Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises

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Journal of Hospital Infection (2006) 64, 100e114 REVIEW Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises
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Journal of Hospital Infection (2006) 64, 100e114 REVIEW Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises J.W. Tang a, *,Y.Li b, I. Eames c, P.K.S. Chan a,d, G.L. Ridgway e a Department of Microbiology, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, China b Department of Mechanical Engineering, The University of Hong Kong, Pokfulam, Hong Kong SAR, China c Department of Mechanical Engineering, University College London, London, UK d School of Public Health, The Chinese University of Hong Kong, Hong Kong SAR, China e Capital Investment and Planning, University College London Hospitals, London, UK Available online 17 August 2006 KEYWORDS Aerosol; Transmission; SARS; Influenza; Droplets; Control; Infection Summary The epidemics of severe acute respiratory syndrome (SARS) in 2003 highlighted both short- and long-range transmission routes, i.e. between infected patients and healthcare workers, and between distant locations. With other infections such as tuberculosis, measles and chickenpox, the concept of aerosol transmission is so well accepted that isolation of such patients is the norm. With current concerns about a possible approaching influenza pandemic, the control of transmission via infectious air has become more important. Therefore, the aim of this review is to describe the factors involved in: (1) the generation of an infectious aerosol, (2) the transmission of infectious droplets or droplet nuclei from this aerosol, and (3) the potential for inhalation of such droplets or droplet nuclei by a susceptible host. On this basis, recommendations are made to improve the control of aerosol-transmitted infections in hospitals as well as in the design and construction of future isolation facilities. ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. Introduction * Corresponding author. Address: Department of Microbiology, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, China. Tel.: þ ; fax: þ address: The experience in 2003 with severe acute respiratory syndrome (SARS) highlighted the issue of aerosol transmission, both short range between healthcare workers and their patients, 1e3 and long /$ - see front matter ª 2006 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi: /j.jhin Aerosol transmission and ventilation control 101 range amongst the residents of the Amoy Gardens estate. 4,5 Aerosol or airborne transmission is already well recognized for many human pathogens. Much work has been performed using air-sampling techniques together with culture and molecular detection methods for viruses 6e16 [particularly varicella zoster virus (VZV)], 17e24 bacteria 25e33 [particularly tuberculosis (Mycobacterium tuberculosis, TB) and other mycobacteria], 34e42 and fungi (particularly Aspergillus spp.). 43e56 Beggs reviewed the importance of airborne transmission of infection in hospitals, focusing mainly on bacteria that are well known to cause nosocomial infections, i.e. Staphylococcus aureus and meticillin-resistant S. aureus (MRSA), M. tuberculosis, Acinetobacter spp., Aspergillus spp., Pseudomonas spp. and Legionella spp. 57 He concluded that, for these infections, although contact spread was still the main route of infection, infections via the airborne route, both direct and indirect (via the settling of airborne pathogens on fomites), were probably underestimated. The generation of such infectious aerosols of infectious human pathogens can occur in many ways, and in many settings, although some have been studied more extensively than others due to their greater clinical significance. The literature on the risks of aerosol transmission of infection in hospital operating theatres is extensive. 58e65 Over 40 studies on the relationship between ventilation systems and the transmission of infection in hospitals, offices, aeroplanes and ships were reviewed recently by Li et al. 66 Studies have also been conducted on how infectious aerosols generated by various procedures in hospital environments can lead to infection in burns care facilities 67e69 and medical intensive care units. 70,71 In particular, the use of oxygen masks, 72,73 and power tools in dental practice 74e77 and orthopaedics 77e84 may pose a risk of aerosol infection. Aerosol dispersal of infectious agents has also been demonstrated in wastewater spray sites, 85 surface waves on the sea, 86 the flushing of the household toilet, 87 and even just opening a standard hinged door. 88 Definitions True long-range aerosol transmission becomes possible when the droplets of infectious material are sufficiently small to remain almost indefinitely airborne and to be transmitted over long distances. One set of infection control guidelines for healthcare settings suggested that only TB, measles (rubeola virus) and chickenpox (VZV) should be considered as true airborne infectious diseases. 89 However, it is likely that other infectious agents may also behave as airborne, given a favourable environment, e.g. whooping cough (Bordetella pertussis), influenza virus, adenovirus, rhinovirus, Mycoplasma pneumoniae, SARS coronavirus (SARS-CoV), group A streptococcus and Neisseria meningitidis. Many more organisms fall into this category, as it probably includes virtually all pathogens where replication and/or colonization occur in the respiratory tract. Table I lists organisms associated with varying degrees of aerosol transmission. 90 Each organism can also be transmitted through direct contact with infected body fluids. A recent systematic review demonstrated that adequate or inadequate ventilation has an effect on the risk of infection via infectious aerosols. 66 This interdisciplinary review, authored by a large group of engineers, microbiologists and epidemiologists, defined the following terms. e Airborne transmission refers to the passage of micro-organisms from a source to a person through aerosols, resulting in infection of the person with or without consequent disease. e Aerosols are a suspension of solid or liquid particles in a gas, with particle size from to over 100 mm. 91 Infectious aerosols contain pathogens. e A droplet nucleus is the airborne residue of a potentially infectious (micro-organismbearing) aerosol from which most of the liquid has evaporated. 92 On the basis of these definitions, the following clinically applicable distinctions are made between short-range airborne infection routes (between individuals, generally less than 1-m apart) and long-range routes (within a room, between rooms or between distant locations, generally greater than 1-m distances): e The short-range airborne infection route depends on the close proximity of the infected source and susceptible host. A study was performed recently (Xie et al., unpublished observations) to define more clearly the size of the droplets originally referred to by Wells. 92 These terms are also in common current use. This study proposes the following size definitions: large-droplet diameter 60 mm, small droplet diameter 60 mm and droplet nuclei diameter 10 mm. Note that small droplets may also participate in short-range transmission, but they are more likely than larger droplets to evaporate to become droplet nuclei and then be considered as having the potential for long-range airborne transmission (see below). 93 102 J.W. Tang et al. Table I Pathogens and diseases that have the potential to be transmitted via the airborne route Pathogen Aerosol route of transmission Anthrax Inhalation of spores Arenaviruses Inhalation of small particle aerosols from rodent excreta Aspergillosis Inhalation of airborne conidia (spores) Blastomycosis Conidia, inhaled in spore-laden dust Brucellosis Inhalation of airborne bacteria Chickenpox/shingles (varicella zoster virus) Droplet or airborne spread of vesicle fluid or respiratory tract secretions Coccidioidomycosis Inhalation of infective arthroconidia Adenovirus Transmitted through respiratory droplets Enteroviruses Aerosol droplet spread (coxsackie virus) Cryptococcosis Presumably by inhalation Human parvovirus Contact with infected respiratory secretions Rotavirus Possible respiratory spread Norwalk virus Airborne transmission from fomites Hantavirus Presumed aerosol transmission from rodent excreta Histoplasmosis Inhalation of airborne conidia Influenza Airborne spread predominates Lassa virus Aerosol contact with excreta of infected rodents Legionellosis Epidemiological evidence supports airborne transmission Lymphocytic choriomeningitis Oral or respiratory contact with virus-contaminated excreta, food or dust Measles Airborne by droplet spread Melioidosis Inhalation of soil dust Meningitis Respiratory droplets from nose and throat (Neisseria meningitidis) Meningitis Droplet infection and discharges from nose and throat (Haemophilus influenzae) Meningitis Droplet spread and contact with respiratory secretions (Streptococcus pneumoniae) Mumps Airborne transmission or droplet spread Nocardia Acquired through inhalation Paracoccidioidomycosis Presumably through inhalation of contaminated soil or dust Whooping cough (Bordetella pertussis) Direct contact with discharges from respiratory mucous membranes of infected persons by the airborne route Plague (Yersinia pestis) Rarely airborne droplets from human patients. In the case of deliberate use, plague bacilli would possibly be transmitted as an aerosol Pneumonia (S. pneumoniae) Droplet spread Pneumonia Probably droplet inhalation (Mycoplasma pneumoniae) Pneumonia Possibilities include airborne spread (Chlamydia pneumoniae a ) Psittacosis (Chlamydia psittaci a ) By inhaling the agent from desiccated droppings, secretions and dust from feathers of infected birds Q fever (Coxiella burnetti) Commonly through airborne dissemination of coxiellae in dust Rabies Airborne spread has been demonstrated in a cave where bats were roosting, and in laboratory settings, but this occurs very rarely Rhinitis/common cold Presumably inhalation of airborne droplets (rhinovirus, coronavirus, parainfluenza, respiratory syncytial virus) Rubella Droplet spread Smallpox (Variola major) Via respiratory tract (droplet spread) Sporotrichosis Pulmonary sporotrichosis presumably arises through inhalation of conidia Aerosol transmission and ventilation control 103 Table I (continued) Pathogen Staphylococcal diseases Streptococcal diseases Toxoplasmosis Tuberculosis Tularaemia (Francisella tularensis) Aerosol route of transmission Airborne spread is rare but has been demonstrated in patients with associated viral respiratory disease Large respiratory droplets. Individuals with acute upper respiratory tract (especially nasal) infections are particularly likely to transmit infection Inhalation of sporulated oocysts was associated with one outbreak Exposure to tubercle bacilli in airborne droplet nuclei By inhalation of dust from contaminated soil, grain or hay Virtually all of these pathogens are also transmissible by direct contact. Pathogens in bold are those which are considered to have the potential to be transmitted by the long-range airborne route. 89 The original wording of the reference text 90 concerning aerosol transmission routes has been retained as much as possible. a Now known as Chlamydophila psittaci and Chlamydophila pneumoniae, but the original classification has been retained here as in the original reference text. 90 Exhaled air from both nose and mouth is able to enter and mix with air in the breathing zone of another person standing nearby (e.g. patients and doctors on a ward round at the bedside). Thus, short-range transmission implies that air flows between individuals may interact to infect one another. 94 In addition, it has been shown that the use of a simple oxygen mask may also generate a short-range ( 1 m) infectious aerosol, with a potential risk to nearby healthcare workers and other patients. 72,73 Together with nebulizers, oxygen masks fall into this classification of potential short-range aerosol transmission sources, but some droplets generated by such masks can evaporate to become droplet nuclei that can also transmit infection over larger distances. 57 e Long-range aerosol transmission refers to the potential for agents to be carried long distances by air flows to cause infection, and includes the traditional terms small-droplet or droplet nuclei and airborne. Virtually all infectious agents that can cause infection at long range can also cause infection at short range as well as by direct contact. Therefore, use of the term long range refers to the greatest distance from their source at which these agents have the potential to cause infection. Infectious agents transmissible by aerosols If the pathogen has some part of its life cycle in the respiratory tract, it is more likely to be present in aerosols generated and projected into the surrounding air by breathing, talking, coughing, sneezing and singing. For truly airborne pathogens (TB, measles and VZV), the routes of acquisition and dissemination of the infectious particles are well recognized to be via the respiratory tract. In the other pathogens listed in Table I, acquisition of the infection is also via the respiratory tract, which is the primary site of infection and replication. Therefore, these other pathogens, such as parvovirus B19, enteroviruses and the organisms of atypical pneumonias [M. pneumoniae, Chlamydophila psittaci (previously Chlamydia psittaci), Chlamydophila pneumoniae (previously Chlamydia pneumoniae), Coxiella burnetti and Legionella pneumophila], have the potential to be transmitted via aerosols as their life cycle involves replication at some point in the respiratory tract. Regarding L. pneumophila, replication also occurs in water systems, and human infection can occur via infected water aerosols, such as showerheads and fountains. With SARS-CoV, viral RNA as well as viable (culturable) virus has been found in air samples. 95,96 Therefore, SARS-CoV can potentially be transmitted by short- and long-range aerosols to cause disease, as has been strongly implicated by several studies. 1e5 With influenza, there is ongoing debate about the nature of transmission between people. A recent review suggested that aerosol-generating procedures.should be performed with proper infection control precautions, but the authors do not elaborate on exactly what these precautions should be. 97 Recent guidelines from the UK review the evidence for aerosol transmission of influenza more comprehensively. 98 The report concluded that whilst close contact with infected individuals seems to be responsible for the vast majority of transmission, most reports of influenza transmission 104 J.W. Tang et al. do not provide enough temporal-spatial data to determine whether transmission is mainly due to droplet, contact or airborne spread. This is probably the most realistic assessment, and this uncertainty is reflected in the large range of values for the basic reproductive number (R 0, the number of secondary cases arising from a single index case in an otherwise totally susceptible population), ranging from 1e2 99 to 2e7 100 to However, there are reports to suggest that in pandemic or large, explosive outbreak situations, influenza can become truly airborne. 12,13 For comparison, the R 0 values of other commonly encountered infections are shown in Table II. In contrast, other pathogens, such as human immunodeficiency virus and hepatitis B and C viruses, replicate mainly outside the respiratory tract and are not naturally transmitted via aerosols. With other organisms that can replicate on many surfaces either inside or outside the body, e.g. S. aureus, the picture is not so clear-cut. Although mainly spread by direct contact, there is a suggestion that patients that carry S. aureus in the respiratory tract can spread the bacteria by short-range aerosols. 57,106 S. aureus on skin epithelial cells on fomites, such as bed sheets, can also be spread during bed making. 57,106 This becomes more important when considering resistant strains such as MRSA. 57 Sources of infectious agents A commonly encountered source is the patient with flu-like symptoms who is coughing, sneezing and dispersing the organism (Figure 1). 107,108 In the diagnostic laboratory, it may be an inoculated Table II The basic reproductive number (R 0 ) of some human infectious agents (adapted from Reference 102 with additional references as indicated) Infectious disease Basic reproductive number (R 0 ) Measles 15e17 Whooping cough 15e17 Chickenpox e12 Mumps 10e12 Rubella 7e8 Diphtheria 5e6 Poliomyelitis 5e6 Smallpox 103 4e7 Influenza 99e e20 SARS 104,105 2e3 SARS, severe acute respiratory syndrome. Small droplets travel as a cloud through the air Large droplets travel ballistically through the air Figure 1 Droplet generation. A flash photo of a human sneeze, showing the expulsion of droplets that may be laden with infectious pathogens. Sneezing can produce as many as droplets of 0.5e12 mm. 107 These particles can be expelled at a velocity of 100 m/s, 108 reaching distances of several metres. Smaller droplets with less mass are less influenced by gravity, and can be transported as a cloud over greater distances by air flows. Larger droplets with more mass are more strongly influenced by gravity and less so by air flows, and move more ballistically, falling to the ground more quickly. Reproduced with the kind permission of Prof. Andrew Davidhazy, School of Photographic Arts and Sciences, Rochester Institute of Technology Rochester, NY, USA. culture medium that is dropped or spilt, as has been reported for laboratory-acquired SARS infection. 109 A more worrying possibility is the deliberate release of a biological agent, such as during the US terrorist anthrax attacks of 2001e2002, 32,33 or an accidental release, such as the anthrax incident in the Russian city of Sverdlovsk of A sneeze can generate up to droplets (Figure 1), 107,108 which can evaporate to produce droplets of 0.5e12 mm in diameter. 107 A cough can generate about 3000 droplet nuclei, the same number as talking for 5 minutes. 111 During normal breathing, exhalation can project droplets up to 1 m in room air, which may be inhaled by another person nearby (Figure 2), 94 whereas sneezing can project droplets several metres (Figure 1). 107,108 In addition, a recent study has shown that some individuals may exhale more particles during quiet breathing than others, suggesting that some people may be more infectious than others when infected with the same organism. 112 The way that an infectious aerosol is generated should be considered when assessing the probable distance of spread. As noted earlier, large droplets can evaporate to become small droplets that can evaporate further to become droplet nuclei and hence become truly airborne if this evaporation process can occur before the Aerosol transmission and ventilation control 105 Figure 2 Smoke visualization of exhalation flow from nose of the right mannequin penetrating into the breathing zone of the left mannequin, which are 0.4 m apart. 94 Reproduced from Figure 12 in Reference 94 with the kind permission of Blackwell Publishing. droplet lands on the ground. The 2003 SARS epidemics also revealed iatrogenic and environmental factors that might contribute to producing virusladen aerosols, such as those produced by nebulizers, tracheostomies, bronchoscopies, 113e116 and, in the Amoy Gardens outbreak, a defective sewage system. 4,5 Mechanics of aerosol transmission of infectious agents Once infectious droplets are released, the main factors that determine how they move are their size and the airflow patterns that carry them around (Figure 3). The droplet size changes with time, depending on the environmental conditions. Humidity in the air alters the rate of drop
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