1887

Abstract

Aiming to contribute with more data on the presence of SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) in outdoor environments, we performed air sampling in outdoor terraces from restaurants in three major cities of Portugal in April 2021, following the third wave lockdown release in the country. Air samples (=19) were collected in 19 restaurant terraces during lunch time. Each air sample was collected using a Coriolis Compact air sampler, followed by RNA extraction and real-time quantitative PCR for the detection of viral RNA. Viral viability was also assessed through RNAse pre-treatment of samples. Only one of the 19 air samples was positive for SARS-CoV-2 RNA, with 7337 gene copies m for the genomic region N2, with no viable virus in this sample. The low number of positive samples found in this study is not surprising, as sampling took place in outdoor settings where air circulation is optimal, and aerosols are rapidly dispersed by the air currents. These results are consistent with previous reports stating that transmission of SARS-CoV-2 in outdoor spaces is low, although current evidence shows an association of exposures in settings where drinking and eating is possible on-site with an increased risk in acquiring SARS-CoV-2 infection. Moreover, the minimal infectious dose for SARS-CoV-2 still needs to be determined so that the real risk of infection in different environments can be accurately established.

Funding
This study was supported by the:
  • EEA Grants (Award AIRCOVID)
    • Principle Award Recipient: JoãoR. Mesquita
  • FCT/MCTES (Award UIDP/00511/2020)
    • Principle Award Recipient: SofiaI.V. Sousa
  • FCT/MCTES (Award UIDB/00511/2020)
    • Principle Award Recipient: SofiaI.V. Sousa
  • FCT/MCTES (Award LA/P/0045/2020)
    • Principle Award Recipient: SofiaI.V. Sousa
  • Fundação para a Ciência e a Tecnologia (Award LA/P/0064/2020)
    • Principle Award Recipient: SofiaI.V. Sousa
  • Fundação para a Ciência e a Tecnologia (Award UIDB/04750/2020)
    • Principle Award Recipient: SofiaI.V. Sousa
  • Fundação para a Ciência e a Tecnologia (Award DFA/BD/7806/2020)
    • Principle Award Recipient: Gomes da SilvaPriscilla
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. The Microbiology Society waived the open access fees for this article.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001659
2023-02-10
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/jmm/72/2/jmm001659.html?itemId=/content/journal/jmm/10.1099/jmm.0.001659&mimeType=html&fmt=ahah

References

  1. WHO Coronavirus disease (COVID-19): How is it transmitted?; 2021 https://www.who.int/news-room/q-a-detail/coronavirus-disease-covid-19-how-is-it-transmitted accessed 16 August 2021
  2. WHO Transmission of SARS-CoV-2: implications for infection prevention precautions. WHO Global; 2020 https://www.who.int/news-room/commentaries/detail/transmission-of-sars-cov-2-implications-for-infection-prevention-precautions accessed 28 September 2020
  3. Lewis D. COVID-19 rarely spreads through surfaces. So why are we still deep cleaning?. Nature 2021; 590:26–28 [View Article] [PubMed]
    [Google Scholar]
  4. Greenhalgh T, Jimenez JL, Prather KA, Tufekci Z, Fisman D et al. Ten scientific reasons in support of airborne transmission of SARS-CoV-2. Lancet 2021; 397:1603–1605 [View Article] [PubMed]
    [Google Scholar]
  5. Bulfone TC, Malekinejad M, Rutherford GW, Razani N. Outdoor transmission of SARS-CoV-2 and other respiratory viruses: a systematic review. J Infect Dis 2021; 223:550–561 [View Article]
    [Google Scholar]
  6. Morawska L, Milton DK. It is time to address airborne transmission of COVID-19. Clin Infect Dis 20201–4 [View Article]
    [Google Scholar]
  7. Bulfone TC, Malekinejad M, Rutherford GW, Razani N. Outdoor transmission of SARS-CoV-2 and other respiratory viruses: a systematic review. J Infect Dis 2021; 223:550–561 [View Article]
    [Google Scholar]
  8. Clouston SAP, Morozova O, Meliker JR. A wind speed threshold for increased outdoor transmission of coronavirus: an ecological study. BMC Infect Dis 2021; 21:1194 [View Article] [PubMed]
    [Google Scholar]
  9. CDC Small and Large Gatherings. About COVID-19; 2022 https://www.cdc.gov/coronavirus/2019-ncov/your-health/gatherings.html#print accessed 5 July 2022
  10. Senatore V, Zarra T, Buonerba A, Choo K-H, Hasan SW et al. Indoor versus outdoor transmission of SARS-COV-2: environmental factors in virus spread and underestimated sources of risk. EuroMediterr J Environ Integr 2021; 6:30 [View Article] [PubMed]
    [Google Scholar]
  11. Xu X, Zhang J, Zhu L, Huang Q. Transmission of SARS-CoV-2 indoor and outdoor environments. Atmosphere 2021; 12:1640 [View Article]
    [Google Scholar]
  12. Conte M, Feltracco M, Chirizzi D, Trabucco S, Dinoi A et al. Airborne concentrations of SARS-CoV-2 in indoor community environments in Italy. Environ Sci Pollut Res Int 2022; 29:13905–13916 [View Article] [PubMed]
    [Google Scholar]
  13. Pivato A, Amoruso I, Formenton G, Di Maria F, Bonato T et al. Evaluating the presence of SARS-CoV-2 RNA in the particulate matters during the peak of COVID-19 in Padua, northern Italy. Sci Total Environ 2021; 784:147129 [View Article] [PubMed]
    [Google Scholar]
  14. Setti L, Passarini F, De Gennaro G, Barbieri P, Perrone MG et al. SARS-Cov-2RNA found on particulate matter of Bergamo in Northern Italy: First evidence. Environ Res 2020; 188:109754 [View Article] [PubMed]
    [Google Scholar]
  15. Chirizzi D, Conte M, Feltracco M, Dinoi A, Gregoris E et al. SARS-CoV-2 concentrations and virus-laden aerosol size distributions in outdoor air in north and south of Italy. Environ Int 2021; 146:106255 [View Article] [PubMed]
    [Google Scholar]
  16. Dunker S, Hornick T, Szczepankiewicz G, Maier M, Bastl M et al. No SARS-CoV-2 detected in air samples (pollen and particulate matter) in Leipzig during the first spread. Sci Total Environ 2021; 755:142881 [View Article] [PubMed]
    [Google Scholar]
  17. Passos RG, Silveira MB, Abrahão JS. Exploratory assessment of the occurrence of SARS-CoV-2 in aerosols in hospital facilities and public spaces of a metropolitan center in Brazil. Environ Res 2021; 195:110808 [View Article] [PubMed]
    [Google Scholar]
  18. Hadei M, Mohebbi SR, Hopke PK, Shahsavani A, Bazzazpour S et al. Presence of SARS-CoV-2 in the air of public places and transportation. Atmos Pollut Res 2021; 12:302–306 [View Article] [PubMed]
    [Google Scholar]
  19. da Silva PG, Nascimento MSJ, Soares RRG, Sousa SIV, Mesquita JR. Airborne spread of infectious SARS-CoV-2: moving forward using lessons from SARS-CoV and MERS-CoV. Sci Total Environ 2021; 764:142802 [View Article]
    [Google Scholar]
  20. Monteiro S, Rente D, Cunha MV, Marques TA, Cardoso E et al. Discrimination and surveillance of infectious severe acute respiratory syndrome Coronavirus 2 in wastewater using cell culture and RT-qPCR. Sci Total Environ 2022; 815:152914 [View Article] [PubMed]
    [Google Scholar]
  21. Instituto Nacional de Saúde Doutor Ricardo Jorge (INSA) COVID-19: curva epidémica e parâmetros de transmissibilidade. Dados R(t); 2021 https://www.insa.min-saude.pt/category/areas-de-atuacao/epidemiologia/covid-19-curva-epidemica-e-parametros-de-transmissibilidade/ accessed 14 October 2022
  22. Santarpia JL, Rivera DN, Herrera VL, Morwitzer MJ, Creager HM et al. Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and isolation care. Sci Rep 2020; 10:12732 [View Article] [PubMed]
    [Google Scholar]
  23. GRISP Research Solutions GRS Viral DNA/RNA Purification Kit; 2022 https://grisp.pt/produto/grs-viral-dna-rna-purification-kit/ accessed 14 October 2022
  24. Vogelstein B, Gillespie D. Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci U S A 1979; 76:615–619 [View Article] [PubMed]
    [Google Scholar]
  25. CDC CDC 2019-Novel Coronavirus (2019-nCoV) real-time RT-PCR diagnostic panel. Centers for Disease Control and Prevention 2020; CDC-006-00:1–80
    [Google Scholar]
  26. Marti E, Ferrary-Américo M, Barardi CRM. Detection of potential infectious enteric viruses in fresh produce by (RT)-qPCR preceded by nuclease treatment. Food Environ Virol 2017; 9:444–452 [View Article]
    [Google Scholar]
  27. Khan KA, Cheung P. Presence of mismatches between diagnostic PCR assays and coronavirus SARS-CoV-2 genome. R Soc Open Sci 2020; 7:200636 [View Article] [PubMed]
    [Google Scholar]
  28. Whiley DM, Sloots TP. Sequence variation in primer targets affects the accuracy of viral quantitative PCR. J Clin Virol 2005; 34:104–107 [View Article] [PubMed]
    [Google Scholar]
  29. Huang J, Jones P, Zhang A, Hou SS, Hang J et al. Outdoor airborne transmission of coronavirus among apartments in high-density cities. Front Built Environ 2021; 7: [View Article]
    [Google Scholar]
  30. Rowe BR, Canosa A, Drouffe JM, Mitchell JBA. Simple quantitative assessment of the outdoor versus indoor airborne transmission of viruses and COVID-19. Environ Res 2021; 198:111189 [View Article] [PubMed]
    [Google Scholar]
  31. Wang CC, Prather KA, Sznitman J, Jimenez JL, Lakdawala SS et al. Airborne transmission of respiratory viruses. Science 2021; 373:eabd9149 [View Article]
    [Google Scholar]
  32. Direção-Geral da Saúde (DGS) RELATÓRIO DE VACINAÇÃO | PORTUGAL | SEMANA 14. Plano de vacinação COVID-19; 2021 https://covid19.min-saude.pt/wp-content/uploads/2022/02/Relatorio_Vacinacao_27122020_11042021_pdf-1906kb.pdf accessed 14 October 2022
  33. Rodríguez RA, Pepper IL, Gerba CP. Application of PCR-based methods to assess the infectivity of enteric viruses in environmental samples. Appl Environ Microbiol 2009; 75:297–307 [View Article] [PubMed]
    [Google Scholar]
  34. Rönnqvist M, Mikkelä A, Tuominen P, Salo S, Maunula L. Ultraviolet light inactivation of murine norovirus and human norovirus GII: PCR may overestimate the persistence of noroviruses even when combined with pre-PCR treatments. Food Environ Virol 2014; 6:48–57 [View Article]
    [Google Scholar]
  35. Pecson BM, Martin LV, Kohn T. Quantitative PCR for determining the infectivity of bacteriophage MS2 upon inactivation by heat, UV-B radiation, and singlet oxygen: advantages and limitations of an enzymatic treatment to reduce false-positive results. Appl Environ Microbiol 2009; 75:5544–5554 [View Article] [PubMed]
    [Google Scholar]
  36. Li D, Baert L, Xia M, Zhong W, Van Coillie E et al. Evaluation of methods measuring the capsid integrity and/or functions of noroviruses by heat inactivation. J Virol Methods 2012; 181:1–5 [View Article] [PubMed]
    [Google Scholar]
  37. Nuanualsuwan S, Cliver DO. Pretreatment to avoid positive RT-PCR results with inactivated viruses. J Virol Methods 2002; 104:217–225 [View Article] [PubMed]
    [Google Scholar]
  38. Nuanualsuwan S, Cliver DO. Capsid functions of inactivated human picornaviruses and feline calicivirus. Appl Environ Microbiol 2003; 69:350–357 [View Article] [PubMed]
    [Google Scholar]
  39. Pan M, Lednicky JA, Wu CY. Collection, particle sizing and detection of airborne viruses. J Appl Microbiol 2019; 127:1596–1611 [View Article] [PubMed]
    [Google Scholar]
  40. Lednicky JA, Lauzard M, Fan ZH, Jutla A, Tilly TB et al. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int J Infect Dis 2020; 100:476–482 [View Article] [PubMed]
    [Google Scholar]
  41. Lednicky JA, Lauzardo M, Alam MM, Elbadry MA, Stephenson CJ et al. Isolation of SARS-CoV-2 from the air in a car driven by a COVID patient with mild illness. Int J Infect Dis 2021; 108:212–216 [View Article] [PubMed]
    [Google Scholar]
  42. Santarpia JL, Herrera VL, Rivera DN, Ratnesar-Shumate S, Reid SP et al. The size and culturability of patient-generated SARS-CoV-2 aerosol. J Expo Sci Environ Epidemiol 2022; 32:706–711 [View Article] [PubMed]
    [Google Scholar]
  43. INSA Evolução do número de casos de COVID-19 em Portugal: 09-04-2021. Lisboa: 2021 https://www.insa.min-saude.pt/wp-content/uploads/2021/04/Report_covid19_09_04_2021.pdf
  44. INSA Evolução do número de casos de COVID-19 em Portugal: 04-06-2021. Lisboa: 2021 https://www.insa.min-saude.pt/wp-content/uploads/2021/06/Report_covid19_04_06_2021.pdf
  45. Suñer C, Coma E, Ouchi D, Hermosilla E, Baro B et al. Association between two mass-gathering outdoor events and incidence of SARS-CoV-2 infections during the fifth wave of COVID-19 in north-east Spain: a population-based control-matched analysis. Lancet Reg Health Eur 2022; 15:100337 [View Article]
    [Google Scholar]
  46. Lin A, Vittinghoff E, Olgin J, Peyser N, Aung S et al. Predictors of incident SARS-CoV-2 infections in an international prospective cohort study. BMJ Open 2021; 11:e052025 [View Article] [PubMed]
    [Google Scholar]
  47. Fisher KA, Tenforde MW, Feldstein LR, Lindsell CJ, Shapiro NI et al. Community and close contact exposures associated with COVID-19 among symptomatic adults ≥18 years in 11 outpatient health care facilities - united states, july 2020. MMWR Morb Mortal Wkly Rep 2020; 69:1258–1264 [View Article]
    [Google Scholar]
  48. Galmiche S, Charmet T, Schaeffer L, Paireau J, Grant R et al. Exposures associated with SARS-CoV-2 infection in France: a nationwide online case-control study. Lancet Reg Health Eur 2021; 7:100148 [View Article]
    [Google Scholar]
  49. Samet JM, Burke TA, Lakdawala SS, Lowe JJ, Marr LC et al. SARS-CoV-2 indoor air transmission is a threat that can be addressed with science. Proc Natl Acad Sci U S A 2021; 118:1–5 [View Article] [PubMed]
    [Google Scholar]
  50. Toms GL, Rosztoczy I, Smith H. The localization of influenza virus: minimal infectious dose determinations and single cycle kinetic studies on organ cultures of respiratory and other ferret tissues. Br J Exp Pathol 1974; 55:116–129 [PubMed]
    [Google Scholar]
  51. Karimzadeh S, Bhopal R, Nguyen Tien H. Review of infective dose, routes of transmission and outcome of COVID-19 caused by the SARS-COV-2: comparison with other respiratory viruses- CORRIGENDUM. Epidemiol Infect 2021; 149:e116 [View Article] [PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001659
Loading
/content/journal/jmm/10.1099/jmm.0.001659
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error