Antimicrobial Performance of an Innovative Technology of Atmospheric Plasma Reactors against Bioaerosols: Effectiveness in Removing Airborne Viable Viruses
Abstract
:1. Introduction
- Filters are made to physically remove airborne particles from the surrounding air in order to enhance the indoor air quality in a specific room or region. HEPA (High-Efficiency Particulate Arresting) filters are now the most popular kind of household filter, however, certain equipment also uses fibrous media air filters. A HEPA filter’s fibers are intended to capture particles with a diameter that might be as small as 0.01 microns [6]. Of course, a key consideration is how frequently air filters should be changed. Airflow across the filter can be impacted by saturation, which also has an impact on filter effectiveness.
- Ozone generators are marketed as air purifiers that purposefully release ozone gas [7]. Ozone is a highly oxidizing molecule composed of three oxygen atoms. One of the oxygen atoms can detach from it and re-attach to other molecules, changing their chemical composition. Ozone, however, is a poisonous gas. In fact, the same chemical qualities that allow ozone in high concentrations to react with organic matter outside the body also allow it to react with comparable organic matter inside the human body, leading to detrimental effects on health.
- Ionizers, often referred to as electrostatic precipitators, are electronic air cleaners that employ a high-voltage wire or carbon fiber brush to charge air particles which causes them to gravitate toward objects with the opposite electrical charge [8]. These items might be the collecting plates found inside the equipment itself or other interior surfaces found throughout the space (such as walls, carpets, etc.) to filter out airborne particles. Due to the fact that these deposited particles stay in the space, when disturbed by human actions, such as walking or cleaning, they may be resuspended from the collection surfaces. The impact of particle charging on particle deposition in the respiratory tract, which rises as particles become charged, is another aspect of ionizers to consider. Ionizer use may not, therefore, result in a reduction in the particle dosage to the lungs. Furthermore, ionizers employ high voltage to create ionized fields, and they may purposefully or unintentionally release ozone gas as a byproduct.
- UVGI (Ultraviolet Germicidal Irradiation) air cleaners are created to employ UV irradiation to kill or deactivate microorganisms such as viruses, bacteria, and fungal spores and fragments that are airborne or growing on surfaces [9]. UVGI air cleaners use UV-A (long wave: 315–400 nm) and UV-C (short wave: 100–280 nm) radiation. UV radiation can enter a microorganism’s outer cells and change its DNA, blocking replication and leading to cell death, given enough exposure time and lamp power. The UVGI cleaner in a typical airstream disinfection application has the potential to reduce the viability of vegetative bacteria and molds and to provide low to moderate reductions in viruses but little reduction in bacterial and mold spores [10].
- Plasma air cleaners use a high-voltage discharge to ionize incoming gases, causing them to lose their chemical bonds and undergo chemical changes [11]. Thermal plasma air cleaners use a high voltage and high current to create a high-temperature plasma flame. By accelerating electrons, non-thermal plasma air cleaners produce reactive ions and radicals (such as hydroxyl radicals, superoxides, and hydrogen peroxide) which oxidize substances and change their chemical composition. Plasma air cleaners have the ability to kill or inactivate airborne microorganisms [11] and can remove some gases and particles with high removal effectiveness. However, a number of hazardous byproducts, such as particulates, ozone, carbon monoxide, and formaldehyde, can also be produced.
2. Materials and Methods
2.1. The Atmospheric Plasma Reactor Technology Included in the KillViDTM Air Cleaner Device
- The electrons during the discharge formation growth in the air/vapor medium surrounding the pathogen-loaded micro-droplets and aerosols create advanced oxidants, including ozone and hydroxyl radicals, in situ, among the micro-droplets and aerosols to be treated.
- The electrons gain energy from the applied electric field, producing energetic electrons in the space among the droplets and thus act directly on each droplet to create hydroxyl ions and radicals in the droplet before a conducting plasma is created.
- The micro-droplets create a very large surface for interaction for a given volume of air, making a highly efficient advanced oxidation reaction zone in a small chamber.
- The THCD process leads to the creation of an ultra-high electric field zone close to the hollow cathode electrode. This ultra-high field is of the order 5 × 105 Vcm−1 (5V across 100 nm) and leads to direct electroporation [22] of the cellular structure of viruses and bacteria.
2.2. Virus Culture and Preparation
2.3. Plating and Enumeration
- The spot containing the fewest PFU was counted to determine the order of magnitude (e.g., 108 PFU/mL).
- A concentration correction was carried out to bring the unit of PFU/10 µL to PFU/mL (e.g., 108 PFU/10 µL corresponding to 1010 PFU/mL).
- The number of lysis areas was counted on the least concentrated spot to obtain the decimal part (e.g., 1010 PFU/mL corresponding to 4 × 1010 PFU/mL if 4 lysis areas were counted in the least concentrated spot).
2.4. Design of the Experiment, Bioaerosol Generation and Sampling
- Cultivating bacteriophage viruses in order to prepare a suspension that filled the bioaerosol generator with 3 mL of virus suspension. The aerosol stream containing a known charge of phi11 viruses was generated using an E-flow mesh nebulizer (Pari GmbH, Starnberg, Germany). The initial concentration of virus introduced into the nebulizer tank was always fixed at 2 × 1010 PFU/mL (see the “virus culture and preparation” section).
- Carrying out an experimental setup (Figure 3 and Figure S1 in Supplementary File) in a confined and controlled environment that consisted of aerosolizing the virus suspension directly into the air cleaner (virucidal activity quantified after a single pass of the bioaerosol in the air cleaner).
- Collecting the aerosolized viruses coming directly from the output of the air cleaner using a Coriolis® biocollector. Airborne viruses were collected in 3 mL of PBS with the Coriolis® Delta high air volume collection tool operating at 300 L/min (Bertin Instruments, Montigny-le-Bretonneux, France). This airflow of the Coriolis® biocollector, fixed at 300 L/min, is responsible for the aspiration. With the APR acting as a resistive load, the airflow at the inlet of the air cleaner was approximately 60 L/min. This airflow was measured at the inlet of the air cleaner (connected directly to the pipe that normally is connected to the nebulizer) prior to each experiment. The airflow measurement instrument used was a COPLEY DFM4 Flow Meter which has a resolution of 0.1 L/min (see Figure S3).
- Measuring the viral load collected in the Coriolis® biocollector by counting the lysis area on a confluent culture of a bacteriophage-susceptible Staphylococcus aureus strain (see the “plating and enumeration” section).
2.5. Statistical Analysis
3. Results
- The first column shows the nebulization duration and the third column the nebulized volume for each experiment. The results demonstrated a very good reproducibility of the nebulization process, indicating the good quality of bioaerosol nebulization for each experiment. There was no significant difference in the nebulization duration in the three conditions (p = 0.3337) nor for the nebulized volume (p = 0.8662).
- The second column shows the airflow rate imposed at the inlet of the purifier which is only imposed by the inspiratory flow rate of the Coriolis® biocollector. These results also demonstrated a very good reproducibility of this flow rate, which is an important indicator of a constant passage time of bioaerosol through the air cleaner for all experimental conditions tested.
- The fifth column shows the volume remaining in the jar of the Coriolis® biocollector, given by:
- The sixth column corresponds to the measurement of the concentration of bacteriophage viruses collected by the Coriolis® device by reading the lysis area.
- The fourth and seventh columns (amount of viruses nebulized in PFU and amount of viruses collected in PFU) are not experimental measurements, but simple calculations of the experimental volume and concentration data determined elsewhere.
4. Discussion
4.1. The Proposed Experimental Setup to Assess the Virucidal Activity of the Air Cleaner Using Different Configurations of APR Technology
4.2. Limitation and Possible Extrapolation to Other Respiratory Pathogenic Viruses with the Use of the phi11 Bacteriophage as a Surrogate Virus
4.3. Relative Positioning of APR Technology Performances Compared to the Effectiveness Reported for Other Devices in the Literature
4.4. Contribution and Limitation of the APR Technology in the Management of Indoor Air Quality with Air Cleaners to Reduce Exposure to Airborne Viruses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Tang, J.W.; Marr, L.C.; Li, Y.; Dancer, S.J. COVID-19 Has Redefined Airborne Transmission. BMJ 2021, 373, n913. [Google Scholar] [CrossRef] [PubMed]
- Greenhalgh, T.; Jimenez, J.L.; Prather, K.A.; Tufekci, Z.; Fisman, D.; Schooley, R. Ten Scientific Reasons in Support of Airborne Transmission of SARS-CoV-2. Lancet 2021, 397, 1603–1605. [Google Scholar] [CrossRef]
- Salimifard, P.; Jones, E.; Allen, J. Portable Air Cleaners: Selection and Application Considerations for COVID-19 Risk Reduction; Harvard School of Public Health: Boston, MA, USA, 2020. [Google Scholar]
- U.S. Environmental Protection Agency. Air Cleaners, HVAC Filters, and Coronavirus (COVID-19). Available online: https://www.epa.gov/coronavirus/air-cleaners-hvac-filters-and-coronavirus-covid-19 (accessed on 26 August 2022).
- U.S. Environmental Protection Agency. Guide to Air Cleaners in the Home 2022; U.S. Environmental Protection Agency: Washington, DC, USA, 2022.
- Residential Air Cleaners—A Technical Summary 2018; U.S. Environmental Protection Agency: Washington, DC, USA, 2018.
- U.S. Environmental Protection Agency. Ozone Generators That Are Sold as Air Cleaners. Available online: https://www.epa.gov/indoor-air-quality-iaq/ozone-generators-are-sold-air-cleaners (accessed on 26 August 2022).
- Pushpawela, B.; Jayaratne, R.; Nguy, A.; Morawska, L. Efficiency of Ionizers in Removing Airborne Particles in Indoor Environments. J. Electrost. 2017, 90, 79–84. [Google Scholar] [CrossRef]
- Kujundzic, E.; Matalkah, F.; Howard, C.J.; Hernandez, M.; Miller, S.L. UV Air Cleaners and Upper-Room Air Ultraviolet Germicidal Irradiation for Controlling Airborne Bacteria and Fungal Spores. J. Occup. Environ. Hyg. 2006, 3, 536–546. [Google Scholar] [CrossRef]
- Kowalski, W.J.; Bahnfleth, W.P. Airborne Respiratory Diseases and Mechanical Systems for Control of Microbes. HPAC Heat. Pip. Air Cond. 1998, 70. Available online: https://www.researchgate.net/publication/286967555_Airborne_respiratory_diseases_and_mechanical_systems_for_control_of_microbes (accessed on 26 August 2022).
- Song, L.; Zhou, J.; Wang, C.; Meng, G.; Li, Y.; Jarin, M.; Wu, Z.; Xie, X. Airborne Pathogenic Microorganisms and Air Cleaning Technology Development: A Review. J. Hazard. Mater. 2022, 424, 127429. [Google Scholar] [CrossRef]
- ANSI/AHAM AC-1-2006—Method for Measuring Performance of Portable Household Electric Room Air Cleaners. Available online: https://webstore.ansi.org/Standards/AHAM/ansiahamac2006 (accessed on 26 August 2022).
- 1467-2013; Air Cleaners of Householdand Similar Use. The Japan Electrical Manufacturer’s Association JEM Standard: Tokyo, Japan, 2013.
- EN ISO 29464:2019; Cleaning of Air and Other Gases—Terminology (ISO 29464:2019). International Organisation for Standardization (ISO): Geneva, Switzerland, 2019. Available online: https://standards.iteh.ai/catalog/standards/cen/e5994e84-3d34-4774-9342-bb613e576cfe/en-iso-29464-2019 (accessed on 26 August 2022).
- Curtius, J.; Granzin, M.; Schrod, J. Testing Mobile Air Purifiers in a School Classroom: Reducing the Airborne Transmission Risk for SARS-CoV-2. Aerosol. Sci. Technol. 2021, 55, 586–599. [Google Scholar] [CrossRef]
- Balarashti, J.; Trolinger, J. Efficacy of The Novaerus NV 1050 Device against Aerosolized MS2 Virus 2020; ARE Labs Inc.: Emeryville, CA, USA, 2020; Volume 39. [Google Scholar]
- Wyndham, E.; Chuaqui, H.; Favre, M.; Choi, P. Observations of Hollow Cathode Light Emission from a Transient Hollow Cathode Discharge. Appl. Phys. Lett. 1991, 59, 2231–2233. [Google Scholar] [CrossRef]
- Choi, P.; Aliaga, R.; Blottiere, B.; Favre, M.; Moreno, J.; Chuaqui, H.; Wyndham, E. Experimental Studies of Ionization Processes in the Breakdown Phase of a Transient Hollow Cathode Discharge. Appl. Phys. Lett. 1993, 63, 2750–2752. [Google Scholar] [CrossRef]
- Choi, P.; Dumitrescu-Zoita, C.; Favre, M.; Moreno, J.; Chuaqui, H.; Wyndham, E.; Zambra, M. Time Resolved Studies of a Pulsed Hollow Cathode Capillary Discharge. Astrophys. Space Sci. 1997, 256, 479–484. [Google Scholar] [CrossRef]
- Favre, M.; Moreno, J.; Chuaqui, H.; Wyndham, E.; Zambra, M.; Choi, P.; Dumitrescu-Zoita, C. Pre-Breakdown Processes in the Hollow Cathode Region of a Transient Hollow Cathode Discharge. Astrophys. Space Sci. 1997, 256, 337–342. [Google Scholar] [CrossRef] [Green Version]
- Choi, P. Apparatus for Decontaminating Ambient Air in an Indoor Environment 2022. WO2022079208A2. Available online: https://worldwide.espacenet.com/patent/search/family/074871455/publication/WO2022079208A2?q=WO2022%2F079208 (accessed on 26 August 2022).
- Tsong, T.Y. Electroporation of Cell Membranes. In Electroporation and Electrofusion in Cell Biology; Neumann, E., Sowers, A.E., Jordan, C.A., Eds.; Springer US: Boston, MA, USA, 1989; pp. 149–163. ISBN 978-1-4899-2528-2. [Google Scholar]
- Whiley, H.; Keerthirathne, T.P.; Nisar, M.A.; White, M.A.F.; Ross, K.E. Viral Filtration Efficiency of Fabric Masks Compared with Surgical and N95 Masks. Pathogens 2020, 9, 762. [Google Scholar] [CrossRef] [PubMed]
- Ács, N.; Gambino, M.; Brøndsted, L. Bacteriophage Enumeration and Detection Methods. Front. Microbiol. 2020, 11, 2662. [Google Scholar] [CrossRef] [PubMed]
- Standards, E. EN 14683+AC. Medical Face Masks: Requirements and Test Methods. Available online: https://www.en-standard.eu/csn-en-14683-ac-medical-face-masks-requirements-and-test-methods/ (accessed on 20 September 2022).
- Armand, Q.; Whyte, H.E.; Verhoeven, P.; Grattard, F.; Leclerc, L.; Curt, N.; Ragey, S.P.; Pourchez, J. Impact of Medical Face Mask Wear on Bacterial Filtration Efficiency and Breathability. Environ. Technol. Innov. 2022, 28, 102897. [Google Scholar] [CrossRef]
- Whyte, H.E.; Joubert, A.; Leclerc, L.; Sarry, G.; Verhoeven, P.; Le Coq, L.; Pourchez, J. Impact of Washing Parameters on Bacterial Filtration Efficiency and Breathability of Community and Medical Facemasks. Sci. Rep. 2022, in press. [CrossRef]
- Whyte, H.E.; Joubert, A.; Leclerc, L.; Sarry, G.; Verhoeven, P.; Le Coq, L.; Pourchez, J. Reusability of Face Masks: Influence of Washing and Comparison of Performance between Medical Face Masks and Community Face Masks. Environ. Technol. Innov. 2022, 28, 102710. [Google Scholar] [CrossRef]
- Whyte, H.E.; Montigaud, Y.; Audoux, E.; Verhoeven, P.; Prier, A.; Leclerc, L.; Sarry, G.; Laurent, C.; Le Coq, L.; Joubert, A.; et al. Comparison of Bacterial Filtration Efficiency vs. Particle Filtration Efficiency to Assess the Performance of Non-Medical Face Masks. Sci. Rep. 2022, 12, 1188. [Google Scholar] [CrossRef]
- Pourchez, J.; Peyron, A.; Montigaud, Y.; Laurent, C.; Audoux, E.; Leclerc, L.; Verhoeven, P.O. New Insights into the Standard Method of Assessing Bacterial Filtration Efficiency of Medical Face Masks. Sci. Rep. 2021, 11, 5887. [Google Scholar] [CrossRef]
- Löfdahl, S.; Zabielski, J.; Philipson, L. Structure and Restriction Enzyme Maps of the Circularly Permuted DNA of Staphylococcal Bacteriophage Phi 11. J. Virol. 1981, 37, 784–794. [Google Scholar] [CrossRef] [Green Version]
- Brown, D.T.; Brown, N.C.; Burlingham, B.T. Morphology and Physical Properties of Staphylococcus Bacteriophage P11-M15. J. Virol. 1972, 9, 664–671. Available online: https://journals.asm.org/doi/10.1128/jvi.9.4.664-671.1972 (accessed on 26 August 2022). [CrossRef] [Green Version]
- Rosenblum, E.D.; Tyrone, S. Serology, Density, and Morphology of Staphylococcal Phages. J. Bacteriol. 1964, 88, 1737–1742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, N.; Zhang, D.; Wang, W.; Li, X.; Yang, B.; Song, J.; Zhao, X.; Huang, B.; Shi, W.; Lu, R.; et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N. Engl. J. Med. 2020, 382, 727–733. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.Y.; Iandolo, J.J. Structural Analysis of Staphylococcal Bacteriophage Phi 11 Attachment Sites. J. Bacteriol. 1988, 170, 2409–2411. Available online: https://journals.asm.org/doi/10.1128/jb.170.5.2409-2411.1988 (accessed on 26 August 2022). [CrossRef] [PubMed] [Green Version]
- Firquet, S.; Beaujard, S.; Lobert, P.-E.; Sané, F.; Caloone, D.; Izard, D.; Hober, D. Survival of Enveloped and Non-Enveloped Viruses on Inanimate Surfaces. Microbes Environ. 2015, 30, 140–144. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Chen, S.; Zhang, Z.W.; Zhang, S.; Pei, J.J.; Liu, J.J. Test Method and Performance Evaluation of Two-Stage Electrostatic Air Filter. In Proceedings of the 4th International Conference On Building Energy, Environment, Melbourne, Australia, 5–9 February 2018; pp. 745–750. [Google Scholar]
- Park, H.; Park, S.; Seo, J. Evaluation on Air Purifier’s Performance in Reducing the Concentration of Fine Particulate Matter for Occupants According to Its Operation Methods. Int. J. Environ. Res. Public. Health 2020, 17, 5561. [Google Scholar] [CrossRef]
- Coyle, J.P.; Derk, R.C.; Lindsley, W.G.; Blachere, F.M.; Boots, T.; Lemons, A.R.; Martin, S.B.; Mead, K.R.; Fotta, S.A.; Reynolds, J.S.; et al. Efficacy of Ventilation, HEPA Air Cleaners, Universal Masking, and Physical Distancing for Reducing Exposure to Simulated Exhaled Aerosols in a Meeting Room. Viruses 2021, 13, 2536. [Google Scholar] [CrossRef]
- Kähler, C.; Fuchs, T.; Hain, R. Can Mobile Indoor Air Cleaners Effectively Reduce an Indirect Risk of SARS-CoV-2 Infection by Aerosols? Universität der Bundeswehr München: Neubiberg, Germany, 2020. [Google Scholar]
- Oberst, M.; Klar, T.; Heinrich, A. The Effect of Mobile Indoor Air Cleaners on the Risk of Infection with SARS-CoV-2 in Surgical Examination and Treatment Rooms with Limited Ventilation Options. Austin J. Public Health Epidemiol. 2010, 8, 1094. [Google Scholar] [CrossRef]
- Batterman, S.; Su, F.-C.; Wald, A.; Watkins, F.; Godwin, C.; Thun, G. Ventilation Rates in Recently Constructed U.S. School Classrooms. Indoor Air 2017, 27, 880–890. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. CDC Ventilation in Buildings; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2019. [Google Scholar]
- ASHRAE. In-Room Air Cleaner Guidance for Reducing COVID-19 in Air in Your Space/Room; ASHRAE: Atlanta, GA, USA, 2021. [Google Scholar]
- Mousavi, E.S.; Godri Pollitt, K.J.; Sherman, J.; Martinello, R.A. Performance Analysis of Portable HEPA Filters and Temporary Plastic Anterooms on the Spread of Surrogate Coronavirus. Build. Environ. 2020, 183, 107186. [Google Scholar] [CrossRef]
- Bluyssen, P.M.; Ortiz, M.; Zhang, D. The Effect of a Mobile HEPA Filter System on ‘Infectious’ Aerosols, Sound and Air Velocity in the SenseLab. Build. Environ. 2021, 188, 107475. [Google Scholar] [CrossRef]
Nebulization Duration (s) | Flow Rate of the Air Cleaner (L/min) | Nebulized Volume (mL) | Viral Load Nebulized (PFU) | Volume Collected by the Coriolis (mL) | {Virus} In Coriolis Jar (PFU/mL) | Virus Load Collected by the Coriolis (PFU) | |
---|---|---|---|---|---|---|---|
Reference condition (air cleaner off, n = 5) | 154 ± 18 | 63.1 ± 0.3 | 2.01 ± 0.08 | 4.02 × 1010 ± 1.52 × 109 | 2.70 ± 0.07 | 3.40 × 105 ± 3.78 × 105 | 9.29 × 105 ± 9.43 × 105 |
6-module configuration (air cleaner on, n = 5) | 144 ± 19 | 61.7 ± 0.9 | 1.97 ± 0.06 | 3.95 × 1010 ± 1.15 × 109 | 2.73 ± 0.12 | 0 ± 0 | 0 ± 0 |
3-module configuration (air cleaner on, n = 3) | 142 ± 12 | 61.3 ± 0.2 | 1.98 ± 0.07 | 3.96 × 1010 ± 1.35 × 109 | 2.70 ± 0.02 | 3.33 ± 5.77 | 9.07 ± 15.7 |
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Pourchez, J.; Peyron, A.; Sarry, G.; Leclerc, L.; Verhoeven, P.O.; Choi, P.; Pierson, C.; Petit, O.; Hernández, F.; Dumitrescu, C. Antimicrobial Performance of an Innovative Technology of Atmospheric Plasma Reactors against Bioaerosols: Effectiveness in Removing Airborne Viable Viruses. Buildings 2022, 12, 1587. https://doi.org/10.3390/buildings12101587
Pourchez J, Peyron A, Sarry G, Leclerc L, Verhoeven PO, Choi P, Pierson C, Petit O, Hernández F, Dumitrescu C. Antimicrobial Performance of an Innovative Technology of Atmospheric Plasma Reactors against Bioaerosols: Effectiveness in Removing Airborne Viable Viruses. Buildings. 2022; 12(10):1587. https://doi.org/10.3390/buildings12101587
Chicago/Turabian StylePourchez, Jérémie, Aurélien Peyron, Gwendoline Sarry, Lara Leclerc, Paul O. Verhoeven, Peter Choi, Claude Pierson, Olivier Petit, Francisco Hernández, and Carmen Dumitrescu. 2022. "Antimicrobial Performance of an Innovative Technology of Atmospheric Plasma Reactors against Bioaerosols: Effectiveness in Removing Airborne Viable Viruses" Buildings 12, no. 10: 1587. https://doi.org/10.3390/buildings12101587