key: cord-330463-j4cf7vzs
authors: Sattar, Syed A.
title: Indoor air as a vehicle for human pathogens: Introduction, objectives, and expectation of outcome
date: 2016-09-02
journal: Am J Infect Control
DOI: 10.1016/j.ajic.2016.06.010
sha: 
doc_id: 330463
cord_uid: j4cf7vzs

Airborne spread of pathogens can be rapid, widespread, and difficult to prevent. In this international workshop, a panel of 6 experts will expound on the following: (1) the potential for indoor air to spread a wide range of human pathogens, plus engineering controls to reduce the risk for exposure to airborne infectious agents; (2) the behavior of aerosolized infectious agents indoors and the use of emerging air decontamination technologies; (3) a survey of quantitative methods to recover infectious agents and their surrogates from indoor air with regard to survival and inactivation of airborne pathogens; (4) mathematical models to predict the movement of pathogens indoors and the use of such information to optimize the benefits of air decontamination technologies; and (5) synergy between different infectious agents, such as legionellae and fungi, in the built environment predisposing to possible transmission-related health impacts of aerosolized biofilm-based opportunistic pathogens. After the presentations, the panel will address a set of preformulated questions on selection criteria for surrogate microbes to study the survival and inactivation of airborne human pathogens, desirable features of technologies for microbial decontamination of indoor air, knowledge gaps, and research needs. It is anticipated that the deliberations of the workshop will provide the attendees with an update on the significance of indoor air as a vehicle for transmitting human pathogens with a brief on what is currently being done to mitigate the risks from airborne infectious agents.

I welcome you all to this multinational workshop! This workshop was conceived over a year ago, and the organizing committee ( Table 1 ) formally requested that ASTM International (www.astm.org/) hold the event under its auspices. ASTM's Committee E35, which deals with pesticides, antimicrobials, and alternative control agents, approved the proposal in April 2015.

Mounting recognition of indoor air as a vehicle for infectious agents is leading government regulators, such as the U.S. Environmental Protection Agency, to refine and update their guidelines, 1 researchers to develop better means of studying airborne pathogens, 2 and civil engineers and architects to find innovative means of making indoor air safer while keeping energy conservation in mind. 3 Although comprehensive guidelines and standardized means are available to study chemical pollutants in indoor air, 4 there remains a general lack of suitable experimental facilities and standardized protocols to quantitatively assess the survival of pathogens in indoor air and to document their removal and inactivation by physical and chemical means. This workshop will address these issues, among others.

The workshop's specific objectives, therefore, are as follows: The deliberations will also focus on the development of standards for assessing indoor air decontamination technologies and government regulations for registration of products to be marketed.

As noted, this workshop has been organized under the auspices and with the support of ASTM International. The City University of New York and the University of Ottawa (Canada) are the 2 academic sponsors of the workshop, and financial support has been provided by RB (Montvale, NJ) and Microbac (Sterling, VA). These 2 companies are also funding publication of the workshop proceedings. We gratefully acknowledge their generous support.

The organizing committee has put together an outstanding group of speakers who will offer a comprehensive yet balanced perspective on the key issues. Table 2 lists the topics to be covered, along with the names and affiliations of the presenters.

Elsevier (www.elsevier.com) has agreed to publish the proceedings of the workshop after peer review. Elsevier will also provide a preview of the proceedings, including the abstracts for each presentation, for release during the 2016 conference of the Association for Professionals in Infection Control and Epidemiology. The workshop proceedings will also contain a summary of the concluding discussions.

Potential members of the audience include researchers in aerobiology, makers of air purification technologies, contract laboratories that assess air decontaminants, government regulators dealing with indoor air quality, and members of standards-setting organizations, such ASTM International (www.astm.org) and American Society of Heating, Refrigerating, and Air-Conditioning Engineers (www.ashrae.org). Table 3 is a glossary of the common terms used throughout this workshop's presentations. This is included in an attempt to create a level playing field while facilitating the understanding of the subject matter by experts in fields other than environmental microbiology. However, the emphasis here is on working definitions, recognizing that efforts are needed to develop a more comprehensive glossary for broader applications in this area.

Aerobiology, the study of living organisms and their components in air, became a full-fledged scientific discipline in 1964. This was followed in 1974 by the founding of the International Association of Aerobiology (https://sites.google.com/site/ aerobiologyinternational/). The initial focus of this group was the study and movement of pollen, but microbes and other life forms were soon added to the mix with a corresponding broadening of the organization's scope (Fig 1) . The microbiologic quality of indoor air comes under the rubric of aerobiology (Fig 2) . This workshop will focus only on indoor air as a vehicle for human pathogens. Indoor air quality

Exposure of humans to indoor air and its contents coincided with cave dwelling >200,000 years ago. 5 Sharing of the human habitat with domesticated animals, such as cattle, dogs, and pigs, facilitated the rise of zoonotic infections, including airborne infections (eg, measles). 6 Exposure to pathogens of humans and animals via the agency of indoor air continues to this day.

Although the focus here is on indoor air, indoor air is not entirely immune to what goes on outdoors. The air from outside an edifice affects the air indoors and vice versa. In fact, the use of fossil fuels for heating the indoors contributes directly and indirectly to overall climate change. An early consequence of energy conservation was sealed buildings and houses, which eventually gave rise to sick building or tight building syndrome as a result of the trapping of airborne pollutants and higher levels of moisture inside. 7

Humans and animals are the main contributors of microbeladen particles indoors. In fact, individuals leave their own personal microbial footprint as a part of the indoor microbiome. 8 Aerosolization of microbes from biofilms and resuspension of dust are the other principal contributors to the microbial content of indoor air (Fig 3) . Although the route by which airborne pathogens cause infections varies between microorganisms, improvements in the quality, quantity, and movement of indoor air can mitigate the airborne spread of many human pathogens by preventing pathogen This phenomenon is especially relevant in aerobiology because a host is often exposed to potentially harmful biologic, chemical, or physical agents simultaneously or sequentially. Droplet nuclei Airborne particles derived from larger droplets after loss of water Such droplets are crucial for the spread of infectious agents by air as their relatively small size (0.5-5.0 μm) allows for their stability in air while also permitting their retention on inhalation. Indoor air quality Quality of the air within buildings and other enclosures, with particular reference to the health and comfort of the occupants

The overall quality of indoor air is dependent on a mix of a variety of factors that may be site and time sensitive.

The capacity of a microbe to infect a given host depends not only on its biology but also on the general health status of the host and the portal of entry into the host.

A microbe capable of causing localized or generalized damage to the host Please see "Infectious agent."

The totality of microorganisms and their collective genetic material present in or on the human body or in another environment A certain proportion of the microbes found in a microbiome may not be culturable but detected and identified via their genomes only.

This term is now preferred over microflora.

Opportunistic pathogen A microbial pathogen capable of infecting hosts whose natural defenses are compromised because of advanced age, immunosuppression, or other underlying causes

The number, variety, and health significance of such pathogens is on the rise in conjunction with the rising numbers of those debilitated by acquired or induced immunosuppression. Pathogen (microbial) Any microbe capable of causing damage to the host Even an otherwise innocuous microbe can become pathogenic depending on the general resistance of the host or the microbe's entry into normally sterile areas of the body where it can become an opportunistic pathogen. Perikairots

Environment-based opportunistic pathogens Biofilm-based microbes such as legionellae and environmental mycobacteria can infect those debilitated because of age or underlying medical conditions. Resident microbiota A mix of microbes normally found in or on the host Many members of the resident microbiota from skin and mucous surfaces are frequently found in indoor air.

Particles small enough to access the alveolar space during normal breathing Such particles may or may not contain viable microbes.

Surrogate microbe A microbe that resembles ≥1 type of pathogens but is safer and easier to work with in the laboratory; also called a simulant

The use of such microbes is crucial in many aspects of microbiology, in general.

The body's automatic inhalation and exhalation process at rest In addition to coughing and sneezing, tidal breathing can release infectious agents into the air. Transient microbiota Microbes temporarily acquired by a host during normal contact with the environment inhalation and reducing the microbial load on environmental surfaces. Indoor air is arguably the fastest and most highly efficient means of pathogen spread in a given setting. As depicted in Figure 2 , indoor air is a complex and dynamic mixture of numerous components in a constant state of flux influenced by many factors both indoors and outdoors. The quality of indoor air represents the outcome of the unique mix of components in a given setting that, in themselves, change temporally.

One major challenge in preventing and controlling the airborne spread of infection is the presence of possibly multiple and mobile sources of pathogens at a given location and time. One or more infected or colonized persons or pets may contaminate the air in their immediate vicinity with exposure of those nearby without the air having reached any available means of pathogen decontamination.

Certain factors that influence indoor air quality may fall under the categories of chemical and physical. For example, smoke from burning wood for cooking fuel is, of course, chemical in nature, but respirable particles in the smoke are the primary means of lung irritation and potential damage leading to cardiopulmonary syndromes, including lung cancer (http://www.who.int/mediacentre/ factsheets/fs292/en/).

The study of indoor air quality received a major boost as a consequence of the severe acute respiratory syndrome outbreak in 2003 9 and the anthrax scares in the United States in 2011. 10 It also spawned much interest in the development, assessment, and application of technologies to decontaminate indoor air.

As shown in Figure 3 , particles >10 μm in diameter entering the air may rapidly fall out of the air because of their mass under prevailing environmental conditions, particularly temperature and relative humidity, whereas smaller particles can not only remain airborne for extended periods but can also be transported readily indoors by air currents over considerable distances. Respirable particles fall in the range of 0.2-5.0 μm in diameter, whereas smaller particles are generally exhaled because of the aerodynamics of breathing. The actual site of retention of the inhaled particles depends on their nominal size. It is noteworthy here that persons with respiratory infections breathe out pathogen-laden particles during tidal breathing. 11 A human adult at rest breathes in an average of 11,000 L of air per day. 12 In any given setting, one may choose not to drink the water or eat the food that is available but generally has little choice in breathing the same air as everyone else. This makes air an environmental equalizer-conferring on it the unique potential to parse out evenly whatever it may contain. Further, infectious agents entering indoor air mix rapidly with no perceptible color or smell.

Although the potential of air to spread respiratory pathogens is well recognized, its ability to transmit enteric pathogens is not as well appreciated. Airborne particles containing enteric pathogens may be retained in the tonsillar region and swallowed for relocation to the gastrointestinal tract with subsequent replication there. 13 Ijaz et al 14 have provided a comprehensive list of human pathogens known or suspected to spread via indoor air.

The following are the main topics to be covered during the workshop.

Despite the recognized significance of indoor air as a vehicle for human pathogens, there are major gaps in our understanding of how well these pathogens remain viable under different environmental conditions. Such information is crucial to assessing the potential of a given pathogen to spread by air. Construction of an aerobiology chamber (approximately 24 m 3 ) will be described, and data from use of the chamber to test airborne survival of Staphylococcus aureus, Klebsiella pneumoniae, and Acinetobacter baumannii will be presented.

Many technologies claiming microbial decontamination of indoor air are on the market, but without proper validation of their claims. Information will be presented on ways to test such technologies using standardized protocols for registration and marketing purposes.

Because they may not be readily available and generally are unsafe and difficult to culture in the laboratory, it is rarely possible to use actual field strains of human pathogens in testing. This necessitates the use of surrogate microbes to generate data predictive of the behavior of pathogens. However, certain surrogates that are used commonly and recommended by regulatory agencies and standardssetting organizations alike are inherently unsuitable for experimental work in aerobiology. For example, K pneumoniae, frequently used as a surrogate for airborne gram-negative bacilli, does not survive aerosolization well because it is relatively fragile and unstable in air. Therefore, data generated with K pneumoniae likely will not be predictive of the behavior of actual human pathogens. This workshop will identify more suitable surrogates with supporting data.

Can microbial decontamination of indoor air reduce the risk for pathogen contamination of environmental surfaces?

Data will be presented to demonstrate that reductions in the levels of airborne microbes can indeed lead to corresponding reductions in the microbial contamination of environmental surfaces in a given setting. The use of integrated models could help analyze outbreaks, evaluate the relative importance of hygiene and infection prevention and control for policymakers, and provide guidance in environmental design for greater occupant safety and comfort. These will be illustrated using some recent examples, including severe acute respiratory syndrome, influenza, and Middle East respiratory syndrome.

Quantitative recovery of viable microbes from air is vital in aerobiologic studies. An update will be given on available methods, including their strengths and limitations.

Experimentation with airborne microbes is generally quite labor intensive and costly and requires special biosafety precautions. Mathematical models can assist greatly in optimizing aerobiology chamber design and in predicting the influence of furniture and other objects on the movement of microbes. Data will be presented with specific reference to a chamber that fully conforms to guidance from the U.S. Environmental Protection Agency.

Biofilms are not only common in the built environment, but they can be common sources of airborne pathogens. Such biofilms often contain several microbial species having complex interactions between them. This will be illustrated with the example of how fungi and legionellae coexist with potential risks to human health.

Product performance test guidelines: OCSPP 810.2500: air sanitizers-efficacy data recommendations

Decontamination of indoor air to reduce the risk of airborne infections: studies on survival and inactivation of airborne pathogens using an aerobiology chamber

Airborne spread of infectious agents in the indoor environment

World Health Organization. WHO guidelines for indoor air quality: selected pollutants

Origins of major human infectious diseases

Domesticated animals and human infectious diseases of zoonotic origins: domestication time matters

Ventilation rates and health: multidisciplinary review of the scientific literature

Humans differ in their personal microbial cloud

the role of super-spreaders in infectious disease

Secondary aerosolization of viable Bacillus anthracis spores in a contaminated US Senate Office

Influenza virus in human exhaled breath: an observational study

How much air do we breathe?

Concentration, size distribution, and infectivity of airborne particles carrying swine viruses

Generic aspects of airborne spread of human pathogens indoors and emerging air-decontamination technologies