Disinfection of Phi6, MS2, and Escherichia coli by Natural Sunlight on Healthcare Critical Surfaces

Gabrielle M. String Lancon Environmental, LLC, Cambridge, Massachusetts;
Department of Civil and Environmental Engineering, Tufts University School of Engineering, Medford, Massachusetts

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Yarmina Kamal Lancon Environmental, LLC, Cambridge, Massachusetts;

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Christine Kelly Lancon Environmental, LLC, Cambridge, Massachusetts;

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David M. Gute Department of Civil and Environmental Engineering, Tufts University School of Engineering, Medford, Massachusetts

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Daniele S. Lantagne Lancon Environmental, LLC, Cambridge, Massachusetts;

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ABSTRACT.

Ultraviolet (UV) radiation systems, commonly used to disinfect surfaces, drinking water, and air, stem from historical practice to use sunlight to disinfect household items after contagious illness. Currently, it is still recommended in viral outbreak contexts such as COVID-19, Ebola, and Marburg to expose soft surfaces to sunlight after washing with detergent or disinfecting with chlorine. However, sunlight that reaches the Earth’s surface is in the UVA/UVB wavelengths, whereas UV disinfection systems typically rely on biocidal UVC. Our goal was to fill the evidence gap on the efficacy of sunlight disinfection on surface materials common in low-resource healthcare settings by seeding four surfaces (stainless steel, nitrile, tarp, cloth) with three microorganisms (viral surrogate bacteriophages Phi6 and MS2 and Escherichia coli bacteria), with and without soil load, and exposing to three sunlight conditions (full sun, partial sun, cloudy). We conducted 144 tests in triplicate and found: solar radiation averaged 737 W/m2 (SD = 333), 519 W/m2 (SD = 65), and 149 W/m2 (SD = 24) for full sun, partial sun, and cloudy conditions; significantly more surfaces averaged ≥ 4 log10 reduction value (LRV) for Phi6 than MS2 and E. coli (P < 0.001) after full sun exposure, and no samples achieved ≥ 4 LRV for partial sun or cloudy conditions. On the basis of our results, we recommend no change to current protocols of disinfecting materials first with a 0.5% chlorine solution then moving to sunlight to dry. Additional field-based research is recommended to understand sunlight disinfection efficacy against pathogenic organisms on healthcare relevant surfaces during actual outbreak contexts.

Author Notes

Address correspondence to Gabrielle M. String, Department of Civil and Environmental Engineering, Tufts University, 200 College Ave., Medford, MA, 02155. E-mail: gabrielle.string@tufts.edu

Financial support: This study was made possible by the generous support of the American people through the US Agency for International Development (USAID). The contents are the responsibility of the coauthors and do not necessarily reflect the views of USAID or the U.S. government.

Authors’ addresses: Gabrielle M. String, Lancon Environmental, LLC, Cambridge, MA, and Department of Civil and Environmental Engineering, Tufts University, Medford, MA, E-mail: gabrielle.string@tufts.edu. Yarmina Kamal, Christine Kelly, and Daniele S. Lantagne, Lancon Environmental, LLC, Cambridge, MA, E-mails: yarminakamal@gmail.com, christine.kelly@tufts.edu, and daniele.lantagne@tufts.edu. David M. Gute, Department of Civil and Environmental Engineering, Tufts University, Medford, MA, E-mail: david.gute@tufts.edu.

  • 1.

    Howard G et al., 2020. COVID-19: urgent actions, critical reflections and future relevance of ‘WaSH’: lessons for the current and future pandemics. J Water Health 37: 613630.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Yates T , Vujcic JA , Joseph ML , Gallandat K , Lantagne D , 2018. Water, sanitation, and hygiene interventions in outbreak response: a synthesis of evidence. Waterlines 37: 530.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    WHO , 2020. Water, Sanitation, Hygiene, and Waste Management for SARS-CoV-2, the Virus That Causes COVID-19: Interim Guidance (Report WHO/2019-nCoV/IPC_WASH/2020.4). Geneva, Switzerland: World Health Organization HQ.

    • PubMed
    • Export Citation
  • 4.

    CDC , 2020. Cleaning and Disinfecting Your Home: Everyday Steps and Extra Steps When Someone is Sick. Available at: https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/disinfecting-your-home.html. Accessed February 11, 2020.

    • PubMed
    • Export Citation
  • 5.

    Centers for Disease Control and Prevention , 2008. Guideline for Disinfection and Sterilization in Healthcare Facilities. Available at: https://www.cdc.gov/infectioncontrol/guidelines/disinfection/disinfection-methods/index.html. Accessed February 23, 2022.

    • PubMed
    • Export Citation
  • 6.

    Gøtzsche P , 2011. Niels Finsen’s treatment for lupus vulgaris. J R Soc Med 104: 4142.

  • 7.

    Kowalski W , 2010. Ultraviolet Germicidal Irradiation Handbook: UVGI for Air and Surface Disinfection. Berlin, Germany: Springer Science & Business Media.

    • PubMed
    • Export Citation
  • 8.

    Meulemans CCE , 1987. The basic principles of UV-disinfection of water. Ozone Sci Eng 9: 299313.

  • 9.

    Reed NG , 2010. The history of ultraviolet germicidal irradiation for air disinfection. Public Health Rep 125: 1527.

  • 10.

    Raeiszadeh M , Adeli B , 2020. A critical review on ultraviolet disinfection systems against COVID-19 outbreak: applicability, validation, and safety considerations. ACS Photonics 7: 29412951.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Hessling M , Haag R , Sieber N , Vatter P , 2021. The impact of far-UVC radiation (200–230 nm) on pathogens, cells, skin, and eyes—a collection and analysis of a hundred years of data. GMS Hyg Infect Control 16: Doc07.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Downes A , Blunt TP , 1877. The influence of light upon the development of bacteria 1. Nature 16: 218.

  • 13.

    Nelson KL et al., 2018. Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches. Environ Sci Process Impacts 20: 10891122.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Anderson RK , 1918. Disinfection after communicable disease. Can Med Assoc J 8: 10801083.

  • 15.

    Schneider F , 1913. Disinfection and disinfectants. Public Health J 4: 300302.

  • 16.

    Russell Jas B , 1884. On disinfection. Glasg Med J 22: 401412.

  • 17.

    Ravenel MP , Smith KW , 1909. Disinfection and Commercial Disinfectants. Madison, WI: University of Wisconsin, Agricultural Experiment Station.

    • PubMed
    • Export Citation
  • 18.

    U.S. Food & Drug Administration , 2021. UV Lights and Lamps: Ultraviolet-C Radiation, Disinfection, and Coronavirus. Available at: https://www.fda.gov/medical-devices/coronavirus-covid-19-and-medical-devices/uv-lights-and-lamps-ultraviolet-c-radiation-disinfection-and-coronavirus. Accessed February 1, 2021.

    • PubMed
    • Export Citation
  • 19.

    World Health Organization , Radiation: Ultraviolet (UV) Radiation. Available at: https://www.who.int/news-room/questions-and-answers/item/radiation-ultraviolet-(uv). Accessed February 26, 2022.

    • PubMed
    • Export Citation
  • 20.

    Fahimipour AK et al., 2018. Daylight exposure modulates bacterial communities associated with household dust. Microbiome 6: 175.

  • 21.

    Amichai B , Grunwald MH , Davidovici B , Shemer A , 2014. “Sunlight is said to be the best of disinfectants”: the efficacy of sun exposure for reducing fungal contamination in used clothes. Isr Med Assoc J 16: 431433.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Sharma SK , Mishra M , Mudgal SK , 2020. Efficacy of cloth face mask in prevention of novel coronavirus infection transmission: a systematic review and meta-analysis. J Educ Health Promot 9: 192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Thomson P , 2007. Ebola & Marburg Outbreak Control Guidance Manual Version 2.0. Brussels, Belgium: Médecins Sans Frontières.

    • PubMed
    • Export Citation
  • 24.

    Gallandat K , Lantagne D , 2017. Selection of a Biosafety Level 1 (BSL-1) surrogate to evaluate surface disinfection efficacy in Ebola outbreaks: comparison of four bacteriophages. PLoS One 12: e0177943.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    String GM , White MR , Gute DM , Mühlberger E , Lantagne DS , 2021. Selection of a SARS-CoV-2 surrogate for use in surface disinfection efficacy studies with chlorine and antimicrobial surfaces. Environ Sci Technol Lett 8: 9951001.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Wood JP , Richter W , Sunderman M , Calfee MW , Serre S , Mickelsen L , 2020. Evaluating the environmental persistence and inactivation of MS2 bacteriophage and the presumed Ebola virus surrogate Phi6 using low concentration hydrogen peroxide vapor. Environ Sci Technol 54: 35813590.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Motlagh AM , Yang Z , 2019. Detection and occurrence of indicator organisms and pathogens. Water Environ Res 91: 14021408.

  • 28.

    Kolus RC , Zahrah M , String G , Lantagne DS , 2021. Culturable E. coli as surrogate for culturable V. cholerae in surface disinfection testing with chlorine. J Environ Eng 147: 06021002.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Poranen MM , Mäntynen S , ICTV Report Consortium , 2017. ICTV virus taxonomy profile: Cystoviridae. J Gen Virol 98: 24232424.

  • 30.

    Laurinavičius S , Käkelä R , Bamford DH , Somerharju P , 2004. The origin of phospholipids of the enveloped bacteriophage Phi6. Virology 326: 182190.

  • 31.

    Vidaver AK , Koski RK , Van Etten JL , 1973. Bacteriophage φ6: a lipid-containing virus of Pseudomonas phaseolicola1. J Virol 11: 799805.

  • 32.

    Aquino de Carvalho N , Stachler EN , Cimabue N , Bibby K , 2017. Evaluation of Phi6 persistence and suitability as an enveloped virus surrogate. Environ Sci Technol 51: 86928700.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Ford BE , 2015. Pseudomonas Bacteriophage Phi6 as a Model for Virus Emergence. New York, NY: City University of New York.

  • 34.

    Casanova LM , Waka B , 2013. Survival of a surrogate virus on N95 respirator material. Infect Control Hosp Epidemiol 34: 13341335.

  • 35.

    Vatter P , Hoenes K , Hessling M , 2021. Photoinactivation of the coronavirus surrogate phi6 by Visible Light. Photochem Photobiol 97: 122125.

  • 36.

    Whitworth C , Mu Y , Houston H , Martinez-Smith M , Noble-Wang J , Coulliette-Salmond A , Rose L , 2020. Persistence of bacteriophage Phi 6 on porous and nonporous surfaces and the potential for its use as an Ebola virus or coronavirus surrogate. Appl Environ Microbiol 86: e01482-20.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Prussin AJ , Schwake DO , Lin K , Gallagher DL , Buttling L , Marr LC , 2018. Survival of the enveloped virus Phi6 in droplets as a function of relative humidity, absolute humidity, and temperature. Appl Environ Microbiol 84: e00551-18.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Silverman AI , Boehm AB , 2020. Systematic review and meta-analysis of the persistence and disinfection of human coronaviruses and their viral surrogates in water and wastewater. Environ Sci Technol Lett. doi: 10.1021/acs.estlett.0c00313.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Bedrosian N , Mitchell E , Rohm E , Rothe M , Kelly C , String G , Lantagne D , 2020. A systematic review of surface contamination, stability, and disinfection data on SARS-CoV-2 (through July 10, 2020). Environ Sci Technol 55: 41624173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Adcock NJ , Rice EW , Sivaganesan M , Brown JD , Stallknecht DE , Swayne DE , 2009. The use of bacteriophages of the family Cystoviridae as surrogates for H5N1 highly pathogenic avian influenza viruses in persistence and inactivation studies. J Environ Sci Health Part A Tox Hazard Subst Environ Eng 44: 13621366.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Turgeon N , Toulouse M-J , Martel B , Moineau S , Duchaine C , 2014. Comparison of five bacteriophages as models for viral aerosol studies. Appl Environ Microbiol 80: 42424250.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Casanova LM , Weaver SR , 2015. Evaluation of eluents for the recovery of an enveloped virus from hands by whole-hand sampling. J Appl Microbiol 118: 12101216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Phillpotts RJ , Thomas RJ , Beedham RJ , Platt SD , Vale CA , 2010. The Cystovirus phi6 as a simulant for Venezuelan equine encephalitis virus. Aerobiologia 26: 301309.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Casanova LM , Weaver SR , 2015. Inactivation of an enveloped surrogate virus in human sewage. Environ Sci Technol Lett 2: 7678.

  • 45.

    Wolfe MK , Gallandat K , Daniels K , Desmarais AM , Scheinman P , Lantagne D , 2017. Handwashing and Ebola virus disease outbreaks: a randomized comparison of soap, hand sanitizer, and 0.05% chlorine solutions on the inactivation and removal of model organisms Phi6 and E. coli from hands and persistence in rinse water. PLoS One 12: e0172734.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Gallandat K , Wolfe MK , Lantagne D , 2017. Surface cleaning and disinfection: efficacy assessment of four chlorine types using Escherichia coli and the Ebola surrogate Phi6. Environ Sci Technol 51: 46244631.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Lin K , Marr LC , 2017. Aerosolization of Ebola virus surrogates in wastewater systems. Environ Sci Technol 51: 26692675.

  • 48.

    Strauss JH , Sinsheimer RL , 1963. Purification and properties of bacteriophage MS2 and of its ribonucleic acid. J Mol Biol 7: 4354.

  • 49.

    Valegård K , Liljas L , Fridborg K , Unge T , 1990. The three-dimensional structure of the bacterial virus MS2. Nature 345: 3641.

  • 50.

    Sherchan SP , Snyder SA , Gerba CP , Pepper IL , 2014. Inactivation of MS2 coliphage by UV and hydrogen peroxide: comparison by cultural and molecular methodologies. J Environ Sci Health Part A Tox Hazard Subst Environ Eng 49: 397403.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Julian TR , Leckie JO , Boehm AB , 2010. Virus transfer between fingerpads and fomites. J Appl Microbiol 109: 18681874.

  • 52.

    Julian TR , Trumble JM , Schwab KJ , 2014. Evaluating efficacy of field-generated electrochemical oxidants on disinfection of fomites using bacteriophage MS2 and mouse norovirus MNV-1 as pathogenic virus surrogates. Food Environ Virol 6: 145155.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Bae J , Schwab KJ , 2008. Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Appl Environ Microbiol 74: 477484.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Sickbert-Bennett EE , Weber DJ , Gergen-Teague MF , Sobsey MD , Samsa GP , Rutala WA , 2005. Comparative efficacy of hand hygiene agents in the reduction of bacteria and viruses. Am J Infect Control 33: 6777.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Tung-Thompson G , Libera DA , Koch KL , de los Reyes FL III , Jaykus L-A , 2015. Aerosolization of a human norovirus surrogate, bacteriophage MS2, during simulated vomiting. PLoS One 10: e0134277.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Park GW , Sobsey MD , 2011. Simultaneous comparison of murine norovirus, feline calicivirus, coliphage MS2, and GII.4 norovirus to evaluate the efficacy of sodium hypochlorite against human norovirus on a fecally soiled stainless steel surface. Foodborne Pathog Dis 8: 10051010.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57.

    Park GW , Boston DM , Kase JA , Sampson MN , Sobsey MD , 2007. Evaluation of liquid- and fog-based application of sterilox hypochlorous acid solution for surface inactivation of human norovirus. Appl Environ Microbiol 73: 44634468.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58.

    Wyrzykowska-Ceradini B et al., 2019. The use of bacteriophage MS2 for development and application of a virucide decontamination test method for porous and heavily soiled surfaces. J Appl Microbiol 127: 13151326.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59.

    Coulliette AD , Perry KA , Fisher EM , Edwards JR , Shaffer RE , Noble-Wang J , 2014. MS2 coliphage as a surrogate for 2009 pandemic influenza A (H1N1) virus (pH1N1) in surface survival studies on N95 filtering facepiece respirators. J Int Soc Respir Prot 21: 1422.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60.

    Percival S , Williams D , Percival S , Yates M , Williams D , Chalmers R & Gray N Microbiology of Waterborne Diseases. 2nd ed. London, United Kingdom: Academic Press/Elsevier, 89118.

    • PubMed
    • Export Citation
  • 61.

    Desmarchelier P , Fegan N & Roginski H Encyclopedia of Dairy Sciences. Oxford, United Kingdom: Elsevier, 948954.

  • 62.

    Hu M , Gurtler JB , 2017. Selection of surrogate bacteria for use in food safety challenge studies: a review. J Food Prot 80: 15061536.

  • 63.

    National Research Council (US) Committee on Indicators for Waterborne Pathogens , 2004. Introduction and historical background. Indicators for Waterborne Pathogens. Washington, DC: National Academies Press. Available at: https://www.ncbi.nlm.nih.gov/books/NBK215658/. Accessed February 23, 2022.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 64.

    String GM , Gutiérrez EV , Lantagne DS , 2020. Laboratory efficacy of surface disinfection using chlorine against Vibrio cholerae. J Water Health 18: 10091019.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65.

    ASTM E35 Committee , 2018. E2197: Quantitative Disk Carrier Test Method for Determining Bactericidal, Virucidal, Fungicidal, Mycobactericidal, and Sporicidal Activities of Chemicals. West Conschohocken, PA: ASTM International.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66.

    Adams M , 1959. Bacteriophages. New York, NY: Interscience Publishers, division of John Wiley & Sons, Inc.

  • 67.

    Rossi P , Aragno M & Muller I. Advances in Biological Tracer Techniques for Hydrology and Hydrogeology Using Bacteriophages: Optimization of the Methods and Investigation of the Behavior of Bacterial Viruses in Surface Waters and in Porous and Fractured Aquifers. Université de Neuchâtel, Neuchâtel, Switzerland. Available at: http://doc.rero.ch/record/2576. Accessed March 10, 2021.

    • PubMed
    • Export Citation
  • 68.

    Bonilla N , Rojas MI , Cruz GNF , Hung S-H , Rohwer F , Barr JJ , 2016. Phage on tap–a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ 4: e2261.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69.

    U.S. Environmental Protection Agency Office of Chemical Safety and Pollution , 2018. Product Performance Test Guidelines. OCSPP 810.2200: Disinfectants for Use on Environmental Surfaces. Guidance for Efficacy Testing. Washington, DC: US EPA.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70.

    Darnell MER , Subbarao K , Feinstone SM , Taylor DR , 2004. Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV. J Virol Methods 121: 8591.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71.

    Ratnesar-Shumate S et al., 2020. Simulated sunlight rapidly inactivates SARS-CoV-2 on surfaces. J Infect Dis 222: 214222.

  • 72.

    Lytle CD , Sagripanti J-L , 2005. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol 79: 1424414252.

  • 73.

    Sinton LW , Hall CH , Lynch PA , Davies-Colley RJ , 2002. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl Environ Microbiol 68: 11221131.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 74.

    Silverman AI , Peterson BM , Boehm AB , McNeill K , Nelson KL , 2013. Sunlight inactivation of human viruses and bacteriophages in coastal waters containing natural photosensitizers. Environ Sci Technol 47: 18701878.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 75.

    Wigginton KR , Kohn T , 2012. Virus disinfection mechanisms: the role of virus composition, structure, and function. Curr Opin Virol 2: 8489.

  • 76.

    Malayeri AH , Mohseni M , Cairns B , Bolton J , 2016. Fluence (UV Dose) Required to Achieve Incremental Log Inactivation of Bacteria, Protozoa, Viruses, and Algae. London, Canada: Trojan Technologies.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 77.

    Samoili S , Farinelli G , Moreno-SanSegundo , McGuigan KG , Marugán J , Pulgarín C , Giannakis S , 2022. Predicting the bactericidal efficacy of solar disinfection (SODIS): from kinetic modeling of in vitro tests towards the in silico forecast of E. coli inactivation. Chem Eng J 427: 130866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 78.

    Silverman AI , Nelson KL , 2016. Modeling the endogenous sunlight inactivation rates of laboratory strain and wastewater E. coli and enterococci using biological weighting functions. Environ Sci Technol 50: 1229212301.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 79.

    Bolton JR , Mayor-Smith I , Linden KG , 2015. Rethinking the concepts of fluence (UV dose) and fluence rate: the importance of photon-based units—a systemic review. Photochem Photobiol 91: 12521262.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 80.

    Apogee Instruments , Silicon Cell Pyranometer Support. Available at: https://www.apogeeinstruments.com/silicon-cell-pyranometer-support/. Accessed February 26, 2022.

    • PubMed
    • Export Citation
  • 81.

    Tuladhar E , Hazeleger WC , Koopmans M , Zwietering MH , Beumer RR , Duizer E , 2012. Residual viral and bacterial contamination of surfaces after cleaning and disinfection. Appl Environ Microbiol 78: 77697775.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 82.

    Kragh KN , Alhede M , Rybtke M , Stavnsberg C , Jensen , Tolker-Nielsen T , Whiteley M , Bjarnsholt T , 2018. The inoculation method could impact the outcome of microbiological experiments. Appl Environ Microbiol 84: e02264-17.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 83.

    Best Practices in Microbiological Methodology Task Force , 2006. Uncertainty Associated with Microbiological Analysis. Rockville, MD: AOAC Methods—US Environmental Protection Agency.

    • PubMed
    • Export Citation
  • 84.

    Parker AE , Hamilton MA , Goeres DM , 2018. Reproducibility of antimicrobial test methods. Sci Rep 8: 12531.

  • 85.

    Sloan A et al., 2021. Simulated sunlight decreases the viability of SARS-CoV-2 in mucus. PLoS One 16: e0253068.

  • 86.

    Sagripanti J-L , Lytle CD , 2011. Sensitivity to ultraviolet radiation of Lassa, vaccinia, and Ebola viruses dried on surfaces. Arch Virol 156: 489494.

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