired values of FEV1% pred were observed among the active smokers compared with ex-smokers and to non-smokers (P=0.011), among older patients compared with younger ones (P=0.032) and among patients with higher needs for oxygen during hospitalization compared with those with lower needs (P=0.038). Higher rates of impaired values of FVC% pred were also observed among the patients infected during the delta variant predominance period compared with patients infected during the alpha and delta variant predominance periods (P=0.008), among older patients compared with younger ones (P=0.019) and among patients with higher needs for oxygen during hospitalization compared with those with lower needs (P=0.012). There were also higher rates of abnormal values of DLCO% pred among females compared with males (P=0.004) and among older patients compared with younger ones (P=0.006). Finally, there were higher rates of impaired values of TLC% pred among the active smokers compared with ex-smokers and to non-smokers (P=0.029) and among patients with higher needs for oxygen during hospitalization compared with those with lower needs (P=0.001; Table IV).
| Table IVAbnormal values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred in the different categories of variants, smoking status, sex, vaccination status and need for oxygen during hospitalization. |
Multivariate logistic regression analysis for abnormal values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred
According to binary logistic regression analysis, active smoking is an independent predictor of abnormal values of FEV1% pred and TLC% pred (P=0.038, OR: 8.574, CI 1.124-65.424 and P=0.004, OR: 14.733, CI 2.323-93.429, respectively), age is an independent predictor of impaired values of FVC% pred and DLCO% pred (P=0.027, OR: 1.124, CI 1.014-1.246 and P=0.011, OR: 1.054, CI 1.012-1.098, respectively) and female sex is an independent predictor of impaired values of DLCO% pred (P=0.009, OR: 1.124, CI 1.014-1.246; Table V). Fig. 3 summarizes the main findings of the present study.
| Table VMultivariate logistic regression analysis for abnormal values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred. |
Discussion
In the cohort of the present study, abnormal values of FVC% pred was observed in 8 (6.9%) patients of DLCO% pred in 33 patients (28.4%) and of TLC% pred in 24 (20.7%) patients. These findings agree with reports from the existing literature (23,32,33).
The role of age in the development of long COVID-19 syndrome has been contentious, with some researchers finding age to be a remarkable predictor of the syndrome and other studies finding decreased risk with age or no relation (34). Age has been described as an independent factor associated with impaired lung function after hospitalization due to COVID-19 pneumonia in other cohorts from the first pandemic waves (35). Age was an independent factor predicting abnormal lung function in the cohort of the present study, which consisted of patients from different periods of the pandemic.
The intricate process of lung aging arises from the cumulative alteration of lung cellular systems caused by damage and restoration. The incapacity of lung cells to maintain baseline homeostasis is a result of age-related alterations in intrinsic processes that support cell regeneration and repair, such as telomere shortening, increased oxidative stress, mitochondrial dysfunction and depletion of adult stem cell reserves. A number of anatomical and functional changes in the respiratory tract are linked to normal lung aging. Several of these changes worsen lung function, modify pulmonary remodeling, reduce regeneration and increase vulnerability to pulmonary illness. The lung has developed a variety of innate and adaptive defense mechanisms to maintain homeostasis and react to external stimuli. Oxygen free radicals and proinflammatory cytokines are produced in greater amounts during immunosenescence (36,37). Innate and adaptive immune responses in the lung have been linked to aging-related alterations in prognosis and recovery in pulmonary inflammatory disorders (38).
According to several studies, females face a greater risk of suffering from long term symptoms following SARS-CoV-2 infection (39-41). Autoimmune-related illnesses have been discovered to affect female patients much more frequently than males and autoimmunity has been proposed as a possible mechanism of long COVID-19 syndrome (42). According to some scientists, higher Toll-like receptor 7 (TLR7) expression results in higher IFN signaling in acute COVID-19 and improved viral clearance in females, but continued IFN signaling may result in excessive immune activation and persistent inflammation, predisposing females to a higher risk of autoimmunity and long-term consequences (43,44). The present study also found that female sex was an independent factor associated with impaired values of DLCO% pred, which indicate lung epithelial damage, or interstitial or pulmonary vascular abnormalities (45,46).
Overall, research indicates that females are more likely than males to have lung disorders and that their degrees of severity, rate of exacerbations, hospitalizations and death are all higher in females than in males. These include pulmonary hypertension, asthma, COPD and certain forms of lung cancer, including adenocarcinoma. Moreover, women almost always have certain uncommon and poorly known lung diseases, such as lymphangioleiomyomatosis (47).
Smoking is an established risk factor for lung function decline (48). It has also been linked to long term consequences after SARS-CoV-2 infection (38,49). In the cohort of the present study, smoking, except for the abnormal values of FEV1% pred, was associated with abnormal values of TLC which indicate a restrictive pattern of pulmonary dysfunction (50). These data suggested that expanding the promotion of tobacco cessation strategies are new priorities in this pandemic era.
The present study demonstrated some important attributes that should be presented. It is one of a handful of studies that include patients from a long period of the pandemic. Although the mean values of DLCO% pred were higher in patients infected during the period of omicron variant predominance, the percentage of patients with abnormal values of FEV1% pred, FVC% pred, DLCO% pred and TLC% pred did not differ among patients infected with the three different variants of SARS-CoV-2, suggesting that a significant proportion of patients who are hospitalized due to COVID-19 pneumonia will develop abnormal lung function regardless of the SARS-CoV-2 variant.
In addition, considering that the majority of the cohort of the present study was unvaccinated against SARS-CoV-2, the present study provided indirect evidence that vaccination against SARS-CoV-2 is not only crucial for preventing severe acute illness but also to limit post-acute sequelae of this infection. The findings of the present study indicated that it is important to build vaccine confidence in the general population and this can potentially reduce lung impairment rates after hospitalization, visits to outpatient clinics for abnormal lung function and overall health costs.
There are several limitations in the present study. First, the lack of pre-SARS-CoV-2 infection PFTs makes it difficult to tell to which extent the infection affected the lung function. Second, this is a single center study on hospitalized COVID-19 patients. Moreover, a low representation of patients with ICU admission in the cohort of the present study does not permit the generalizability of the present study findings to this specific population. In addition, the specific viral variations of patients were not identified. The prevalent variant at the time the patient was identified as having SARS-CoV2 infection served as the basis for the variant assignment.
In conclusion, the present study in a predominantly unvaccinated cohort of patients hospitalized for COVID-19 pneumonia revealed independent associations between age, female sex, smoking and abnormal lung function three months post-acute infection. These findings underscore the importance of considering these factors in the post-acute care of COVID-19 survivors. While the percentage of patients developing abnormal lung function did not vary significantly across different variant predominance periods, future research should explore these associations in more diverse cohorts. These insights contribute to our evolving understanding of the long-term consequences of COVID-19 and offer valuable considerations for clinical practice and future investigations.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The data generated in the present study are included in the figures and/or tables of this article. The raw data is available from the corresponding author upon reasonable request.
Authors' contributions
NVS and VEG conceptualized the present study. VEG, AG, SM, DAS, MNG, EA, PP, IGL, SP and NVS made a substantial contribution to data interpretation and analysis and wrote and prepared the draft of the manuscript. VEG and NVS analyzed the data and provided critical revisions. VEG and NVS confirm the authenticity of all the data. All authors contributed to manuscript revision and approved the final version of the manuscript.
Ethics approval and consent to participate
The present study was conducted in line with the Declaration of Helsinki and gained approval by the Institutional Review Board of Laiko General Hospital (approval no. 765/12-2021). Written informed consent was obtained from the patients for participation and publication of the data.
Patient consent for publication
Not applicable.
Competing interests
DAS is the Editor-in-Chief for the journal, but had no personal involvement in the reviewing process, or any influence in terms of adjudicating on the final decision, for this article. The other authors declare that they have no competing interests.
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