Norovirus recovery from floors and air after various decontamination protocols



      The dispersal of airborne norovirus (NoV) particles from the floor after contamination with faeces or vomit is a challenge for infection control, as this pathogen is infectious at low doses. Therefore, it is imperative to establish a safe protocol for floor decontamination.


      To assess the presence of residual NoV-GII particles on floors and airborne particles following various floor decontamination procedures.


      Two types of floor (vinyl and granite) were contaminated intentionally with 10% human faeces, positive for NoV-GII. Two decontamination protocols were implemented: cleaning followed by disinfection using 1% sodium hypochlorite, and cleaning followed by disinfection using a manual ultraviolet C (UV-C) light device. Swab samples were taken from the floors, and air samples were obtained using an air sampler. The TaqMan method for real-time reverse transcription-quantitative polymerase chain reaction was employed for analysis.


      The disinfection protocol using 1% sodium hypochlorite after cleaning proved to be more effective than cleaning followed by UV-C light exposure (P<0.001). Viral particles were detected in 27 of 36 air samples after cleaning, with no significant difference between the two floor types. On average, 617 genome copies/sample were identified in air samples after cleaning, but the number decreased gradually after disinfection.


      NoV-GII can be aerosolized during floor cleaning, and its particles may be inhaled and then swallowed or can settle on surfaces. Therefore, residual viral particles on floors must be fully eliminated. Cleaning followed by 10 min of 1% sodium hypochlorite disinfection proved to be the superior decontamination protocol.


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Journal of Hospital Infection
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Morillo S.G.
        • Luchs A.
        • Cilli A.
        • Ribeiro C.D.
        • Carmona R.D.C.C.
        • Timenetsky M.D.C.S.T.
        Norovirus GII. Pe genotype: tracking a foodborne outbreak on a cruise ship through molecular epidemiology, Brazil, 2014.
        Food Environ Virol. 2017; 9: 142-148
        • Cheesbrough J.S.
        • Green J.
        • Gallimore C.I.
        • Wright P.A.
        • Brown D.W.
        Widespread environmental contamination with Norwalk-like viruses (NLV) detected in a prolonged hotel outbreak of gastroenteritis.
        Epidemiol Infect. 2000; 125: 93-98
        • Nenonen N.P.
        • Hannoun C.
        • Svensson L.
        • Toren K.
        • Andersson L.M.
        • Westin J.
        • et al.
        Norovirus GII.4 detection in environmental samples from patient rooms during nosocomial outbreaks.
        J Clin Microbiol. 2014; 52: 2352-2358
        • Bonifait L.
        • Charlebois R.
        • Vimont A.
        • Turgeon N.
        • Veillette M.
        • Longtin Y.
        • et al.
        Detection and quantification of airborne norovirus during outbreaks in healthcare facilities.
        Clin Infect Dis. 2015; 61: 299-304
        • Tung-Thompson G.
        • Gentry-Shields J.
        • Fraser A.
        • Jaykus L.A.
        Persistence of human norovirus RT-qPCR signals in simulated gastric fluid.
        Food Environ Virol. 2015; 7: 32-40
        • Morawska L.
        Droplet fate in indoor environments, or can we prevent the spread of infection?.
        Indoor Air. 2006; 16: 335-347
        • Verreault D.
        • Moineau S.
        • Duchaine C.
        Methods for sampling of airborne viruses.
        Microbiol Mol Biol Rev. 2008; 72: 413-444
        • Hobday R.A.
        • Dancer S.J.
        Roles of sunlight and natural ventilation for controlling infection: historical and current perspectives.
        J Hosp Infect. 2013; 84: 271-282
        • Marks P.J.
        • Vipond I.B.
        • Regan F.M.
        • Wedgwood K.
        • Fey R.E.
        • Caul E.O.
        A school outbreak of Norwalk-like virus: evidence for airborne transmission.
        Epidemiol Infect. 2003; 131: 727-736
        • Marks P.J.
        • Vipond I.B.
        • Carlisle D.
        • Deakin D.
        • Fey R.E.
        • Caul E.O.
        Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant.
        Epidemiol Infect. 2000; 124: 481-487
        • Repp K.K.
        • Keene W.E.
        A point-source norovirus outbreak caused by exposure to fomites.
        J Infect Dis. 2012; 205: 1639-1641
        • Otter J.A.
        • Donskey C.
        • Yezli S.
        • Douthwaite S.
        • Goldenberg S.D.
        • Weber D.J.
        Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination.
        J Hosp Infect. 2016; 92: 235-250
        • Weber D.J.
        • Anderson D.
        • Rutala W.A.
        The role of the surface environment in healthcare-associated infections.
        Curr Opin Infect Dis. 2013; 26: 338-344
        • Caul E.O.
        Small round structured viruses: airborne transmission and hospital control.
        Lancet. 1994; 343: 1240-1242
        • Kramer A.
        • Schwebke I.
        • Kampf G.
        How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
        BMC Infect Dis. 2006; 6: 130
        • Tung G.
        • Macinga D.
        • Arbogast J.
        • Jaykus L.A.
        Efficacy of commonly used disinfectants for inactivation of human noroviruses and their surrogates.
        J Food Prot. 2013; 76: 1210-1217
        • Barker J.
        • Vipond I.B.
        • Bloomfield S.F.
        Effects of cleaning and disinfection in reducing the spread of norovirus contamination via environmental surfaces.
        J Hosp Infect. 2004; 58: 42-49
        • Booth C.M.
        Vomiting Larry: a simulated vomiting system for assessing environmental contamination from projectile vomiting related to norovirus infection.
        J Infect Prev. 2014; 15: 176-180
        • United States Pharmacopeia
        The United States pharmacopeia 39. The national formulary 34 (USP 39-NF 34).
        Microbiological examination of nonsterile products: microbial enumeration tests. c. 61. United States Pharmacopeia Convention, Rockville, MD2016
        • Hedin G.
        • Rynback J.
        • Lore B.
        New technique to take samples from environmental surfaces using flocked nylon swabs.
        J Hosp Infect. 2010; 75: 314-317
        • Kageyama T.
        • Kojima S.
        • Shinohara M.
        • Uchida K.
        • Fukushi S.
        • Hoshino F.B.
        • et al.
        Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR.
        J Clin Microbiol. 2003; 41: 1548-1557
        • Rashid T.
        • Vonville H.
        • Hasan I.
        • Garey K.W.
        Mechanisms for floor surfaces or environmental ground contamination to cause human infection: a systematic review.
        Epidemiol Infect. 2017; 145: 347-357
        • Koganti S.
        • Alhmidi H.
        • Tomas M.E.
        • Cadnum J.L.
        • Jencson A.
        • Donskey C.J.
        Evaluation of hospital floors as a potential source of pathogen dissemination using a nonpathogenic virus as a surrogate marker.
        Infect Control Hosp Epidemiol. 2016; 37: 1374-1377
        • Mahida N.
        • Boswell T.
        Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?.
        J Hosp Infect. 2016; 94: 273-275
        • Galvin J.
        • Almatroudi A.
        • Vickery K.
        • Deva A.
        • Lopes L.K.
        • Costa D.M.
        • et al.
        Patient shoe covers: transferring bacteria from the floor onto surgical bedsheets.
        Am J Infect Control. 2016; 44: 1417-1419
        • Ayliffe G.A.
        • Collins B.J.
        • Lowbury E.J.
        Cleaning and disinfection of hospital floors.
        Br Med J. 1966; 2: 442-445
        • Sattar S.A.
        • Bradley C.
        • Kibbee R.
        • Wesgate R.
        • Wilkinson M.A.
        • Sharpe T.
        • et al.
        Disinfectant wipes are appropriate to control microbial bioburden from surfaces: use of a new ASTM standard test protocol to demonstrate efficacy.
        J Hosp Infect. 2015; 91: 319-325
        • Ray A.J.
        • Deshpande A.
        • Fertelli D.
        • Sitzlar B.M.
        • Thota P.
        • Sankar C.T.
        • et al.
        A multicenter randomized trial to determine the effect of an environmental disinfection intervention on the incidence of healthcare-associated clostridium difficile infection.
        Infect Control Hosp Epidemiol. 2017; 38: 777-783
        • Tuladhar E.
        • Hazeleger W.C.
        • Koopmans M.
        • Zwietering M.H.
        • Beumer R.R.
        • Duizer E.
        Residual viral and bacterial contamination of surfaces after cleaning and disinfection.
        Appl Environ Microbiol. 2012; 78: 7769-7775
        • Cook N.
        • Knight A.
        • Richards G.P.
        Persistence and elimination of human norovirus in food and on food contact surfaces: a critical review.
        J Food Prot. 2016; 79: 1273-1294
        • Dancer S.J.
        Dos and don'ts for hospital cleaning.
        Curr Opin Infect Dis. 2016; 29: 415-423
        • Weber D.J.
        • Rutala W.A.
        • Anderson D.J.
        • Chen L.F.
        • Sickbert-Bennett E.E.
        • Boyce J.M.
        Effectiveness of ultraviolet devices and hydrogen peroxide systems for terminal room decontamination: focus on clinical trials.
        Am J Infect Control. 2016; 44: e77-e84
        • Ronnqvist M.
        • Mikkela 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
        • Oristo S.
        • Lee H.J.
        • Maunula L.
        Performance of pre-RT-qPCR treatments to discriminate infectious human rotaviruses and noroviruses from heat-inactivated viruses: applications of PMA/PMAxx, benzonase and RNase.
        J Appl Microbiol. 2018; 124: 1008-1016
        • Ettayebi K.
        • Crawford S.E.
        • Murakami K.
        • Broughman J.R.
        • Karandikar U.
        • Tenge V.R.
        • et al.
        Replication of human noroviruses in stem cell-derived human enteroids.
        Science. 2016; 353: 1387-1393
        • Costantini V.
        • Morantz E.K.
        • Browne H.
        • Ettayebi K.
        • Zeng X.L.
        • Atmar R.L.
        • et al.
        Human norovirus replication in human intestinal enteroids as model to evaluate virus inactivation.
        Emerg Infect Dis. 2018; 24: 1453-1464
        • Paton S.
        • Thompson K.A.
        • Parks S.R.
        • Bennett A.M.
        Reaerosolization of spores from flooring surfaces to assess the risk of dissemination and transmission of infections.
        Appl Environ Microbiol. 2015; 81: 4914-4919
        • Verstraeten T.
        • Jiang B.
        • Weil J.G.
        • Lin J.H.
        Modelling estimates of norovirus disease in patients with chronic medical conditions.
        PLoS One. 2016; 11e0158822
      1. American Society of Heating Refrigerating and Air-Conditioning Engineers. Infection control.
        in: Handbook heating, ventilating, and air-conditioning applications. ASHRAE, Atlanta, GA2013: 19-34
        • Price E.H.
        • Ayliffe G.
        Hot hospitals and what happened to wash, rinse and dry? Recent changes to cleaning, disinfection and environmental ventilation.
        J Hosp Infect. 2008; 69: 89-91
        • Escombe A.R.
        • Ticona E.
        • Chavez-Perez V.
        • Espinoza M.
        • Moore D.A.J.
        Improving natural ventilation in hospital waiting and consulting rooms to reduce nosocomial tuberculosis transmission risk in a low resource setting.
        BMC Infect Dis. 2019; 19: 88
        • Gilkeson C.A.
        • Camargo-Valero M.A.
        • Pickin L.E.
        • Noakes C.J.
        Measurement of ventilation and airborne infection risk in large naturally ventilated hospital wards.
        Build Environ. 2013; 65: 35-48