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RESEARCH ARTICLE       APRIL 10, 2020

Ozone efficacy for the control of airborne viruses: Bacteriophage and norovirus models

Abstract
This study was designed to test the efficacy of an air treatment using ozone and relative humidity (RH) for the inactivation of airborne viruses. Four phages (φX174, PR772, MS2 and φ6) and one eukaryotic virus (murine norovirus MNV-1) were exposed to low ozone concentrations (1.23 ppm for phages and 0.23 ppm for MNV-1) and various levels of RH for 10 to 70 minutes. The inactivation of these viruses was then assessed to determine which of the tested conditions provided the greatest reduction in virus infectivity. An inactivation of atleast two orders of magnitude for φX174, MS2 and MNV-1 was achieved with an ozone exposure of 40 minutes at 85% RH. For PR772 and φ6, exposure to the reference condition at 20% RH for 10 minutes yielded the same results. These findings suggest that ozone used at a low concentration is a powerful disinfectant for airborne viruses when combined with a high RH.Air treatment could therefore be implemented inside hospital rooms ventilated naturally.

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Introduction
Viral infections can be acquired in numerous indoor public spaces, including hospitals, cruise ships, schools, daycare centres, restaurants, and transport and commuting services [1, 2]. Evidence for the presence of multiple viruses in these settings, including influenza, rhinovirus, coronavirus, adenovirus, enterovirus, norovirus and the respiratory syncytial virus (RSV) have been reviewed [3]. Infections acquired in hospital settings are a major concern for patients, workers and visitors. They are responsible for longer hospital stays [4], increased costs [4–8], absenteeism among healthcare workers [4], and even patient deaths [9]. Norovirus, influenza, rotavirus and RSV are among the most common viruses acquired in hospital settings [10, 11]. On various occasions, cruise ships have been struck by norovirus outbreaks, infecting hundreds of people at once [12–18]. As mentioned by Lopman et al. (2012) [1], norovirus has also been problematic in other indoor environments, including restaurants, schools and kindergartens,concert halls, airplanes and buses.

Viruses are transmitted through multiple routes [3], including transmission through contact, transmission by a vehicle (water, food, fomites or inanimate objects) or a vector (insects) and finally airborne transmission [19]. Large aerosol droplets usually travel shorter distances,

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Conclusion

The results obtained in this study demonstrate the efficacy of an air treatment for phage and MNV-1 inactivation using low ozone concentrations, 1.13 ppm ± 0.26 ppm and 0.23 ppm ± 0.03 ppm, respectively, at various RH levels and exposure times of up to 70 minutes. An exposure of 40 minutes at 85% RH yields the inactivation of at least two orders of magnitude for φX174, MS2 and MNV-1. An exposure to the reference conditions at 20% RH for 10 minutes for PR772 and φ6 was enough to yield the same results. The inactivation of other problematic viruses should be tested to obtain supplementary evidence regarding this air treatment and with the eventual possibility of implementing it in hospital settings. Since Influenza is an enveloped virus, it would be interesting to evaluate if the treatment efficacy is the same as its surrogate phage, φ6. In the context of the SARS-CoV-2 pandemic, future work is needed to assess the efficacy of an ozone treatment in order to reduce the transmission of this virus in hospital settings and other indoor public spaces. This treatment could also be tested with bacteria resistant to antibiotics, including Clostridium difficile, methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci, which are serious threats to hospitalized patients. Lastly, low ozone concentrations could be used for air treatment inside hospital rooms ventilated naturally, providing an additional tool for hospitals that do not possess HVAC plenums.

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