Selective change in the bacterial flora in respiratory sputum from elderly patients during the SARS-CoV-2 pandemic

doi:10.21203/rs.3.rs-2106304/v1

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Selective change in the bacterial flora in respiratory sputum from elderly patients during the SARS-CoV-2 pandemic

https://doi.org/10.21203/rs.3.rs-2106304/v1

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The pandemic of SARS-CoV-2 has affected the social lifestyle and consequently the prevalence of infections, such as seasonal influenza. It has been reported that invasive pneumococcal infection is markedly decreased worldwide.

We retrospectively investigated the bacterial flora of 23,052 respiratory sputum samples obtained at our hospital from April 2015 to March 2022. The average patient age was 71.8 years old with a standard deviation of 16.0 years old. There was no significant difference in the age of the patients or the female-to-male ratio between each year. The detection ratio of bacteria was analyzed in accordance with sputum quality based on the Geckler classification.

The detection ratio of community-acquired pneumonia pathogens such as Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae increased in parallel with the quality of the sputum, while that of hospital-acquired pneumonia pathogens such as Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus was not significantly affected by the quality of the sputum. The former detection ratio decreased significantly since April 2020 by 60–80% for two years in a row, while that of the latter did not change between each year.

The pandemic of SARS-CoV-2 reduced the detection ratio of community-acquired pathogens such as Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae but not hospital-acquired pneumonia pathogens such as Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus in the respiratory sputum from elderly patients.

Infectious Diseases

SARS-CoV-2 pandemic

Haemophilus influenzae

Streptococcus pneumoniae

community acquired pneumonia

hospital acquired pneumonia

respiratory sputum

Geckler classification

It is well known that the pandemic of the new coronavirus, systemic acute respiratory syndrome coronavirus 2 (SARS-CoV-2), is not only a global health problem but also has a great impact on the global economy and changes in people's social behavior[1, 2]. It is also known that infectious diseases are closely related to people's social activities. It has already been reported that the pandemic of SARS-CoV-2 has markedly reduced the worldwide seasonal influenza prevalence[3–6] and invasive pneumococcal infections[7–10]. Against this background, we investigated the effects of the SARS-CoV-2 pandemic on the respiratory bacterial flora from elderly patients by analyzing the respiratory sputum samples obtained at our hospital in accordance with the quality of the sputum based on the Geckler classification between April 2015 and March 2022.

Respiratory sputum samples obtained from patients to evaluate respiratory infection at our hospital between April 2015 and March 2022 were investigated. Each sample quality was graded based on the Geckler classification, and the detection ratio of each bacterium in the graded samples was calculated and compared. Basically, analysis was performed by using the first detected bacterium. However, the same analysis was performed as well by using the sum of the first, second, and third detected bacteria. Statistical analysis was performed by Student’s t-test and the chi-square test.

This study was approved by our institutional review board as No 3028.

The total sample number analyzed was 23,052. The sample number and the patient age are presented in Table 1, and there was no significant difference in the patient age or female-to-male ratio between each year. The average age of the patients was 71.8 years old with a standard deviation of 16.0 years old. The age distribution of the patients from whom the respiratory sputum sample was obtained is presented in Table 2. More than 90% of the patients were 50 years old or older. Figure 1 shows the distribution of Geckler classification in the samples by each year. The ratio of Geckler1 and 2 has increased since April 2020, which is considered partly due to the SARS-CoV-2 pandemic because the splash producing procedure, which is necessary to obtain good quality sputum, was restricted to some extent to prevent the accidental spread of SARS-CoV-2. Figure 2 presents the detection ratio of each bacterium according to the Geckler classification. The detection ratio of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae increased in parallel with the quality of the sputum, while that of Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus was not significantly affected by the quality of the sputum. Data not shown, this trend was consistently and equally found between each year. The detection ratio of each bacterium in the samples classified as Geckler5 in each year is presented in Fig. 3. Notably, the detection ratio of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae significantly decreased by 60–80% (p < 0.001) since April 2020 for two years in a row. However, the abundances of Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus did not change significantly. Data not shown, the results are the same when the detection ratio of the sum of the first, second, and third detected bacteria was analyzed.

Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae are the most frequently detected pathogens of bacterial pneumonia in children[11–13]. These bacteria are transmitted and spread between persons and induce respiratory infection. Additionally, in elderly people, these pathogens comprise an important part of community-acquired pneumonia[14–16]. In contrast, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus are the main causative pathogens of hospital-acquired pneumonia, such as aspiration pneumonia[17].

In this study, it was clearly shown that the detection ratio of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae increased in parallel with the quality of the sputum, while the detection ratio of Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus was not significantly affected by the quality of the sputum. This finding indicates that these bacteria are detected in sputum from elderly patients irrespective of pneumonia. In light of these observations, it is quite interesting that the detection ratio of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae has been reduced significantly during the SARS-CoV-2 pandemic since April 2020 for two consecutive years. Since the onset of the SARS-CoV-2 pandemic, social activities and the flow of people have been restricted and reduced, and public hygiene procedures such as universal masking and hand washing are encouraged. It has been reported that invasive infection with Haemophilus influenzae, Streptococcus pneumoniae, and Neisseria meningitidis has been reduced since the onset of the SARS-CoV-2 pandemic. In this context, it is concluded that the transmission of Haemophilus influenzae, Moraxella catarrhalis, and Streptococcus pneumoniae among elderly people is reduced during the SARS-CoV-2 pandemic. Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus are considered mainly endogenous pathogens; therefore, the detection ratio of these bacteria did not change during the SARS-CoV-2 pandemic. It is not the case that the detection ratio of Pseudomonas aeruginosa is partly affected by the quality of the sputum, indicating transmission between the patients and possibly the health care workers in part, and the detection ratio of Pseudomonas aeruginosa is not affected by the SARS-CoV-2 pandemic.

As previously mentioned, Haemophilus influenzae and Streptococcus pneumoniae are the major pathogens of respiratory infection during childhood, and it has been reported that they comprise more than 80% of bacterial community-acquired pneumonia in patients under 15 years old and more than 95% in patients under two years old[11, 12], which is a much higher ratio than that in the elderly patients observed in this study. As shown in Table 2, the sample number from the children (0–14 years old) comprised as few as 0.4% of the total sample number in this study. Data not shown, Haemophilus influenzae and Streptococcus pneumoniae were detected only in seven and eleven Geckler5-graded sputum samples from the children, respectively. This shows that our results almost reflected the bacterial flora of the respiratory sputum from elderly patients. We have recently reported that respiratory viruses are transmitted between children and adults reciprocally in the community from epidemiological observations[18]. Although we could not have enough bacterial flora data of the respiratory sputum from the children, it is feasible to speculate that Haemophilus influenzae and Streptococcus pneumoniae infection in the children is also reduced during the SARS-CoV-2 pandemic, which also leads to the reduction of the detection ratio of Haemophilus influenzae and Streptococcus pneumoniae in the respiratory sputum from the elderly patients in the reciprocal manner. In accordance with this, it has been reported that invasive pneumococcal infection is markedly reduced in children as well as in elderly people worldwide.

The limitation of this study is that we could not validate the time of sputum sampling or the clinical background of the patients, including the comorbidities and antibiotic treatment.

Our observation presents the different transmission characteristics of respiratory pathogenic bacteria among elderly patients and the impact of the SARS-CoV-2 pandemic on the bacterial flora of the respiratory sputum in elderly patients. This also indicates the usefulness and limitation of infection control procedures performed during the SARS-CoV-2 pandemic.

Data availability statement

Data available on request from the authors.

Funding statement

The authors have no funding received in relation to this work.

Conflict of interest disclosure

The authors have no conflicts of interest to declare.

Ethics approval statement

This study was approved by the institutional review board of Musashino Red Cross Hospital as research No 3028.

Patient consent statement

Informed consent was secured by the opt-out method.

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Table 1: The annual respiratory sputum sample number between April 2015 and March 2022

Table 2: Respiratory sputum sample number by age

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Selective change in the bacterial flora in respiratory sputum from elderly patients during the SARS-CoV-2 pandemic

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