SARS-CoV-2 RNA viability on high-touch surfaces and evaluation of a continuous-flow ozonation treatment
Keywords:
SARS-CoV-2, ozone, surfaces, virus, decontamination, disinfectionAbstract
Background. The COVID-19 emergency has highlighted the importance of prevention systems and environmental microbiological monitoring as fundamental elements in the response to epidemics and other such threats to individual and collective health. The use of automated “No-touch” room disinfection systems eliminates or reduces the dependence on operators, thus allowing an improvement in the effectiveness of terminal disinfection.
Study design. In the present study, we focused on possible SARS-CoV-2 contamination of surfaces of commercial services, and the effectiveness of ozone treatment on the virus.
Methods. Analyses were conducted on 4-7 October and 27-30 December 2021 in four supermarkets in an Apulian city; supermarkets A and B were equipped with an ozonisation system, while C and D were without any environmental remediation.
Results. SARS-CoV-2 RNA was detected by real-time RT-PCR only in December, in 6% of the surfaces tested, and all examined samples were found to be negative after viral culture, since no cytopathic effect was observed. A statistically significant difference emerged from the comparison of October vs. December (p = 0.0289), but no statistically significant difference (p = 0.6777) emerged from the comparison between supermarkets with and without the ozonisation system.
Conclusions. Although no important changes were observed by treating the environments with ozonisation systems, further studies are needed to validate the effectiveness of environmental treatments with airborne disinfectants.
References
1. Irie MS, Dietrich L, Souza GL, et al. Ozone disinfection for viruses with applications in healthcare environments: a scoping review. Braz Oral Res. 2022 Jan 1; 36: e006. doi: 10.1590/18073107bor-2022.vol36.0006.
2. Gola M, Caggiano G, De Giglio O, et al. SARSCoV-2 indoor contamination: considerations on anti-COVID-19 management of ventilation systems, and finishing materials in healthcare facilities. Ann Ig. 2021 Jul-Aug; 33(4): 381-92. doi: 10.7416/ai.2020.2396. Epub 2020 Dec 4.
3. Otter JA, Yezli S, Perl TM, Barbut F, French GL. The role of ‘no-touch’ automated room disinfection systems in infection prevention and control. J Hosp Infect. 2013 Jan; 83(1): 1-13. doi: 10.1016/j.jhin.2012.10.002. Epub 2012 Nov 26.
4. Caggiano G, Triggiano F, Apollonio F, et al. SARS-CoV-2 RNA and Supermarket Surfaces: A Real or Presumed Threat? Int J Environ Res Public Health. 2021 Sep 6; 18(17): 9404. doi:
10.3390/ijerph18179404.
5. Petrillo S, Carrà G, Bottino P, et al. A Novel Multiplex qRT-PCR Assay to Detect SARS-CoV-2 Infection: High Sensitivity and Increased Testing Capacity. Microorganisms. 2020 Jul 17; 8(7): 1064. doi: 10.3390/microorganisms807106.
6. Chia PY, Coleman KK, Tan YK, et al. Singapore 2019 Novel Coronavirus Outbreak Research Team. Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients. Nat Commun. 2020 May 29; 11(1): 2800. doi: 10.1038/s41467-020-16670-2.
7. Harvey PA, Fuhrmeister ER, Cantrell ME, et al. Longitudinal Monitoring of SARS-CoV-2 RNA on High-Touch Surfaces in a Community Setting. Environ Sci Technol Lett. 2021 Feb 9; 8(2): 168-75. doi: 10.1021/acs.estlett.0c00875. Epub 2020 Dec 14.
8. Liu Y, Li T, Deng Y, et al. Stability of SARSCoV-2 on environmental surfaces and in human excreta. J Hosp Infect. 2021 Jan; 107: 105-7. doi: 10.1016/j.jhin.2020.10.021. Epub 2020 Nov 1.
9. van Doremalen N, Bushmaker T, Morris DH, et al. Aerosol and Surface Stability of SARSCoV-2 as Compared with SARS-CoV-1. N
Engl J Med. 2020 Apr 16; 382(16): 1564-7. doi:
10.1056/NEJMc2004973. Epub 2020 Mar 17.
10. Mazur-Panasiuk N, Botwina P, Kutaj A, Woszczyna D, Pyrc K. Ozone Treatment Is Insufficient to Inactivate SARS-CoV-2 Surrogate under Field Conditions. Antioxidants (Basel). 2021 Sep 16; 10: 1480. doi: 10.3390/antiox10091480.
11. Viana Martins CP, Xavier CSF, Cobrado L. Disinfection methods against SARS-CoV-2: a systematic review. J Hosp Infect. 2022 Jan; 119: 84-117. doi: 10.1016/j.jhin.2021.07.014. Epub 2021 Oct 18.
12. Panebianco F, Rubiola S, Di Ciccio PA. The Use of Ozone as an Eco-Friendly Strategy against Microbial Biofilm in Dairy Manufacturing Plants: A Review. Microorganisms. 2022 Jan 13; 10(1):
162. doi: 10.3390/microorganisms10010162.
13. Botta C, Ferrocino I, Pessione A, Cocolin L, Rantsiou K. Spatiotemporal Distribution of the Environmental Microbiota in Food Processing
Plants as Impacted by Cleaning and Sanitizing Procedures: the Case of Slaughterhouses and Gaseous Ozone. Appl Environ Microbiol. 2020
Nov 10; 86(23): e01861-20. doi: 10.1128/ AEM.01861-20.
14. Marino M, Maifreni M, Baggio A, Innocente N. Inactivation of Foodborne Bacteria Biofilms by Aqueous and Gaseous Ozone. Front Microbiol. 2018 Aug 28; 9: 2024. doi: 10.3389/ fmicb.2018.02024.
15. Castaño N, Cordts SC, Kurosu Jalil M, et al. Fomite transmission, physicochemical origin of virus-surface interactions, and disinfection strategies for enveloped viruses with applications to SARS-CoV-2. ACS Omega. 2021 Mar 5; 6(10): 6509-27. doi: 10.1021/acsomega.0c06335.
16. Tseng C, Li C. Inactivation of surface viruses by gaseous ozone. J Environ Health. 2008 Jun; 70(10): 56-62.
17. Tseng CC, Li CS. Ozone for inactivation of aerosolized bacteriophages. Aerosol Sci Technol. 2006 Aug 23; 40: 683-9. 10.1080/02786820600796590.
18. Sato H, Wananabe Y, Miyata H. Virucidal effect of ozone treatment of laboratory animal viruses. Jikken Dobutsu. 1990 Apr; 39(2): 223-9. doi: 10.1538/expanim1978.39.2_223.
19. Caggiano G, Apollonio F, Triggiano F, et al. SARS-CoV-2 and Public Transport in Italy. Int J Environ Res Public Health. 2021 Oct 29; 18(21): 11415. doi: 10.3390/ijerph182111415.
20. Montagna MT, De Giglio O, Calia C, et al. First Detection of Severe Acute Respiratory Syndrome Coronavirus 2 on the Surfaces of TouristRecreational Facilities in Italy. Int J Environ Res Public Health. 2021 Mar 21; 18(6): 3252. doi: 10.3390/ijerph18063252.
21. Caggiano G, Lopuzzo M, Spagnuolo V, et al. Investigations on the Efficacy of Ozone as an Environmental Sanitizer in Large Supermarkets. Pathogens. 2022 May 23; 11(5): 608. doi: 10.3390/pathogens11050608.
22. La Rosa G, Mancini P, Bonanno Ferraro G, et al. SARS-CoV-2 Has been Circulating in Northern Italy since December 2019: Evidence from Environmental Monitoring. Sci Total Environ. 2021 Jan 1; 750: 141711. doi: 10.1016/j.
scitotenv.2020.141711. Epub 2020 Aug 15.
23. Moreno T, Pintó RM, Bosch A, et al. Tracing Surface and Airborne SARS-CoV-2 RNA Inside Public Buses and Subway Trains. Environ.
Int. 2021 Feb; 147: 106326. doi: 10.1016/j.
envint.2020.106326. Epub 2020 Dec 9.
24. Di Carlo P, Chiacchiaretta P, Sinjari B, et al. Air and Surface Measurements of SARS-CoV-2 Inside a Bus During Normal Operation. PLoS One. 2020 Nov 5; 15(11): e0235943. doi: 10.1371/ journal.pone.0235943.
25. Stelzer-Braid S, Walker GJ, Aggarwal A, et al. Virus isolation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) for diagnostic and research purposes. Pathology. 2020 Dec; 52(7): 760–3. doi: 10.1016/j.pathol.2020.09.012. Epub 2020 Oct 8.
26. Manzulli V, Scioscia G, Giganti G, et al. Real Time PCR and Culture-Based Virus Isolation
Test in Clinically Recovered Patients: Is the Subject Still Infectious for SARS-CoV2? J Clin Med. 2021 Jan 15; 10(2): 309. doi: 10.3390/ jcm10020309.
27. Ministero della Salute. Covid-19 - Dati andamento nazionale. Available on: https://github. com/pcm-dpc/COVID-19/tree/master/datiregioni [Last accessed: 2022 Sep 2].
28. Azimi P, Keshavarz Z, Laurent JGC, Stephens B, Allen JG. Mechanistic transmission modeling of COVID-19 on the iamond Princess cruise ship demonstrates the importance of aerosol transmission. Proc Natl Acad Sci USA. 2021 Feb 23; 118(8): e2015482118. doi: 10.1073/ pnas.2015482118.
29. Tharayil A, Rajakumari R, Mozetic M, Primc
G, Thomas S. Contact transmission of SARSCoV-2 on fomite surfaces: surface survival and risk reduction. Interface Focus. 2021 Dec 10; 12(1): 20210042. doi: 10.1098/rsfs.2021.0042.
30. Jones RM. Relative contributions of transmission routes for COVID-19 among healthcare personnel providing patient care. J Occup Environ Hyg. 2020 Sep; 17(9): 408-15. doi: 10.1080/15459624.2020.1784427.Epub 2020
Jul 9.
31. La Scola B, Le Bideau M, Andreani J, et al. Viral RNA load as determined by cell culture as a management tool for discharge of SARSCoV-2 patients from infectious disease wards. Eur J Clin Microbiol Infect Dis. 2020 Jun; 39(6): 1059-61. doi: 10.1007/s10096-020-03913-9. Epub 2020 Apr 27.
32. Gallè F, Sabella EA, Roma P, et al. Acceptance of COVID-19 Vaccination in the Elderly: A Cross-Sectional Study in Southern Italy. Vaccines (Basel). 2021 Oct 21; 9(11): 1222. doi: 10.3390/vaccines9111222.
33. Tizaoui C, Stanton R, Statkute E, et al. Ozone for SARS-CoV-2 inactivation on surfaces and in liquid cell culture media. J Hazard Mater.
2022 Apr 15; 428: 128251. doi: 10.1016/j.
jhazmat.2022.128251. Epub 2022 Jan 10.
34. Bryant C, Wilks SA, Keevil CW. Rapid inactivation of SARS-CoV-2 on copper touch surfaces determined using a cell culture infectivity assay. bioRxiv. 2021 Jan 2: 424974. Preprint doi: https://doi.org/10.1101/2021.01.02.424974.
35. Yano H, Nakano R, Suzuki Y, Nakano A, Kasahara K, Hosoi H. Inactivation of severe acute respiratory syndrome coronavirus 2 (SARSCoV-2) by gaseous ozone treatment. J Hosp Infect 2020 Dec; 106(4): 837-8. doi: 10.1016/j. jhin.2020.10.004. Epub 2020 Oct 10.
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