Lifting the lid on toilet plume aerosol: A literature review with suggestions for future research

Background The potential risks associated with “toilet plume” aerosols produced by flush toilets is a subject of continuing study. This review examines the evidence regarding toilet plume bioaerosol generation and infectious disease transmission. Methods The peer-reviewed scientific literature was searched to identify articles related to aerosol production during toilet flushing, as well as epidemiologic studies examining the potential role of toilets in infectious disease outbreaks. Results The studies demonstrate that potentially infectious aerosols may be produced in substantial quantities during flushing. Aerosolization can continue through multiple flushes to expose subsequent toilet users. Some of the aerosols desiccate to become droplet nuclei and remain adrift in the air currents. However, no studies have yet clearly demonstrated or refuted toilet plume-related disease transmission, and the significance of the risk remains largely uncharacterized. Conclusion Research suggests that toilet plume could play a contributory role in the transmission of infectious diseases. Additional research in multiple areas is warranted to assess the risks posed by toilet plume, especially within health care facilities.

[1]  T. Eickhoff.  Airborne Nosocomial Infection: A Contemporary Perspective , 1994, Infection Control & Hospital Epidemiology.

[2]  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.

[3]  M. Estes,et al.  Norovirus gastroenteritis. , 2009, The New England journal of medicine.

[4]  D. Milton,et al.  Airborne transmission of communicable infection--the elusive pathway. , 2004, The New England journal of medicine.

[5]  J Barker,et al.  The potential spread of infection caused by aerosol contamination of surfaces after flushing a domestic toilet , 2005, Journal of applied microbiology.

[6]  D. Graham,et al.  Norwalk Virus Shedding after Experimental Human Infection , 2008, Emerging infectious diseases.

[7]  Carla A. Winston,et al.  Reported tuberculosis in the United States, 2010 , 2004 .

[8]  J. Bresee,et al.  Epidemic infectious gastrointestinal illness aboard U.S. Navy ships deployed to the Middle East during peacetime operations – 2000–2001 , 2006, BMC gastroenterology.

[9]  J. Falkinham,et al.  Epidemiology of infection by nontuberculous mycobacteria , 1996, Clinical microbiology reviews.

[10]  C. V. Chapin.  The Sources and Modes of Infection , 2009 .

[11]  L. Finelli,et al.  Emergence of a novel swine-origin influenza A (H1N1) virus in humans. , 2009, The New England journal of medicine.

[12]  E. Caul,et al.  Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant , 2000, Epidemiology and Infection.

[13]  L. Sehulster,et al.  Guidelines for environmental infection control in health-care facilities. Recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). , 2003, MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports.

[14]  William H. Horrocks.  Experiments Made to Determine the Conditions under which "Specific" Bacteria Derived from Sewage may be Present in the Air of Ventilating Pipes, Drains, Inspection Chambers and Sewers , 1907 .

[15]  J. Griffiths,et al.  Cruise ship environmental hygiene and the risk of norovirus infection outbreaks: an objective assessment of 56 vessels over 3 years. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[16]  A. Langmuir.  PART I. KEYNOTE ADDRESS: EPIDEMIOLOGY OF AIRBORNE INFECTION , 1961 .

[17]  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.

[18]  E. Scott,et al.  Cross‐contamination and infection in the domestic environment and the role of chemical disinfectants , 1997, Journal of applied microbiology.

[19]  Tze Wai Wong,et al.  Evidence of airborne transmission of the severe acute respiratory syndrome virus. , 2004, The New England journal of medicine.

[20]  B. Parker,et al.  Epidemiology of Infection by Nontuberculous Mycobacteria , 1987 .

[21]  W. F. Wells,et al.  On Air-borne Infection. Study II. Droplets and Droplet Nuclei. , 1934 .

[22]  A. R. Escombe,et al.  Evaluation of Molecular Tools for Detection and Drug Susceptibility Testing of Mycobacterium tuberculosis in Stool Specimens from Patients with Pulmonary Tuberculosis , 2010, Journal of Clinical Microbiology.

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

[24]  Kow-Tong Chen,et al.  Transmission of the severe acute respiratory syndrome on aircraft. , 2003, The New England journal of medicine.

[25]  J. Peiris,et al.  Viral load in patients infected with pandemic H1N1 2009 influenza A virus , 2009, Journal of medical virology.

[26]  J. W. Winchester,et al.  Water-to-Air Fractionation of Bacteria , 1980, Applied and environmental microbiology.

[27]  R. Atkinson,et al.  Bacterial aerosol from water closets. A comparison of two types of pan and two types of cover. , 1966, Lancet.

[28]  O. Raabe.  The dilution of monodisperse suspensions for aerosolization. , 1968, American Industrial Hygiene Association journal.

[29]  M. Wilcox,et al.  Potential for aerosolization of Clostridium difficile after flushing toilets: the role of toilet lids in reducing environmental contamination risk. , 2012, The Journal of hospital infection.

[30]  M. Iturriza-Gómara,et al.  Laboratory diagnosis of SARS. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  Caul Eo.  Small round structured viruses: airborne transmission and hospital control , 1994 .

[32]  Linsey C Marr,et al.  Concentrations and size distributions of airborne influenza A viruses measured indoors at a health centre, a day-care centre and on aeroplanes , 2011, Journal of The Royal Society Interface.

[33]  J. McLauchlin,et al.  Unravelling Cryptosporidium and Giardia epidemiology. , 2005, Trends in parasitology.

[34]  O. Lidwell,et al.  A slit sampler for collecting and counting air-borne bacteria , 1941, Journal of Hygiene.

[35]  C. Gerba,et al.  Microbiological hazards of household toilets: droplet production and the fate of residual organisms. , 1975, Applied microbiology.

[36]  H. M. Darlow,et al.  Infective hazards of water-closets. , 1959, Lancet.

[37]  Vital Hepatitis Std Aids,et al.  Reported tuberculosis in the United States 2013 , 2014 .

[38]  S. Newsom.  Microbiology of hospital toilets. , 1972, Lancet.

[39]  Roger I Glass,et al.  Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus--United States, 2002. , 2004, The Journal of infectious diseases.

[40]  Guang Zeng,et al.  Lack of Airborne Transmission during Outbreak of Pandemic (H1N1) 2009 among Tour Group Members, China, June 2009 , 2009, Emerging infectious diseases.

[41]  L. Lambert,et al.  Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care settings, 2005. , 2005, MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports.

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

[43]  K. Ward,et al.  Pandemic (H1N1) 2009 influenza. , 2010, New South Wales public health bulletin.

[44]  R. Glass,et al.  Probable transmission of norovirus on an airplane. , 2005, JAMA.

[45]  E. Caul.  Small round structured viruses: airborne transmission and hospital control , 1994, The Lancet.

[46]  C. Fraser,et al.  Household transmission of 2009 pandemic influenza A (H1N1) virus in the United States. , 2009, The New England journal of medicine.

[47]  P. Teunis,et al.  Norwalk virus: How infectious is it? , 2008, Journal of medical virology.

[48]  H. Maguire,et al.  The importance of school and social activities in the transmission of influenza A(H1N1)v: England, April - June 2009. , 2009, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[49]  R. I. Hutchinson.  Some observations on the method of spread of Sonne dysentery. , 1956, Monthly bulletin of the Ministry of Health and the Public Health Laboratory Service.

[50]  Curtis J Donskey,et al.  Reduction of Clostridium Difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods , 2007, BMC infectious diseases.

[51]  Michel Roger,et al.  Household transmission of the 2009 pandemic A/H1N1 influenza virus: elevated laboratory‐confirmed secondary attack rates and evidence of asymptomatic infections. , 2010, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[52]  John M Boyce,et al.  Widespread Environmental Contamination Associated With Patients With Diarrhea and Methicillin-Resistant Staphylococcus aureus Colonization of the Gastrointestinal Tract , 2007, Infection Control & Hospital Epidemiology.

[53]  M. Estes,et al.  Noroviruses everywhere: has something changed? , 2006, Current opinion in infectious diseases.

[54]  M. Estes,et al.  The epidemiologic and clinical importance of norovirus infection. , 2006, Gastroenterology clinics of North America.

[55]  C. S. Cox.  The Aerobiological Pathway of Microorganisms , 1988, 1988.

[56]  D. Blanchard,et al.  Mechanism for the Water-to-Air Transfer and Concentration of Bacteria , 1970, Science.

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

[58]  Hutchinson Ri.  Some observations on the method of spread of Sonne dysentery. , 1956, Monthly bulletin of the Ministry of Health and the Public Health Laboratory Service.

[59]  Ismail Celik,et al.  Measurement of airborne influenza virus in a hospital emergency department. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

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

[61]  S. Bloomfield,et al.  Survival of Salmonella in bathrooms and toilets in domestic homes following salmonellosis , 2000, Journal of applied microbiology.

[62]  Pan‐Chyr Yang,et al.  Lower gastrointestinal tract tuberculosis: an important but neglected disease , 2009, International Journal of Colorectal Disease.

[63]  REPORT OF THE MEDICAL OFFICER TO THE LOCAL GOVERNMENT BOARD , 1911, British medical journal.

[64]  C. Bopp,et al.  Epidemiology of gastroenteritis on cruise ships, 2001-2004. , 2006, American journal of preventive medicine.

[65]  S. Thomson.  The Numbers of Pathogenic Bacilli in Faeces in Intestinal Diseases , 1955, Journal of Hygiene.

[66]  R. Piso,et al.  Low transmission rate of 2009 H1N1 Influenza during a long-distance bus trip , 2011, Infection.

[67]  M. Ho,et al.  VIRAL GASTROENTERITIS ABOARD A CRUISE SHIP , 1989, The Lancet.

[68]  Hong Yang,et al.  Long-term SARS Coronavirus Excretion from Patient Cohort, China , 2004, Emerging infectious diseases.

[69]  R. Glass,et al.  Norovirus Transmission on Cruise Ship , 2005, Emerging infectious diseases.

[70]  A. Kelso,et al.  Transmission of pandemic A/H1N1 2009 influenza on passenger aircraft: retrospective cohort study , 2010, BMJ : British Medical Journal.

[71]  J. McCullers,et al.  Are toilet seats a vector for transmission of methicillin-resistant Staphylococcus aureus? , 2009, American journal of infection control.

[72]  Architectural Studies of Air Flow at Amoy Gardens , Kowloon Bay , Hong Kong , and its Possible Relevance to the Spread of SARS status report , 2003 .

[73]  M. F. Mendes,et al.  A bacteriological survey of washrooms and toilets , 1976, Journal of Hygiene.

[74]  B. Parker,et al.  Epidemiology of infection by nontuberculous Mycobacteria. III. Isolation of potentially pathogenic mycobacteria from aerosols. , 1980, The American review of respiratory disease.

[75]  T R Bender,et al.  An outbreak of influenza aboard a commercial airliner. , 1979, American journal of epidemiology.

[76]  B. Oppenheim,et al.  A Study of the Relationship Between Environmental Contamination with Methicillin-Resistant Staphylococcus aureus (MRSA) and Patients' Acquisition of MRSA , 2006, Infection Control & Hospital Epidemiology.

[77]  A. Langmuir.  Epidemiology of airborne infection. , 1961, Bacteriological reviews.