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Fomites and the Environment Did Not Have an Important Role in COVID-19 Transmission in a Brazilian Mid-Sized City

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Fomites and the Environment Did Not Have an Important Role in COVID-19 Transmission in a Brazilian Mid-Sized City www.nature.com/scientificreports OPEN Fomites and the environment did not have an important role in COVID‑19 transmission in a Brazilian mid‑sized city Ana Luíza Silva Rocha1,5, Josilene Ramos Pinheiro1,2,5, Thamilin Costa Nakamura3, José Domingos Santos da Silva3, Beatriz Gonçalves Silva Rocha4, Raphael Contelli Klein1, Alexander Birbrair4* & Jaime Henrique Amorim1,2* It is not clear if COVID‑19 can be indirectly transmitted. It is not possible to conclude the role of the environment in transmission of SARS‑CoV‑2 without studying areas in which people transit in great numbers. In this work we aimed to better understand the role of environment in the spread of COVID‑19. We investigated the presence of SARS‑CoV‑2 in fomites as well as in the air and in the sewage using RT‑qPCR. We studied both, a reference market area and a COVID‑19 reference hospital at Barreiras city, Brazil. We collected and analyzed a total of 418 samples from mask fronts, cell phones, paper money, card machines, sewage, air and bedding during the ascendant phase of the epidemiological curve of COVID‑19 in Barreiras. As a result, we detected the human RNAse P gene in most of samples, which indicates the presence of human cells or their fragments in specimens. However, we did not detect any trace of SARS‑CoV‑2 in all samples analyzed. We conclude that, so far, the environment and inanimate materials did not have an important role in COVID‑19 transmission in Barreiras city. Therefore, similar results can probably be found in other cities, mainly those with COVID‑19 epidemiological scenarios similar to that of Barreiras city. Our study is a small piece indicating the possibility that fomites and the environment do not have an important role in COVID‑19 transmission. However, further studies are necessary to better understand the world scenario. COVID-19 (coronavirus disease 2019) is caused by the new coronavirus SARS-CoV-2 (Severe acute respiratory syndrome coronavirus 2) identifed in China, in late 20191–3. Te disease is highly efciently transmitted and was spread to all continents, becoming a pandemic. Current evidence suggests that SARS-CoV-2 has a natural animal origin, most likely from bats, as these animals are ecological reservoirs of these viruses 4,5. However, it is more likely that the transmission of SARS-CoV-2 to humans happened through an intermediate host, which so far has not been identifed. Te presence of an intermediate host in this context would be explained by the low probability of direct transmission between bats and humans, since there is limited contact between them. As for the initial cases of COVID-19, the frst patients were notifed in late December 2019 and early 2020 4. Tey were directly related to the Wholesale Seafood Market of Huanan in the city of Wuhan, China. Environmental samples collected from the market in December 2019 tested positive for SARS-CoV-2 and, therefore, the market was inter- preted as the source of the frst outbreak of COVID-19. However, subsequent investigations led to the conclusion that the frst cases of humans infected with the new coronavirus showed symptoms in early December and that these people were likely to have been infected as early as November. Furthermore, these cases had no direct link to the Wuhan Wholesale Seafood Market4. Even from this most recent information, the question remains about the period when the virus was introduced into the human population and how it actually happened. 1Laboratório de Agentes Infecciosos e Vetores (LAIVE), Centro das Ciências Biológicas e da Saúde, Universidade Federal do Oeste da Bahia, Rua da Prainha, 1326, Morada Nobre, Barreiras, BA CEP 47810-047, Brazil. 2Programa de Pós-Graduação em Biologia e Biotecnologia de Microrganismos, Universidade Estadual de Santa Cruz, Ilhéus, BA, Brazil. 3Programa de Pós-Graduação em Química Pura e Aplicada, Centro das Ciências Exatas e Tecnológicas, Universidade Federal do Oeste da Bahia, Barreiras, BA, Brazil. 4Departamento de Patologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. 5These authors contributed equally: Ana Luíza Silva Rocha and Josilene Ramos Pinheiro. *email: [email protected]; [email protected] Scientifc Reports | (2021) 11:15960 | https://doi.org/10.1038/s41598-021-95479-5 1 Vol.:(0123456789) www.nature.com/scientificreports/ According to the World Health Organization (WHO), more than 186,000,000 cases with more than 4,000,000 deaths were confrmed worldwide as of July 13, 20216. To date, there is no specifc antiviral drug capable of ef- ciently controlling SARS-CoV-2 approved for use in humans, although therapies based on anti-coagulants and convalescent plasma have been shown to be promising7–9. Fortunately, there are several vaccine formulations approved for use in humans10. However, vaccination of the majority of world populations is not being achieved, which prevents the containment of the pandemic. In addition, the raising of genetic variants of SARS-CoV-2 with increased transmission capacity and immune escape potential is a relevant concern 11, due to the possibility of both, increasing in transmission speed of COVID-19 and compromising of vaccines efcacy. Te cost of dealing with the COVID-19 is huge. Hospitalization, testing, tracing, mitigating strategies, masks and cleaning of fomites demand a new routine of increased costs for governments and businessmen and also impact the domestic budgets. Te increased use of disinfectants in inanimate materials is now a new normal scenario, due to the concern regarding indirect transmission of SARS-CoV-2. By the end of 2020, a total of US$4.5 billion in disinfectants was sold, an increase of more than 30% over 2019 12. However, it is not clear if COVID-19 can be indirectly transmitted through fomites. Tis is an important issue also regarding the story of animal source origins. Te presence of SARS-CoV-2 in the air and inanimate surfaces of intensive care units was reported in the middle of 2020 and in the beginning of 2021 13–15. However, the viral load was not informed. It is not possible to understand the role of inanimate surfaces and the environment in transmission of SARS-CoV-2 without sampling in areas in which people transit in great numbers, such as market areas. Are we exaggerating the risk of transmission of COVID-19 by fomites? What is the risk of SARS-CoV-2 transmission by fomites in real-life conditions? In this work we aimed to answer these questions and contribute to the understanding regarding the role of environment in the transmission of COVID-19 using Barreiras city, Brazil, as a model. Materials and methods Ethics statement. All methods were carried out in accordance with relevant guidelines and regulations. Ethics approval was obtained from institutional review board (ethics committee) (CAAE 40779420.6.0000.8060) of the Universidade Federal do Oeste da Bahia. Te need of informed consents was waived by the ethics commit- tee due to risks involved in the pandemic situation. Epidemiological data was retrieved from the epidemiological bulletins on the website of the city’s municipal health department and Instituto Brasileiro de Geografa e Estatís- tica (IBGE)16. We did not have access to personal data. Aim and specifc aims. In this study, we aimed to understand the role of the environment in the transmis- sion of COVID-19. Specifc aims were: (i) to investigate the presence of SARS-CoV-2 in inanimate objects using RT-qPCR and (ii) to investigate the presence of SARS-CoV-2 in the air and in the sewage using RT-qPCR. Study area. Te investigation was carried out in Barreiras city, which is located in the western region of the state of Bahia, Brazil, from June 2020 to May 2021. Barreiras is the 10th largest city in the state and the largest in the west of Bahia, with more than 150,000 inhabitants. Due to its economic potential and health structure, the city receives people from all over the western region and now, in the pandemic period, it receives a relevant number of COVID-19 patients, as Barreiras has the largest number of beds in Intensive Care Units (ICU)17 in the western region of Bahia. Study design. In order to verify the presence of SARS-CoV-2 in the environment, we studied the main market area of Barreiras which includes stores, supermarkets, restaurants, snack bars, bars and a variety of com- mercial points. We also studied the Eurico Dutra Hospital, a city reference health unit for COVID-19. We col- lected samples of mask fronts, cell phones, paper money, card machines, sewage, air and bedding. Samples were kept refrigerated at 4–8 °C and analyzed up to 6 h afer being collected. Te study was conducted during the ascendant phase of the epidemiological curve of COVID-19 in Barreiras city. Viral detection using the RT-qPCR method was performed at the Laboratório de Agentes Infecciosos e Vetores, Universidade Federal do Oeste da Bahia, in Barreiras, Brazil. To determine the sample size we considered a margin of error of 5%. In addition, we considered the total population of Barreiras city as potential donors of samples, as previously described 18,19. According to IBGE, the population of Barreiras city is of 156,975 inhabitants. Tus, we calculated a minimum of 383 samples in order to represent the city. Environmental samples. Sampling was carried out from June 1, 2020 to May 13, 2021. Four of these samplings were carried out at the main market area of Barreiras (an open public place with intense circulation of people). On June 1, 2020 (maximum temperature of 31.3 °C; minimum humidity of 49%) we collected fve samples of sewage, 27 samples from cell phones and 30 samples from paper money.
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