The Effect of Mask Use on Seasonal Virus Diversity in SARS CoV-2 Negative Patients Treated as Inpatients During the 2021–2022 and 2022–2023 Seasonal Flu Period

Influenza and non-influenza respiratory tract viruses are a significant cause of mortality and morbidity, leading to epidemics during the flu season worldwide, especially in patients with underlying chronic diseases (Chow et al. 2023). COVID-19 was announced to be a pandemic on March 11, 2020, by the World Health Organization. After the start of the COVID-19 pandemic, non-pharmacological measures such as quarantine, travel restrictions, social distancing, schools, closure of workplaces, wearing masks, and use of surface disinfectants and hand hygiene implemented by most countries have also disrupted the circulation of other common respiratory tract viruses (Dhanasekaran et al. 2022). The measures implemented by countries in response to the COVID-19 pandemic caused a decrease in the seasonal viral agents and their diversity, resulting in a decline in flu epidemics as well (Huang et al. 2020; Lei et al. 2020; Feng et at. 2021; Achangwa et al. 2022). Following the easing of these measures or lifting restrictions towards the end of the COVID-19 pandemic, seasonal flu cases have been observed (Hodjat et al. 2021).

Epidemiological studies have shown that respiratory virus outbreaks have a seasonal distribution. Influenza, human coronavirus, and respiratory syncytial virus (RSV) increase significantly in the winter months; they are also called winter viruses. Human bocavirus, human metapneumovirus, and rhinovirus are monitored throughout the year. The detection frequency and number of cases of enterovirus infections increase in the summer months. They increase in spring and autumn, depending on the type of parainfluenza virus. Although rhinovirus infection occurs all year round, severe infections occur in the winter months (Moriyama et al. 2020).

There is compelling evidence that the use of masks can effectively prevent respiratory virus outbreaks. Studies have consistently shown that masks provide protection for droplet sizes in the range of 2–3 μm, regardless of the droplet amount and exposure time (Djeghdir et al).

Currently, two types of masks are in use: the surgical face mask and the high barrier N95, FFP2 or FFP3 mask. While surgical face masks with standard protection are suitable for general use, masks with high protection are recommended for healthcare workers involved in patient treatment (Azap et al. 2020).

The main objective of this study was to assess the effect of mask use on the diversity and transmission of seasonal flu viruses. To achieve this, we compared the seasonal flu agents of SARS-CoV-2 negative patients during 2021–2022, when all restrictions were eased except for the mask mandate, and 2022–2023, when the mask mandate was also lifted.

The data of 1,335 patients, 483 female and 852 male, who were hospitalized at our pulmonary disease clinic between October 2021 and May 2023 with the diagnoses of asthma attack, COPD exacerbation, and pneumonia were examined retrospectively. The patients’ mean age was found to be 66.4 ± 13.6 years (females: 67 ± 15.3, males: 66.1 ± 12.6). The most frequent comorbidities were hypertension (59%), COPD (53.2%), and ischemic heart disease (35%). The demographic features of the patients are exhibited in Table I.

When the viral agents were examined according to the hospitalization diagnoses of the patients, in the patients with COPD exacerbation, influenza A with 11.2% (H1N1: 9.5%, H3N2: 8.1%) was found to be the most frequent viral agent, followed by enterovirus/rhi-novirus with 5.3%, and human coronavirus with 4%. For those hospitalized with pneumonia, influenza A was detected at a rate of 10.8% (H1N1: 9%, H3N2: 5.7%), followed by enterovirus/rhinovirus with 6%, and human coronavirus with 3.9%. For asthma attack patients, influenza A was 12.2% (H1N1: 9.8%, H3N2: 8.6%), enterovirus/rhinovirus was 7.5%, and human coronavirus was 5.5% (Table II).

The comparison of the viral agents between the first period with mandatory mask use and the second period when the mask mandate was lifted revealed that the viral agents detected in the second period (41.6%) increased significantly compared to the first period (23.4%) (p < 0.001). During the period after the mask mandate was lifted, a significant increase was detected in influenza A, H1N1, and RSV/AB (p = 0.019, p = 0.003, p < 0.001), whereas coronavirus HKU1, coronavirus 229E, human metapneumovirus, and parainfluenzavirus 2 and 4 decreased. Parechovirus and the bacteria – Mycoplasma spp. were not detected in both periods (Table III, Fig. 1).

Fig. 1.

Viral panel PCR results in the first and second periods.

In the seasonal comparison of the viral agents detected in the first and second periods, it was seen that during the first period, there was a marked increase in H1N1 and RSV/AB during the winter and in Influenza A and B during the spring. In the second period, when mandatory mask use was lifted, there was a marked decrease in parainfluenzavirus 1–4, human metapneumovirus during winter, and enterovirus/rhinovirus during spring. Co-infection was found in six patients in the first and 15 patients in the second periods (p > 0.05).

Recent literature has shown that restrictions such as travel bans, curfews, closure of schools, bars, restaurants, and cafes, prohibition of public transportation, and mandatory mask-wearing, which are called non-pharmacological measures taken by countries due to the pandemic, mitigate the spread and transmission of COVID-19. Furthermore, it has been reported that these non-pharmacological measures reduce the burden of virus exposure (Doshi 2020). Among the studies evaluating respiratory tract viruses before and during the pandemic period, those conducted by Olsen et al. (2020), Lei et al. (2020), and Feng et al. (2021) indicated that non-pharmacological measures reduced influenza activity during the pandemic by 98%, 64%, and 79.2%, respectively. Sullivan et al. (2020) observed a significant decrease in hospitalizations and deaths related to influenza and RSV, along with increased rhinovirus cases. Similarly, Redlberger-Fritz et al. (2021) reported a marked decrease in influenza, RSV, human metapneumovirus, and rhinoviruses during the quarantine period; however, rhinovirus cases significantly increased after quarantine measures were lifted. Park et al. (2021) has found influenza, rhinovirus/enterovirus or parainfluenza virus test positivity to be 35% before and 7.2% during the pandemic period. Huang et al. (2020) detected that during the pandemic period, the circulation of the influenza virus decreased by 99.9%, RSV by 98%, human metapneumovirus by 92.2%, enterovirus by 82.2%, adenovirus by 81.4%, parainfluenza virus types 1–3 by 80.1% and rhinovirus by 74.6%, and rhinovirus levels (33%) increased first once the quarantine restrictions were eased. According to the study by Doroshenko et al. (2021), implementing pandemic measures resulted in significant reductions in the positivity rates of various respiratory viruses. The positivity rates of influenza A/B, RSV, seasonal coronaviruses (HKU1, 229E, OC43, NL63), human metapneumovirus, enterovirus/rhinovirus, and parainfluenza viruses (1–4) decreased from 17.98% to 0.98%, 6.99% to 0.56%, 3.79% to 1.21%, 4.2% to 1.07%, 15.81% to 3.98%, and 4.4% to 0.31%, respectively (Doroshenko et al 2021). In a study comparing the period of complete lockdown with the period of eased lockdown measures in terms of viral agents, Hodjad et al. (2021) reported a decrease in all viral agents during the complete lockdown period. They also noted that the agents that first returned to pre-pandemic levels with gradual relaxation of measures were rhinovirus/enterovirus. There are reports in the literature indicating that the lifting of COVID-19 measures, including the mask mandate, led to the return of various respiratory viruses such as influenza, seasonal coronaviruses, RSV A/B, and parainfluenza virus to pre-pandemic levels (Hodjad et al. 2021). In relation to that, Marriot et al. (2021) found a significant decrease in test positivity for both COVID-19 and other respiratory viruses 11 weeks after the initiation of the lockdown period. In our study, a similar trend was observed in which seasonal influenza (influenza A and H1N1) and RSV A/B increased after the mask mandate was lifted. This suggested that wearing a mask is protective against the transmission of influenza and RSV A/B.

On the other hand, unlike other relevant studies, even though we found rhinovirus/enterovirus to be high in both periods, the difference between the periods was not significant. Thus, we considered that non-enveloped viruses are more resistant or that the effectiveness of masks in preventing the transmission of non-enveloped viruses may be lower. Besides, in our study, different from others, we also detected a decrease in coronavirus HKU1, coronavirus 229E, human metapneumovirus, and parainfluenzavirus 2 and 4. Although the exact reason for this different result cannot be fully explained, it could be attributed to the fact that the study excluded asymptomatic patients. Moreover, differing from other similar studies, we also investigated the co-infection status of the viruses. We determined that despite not being statistically significant, there was a proportional increase in co-infection diversity after mask mandates were lifted. This finding suggested that masks can affect virus diversity.

Our study had certain limitations due to its retrospective nature and the inability to monitor individual behaviors despite the mask-wearing mandate continuously. Additionally, the study only included symptomatic patients who were hospitalized. Consequently, the results of asymptomatic individuals in the community were not included. Additionally, although travel restrictions have been lifted in 2021, this is only valid for some countries. For this reason, the decrease in our results in 2021 may be due to the decrease in the entry of viruses into the country and the obligation to use masks. We may have ignored the increase in our results by attributing the )increase to the removal of the obligation to use masks without considering the increase in RSV and influenza in the world in 2022.

In conclusion, the results of our study are of significant importance, as they demonstrate the protective effect of mask use against the transmission of respiratory tract viruses during the pandemic. We believe that mask use can be beneficial, especially during influenza and RSV epidemics.