The present study shows that NPI measures implemented during the COVID-19 pandemic contribute to the containment of the SARS-CoV-2 virus and considerably influence the occurrence of other infections. Furthermore, the changes in demand for healthcare services and implement prevention and control measures led to a significant change in transmission dynamics.
The analysis of the laboratory detections of Marburg University Hospital shows that due to the implementation of the NPI measures, gastroenterological and respiratory viral infections were drastically reduced. The number of norovirus infections dropped dramatically, which became statistically significant after the pandemic emerged (P = 0.028). The same applies to rotavirus (up to 89%) and adenovirus enteritis, showing significantly lower detection rates. Seasonal clusters, which usually occur with norovirus and rotavirus infections, completely failed to appear after implementing social intervention. Similar data were reported by Grochowska et al., who focused on changes in the occurrence of transmissible viral infections in children [10]. Their microbiological analysis (until April 2021) documented 87% fewer rotavirus infections and 47% norovirus infections during the pandemic. The drastic drop in the detection rates of gastroenteritis viruses at the Marburg University Medical Center was significantly correlated with the decline in mobility in the county (P < 0.05) caused by social and travel restrictions, working at home, and the extensive limitations of public events. The abrupt interruption of common chains of infections may be caused by limiting private and public contact. Especially in the winter months, during which norovirus and rotavirus predominantly circulate, social contacts between more than 10 people rarely occur. The contact monitor at the Humboldt University Berlin clearly shows this. Based on the assumption that transmissions occur if people have social contacts, a group of researchers analyzed the GPS data of mobile phones in Germany after the social restriction was implemented; thus, it displayed the course of the pandemic with regard to social contacts [11]. During the first lockdown (beginning March 22, 2020), a massive drop in social contacts of approximately 50% was observed compared with the pre-pandemic level (19 compared with 9 contacts per person per day). Furthermore, the discontinuation of mass catering at restaurants or cultural events plays a significant role in reducing the risk of transmission by contaminated food. The temporary closing of schools and nurseries also led to the absence of one of the predominant locations of transmission of gastroenteritis in children. The enhanced awareness of the population regarding hand hygiene measures may also represent an important reason for the significant reduction in viral gastroenteritis.
Additionally, a significant decline was observed in respiratory viral infections. There was no increase in influenza cases in the winter of 2020/2021. The usual pre-pandemic seasonal occurrence of RSV detection in the first quarter of 2021 (-98% compared with Q1 2020) did not occur. These changes in detection rates were also significantly correlated (P < 0.05) with the changes in mobility. Apart from the aforementioned causes, the general mask mandate, social distancing, and proactive self-isolation in the case of respiratory symptoms due to social expectancy were mainly responsible for the changing dynamics of transmission and the nonoccurrence of detections. During the influenza A (H1N1) pandemic in 2009, national and international public health authorities recommended wearing masks to reduce the risk of transmission. However, owing to the insufficient availability of data, no actual evidence regarding the protective effect of this barrier precaution can be delivered [12]. Nevertheless, the latest studies conducted during the COVID-19 pandemic showed that surgical masks could reduce the transmission of human coronaviruses and influenza viruses by people with symptoms [13]. A meta-analysis by Liang et al., which included 21 studies, confirmed the significant protective effect of masks against influenza virus (odds ratio [OR] = 0.55), SARS (OR = 0.6), and SARS-CoV-2 (OR = 0.04) [14]. Thus, wearing a mask during the SARS-CoV-2 pandemic seems to be one of the main reasons for the detection rates of influenza and RSV.
The implementation of social distancing contributes to the massive reduction in respiratory viral infections. In a meta-analysis including 172 observational studies, Chu et al. stated that the risk of transmission of SARS-CoV-2 viruses could be significantly reduced by a physical distance of 1 m or more (n = 10 736, pooled adjusted OR [aOR] 0.18, 95% CI 0.09 to 0.38) [15]. The level of protection increased with increasing distance (change in relative risk [RR] 2.02 per m; P = 0.041). Infections caused by C. difficile were reduced by up to 44% (Q1 2021) during the pandemic. This was confirmed by Bentivegna et al., who observed a significant decline in C. difficile cases after the outbreak of the COVID-19 pandemic. Their analysis covered the period from March to June 2020; however, they excluded intensive care units and children’s medical units [16]. The reduction in detection at the Marburg University Hospital was significantly correlated with the change in nationwide mobility. The reason for this seems to be particularly the reduced demand for outpatient services, which caused a reduction in antibiotic prescriptions; thus, led to a reduction in CDI rates. A change in risk factors for the development of an antibiotic therapy-related CDI in the hospital is unlikely due to the unchanged application of antibiotics and the efforts of antibiotic stewardship and suggests changes in outpatient medical and public areas. However, a reduction in C. difficile cases due to intensified hygiene measures in hospitals and other medical centers, as suggested by Sipos et al. [17] and Bentivegna et al. [16], seems unlikely from our perspective. For example, intensified hygiene measures indicated increased cleaning and disinfection intervals and use of personal protective equipment, pose a relevant factor only if the level of standard hygiene was low before the pandemic. Regional and national differences with respect to hygiene requirements in hospitals and their implementation are reasons for the diminished comparability of the initial situation. An increase in already established standard hygiene measures could not be observed at the Marburg University Hospital, except for the use of hand disinfectants, which, according to other studies, does not correlate with the incidence of CDI [18].
At the Marburg University Hospital, enhanced infection prevention and control (IPC) did not lead to reduced detection of antibiotic-resistant bacteria, as has been suggested by various research groups. No changes were observed with respect to the MRSA, MDR, and XDR rates. Wee et al. observed a reduction in MRSA acquisitions from 11.7 cases per 10,000 hospitalization days to 6.4 cases (P < 0.05). However, with respect to the acquisition of carbapenem-resistant Enterobacteriaceae (CRE), no noteworthy changes could be discovered during the observation period. Baccolini et al. observed an increase in the incidence of patients with healthcare-associated infections (HAIs), especially device related HAIs, which may be attributed to a collateral damage to long-established infection control measures by focusing resources to primarily mitigate the spread of SARS-CoV-2 [19].
The decline in MRSA detection rates during the pandemic discovered by several studies can be evaluated as a result of intensified hygiene measures [20, 21]. Similar effects were not observed at the Marburg University Hospital despite the significantly increased use of disinfectants. A possible reason for this could be the point in time or indication for hand disinfection, for which increased consumption was recorded during the pandemic. According to the observation of hand disinfection by Israel et al., personal protection and patient protection moments must be differentiated [22]. Thus, after contact with the patient, disinfection measures serve to protect the patient. Therefore, it can be assumed that increased use of disinfectants first helped protect the staff and did not influence the detection rates of the patients.
Furthermore, it seems clear that the pre-pandemic level of measures for infection prevention is the predominant factor for effect displayed on MDR and XDR rates due to intensified IPC measures during the COVID-19 pandemic. High-income countries already have high standards of antibiotic stewardship and infection prevention; thus, the enhancements of resistance situations and detection rates are perceived as smaller. The same applies to the effect of intensification of hygiene measures, such as hand disinfection. At the Marburg University Hospital, compliance with hand disinfection and basic hygiene standards had already been high. Therefore, the application of antibiotics and the efforts of antibiotic stewardship did not change during the pandemic. This seems to be one possible explanation for the consistent MDR rates. However, one limiting factor of our study is that it was conducted with a single healthcare provider; hence, the findings may not be fully generalizable to other settings.