In this retrospective study, we assessed the epidemiological characteristics of common respiratory pathogens in children with community-acquired pneumonia before and during the local COVID19 pandemic. Our study showed an important influence of the COVID19 epidemic on the spread of common respiratory pathogens in Shanghai, China. Through a series of strict NPIs such as wearing masks, closing schools and maintaining social distance, not only the diffusion of SARS-CoV2 had been reduced, but also the epidemic pattern of other common pathogens [8], especially respiratory virus and Mycoplasma pneumoniae.
Compared with 2019, the number of hospitalized children with pneumonia in our department diminished by 61.25% in 2020. And the total detection rate of respiratory pathogens also fell off significantly (from 77.55–56.00%), whether single or mixed infection. In one research conducted in New Zealand, incidence rate of severe acute respiratory illness among hospitalized patients showed very low owing to the use of strict NPIs such as the blockade and border closures in 2020 [9]. However, our findings showed that the prevalence of pneumonia in children with congenital heart disease and the proportion of children with severe pneumonia requiring oxygen inhalation increased compared with 2019, and bacterial or RSV infection was the main cause. In terms of age, the proportion of infants had increased, probably because it was difficult for children under the age of 3 to wear masks. Perhaps, NPIs could not reduce the incidence of infants, children with underlying diseases and severe pneumonia.
Compared with 2019, the whole detection rate of viruses decreased in 2020, but the rate of RSV increased (8.93% vs. 9.38%), especially the winter peak of RSV reappeared as usual. RSV disease occurs in all age groups, but the incidence is higher under 2 years of age [10]. RSV infection has been supported to be in association with asthma and acute lower respiratory tract infection, leading mortality and morbidity to increase in children [11–13]. In this study, RSV was still the most common source of respiratory viral infection in infants (age: < 3 years), children with congenital heart disease, and severe pneumonia. Therefore, further research is needed on preventive measures for RSV. There was a small pinnacle in the positive detection rate of HPIV in the spring and summer of 2019, but it did not appear in the same period in 2020. Instead, the number of HPIV tests increased dramatically after September. Human behavior is one of the main factors influencing the seasonality infections of respiratory viruses. As a matter of fact, in the context of the easing of the domestic COVID-19 in China, people in low-risk areas have basically resumed their normal work and life, which might be the reason for the surge in RSV and HPIV infections from September to December 2020 [14]. These results showed outbreaks may take place outside of the typical season during the COVID19 pandemic. As NPIs are relaxed, it is necessary for healthcare systems to prepare for future outbreaks of ordinary respiratory viruses in children. Many studies have shown that influenza has spread in a similar way to COVID-19, such as droplet and contract transmission [15, 16]. Therefore, non-pharmaceutical interventions in linkage to reducing the spread of COVID-19 may also significantly reduce influenza [17, 18]. Despite returning to school, resumption of work and seasonal epidemics, the detection rate of 2020 influenza remained low. First, the Shanghai government increased the scope of influenza vaccination, especially for young children aged 3–6 in kindergartens in September 2020. Next, the COVID19 pandemic has changed health-seeking behavior and increased the focus on non-pharmacological interventions to decrease the risk of infection with the spread of influenza [19]. Meanwhile, many viral-viral interactions may also affect the incidence of respiratory viral infections. Interferon-stimulated immunity caused by infection with one virus can provide nonspecific interference that makes it difficult for other viruses to establish in a population [20]. Increased circulating levels of influenza A virus have been shown to limit rhinovirus epidemics, possibly through an interferon-mediated mechanism [21]. Interestingly, despite the adoption of NPIs in 2020, the detection rate of HRV increased significantly, a trend not seen with other viruses after the restarting of schools in June. A former study showed that surgical masks could keep human coronaviruses and influenza viruses from transmitting, but not rhinoviruses transmission by respiratory droplets and aerosols in symptomatic patients with acute respiratory disease [22]. In addition, rhinoviruses are non-enveloped viruses, so might be inherently less inactivated by washing hand with soap and water or by ethanol-containing disinfectant [23, 24]. Furthermore, the quality of children's hand washing may be poor. These factors may explain the reason that rhinovirus infection remained its usual circulation level.
In terms of bacteria, the most common ones in 2019 were Streptococcus pneumoniae and Haemophilus influenzae, which were common bacteria in children with community-acquired pneumonia. Notably, Global Action Plan For Prevention and Control of Pnuemonia by the World Health Organization in 2008 listed immunization coverage for Haemophilus influenzae and Streptococcus pneumoniae, and immunization against pertussis and measles as primary prevention strategies. Given that vaccines covering for either were not routinely used in China, it was not surprising that the rates of pneumococcal and Haemophilus influenzae B infection in children were relatively high. However, by June 2020, the detection rate of bacteria increased, dominated by Staphylococcus aureus and Escherichia coli. The reason was that in the late stage of the epidemic, congenital heart disease complicated with pneumonia increased in children hospitalized in the respiratory department, whose sputum cultures were mainly Staphylococcus aureus, Escherichia coli and Klebsiella pneumoniae, considering with large-scale use of antibiotics, pathogenic bacteria variation, regional differences, pathogenic bacteria changes and other factors. Moreover, children with congenital heart disease are more likely to be infected with Staphylococcus aureus in infancy or winter than ordinary children, which may be related to factors such as their own hemodynamic characteristics and low immunity.
MP is the one of the most popular pathogen of community-acquired pneumonia, which especially occurs in school-aged children. It can cause obvious disturbance of immune function in children. And if treatment is not timely, it will cause breathing difficulties, heart failure, etc., and even death in severe cases [25]. Mycoplasma pneumoniae pneumonia occurs in regional outbreaks every 3 to 7 years, and each may endure 1 to 1.5 years. The last two epidemics of MP were in 2013 and 2016 [25, 26]. When encountering epidemic years, the infection rate of MP would increase by 3 to 4 times in children and adolescents. Our study showed that the detection rate of Mycoplasma pneumoniae was close to 50% in 2019, based on a combination of molecular assays and serology, which was considered an outbreak of MP infection. This might also be the reason why the positive rate of school-aged children in 2019 was markedly higher than that of the other two groups of age groups. Climatic conditions, such as humidity and temperature, have been reported to affect the survival and spread of airborne M. pneumoniae significantly [27, 28]. 37°C is the optimum growth temperature for MP, which grows best in the hottest months in China such as July, August and September. But in 2020 fewer patients visited clinicians following the outbreak of the COVID-19 pandemic and restrictive means against COVID-19 cut down the incidence of respiratory infections, there was a considerable reduction in the positive rate of MP since March, which remained at a comparatively low level afterwards, consistent with previous findings in other studies [29–31]. At the start of the new term, the "Guidelines for the Prevention and Control of the Novel Coronavirus Pneumonia in Primary and Secondary Schools" was issued by the Ministry of Education to give a guide and assistant on the prevention and control of the epidemic in schools. These restrictive measures on COVID-19 could effectively reduce the transmission of Mycoplasma pneumonia, which led to a rapid decline in the positive rate of school-aged children in 2020 as well. And it might be that older children were better able to comply with various defensive measures.
This paper not only compared the epidemiological features of common respiratory viruses in children, but also bacteria and Mycoplasma pneumoniae during the COVID-19 pandemic in China. However, there are some limitations in it. First, this study was conducted in a single center and all of the patients were hospitalized, which might lead to a preselection bias. Second, the methods used to detect respiratory pathogens such as viruses and bacteria were relatively simple, which might lead to false negative. Third, during the pandemic, a lot of public health interventions were enforced and some measures (such as wearing masks) still exist later. Consequently, the sample size should be further expanded to study which of these measures may be the most forceful prevention on the spread of respiratory pathogens.