- Email: [email protected]
The survival of influenza A(H1N1)pdm09 virus on 4 household surfaces
American Journal of Infection Control 42 (2014) 423-5
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
The survival of influenza A(H1N1)pdm09 virus on 4 household surfaces John Oxford PSc a, *, Eitan N. Berezin MD, PhD b, c, Patrice Courvalin MD d, Dominic E. Dwyer MD e, Martin Exner PhD f, Laura A. Jana MD g, Mitsuo Kaku MD, PhD h, Christopher Lee FRCP i, Kgosi Letlape FCS(Ophth), FRCS(Ophth) j, k, Donald E. Low MD l, Tariq Ahmed Madani MD, FRCPC m, Joseph R. Rubino MA n, Narendra Saini MD o, Barry D. Schoub MD, DSc, FRCPath p, q, Carlo Signorelli PhD r, s, Philip M. Tierno PhD t, Xuhui Zhong MD u a
Blizard Institute of Cell and Molecular Science, St Barts and The London School of Medicine and Dentistry, London, United Kingdom Faculdade de Ciencias Medicas, Santa Casa, Sao Paulo, Brazil c Infectious Diseases Society, Sao Paulo, Brazil d Institut Pasteur, Paris, France e Centre for Infectious Diseases and Microbiology and Institute for Clinical Pathology and Medical Research, Westmead Hospital and University of Sydney, Westmead, New South Wales, Australia f Institute of Hygiene and Public Health, University of Bonn, Bonn, Germany g Practical Parenting Consulting, Omaha, NE h Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan i Sungai Buloh Hospital, Sungai Buloh, Selangor, Malaysia j Africa Medical Association, Pretoria, South Africa k Tshepang Trust, Johannesburg, South Africa l Ontario Agency for Health Protection and Promotion, Toronto, Ontario, Canada m Department of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia n Research & Development, Reckitt Benckiser, Montvale, NJ o Pushpanjali Crosslay Hospital, Uttar Pradesh, India p University of the Witwatersrand, Johannesburg, South Africa q National Institute for Communicable Diseases, Johannesburg, South Africa r Public Health Unit, University of Parma, Parma, Italy s Italian Society of Hygiene, Preventive Medicine and Public Health, Rome, Italy t New York University Langone Medical Center and School of Medicine, New York, NY u Peking University First Hospital, Beijing, China b
Key Words: Home Hygiene Handwashing Cleaning Wood Cloth Stainless steel Plastic Infection Transmission
We investigated the survival of a pandemic strain of influenza A H1N1 on a variety of common household surfaces where multiple samples were taken from 4 types of common household fomite at 7 time points. Results showed that influenza A H1N1sw virus particles remained infectious for 48 hours on a wooden surface, for 24 hours on stainless steel and plastic surfaces, and for 8 hours on a cloth surface, although virus recovery from the cloth may have been suboptimal. Our results suggest that pandemic influenza A H1N1 can survive on common household fomites for extended periods of time, and that good hand hygiene and regular disinfection of commonly touched surfaces should be practiced during the influenza season to help reduce transmission. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
* Address correspondence to John Oxford, Blizard Institute of Cell and Molecular Science, St Barts and The London School of Medicine and Dentistry, 4 Newark St, London, E1 2AT, United Kingdom. E-mail address: [email protected] (J. Oxford). This study was performed on behalf of the Global Hygiene Council by Retroscreen Virology Ltd with financial support from Reckitt Benckiser, Montvale, NJ. Conflicts of interest: None to report.
Influenza is a major cause of morbidity worldwide, and occurs in annual epidemics that cause mortality in at-risk populations such as the young and elderly, as well as those with other underlying illnesses.1 Influenza also has the potential to cause pandemics, and the emergence of a novel strain of influenza A H1N1 from swine (ie, influenza A[H1N1]pdm09) during April 2009 signaled the start
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.10.016
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J. Oxford et al. / American Journal of Infection Control 42 (2014) 423-5
of the first pandemic of the 21st century.2 By August 2010, the pandemic influenza strain had been reported in more than 214 countries worldwide and was estimated to have caused at least 18,450 deaths.3 More recent estimates suggest that the pandemic flu caused up to 575,500 deaths globally.4 The major route of transmission for influenza is via inhalation of aerosolized droplets.5 However, a number of studies have shown that influenza virus can survive on surfacesdor fomitesdfor extended periods of time, and may be spread from these to the hands and then into the respiratory tract when individuals touch their eyes or nose.6,7 Thus, the presence of influenza viruses on household surfaces may play a role in the spread of infection, and methods to prevent this route of transmission should be investigated. Our in vitro study was conducted to investigate the survival of viable influenza A(H1N1)pdm09 virus particles on a range of common household surfaces under laboratory conditions. METHODS The surfaces tested were wooden chopping boards, cotton pillowcases, stainless steel sheets, and plastic toy ducks. Sufficient identical test items were purchased to allow for multiple samples to be taken at 7 time points on each surface. All test items were newly purchased from local shops. The challenge virus was NIBRG-121sw (strain A/California/7/ 2009) obtained from the reference collection of the UK National Institute for Biological Standards and Control. The challenge virus had been passaged 3 times in allantoic fluid and had a stock titer of approximately 5.5 log10 (the dose that is infective in 50% of tissue culture samples) per milliliter. Squares measuring 4 4 cm were marked on each of the items to be tested using a marker pen. One square was drawn for each of 7 time points (0, 1, 8, 24, 48, 60, and 72 hours). Undiluted influenza virus from the stock (500 mL) was pipetted onto the surface within the marked area and spread using a pipette tip to cover the area. The test items were then left in a class 2 cabinet at room temperature until the designated time point (ie, up to 72 hours). At each time point, 1 mL culture medium (Influenza Virus Infection Media; Retroscreen Virology Ltd, London, UK) was used to rinse the surface of 1 of the marked squares and was collected. This was done with a single channel pipette that was primed using culture medium. The medium was expelled onto the surface ensuring coverage of the marked area. This was then taken off the surface using the same pipette and transferred to an appropriate container. It was also recorded if the virus was damp or dry on the surface at the time of virus recovery. Each experiment was performed in quadruplicate as was the titration for residual virus infectivity. The viability of the influenza virus was determined by infection of Madin Darby Canine Kidney (MDCK) cells, followed by determination of virus titers using the hemagglutination (HA) assay. MDCK cells were seeded in 96-well plates at a density of w5 104 cells/mL, and incubated at 37 C (2 C) with 5% carbon dioxide in MDCK growth medium for w24 hours, or until 70%-80% confluent. Before use in the assay, growth medium was removed from the cells and replaced with 100 mL/well of influenza infection media. A proportion (111 mL) of the recovered virus sample was inoculated onto the first row of MDCK cells and serially diluted 10-fold across the plate (11 mL titrated from the first well to subsequent wells containing 100 mL infection media). Inoculated cells were incubated at 37 C (2 C) with 5% carbon dioxide for 3 days; the titer of the recovered virus was then determined using the HA assay. Materials were not heat and chemically sterilized to avoid structural changes. There were no issues of inherent cytotoxicity of these materials.
Fig 1. Influenza A(H1N1)pdm09 virus recovery from 4 surfaces over time. TCID50, the dose that is infective in 50% of tissue culture samples.
For the HA assay, 50 mL supernatant from the titration plate were transferred to a 96-well plate; 50 mL turkey red blood cells at 0.5% vol/vol were then added. The plates were incubated at room temperature for 30 minutes and then examined for hemagglutination. Appropriate positive and negative controls were used at each stage. From the HA assay, the dose that is infective in 50% of tissue culture samples per milliliter for each test surface and the controls was calculated using the Karber Calculation. RESULTS Survival of the influenza A H1N1sw virus decreased most rapidly on the cloth surface, with no infectious virus particles being recovered after 8 hours (Fig 1). In Figure 1 the data are represented as residual virus infectivity. Influenza A/H1N1sw virus particles survived for the longest time on the wooden surface, with infectious virus particles still being recovered after 48 hours. Survival of the virus on stainless steel and plastic was intermediate between cloth and wood, with detectable infectious virus particles at 24 hours but not at 48 hours. DISCUSSION Of the 4 surfaces tested, influenza A(H1N1)pdm09 virus particles survived longest on the wood, and for the shortest time on the cloth. The immediate decline in infectivity at time 0 in the samples recovered from the cloth suggests that the technique used to elute the virus may not have been effective on this surface (or that inhibitory substances were present in the fibers). Previous studies have shown that influenza virus particles lose infectivity less rapidly on nonporous surfaces compared with porous ones,7-9 but it has also been acknowledged that this could be due to inefficient recovery of virus particles from the porous surfaces.8 The findings of our study are supported by the literature. Bean et al7 reported that influenza A and B virus particles remained viable for 24-48 hours on stainless steel or plastic, but survived for less than 8-12 hours on cloth; findings very closely mirrored in our study. Tiwari et al8 found that avian influenza virus particles could survive on nonporous surfaces for up to 6 days. More recently, Greatorex et al9 have shown that a pandemic strain of influenza A/ H1N1 did not remain viable for >9 hours on a range of household surfaces. However, surfaces allowing the viruses to survive the longest included plastic and stainless steel, in agreement with our study. In contrast to our study, wooden surfaces did not support viral survival, with virus inoculates becoming inactivated after <4 hours. The difference in these findings may be due to the various types of wood tested, or may be related to the experimental procedures.
J. Oxford et al. / American Journal of Infection Control 42 (2014) 423-5
Previous studies have shown transmission of influenza via contact with virus particles on fomites. Measurable quantities of influenza A could be transferred from stainless steel to hands for a period of 24 hours after surface contamination, and from tissues to hands for up to 15 minutes after contamination.7 Boone et al6 showed that 59% of fomites tested in homes during the influenza season had detectable influenza virus, and Simmerman et al10 showed that 17.8% of household surfaces were positive for influenza A H1N1 in households with infected children during the 2009 H1N1 pandemic. This suggests that fomites play an important role in the spread of influenza.5 How can contamination of influenza virus on surfaces be reduced? Regular handwashing can reduce fomite contamination. In the study by Simmerman et al,10 households randomized to a handwashing protocol had a lower prevalence of fomites contaminated with influenza A(H1N1)pdm09 (11.1%) than control households (24.4%) (P ¼ .09). In terms of destroying influenza A H1N1 on fomites directly, a study by Greatorex et al1 demonstrated that simple household products, such as 1% bleach, 10% vinegar, and 0.01% washing-up liquid, as well as antibacterial wipes and antiviral tissues, were all highly effective at reducing virus infectivity. CONCLUSIONS Our study has demonstrated that the influenza A(H1N1) pdm09 virus can survive on cloth for at least 8 hours on stainless steel and plastic for up to 24 hours, and on wood for up to 48 hours. All of these surfaces are commonly found in households, and could potentially act as fomites for influenza virus transmission amongst household members. To prevent or reduce contamination of surfaces with influenza virus during the influenza season, it is recommended that individuals pay particular
425
attention to good hand hygiene and clean and disinfect frequently touched surfaces.
Acknowledgments The authors thank Toby Allinson for providing editorial assistance during the preparation of the manuscript.
References 1. Greatorex JS, Page RF, Curran MD, Digard P, Enstone JE, Wreghitt T, et al. Effectiveness of common household cleaning agents in reducing the viability of human influenza A/H1N1. PLoS One 2010;5:e8987. 2. World Health Organization. World now at the start of 2009 influenza pandemic. 2009. Available from: http://www.who.int/mediacentre/news/statements/ 2009/h1n1_pandemic_phase6_20090611/en/. Accessed November 15, 2013. 3. World Health Organization. Global Alert and Response (GAR): pandemic (H1N1) 2009 e update 112. 2010. Available from: http://www.who.int/csr/don/ 2010_08_06/en/index.html. Accessed November 15, 2013. 4. Dawood FS, Iuliano AD, Reed C, Meltzer MI, Shay DK, Cheg PY, et al. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 2012;12: 687-95. 5. Boone SA, Gerba CP. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol 2007;73:1687-96. 6. Boone SA, Gerba CP. The occurrence of influenza A virus on household and day care center fomites. J Infect 2005;51:103-9. 7. Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH Jr. Survival of influenza viruses on environmental surfaces. J Infect Dis 1982;146:47-51. 8. Tiwari A, Patnayak DP, Chander Y, Parsad M, Goyal SM. Survival of two avian respiratory viruses on porous and nonporous surfaces. Avian Dis 2006;50:284-7. 9. Greatorex JS, Digard P, Curran MD, Moynihan R, Wensley H, Wreghitt T, et al. Survival of influenza A(H1N1) on materials found in households: implications for infection control. PLoS One 2011;6:e27932. 10. Simmerman JM, Suntarattiwong P, Levy J, Gibbons RV, Cruz C, Shaman J, et al. Influenza virus contamination of common household surfaces during the 2009 influenza A (H1N1) pandemic in Bangkok, Thailand: implications for contact transmission. Clin Infect Dis 2010;51:1053-61.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
The survival of influenza A(H1N1)pdm09 virus on 4 household surfaces John Oxford PSc a, *, Eitan N. Berezin MD, PhD b, c, Patrice Courvalin MD d, Dominic E. Dwyer MD e, Martin Exner PhD f, Laura A. Jana MD g, Mitsuo Kaku MD, PhD h, Christopher Lee FRCP i, Kgosi Letlape FCS(Ophth), FRCS(Ophth) j, k, Donald E. Low MD l, Tariq Ahmed Madani MD, FRCPC m, Joseph R. Rubino MA n, Narendra Saini MD o, Barry D. Schoub MD, DSc, FRCPath p, q, Carlo Signorelli PhD r, s, Philip M. Tierno PhD t, Xuhui Zhong MD u a
Blizard Institute of Cell and Molecular Science, St Barts and The London School of Medicine and Dentistry, London, United Kingdom Faculdade de Ciencias Medicas, Santa Casa, Sao Paulo, Brazil c Infectious Diseases Society, Sao Paulo, Brazil d Institut Pasteur, Paris, France e Centre for Infectious Diseases and Microbiology and Institute for Clinical Pathology and Medical Research, Westmead Hospital and University of Sydney, Westmead, New South Wales, Australia f Institute of Hygiene and Public Health, University of Bonn, Bonn, Germany g Practical Parenting Consulting, Omaha, NE h Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan i Sungai Buloh Hospital, Sungai Buloh, Selangor, Malaysia j Africa Medical Association, Pretoria, South Africa k Tshepang Trust, Johannesburg, South Africa l Ontario Agency for Health Protection and Promotion, Toronto, Ontario, Canada m Department of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia n Research & Development, Reckitt Benckiser, Montvale, NJ o Pushpanjali Crosslay Hospital, Uttar Pradesh, India p University of the Witwatersrand, Johannesburg, South Africa q National Institute for Communicable Diseases, Johannesburg, South Africa r Public Health Unit, University of Parma, Parma, Italy s Italian Society of Hygiene, Preventive Medicine and Public Health, Rome, Italy t New York University Langone Medical Center and School of Medicine, New York, NY u Peking University First Hospital, Beijing, China b
Key Words: Home Hygiene Handwashing Cleaning Wood Cloth Stainless steel Plastic Infection Transmission
We investigated the survival of a pandemic strain of influenza A H1N1 on a variety of common household surfaces where multiple samples were taken from 4 types of common household fomite at 7 time points. Results showed that influenza A H1N1sw virus particles remained infectious for 48 hours on a wooden surface, for 24 hours on stainless steel and plastic surfaces, and for 8 hours on a cloth surface, although virus recovery from the cloth may have been suboptimal. Our results suggest that pandemic influenza A H1N1 can survive on common household fomites for extended periods of time, and that good hand hygiene and regular disinfection of commonly touched surfaces should be practiced during the influenza season to help reduce transmission. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
* Address correspondence to John Oxford, Blizard Institute of Cell and Molecular Science, St Barts and The London School of Medicine and Dentistry, 4 Newark St, London, E1 2AT, United Kingdom. E-mail address: [email protected] (J. Oxford). This study was performed on behalf of the Global Hygiene Council by Retroscreen Virology Ltd with financial support from Reckitt Benckiser, Montvale, NJ. Conflicts of interest: None to report.
Influenza is a major cause of morbidity worldwide, and occurs in annual epidemics that cause mortality in at-risk populations such as the young and elderly, as well as those with other underlying illnesses.1 Influenza also has the potential to cause pandemics, and the emergence of a novel strain of influenza A H1N1 from swine (ie, influenza A[H1N1]pdm09) during April 2009 signaled the start
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.10.016
424
J. Oxford et al. / American Journal of Infection Control 42 (2014) 423-5
of the first pandemic of the 21st century.2 By August 2010, the pandemic influenza strain had been reported in more than 214 countries worldwide and was estimated to have caused at least 18,450 deaths.3 More recent estimates suggest that the pandemic flu caused up to 575,500 deaths globally.4 The major route of transmission for influenza is via inhalation of aerosolized droplets.5 However, a number of studies have shown that influenza virus can survive on surfacesdor fomitesdfor extended periods of time, and may be spread from these to the hands and then into the respiratory tract when individuals touch their eyes or nose.6,7 Thus, the presence of influenza viruses on household surfaces may play a role in the spread of infection, and methods to prevent this route of transmission should be investigated. Our in vitro study was conducted to investigate the survival of viable influenza A(H1N1)pdm09 virus particles on a range of common household surfaces under laboratory conditions. METHODS The surfaces tested were wooden chopping boards, cotton pillowcases, stainless steel sheets, and plastic toy ducks. Sufficient identical test items were purchased to allow for multiple samples to be taken at 7 time points on each surface. All test items were newly purchased from local shops. The challenge virus was NIBRG-121sw (strain A/California/7/ 2009) obtained from the reference collection of the UK National Institute for Biological Standards and Control. The challenge virus had been passaged 3 times in allantoic fluid and had a stock titer of approximately 5.5 log10 (the dose that is infective in 50% of tissue culture samples) per milliliter. Squares measuring 4 4 cm were marked on each of the items to be tested using a marker pen. One square was drawn for each of 7 time points (0, 1, 8, 24, 48, 60, and 72 hours). Undiluted influenza virus from the stock (500 mL) was pipetted onto the surface within the marked area and spread using a pipette tip to cover the area. The test items were then left in a class 2 cabinet at room temperature until the designated time point (ie, up to 72 hours). At each time point, 1 mL culture medium (Influenza Virus Infection Media; Retroscreen Virology Ltd, London, UK) was used to rinse the surface of 1 of the marked squares and was collected. This was done with a single channel pipette that was primed using culture medium. The medium was expelled onto the surface ensuring coverage of the marked area. This was then taken off the surface using the same pipette and transferred to an appropriate container. It was also recorded if the virus was damp or dry on the surface at the time of virus recovery. Each experiment was performed in quadruplicate as was the titration for residual virus infectivity. The viability of the influenza virus was determined by infection of Madin Darby Canine Kidney (MDCK) cells, followed by determination of virus titers using the hemagglutination (HA) assay. MDCK cells were seeded in 96-well plates at a density of w5 104 cells/mL, and incubated at 37 C (2 C) with 5% carbon dioxide in MDCK growth medium for w24 hours, or until 70%-80% confluent. Before use in the assay, growth medium was removed from the cells and replaced with 100 mL/well of influenza infection media. A proportion (111 mL) of the recovered virus sample was inoculated onto the first row of MDCK cells and serially diluted 10-fold across the plate (11 mL titrated from the first well to subsequent wells containing 100 mL infection media). Inoculated cells were incubated at 37 C (2 C) with 5% carbon dioxide for 3 days; the titer of the recovered virus was then determined using the HA assay. Materials were not heat and chemically sterilized to avoid structural changes. There were no issues of inherent cytotoxicity of these materials.
Fig 1. Influenza A(H1N1)pdm09 virus recovery from 4 surfaces over time. TCID50, the dose that is infective in 50% of tissue culture samples.
For the HA assay, 50 mL supernatant from the titration plate were transferred to a 96-well plate; 50 mL turkey red blood cells at 0.5% vol/vol were then added. The plates were incubated at room temperature for 30 minutes and then examined for hemagglutination. Appropriate positive and negative controls were used at each stage. From the HA assay, the dose that is infective in 50% of tissue culture samples per milliliter for each test surface and the controls was calculated using the Karber Calculation. RESULTS Survival of the influenza A H1N1sw virus decreased most rapidly on the cloth surface, with no infectious virus particles being recovered after 8 hours (Fig 1). In Figure 1 the data are represented as residual virus infectivity. Influenza A/H1N1sw virus particles survived for the longest time on the wooden surface, with infectious virus particles still being recovered after 48 hours. Survival of the virus on stainless steel and plastic was intermediate between cloth and wood, with detectable infectious virus particles at 24 hours but not at 48 hours. DISCUSSION Of the 4 surfaces tested, influenza A(H1N1)pdm09 virus particles survived longest on the wood, and for the shortest time on the cloth. The immediate decline in infectivity at time 0 in the samples recovered from the cloth suggests that the technique used to elute the virus may not have been effective on this surface (or that inhibitory substances were present in the fibers). Previous studies have shown that influenza virus particles lose infectivity less rapidly on nonporous surfaces compared with porous ones,7-9 but it has also been acknowledged that this could be due to inefficient recovery of virus particles from the porous surfaces.8 The findings of our study are supported by the literature. Bean et al7 reported that influenza A and B virus particles remained viable for 24-48 hours on stainless steel or plastic, but survived for less than 8-12 hours on cloth; findings very closely mirrored in our study. Tiwari et al8 found that avian influenza virus particles could survive on nonporous surfaces for up to 6 days. More recently, Greatorex et al9 have shown that a pandemic strain of influenza A/ H1N1 did not remain viable for >9 hours on a range of household surfaces. However, surfaces allowing the viruses to survive the longest included plastic and stainless steel, in agreement with our study. In contrast to our study, wooden surfaces did not support viral survival, with virus inoculates becoming inactivated after <4 hours. The difference in these findings may be due to the various types of wood tested, or may be related to the experimental procedures.
J. Oxford et al. / American Journal of Infection Control 42 (2014) 423-5
Previous studies have shown transmission of influenza via contact with virus particles on fomites. Measurable quantities of influenza A could be transferred from stainless steel to hands for a period of 24 hours after surface contamination, and from tissues to hands for up to 15 minutes after contamination.7 Boone et al6 showed that 59% of fomites tested in homes during the influenza season had detectable influenza virus, and Simmerman et al10 showed that 17.8% of household surfaces were positive for influenza A H1N1 in households with infected children during the 2009 H1N1 pandemic. This suggests that fomites play an important role in the spread of influenza.5 How can contamination of influenza virus on surfaces be reduced? Regular handwashing can reduce fomite contamination. In the study by Simmerman et al,10 households randomized to a handwashing protocol had a lower prevalence of fomites contaminated with influenza A(H1N1)pdm09 (11.1%) than control households (24.4%) (P ¼ .09). In terms of destroying influenza A H1N1 on fomites directly, a study by Greatorex et al1 demonstrated that simple household products, such as 1% bleach, 10% vinegar, and 0.01% washing-up liquid, as well as antibacterial wipes and antiviral tissues, were all highly effective at reducing virus infectivity. CONCLUSIONS Our study has demonstrated that the influenza A(H1N1) pdm09 virus can survive on cloth for at least 8 hours on stainless steel and plastic for up to 24 hours, and on wood for up to 48 hours. All of these surfaces are commonly found in households, and could potentially act as fomites for influenza virus transmission amongst household members. To prevent or reduce contamination of surfaces with influenza virus during the influenza season, it is recommended that individuals pay particular
425
attention to good hand hygiene and clean and disinfect frequently touched surfaces.
Acknowledgments The authors thank Toby Allinson for providing editorial assistance during the preparation of the manuscript.
References 1. Greatorex JS, Page RF, Curran MD, Digard P, Enstone JE, Wreghitt T, et al. Effectiveness of common household cleaning agents in reducing the viability of human influenza A/H1N1. PLoS One 2010;5:e8987. 2. World Health Organization. World now at the start of 2009 influenza pandemic. 2009. Available from: http://www.who.int/mediacentre/news/statements/ 2009/h1n1_pandemic_phase6_20090611/en/. Accessed November 15, 2013. 3. World Health Organization. Global Alert and Response (GAR): pandemic (H1N1) 2009 e update 112. 2010. Available from: http://www.who.int/csr/don/ 2010_08_06/en/index.html. Accessed November 15, 2013. 4. Dawood FS, Iuliano AD, Reed C, Meltzer MI, Shay DK, Cheg PY, et al. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 2012;12: 687-95. 5. Boone SA, Gerba CP. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol 2007;73:1687-96. 6. Boone SA, Gerba CP. The occurrence of influenza A virus on household and day care center fomites. J Infect 2005;51:103-9. 7. Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH Jr. Survival of influenza viruses on environmental surfaces. J Infect Dis 1982;146:47-51. 8. Tiwari A, Patnayak DP, Chander Y, Parsad M, Goyal SM. Survival of two avian respiratory viruses on porous and nonporous surfaces. Avian Dis 2006;50:284-7. 9. Greatorex JS, Digard P, Curran MD, Moynihan R, Wensley H, Wreghitt T, et al. Survival of influenza A(H1N1) on materials found in households: implications for infection control. PLoS One 2011;6:e27932. 10. Simmerman JM, Suntarattiwong P, Levy J, Gibbons RV, Cruz C, Shaman J, et al. Influenza virus contamination of common household surfaces during the 2009 influenza A (H1N1) pandemic in Bangkok, Thailand: implications for contact transmission. Clin Infect Dis 2010;51:1053-61.