According to COVID-19 risk level, 8/180 (4.4%) samples were positive from super markets located in areas at the orange level and 5/120 (4.2%) samples from those located in red-level zones. No significant difference was observed between swab positivity among supermarkets in areas at different risk levels (p = 1.00).

4. Discussion

It is scientifically proven that surfaces contaminated with viruses and bacteria can act as a medium for the transfer of microorganisms to the hands, and subsequently, to the gastrointestinal or respiratory tract [19]. With respect to SARS-CoV-2, it has been widely demonstrated that infection with this virus mainly occurs via the respiratory tract [2,3]. However, contact of mucous membraneswithacontaminatedsurface and/orwithdroplets can also lead to infection with SARS-CoV-2 [12]. There are many opportunities for envi ronmental contamination (air and surfaces) with SARS-CoV-2 in hospital settings where COVID-19 patients may be present [4,7,8]. On the contrary, evidence regarding environ mental spread of SARS-CoV-2 in the community is lacking. Pitol et al. [20], evaluated that he risks of community transmission of SARS-CoV-2 through surfaces are low and that the effectiveness of surface disinfection is highly dependent on the infection prevalence and the frequency of contacts. Although it is estimated that the transmission of SARS-CoV-2 via fomites is low, it is possible and can favor the onset of new cases during outbreaks. In our study, we examined different surfaces in supermarkets during periods of limited mobility owing to COVID-19 restrictions. We found the presence of SARS-CoV-2 RNAcontamination in 4.3% of the swab samples analyzed. These results are consistent with other papers in which less than 10% of the swabs were contaminated by SARS-CoV-2 [10]. No significant difference between supermarkets in areas at the two highest (red and orange) risk levels were found. A potential hypothesis to explain this result can be due to the lack of period between the contamination of SARS CoV-2 on surfaces and the real onset of infection or disease. It is important to emphasize that entering supermarkets at these risk levels involved the obligatory use of masks and disinfection/sanitization practices. However, we found that freezer handles and trolley handles were frequently positive in testing for SARS-CoV-2 RNAcontamination. Thehighestcontaminationofthesesurfaces is probably related to the occurrence of use. In fact, they were frequently touched by customers and were all non-porous surfaces with the same ability to retain contamination of SARS-CoV-2. Regarding the shopping trolleys, weobserved a significant contamination of the trolley handles. This result can be correlated with the availability of dispensers for hand sanitation. In our study, in all supermarkets, the hand hygiene dispenser was positioned near the push trolley deposit at the entrance to the supermarket, and the other shopping trolleys were in areas diametrically opposite to the disinfectant dispenser. We can assume that although it was strongly recommended to sanitize hands, not all customers disinfected their hands at the entrance, but rather they immediately went to take the shopping trolleys. Therefore, customers using the push shopping trolleys were more likely to disinfect their hands before using the shopping trolleys because the dispenser was near. These data lead us to underline the importance of more careful sanitization on these surfaces during the cleaning and disinfection procedures. This is essential hand hygiene, so it is necessary to increase the number of sanitation systems in community environments, in particular in proximity to surfaces that are the most frequently touched. Scientific evidence has shown that the presence of SARS-CoV-2 RNA on a surface does not mean that the surface itself is infectious. We found Ct values between 36.88 and 38.63 in our positive samples, i.e., tending toward high values; however, some studies have shown that high values are indicative of partial RNA degradation or low viral load [21,22]. Consequently, we can hypothesize that, despite compliance with precautionary measures, SARS-CoV-2 RNA can circulate in enclosed environments frequented by healthy, perhaps asymptomatic, individuals. These observations do not mean that the surfaces contaminated bySARS-CoV-2RNArepresentahighdangeroftransmission of the virus, in fact the results of our study cannot irrefutably support these theories but can only show the presence of SARS-CoV-2 genetic material, not how much this can be correlated to the danger of infection. The virus can survive on surfaces made of various materials and its degree of infectiv ity can vary from hours to days, depending on the environmental conditions; environments with high temperatures and high humidity can inactivate the virus more quickly [23,24]. SARS-CoV-2 has been shown to survive for up to 4 h on copper surfaces, for up to 24 h on cardboard, and for up to 2–3 days on plastic and stainless steel [11,25]. In China, COVID-19 clusters have been repeatedly linked to imported frozen raw foods. SARS-CoV-2 RNA has been detected on food packaging materials (frozen shrimp packaging), food storage environments (shipping containers), and even some foods (frozen chicken wings) [3]. In this study, we did not analyze the type of material at each sampling point. We were more interested in verifying whether this virus could be found in environments that are frequented by the public during periods of restricted mobility in the COVID-19 pandemic. Int. J. Environ. Res. Public Health 2021, 18, 9404 7 of 9 In terms of both significant and non-significant data, our findings suggest interesting con clusions. We further confirmed that surfaces of public environments can be contaminated by SARS-CoV-2 RNAandwehypothesize that they could be a potential virus transmission vehicle. It is notable that more frequently positive surfaces were those hypothesized to be most often touched by hands. Thus, we highlight the need to pay particular attention to hand and environmental hygiene. Detection of SARS-CoV-2 on surfaces believed to be touched frequently and by many people in a community indicates that increased sanitization and hand hygiene in public spaces, such as grocery stores, may be useful in decreasing SARS-CoV-2 transmission via fomites. During periods with high circulation of SARS-CoV-2 RNA, it is necessary to intensify cleaning management programs, such as by installing disinfectant solution dispensers near high-contact surfaces used by the public [26]. Furthermore, to continue drawing attention to the need for adopting adequate preventive procedures, it is necessary to increase the number of graphic signs in public places, as well as repeated broadcast messages [27]. With a view to the protection and safety of employees, adoption of a specific protocol to avoid the spread of SARS-CoV-2 RNAisneededinstoresfrequented by large numbers of people each day [26]. This is in addition to recent recommendations of the Italian Institute of Health [28]. This study has some limitations. First, we did not isolate the virus from samples to assess viability; we also did not collect air samples or test supermarket customers. Furthermore, more in-depth multivariate analysis of factors with non-significant results is warranted, as well as including other parameters (e.g., size of POS devices, frequency of POSuse, cases occurring specifically in the municipalities where sampled supermarkets are located). In light of the emergence of new viral variants, this is our future aim, using more standardized environmental detection techniques. Moreover, the introduction of quantitative methodologies to search for SARS-CoV-2 on swab samples is another possible development of our research. This methodology would allow us to apply a QMRAmodel[10] to estimate infection risk of the disease on every surface.

5. Conclusions

 Our study shows that surfaces in non-hospital environments can be contaminated by SARS-CoV-2 RNA. Contamination in public spaces can occur and warrants further investigation to evaluate viability and risk, including collection of behavioral data to understand what surfaces are touched the most often, how often people hand sanitize, and how often they touch their face. Considering that surfaces such as trolleys with handles have been found to be more often contaminated, perhaps it would be appropriate to pay more attention to these surfaces during the sanitization procedures. Certainly, it remains essential to underline the importance of prevention measures such as ventilation of environments, careful hand sanitation, and correct usage of masks in public locations in the community, such as supermarkets, and commensurate with the number of visitors at such locations. Author Contributions: M.T.M., G.C. and O.D.G. conceived the study; V.M., G.T.S., P.M. and D.P.S. collected surface samples; F.A., F.T., M.D. carried out the molecular investigation; G.D., F.F., M.L., P.S. analyzed the results; M.T.M., G.C., F.A. and F.T. wrote the manuscript. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Not applicable. Acknowledgments: We thank Analisa Avila, MPH, ELS for editing a draft of this manuscript.