Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination☆

Summary Viruses with pandemic potential including H1N1, H5N1, and H5N7 influenza viruses, and severe acute respiratory syndrome (SARS)/Middle East respiratory syndrome (MERS) coronaviruses (CoV) have emerged in recent years. SARS-CoV, MERS-CoV, and influenza virus can survive on surfaces for extended periods, sometimes up to months. Factors influencing the survival of these viruses on surfaces include: strain variation, titre, surface type, suspending medium, mode of deposition, temperature and relative humidity, and the method used to determine the viability of the virus. Environmental sampling has identified contamination in field-settings with SARS-CoV and influenza virus, although the frequent use of molecular detection methods may not necessarily represent the presence of viable virus. The importance of indirect contact transmission (involving contamination of inanimate surfaces) is uncertain compared with other transmission routes, principally direct contact transmission (independent of surface contamination), droplet, and airborne routes. However, influenza virus and SARS-CoV may be shed into the environment and be transferred from environmental surfaces to hands of patients and healthcare providers. Emerging data suggest that MERS-CoV also shares these properties. Once contaminated from the environment, hands can then initiate self-inoculation of mucous membranes of the nose, eyes or mouth. Mathematical and animal models, and intervention studies suggest that contact transmission is the most important route in some scenarios. Infection prevention and control implications include the need for hand hygiene and personal protective equipment to minimize self-contamination and to protect against inoculation of mucosal surfaces and the respiratory tract, and enhanced surface cleaning and disinfection in healthcare settings.

[1]  T. Perl,et al.  The role of 'no-touch' automated room disinfection systems in infection prevention and control. , 2013, The Journal of hospital infection.

[2]  Karen Ekernas,et al.  Facemasks and Hand Hygiene to Prevent Influenza Transmission in Households: A Cluster Randomized Trial , 2010 .

[3]  A. Coates,et al.  Transmission of Influenza Virus via Aerosols and Fomites in the Guinea Pig Model , 2009, The Journal of infectious diseases.

[4]  Josep M. Pujol,et al.  Informing Optimal Environmental Influenza Interventions: How the Host, Agent, and Environment Alter Dominant Routes of Transmission , 2010, PLoS Comput. Biol..

[5]  M. H. Wolff,et al.  Transmission of viruses via contact in ahousehold setting: experiments using bacteriophage φX174 as a model virus , 2000 .

[6]  D. Musher How contagious are common respiratory tract infections? , 2003, The New England journal of medicine.

[7]  J. Peiris,et al.  Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS) , 2003, The Lancet.

[8]  H. Doerr,et al.  Stability and inactivation of SARS coronavirus , 2004, Medical Microbiology and Immunology.

[9]  K. Lokuge,et al.  Environmental Sampling for Avian Influenza Virus A (H5N1) in Live-Bird Markets, Indonesia , 2010, Emerging infectious diseases.

[10]  K. Kousoulas,et al.  Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child , 1994, Journal of medical virology.

[11]  K. Wada,et al.  Maintenance of influenza virus infectivity on the surfaces of personal protective equipment and clothing used in healthcare settings , 2010, Environmental health and preventive medicine.

[12]  John Steel,et al.  High Temperature (30°C) Blocks Aerosol but Not Contact Transmission of Influenza Virus , 2008, Journal of Virology.

[13]  Sheng Li,et al.  Dynamics and control of infections transmitted from person to person through the environment. , 2009, American journal of epidemiology.

[14]  Stability of human metapneumovirus and human coronavirus NL63 on medical instruments and in the patient environment , 2008, Journal of Hospital Infection.

[15]  P. Talbot,et al.  Survival of human coronaviruses 229E and OC43 in suspension and after drying onsurfaces: a possible source ofhospital-acquired infections , 2000, Journal of Hospital Infection.

[16]  D. Swayne,et al.  Avian influenza: public health and food safety concerns. , 2011, Annual review of food science and technology.

[17]  R. Duval,et al.  Human Coronaviruses: Insights into Environmental Resistance and Its Influence on the Development of New Antiseptic Strategies , 2012, Viruses.

[18]  E. Baron,et al.  Long-term Shedding of Influenza A Virus in Stool of Immunocompromised Child , 2010, Emerging infectious diseases.

[19]  William A Rutala,et al.  Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. , 2010, American journal of infection control.

[20]  M. Jit,et al.  Modelling the transmission of healthcare associated infections: a systematic review , 2013, BMC Infectious Diseases.

[21]  T. Matsuyama,et al.  Influenza A virus survival in water is influenced by the origin species of the host cell , 2013, Influenza and other respiratory viruses.

[22]  C A Mitchell,et al.  Influenza A of human, swine, equine and avian origin: comparison of survival in aerosol form. , 1972, Canadian journal of comparative medicine : Revue canadienne de medecine comparee.

[23]  F. Hayden,et al.  Symptom pathogenesis during acute influenza: Interleukin‐6 and Other cytokine responses , 2001, Journal of medical virology.

[24]  M. Saijo,et al.  Pathology and virus dispersion in cynomolgus monkeys experimentally infected with severe acute respiratory syndrome coronavirus via different inoculation routes , 2007, International journal of experimental pathology.

[25]  Eva Navas,et al.  Accepted Manuscript , 2022 .

[26]  M. Wolff,et al.  Transmission of viruses via contact in ahousehold setting: experiments using bacteriophage straight phiX174 as a model virus. , 2000, The Journal of hospital infection.

[27]  S. Sattar,et al.  Survival characteristics of airborne human coronavirus 229E. , 1985, The Journal of general virology.

[28]  D. Oelberg,et al.  Detection of pathogen transmission in neonatal nurseries using DNA markers as surrogate indicators. , 2000 .

[29]  V. Munster,et al.  Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. , 2013, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[30]  X. Zhu,et al.  Concentration and detection of SARS coronavirus in sewage from Xiao Tang Shan Hospital and the 309th Hospital of the Chinese People's Liberation Army. , 2005, Water science and technology : a journal of the International Association on Water Pollution Research.

[31]  Khai Tran,et al.  Aerosol Generating Procedures and Risk of Transmission of Acute Respiratory Infections to Healthcare Workers: A Systematic Review , 2012, PloS one.

[32]  Mark H. Weir,et al.  Development of a Dose‐Response Model for SARS Coronavirus , 2010, Risk analysis : an official publication of the Society for Risk Analysis.

[33]  B. Bean,et al.  Survival of influenza viruses on environmental surfaces. , 1982, The Journal of infectious diseases.

[34]  M. St. Claire,et al.  Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys , 2004, Virology.

[35]  L. Poon,et al.  Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia : a prospective study , 2003 .

[36]  R. Compans,et al.  Oral vaccination with inactivated influenza vaccine induces cross-protective immunity. , 2012, Vaccine.

[37]  L. Saif,et al.  Stability of bovine coronavirus on lettuce surfaces under household refrigeration conditions , 2011, Food Microbiology.

[38]  M. First,et al.  Role of Absolute Humidity in the Inactivation of Influenza Viruses on Stainless Steel Surfaces at Elevated Temperatures , 2010, Applied and Environmental Microbiology.

[39]  M. Sobsey,et al.  Coronavirus Survival on Healthcare Personal Protective Equipment , 2010, Infection Control & Hospital Epidemiology.

[40]  W. J. Macneal,et al.  Resistance of the Melbourne Strain of Influenza Virus to Desiccation. , 1944 .

[41]  C. Hall Respiratory syncytial virus: its transmission in the hospital environment. , 1982, The Yale journal of biology and medicine.

[42]  P. Woo,et al.  Viral Loads in Clinical Specimens and SARS Manifestations , 2004, Emerging infectious diseases.

[43]  C. Gerba,et al.  Comparative surface‐to‐hand and fingertip‐to‐mouth transfer efficiency of gram‐positive bacteria, gram‐negative bacteria, and phage , 2002, Journal of applied microbiology.

[44]  Christian Drosten,et al.  Commentary: Middle East Respiratory Syndrome Coronavirus (MERS-CoV): Announcement of the Coronavirus Study Group , 2013, Journal of Virology.

[45]  Z. Memish,et al.  Environmental sampling for respiratory pathogens in Jeddah airport during the 2013 Hajj season , 2014, American Journal of Infection Control.

[46]  A. Bennett,et al.  Influenza Aerosols in UK Hospitals during the H1N1 (2009) Pandemic – The Risk of Aerosol Generation during Medical Procedures , 2013, PloS one.

[47]  Xiao-Ping Dong,et al.  Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation. , 2003, Biomedical and environmental sciences : BES.

[48]  C B Hall,et al.  Viral shedding patterns of children with influenza B infection. , 1979, The Journal of infectious diseases.

[49]  Charles P Gerba,et al.  Occurrence of Bacteria and Viruses on Elementary Classroom Surfaces and the Potential Role of Classroom Hygiene in the Spread of Infectious Diseases , 2010, The Journal of school nursing : the official publication of the National Association of School Nurses.

[50]  F. Hayden Respiratory viral threats , 2006, Current opinion in infectious diseases.

[51]  C. W. Keevil,et al.  Inactivation of Influenza A Virus on Copper versus Stainless Steel Surfaces , 2007, Applied and Environmental Microbiology.

[52]  W. Marasco,et al.  An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus , 2005, The Journal of pathology.

[53]  Marco Perino,et al.  Natural Ventilation for Infection Control in Health-Care Settings , 2009 .

[54]  A. Kramer,et al.  How long do nosocomial pathogens persist on inanimate surfaces? A systematic review , 2006, BMC infectious diseases.

[55]  Geethamma Jolly,et al.  Middle East Respiratory Syndrome Coronavirus (MERS-CoV) , 2016 .

[56]  C. Bridges,et al.  Transmission of influenza: implications for control in health care settings. , 2003, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[57]  G. Ruiz-Palacios,et al.  Controlling the novel A (H1N1) influenza virus: don't touch your face! , 2009, The Journal of hospital infection.

[58]  F. L. Schaffer,et al.  Survival of airborne influenza virus: Effects of propagating host, relative humidity, and composition of spray fluids , 2005, Archives of Virology.

[59]  A. Ike,et al.  Long-Term Study on Tenacity of Avian Influenza Viruses in Water (Distilled Water, Normal Saline, and Surface Water) at Different Temperatures , 2010, Avian diseases.

[60]  A. Fontanet,et al.  Clinical features and viral diagnosis of two cases of infection with Middle East Respiratory Syndrome coronavirus: a report of nosocomial transmission , 2013, The Lancet.

[61]  V. Franková Inhalatory infection of mice with influenza A0/PR8 virus. I. The site of primary virus replication and its spread in the respiratory tract. , 1975, Acta virologica.

[62]  M. Sobsey,et al.  Effects of Air Temperature and Relative Humidity on Coronavirus Survival on Surfaces , 2010, Applied and Environmental Microbiology.

[63]  M. Sobsey,et al.  Inactivation of surrogate coronaviruses on hard surfaces by health care germicides , 2011, American Journal of Infection Control.

[64]  A. Dublineau,et al.  Persistence of the 2009 Pandemic Influenza A (H1N1) Virus in Water and on Non-Porous Surface , 2011, PloS one.

[65]  S. Goyal,et al.  Evaluating the virucidal efficacy of hydrogen peroxide vapour , 2014, Journal of Hospital Infection.

[66]  Raymond Tellier,et al.  Review of Aerosol Transmission of Influenza A Virus , 2006, Emerging infectious diseases.

[67]  E. Larson,et al.  Survival of influenza virus on hands and fomites in community and laboratory settings. , 2012, American journal of infection control.

[68]  A. Franklin,et al.  Shedding Light on Avian Influenza H4N6 Infection in Mallards: Modes of Transmission and Implications for Surveillance , 2010, PloS one.

[69]  S Cauchemez,et al.  Virus shedding and environmental deposition of novel A (H1N1) pandemic influenza virus: interim findings. , 2010, Health technology assessment.

[70]  J. Sung,et al.  Fecal detection of influenza A virus in patients with concurrent respiratory and gastrointestinal symptoms. , 2009, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[71]  Michael P. Atkinson,et al.  Quantifying the Routes of Transmission for Pandemic Influenza , 2008, Bulletin of mathematical biology.

[72]  Philip Smith,et al.  Lessons Learned: Critical Care Management of Patients With Ebola in the United States* , 2015, Critical care medicine.

[73]  S F Bloomfield,et al.  Effects of Cleaning and Disinfection in Reducing the Spread of Norovirus Contamination via Environmental Surfaces , 2004, Infection Control & Hospital Epidemiology.

[74]  D. Patnayak,et al.  Survival of Two Avian Respiratory Viruses on Porous and Nonporous Surfaces , 2006, Avian diseases.

[75]  Jijun Zhao,et al.  Model Analysis of Fomite Mediated Influenza Transmission , 2012, PloS one.

[76]  Jonathan Z Kaye,et al.  Environmental persistence of a highly pathogenic avian influenza (H5N1) virus. , 2010, Environmental science & technology.

[77]  X. Jiang,et al.  Pathogen transmission in child care settings studied by using a cauliflower virus DNA as a surrogate marker. , 1998, The Journal of infectious diseases.

[78]  Elizabeth L Beam,et al.  A method for evaluating health care workers’ personal protective equipment technique , 2011, American Journal of Infection Control.

[79]  J. Peiris,et al.  The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus , 2011, Advances in virology.

[80]  R. Schwartz,et al.  Respiratory Viral RNA on Toys in Pediatric Office Waiting Rooms , 2010, The Pediatric infectious disease journal.

[81]  J. Edwards,et al.  Persistence of the 2009 Pandemic Influenza A (H1N1) Virus on N95 Respirators , 2013, Applied and Environmental Microbiology.

[82]  J. Otter,et al.  Minimum Infective Dose of the Major Human Respiratory and Enteric Viruses Transmitted Through Food and the Environment , 2011, Food and Environmental Virology.

[83]  Raymond Tellier,et al.  Transmission of influenza A in human beings. , 2007, The Lancet. Infectious diseases.

[84]  Mark D Sobsey,et al.  Survival of surrogate coronaviruses in water , 2009, Water Research.

[85]  E. Krisiunas Interim guidance on infection control measures for 2009 H1N1 influenza in healthcare settings, including protection of healthcare personnel. , 2009, Mississippi RN.

[86]  S. Paton,et al.  Detection of Airborne Severe Acute Respiratory Syndrome (SARS) Coronavirus and Environmental Contamination in SARS Outbreak Units , 2005, The Journal of infectious diseases.

[87]  R. Douglas,et al.  Assessment of experimental and natural viral aerosols. , 1966, Bacteriological reviews.

[88]  M. Rupp,et al.  Improving Cleaning of the Environment Surrounding Patients in 36 Acute Care Hospitals , 2008, Infection Control & Hospital Epidemiology.

[89]  J. A. Salkeld,et al.  Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings. , 2013, American journal of infection control.

[90]  Yuguo Li,et al.  Transmission of influenza A in human beings , 2007, The Lancet Infectious Diseases.

[91]  Rachael M. Jones,et al.  Relative Contributions of Four Exposure Pathways to Influenza Infection Risk , 2009, Risk analysis : an official publication of the Society for Risk Analysis.

[92]  Charles P. Gerba,et al.  Significance of Fomites in the Spread of Respiratory and Enteric Viral Disease , 2007, Applied and Environmental Microbiology.

[93]  Victor M Corman,et al.  Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection , 2013, The Lancet Infectious Diseases.

[94]  A. Osterhaus,et al.  Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. , 2012, The New England journal of medicine.

[95]  C. Donskey,et al.  Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms. , 2012, American journal of infection control.

[96]  A. Apisarnthanarak,et al.  Intervention with an Infection Control Bundle to Reduce Transmission of Influenza-Like Illnesses in a Thai Preschool , 2009, Infection Control & Hospital Epidemiology.

[97]  W. Henle,et al.  Experimental exposure of human subjects to viruses of influenza. , 1946, Journal of immunology.

[98]  J. Petitjean,et al.  Detection of the New Human Coronavirus HKU1: A Report of 6 Cases , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[99]  Charles P Gerba,et al.  The occurrence of influenza A virus on household and day care center fomites. , 2005, The Journal of infection.

[100]  L. Kaiser,et al.  Survival of Influenza Virus on Banknotes , 2008, Applied and Environmental Microbiology.

[101]  I. Kim,et al.  Inactivation of influenza A virus H1N1 by disinfection process. , 2010, American journal of infection control.

[102]  H. Fineberg Pandemic preparedness and response--lessons from the H1N1 influenza of 2009. , 2014, The New England journal of medicine.

[103]  A. Bosch,et al.  Survival of enteric viruses on environmental fomites , 1994, Applied and environmental microbiology.

[104]  S. Dowell,et al.  Severe Acute Respiratory Syndrome Coronavirus on Hospital Surfaces , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[105]  C. Gerba,et al.  Survival of Respiratory Viruses on Fresh Produce , 2013, Food and Environmental Virology.

[106]  J. Hendley,et al.  Transmission of experimental rhinovirus infection by contaminated surfaces. , 1982, American journal of epidemiology.

[107]  Jonathan S. Nguyen-Van-Tam,et al.  Survival of Influenza A(H1N1) on Materials Found in Households: Implications for Infection Control , 2011, PloS one.

[108]  W. Lim,et al.  Survival of Severe Acute Respiratory Syndrome Coronavirus , 2005, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[109]  T. R. Peters,et al.  Exposure to influenza virus aerosols during routine patient care. , 2013, The Journal of infectious diseases.

[110]  Gabriel M Leung,et al.  Using models to identify routes of nosocomial infection: a large hospital outbreak of SARS in Hong Kong , 2007, Proceedings of the Royal Society B: Biological Sciences.

[111]  R. Jarman,et al.  Influenza virus contamination of common household surfaces during the 2009 influenza A (H1N1) pandemic in Bangkok, Thailand: implications for contact transmission. , 2010, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[112]  R. Shaffer,et al.  Evaluation of Five Decontamination Methods for Filtering Facepiece Respirators , 2009, The Annals of occupational hygiene.

[113]  S. Goyal,et al.  Comparison of spike and aerosol challenge tests for the recovery of viable influenza virus from non‐woven fabrics , 2013, Influenza and other respiratory viruses.

[114]  J. Tang,et al.  SARS: clinical presentation, transmission, pathogenesis and treatment options. , 2006, Clinical science.

[115]  J. Otter,et al.  The Role Played by Contaminated Surfaces in the Transmission of Nosocomial Pathogens , 2011, Infection Control & Hospital Epidemiology.