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Do high-touch surfaces in public spaces pose a risk for influenza transmission? A virologic study during the peak of the 2009 influenza A(H1N1) pandemic in Geneva, Switzerland

  • Amrei von Braun
    Affiliations
    Infection Control Program, Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland
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  • Yves Thomas
    Affiliations
    Swiss National Reference Center for Influenza, Central Laboratory of Virology, University of Geneva Hospitals, Geneva, Switzerland
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  • Hugo Sax
    Correspondence
    Address correspondence to Hugo Sax, MD, Infection Control Program, Division of Infectious Diseases and Hospital Epidemiology, University Hospital of Zurich, HAL 14, Raemistrasse 100, CH-8091 Zurich, Switzerland.
    Affiliations
    Infection Control Program, Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland
    Infection Control Program, University of Geneva Hospitals and Medical Faculty, Geneva, Switzerland
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Published:August 17, 2015DOI:https://doi.org/10.1016/j.ajic.2015.07.012
      To the Editor:
      In 2009, the influenza A(H1N1) virus caused the first influenza pandemic of the 21st century, lasting from April 2009 through August 2010.
      • Dawood F.S.
      • Jain S.
      • Finelli L.
      • Shaw M.W.
      • Lindstrom S.
      • Garten R.J.
      • et al.
      Emergence of a novel swine-origin influenza A (H1N1) virus in humans.
      An estimated 151,700-575,400 people worldwide died of the virus.
      • Dawood F.S.
      • Iuliano A.D.
      • Reed C.
      • Meltzer M.I.
      • Shay D.K.
      • Cheng P.Y.
      • et al.
      Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study.
      To characterize the epidemiology of the virus and advise public health policy makers, research focused on notorious hot spots for transmission, such as health care facilities, schools, and households with laboratory-confirmed cases. The possibility of infection through contact with virus on surfaces shortly before touching the nose or mouth was assessed by studying the survival of the virus on everyday objects, including bank notes.
      • Thomas Y.
      • Vogel G.
      • Wunderli W.
      • Suter P.
      • Witschi M.
      • Koch D.
      • et al.
      Survival of influenza virus on banknotes.
      We aimed to complement these investigations in a real live setting of a highly frequented public transport system and other public areas at the peak of the pandemic by screening surfaces for influenza A(H1N1)pdm09 in Geneva, Switzerland. The idea was sparked by vivid social marketing campaigns warning the public of influenza virus lurking in the public transport system and elevators.
      A senior infection control physician and 3 medical students performed the specimen collection for virology testing. The times and locations for collection were chosen conveniently on December 3 and 4, 2009, with the objective of covering a broad range of public spaces in the town of Geneva as well as in the University Hospital and Medical School. Swabs were also taken from the immediate surroundings of a patient infected with the pandemic influenza strain. The samples were collected at all times of day, purposefully targeting rush hours.
      Reverse-transcription polymerase chain reaction (RT-PCR) and cell culture of influenza viruses were performed at the virology laboratory of the University of Geneva Hospitals, as described previously.
      • Thomas Y.
      • Boquete-Suter P.
      • Koch D.
      • Pittet D.
      • Kaiser L.
      Survival of influenza virus on human fingers.
      In brief, nylon flocked swabs were moistened in 3 mL of Universal Transport Medium (Copan Italia, Brescia, Italy), rubbed on the investigational surface, and then transported to the laboratory in the transport medium tube. A total of 0.4 mL was used for nucleic extraction and RT-PCR analysis (http://www.who.int/csr/resources/publications/swineflu/WHO_Diagnostic_RecommendationsH1N1_20090521.pdf). If results were positive, then 0.4 mL of the sample was used to inoculate Madin-Darby canine kidney cells (CCL34; American Type Culture Collection, Manassas, VA). The cells were collected and submitted to immunofluorescence analysis after 7 days at 37°C under 5% CO2. According to Swiss law on research on humans, ethics approval was not warranted for this type of study.
      A total of 49 swabs were collected, including 22 (45%) in the morning, 20 (41%) in the afternoon, and 7 (14%) in the evening. The swabs were collected from high-touch surfaces in public transport vehicles, from ticket and coffee vending machines, and from elevator buttons and door handles at the hospital and medical school (Table 1; online). Only 1 specimen tested positive for A(H1N1)pdm09: the swab from the right bedrail of a female A(H1N1) patient. The corresponding culture remained negative, however.
      Although busy public transportation systems in large cities are known to pose a significant risk for airborne transmission of viral infections, surprisingly, during the peak of the pandemic, we did not detect influenza A(H1N1)pdm09 on high-touch surfaces of the public transport system or within the hospital and medical school, except in the vicinity of an infected patient. The incidence of influenza A(H1N1) was 40/100,000 in Geneva during the study week, as reported by the Swiss Federal Office of Public Health, and was higher in the 3 preceding weeks, with a maximum rate of 80/100,000. Thus, sampling during different time points could have increased the chance of obtaining positive swabs.
      Our samples were taken from nonporous metal, glass, and plastic objects, which showed a virus survival time of 24-48 hours in previous studies.
      • Bean B.
      • Moore B.M.
      • Sterner B.
      • Peterson L.R.
      • Gerding D.N.
      • Balfour H.H.
      Survival of influenza viruses on environmental surfaces.
      Survival of virus particles were also found to vary, from 8 hours on cloth,
      • Oxford J.
      • Berezin E.N.
      • Courvalin P.
      • Dwyer D.E.
      • Exner M.
      • Jana L.A.
      • et al.
      The survival of influenza A(H1N1)pdm09 virus on 4 household surfaces.
      30-60 minutes on human fingers,
      • Thomas Y.
      • Boquete-Suter P.
      • Koch D.
      • Pittet D.
      • Kaiser L.
      Survival of influenza virus on human fingers.
      • Grayson M.L.
      • Melvani S.
      • Druce J.
      • Barr I.G.
      • Ballard S.A.
      • Johnson P.D.
      • et al.
      Efficacy of soap and water and alcohol-based hand-rub preparations against live H1N1 influenza virus on the hands of human volunteers.
      and several days on bank notes,
      • Thomas Y.
      • Vogel G.
      • Wunderli W.
      • Suter P.
      • Witschi M.
      • Koch D.
      • et al.
      Survival of influenza virus on banknotes.
      depending on virus quantity, material, and beneficial microenvironment, including temperature, pH, and humidity. We speculate that our negative results could have been linked to low virus quantity, given that people acutely infected with influenza A(H1N1)pdm09, shedding large amounts of virus, were presumably less likely to use public transport systems. Furthermore, the samples were taken from highly frequented surfaces, which could result in a decrease in virus concentration with each consecutive touch. Furthermore, increased vigilance during the pandemic might have fostered overall hand hygiene among the public.
      In contrast to the message portrayed by public advertisements during the pandemic, we did not detect influenza A(H1N1)pdm09 on surfaces in buses and trams. Larger studies are needed to assess the true risk of acquiring influenza infections through contact with potentially contaminated surfaces in high-touch areas.
      The authors thank Ruoxi Ren, Yassaman Alipour Tehrany, and Babtiste Waeber for their help with swab collection, and Francisca Morán Cadenas, Federal Office of Public Health Switzerland, for providing the epidemiologic data.

      Supplementary data

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