Introduction to the A&WMA 2023 Critical Review: Environmental sampling for disease surveillance: Recent advances and recommendations for best practice

Roya Mortazavi

The important role of bioaerosols in both human health and in atmospheric sciences has been highlighted by many worldwide incidences that occurred in the last two decades. The global incidence of Severe Acute Respiratory Syndrome (SARS) epidemic in 2003, China, (Zhong et al. 2003), H1N1 influenza epidemic in 2009, Mexico, and California (USA) (Van Kerkhove et al. 2011), Middle East Respiratory Syndrome (MERS) in 2013, Saudia Arabia (Hageman 2020), the 2019 pandemic Covid-19, caused by SARS-CoV-2, China (Rothan and Byrareddy 2020), and the ongoing threat of bio-terror attack by the deliberate release of agents such as anthrax or smallpox (Taylor, Lai, and Nasir 2012), further emphasize the necessity of having a more holistic critical views on the significance of bioaerosols. It calls for the fundamental, coherent, and standardized research toward execution of the role of bioaerosols, including its interactions with other molecules, exposure, and its mechanism of action.

Bioaerosols are simply defined as biological airborne particles that are temporally and spatially directly released into the atmosphere from all types of environments, including soil, freshwater, and oceans. They may originate from plants, animals, or microorganism (live/dead bacteria, fungi and viruses) or comprise their by-products such as fungal spores, plant pollen, various fragments and excretions (Humbal, Gautam, and Trivedi 2018). The complexity, and diversity of bioaerosols composition/shapes are also reflected into its size, which range from 0.001 to 100 µm (Kim, Kabir, and Jahan 2018).

Bioaerosols form a complex mixture of particulate matter (PM) with chemical aerosols (e.g., inorganic and organic components) (Jahne et al. 2015) which impact the atmospheric chemistry and physics. They can influence the global climate system and precipitation through different mechanisms such as scattering and absorbing radiation (Després et al. 2012), cloud micro physical processes by acting as ice nuclei (Vali et al. 1976), and cloud condensation nuclei (Fröhlich-Nowoisky et al. 2016). The dispersion and transport of bioaerosols through atmospheric long distances movement (Maki et al. 2019; Meola, Lazzaro, and Zeyer 2015; Peter et al. 2014) also generate an increase in diversity of genetic poll with the potential of the evolvement and alteration of the ecosystem’s dynamic (Burrows et al. 2009).

The spread and exposure to airborne pathogen may have adverse impact on agriculture and human public health (Humbal, Gautam, and Trivedi 2018). The main categories of diseases associated with exposure to bioaerosols are: i) acute toxic effects, ii) infectious diseases, iii) respiratory diseases, and iv) cancer. Respiratory inflammation and sensitivities (i.e., asthma) are triggered and developed upon exposure to the microbial and their cellular components (e.g., pollen and fungal allergens and lipopolysaccharide) (Beck, Young, and Huffnagle 2012; Rohr et al. 2015), microorganism-derived molecules (endotoxins, membrane lipopolysaccharides shed by Gram-negative bacteria) and fungal mycotoxins (Braun-Fahrländer et al. 2002; Jie et al. 2011).

Exposure to bioaerosols occurs in indoor environment as well as in diverse industrial occupational activities such as waste sorting, composting, and recycling industry (Van Tongeren, Van Amelsvoort, and Heederik 1997; Wikuats et al. 2020); detergent industry (Schweigert, Mackenzie, and Sarlo 2000); agricultural and food processing activities (Sandiford, Tee, and Taylor 1994); and in the livestock industry. In accord to high level exposure, elevated prevalence of respiratory symptoms and airway inflammation have been documented in industrial workers (Papageorgiou et al. 2021; Sigsgaard et al. 1994; Thorn, Beijer, and Rylander 1998; Wouters et al. 2002).

Besides in industrial facilities, it is estimated that bioaerosols are responsible for approximately 5% to 34% of indoor PM air pollution (Mandal and Brandl, 2011). Bioaerosols from outdoor sources enter residential indoor air by passing through windows, doors, heating ventilation, and air conditioning systems. Plus, major indoor sources are recognized as: building materials, furnishings, pets, house plants, and humidifiers (Wéry, Galès, and Brunet 2017). Regular or ordinary human activities (e.g., coughing, washing, toilet flushing, talking, walking, sneezing, and sweeping floors) are also capable of generating bioaerosols (Chen and Hildemann 2009; Nazaroff 2016). Though, the extent of formation and dispersion of microorganism are substantially controlled by ventilation system and environmental conditions such as humidity and temperature (Dedesko and Siegel 2015; Kohanski, Lo, and Waring 2020; Morawska et al. 2020).

With the exception of specific traditional pulmonary infectious agents, such as influenza virus (causing common flu), Streptococcus pneumoniae (causing pneumonia), Mycobacterium tuberculosis (causing tuberculosis), and Aspergillus fumigatus (causing lung aspergillosis) (Hunter 2016; Latgé and Chamilos 2019; Pleschka 2013) and a few individual components such as bacterial endotoxin and specific allergens; little is known about the specific entity(s) of bioaerosol responsible for adverse health effect, mechanism of action and the precise role of biological entities. Additionally, there are no limits of exposure for the constituents of bioaerosols. This is due to the difficulty of establishing dose-response effect and safe levels of exposure to bioaerosols for not having background data contamination, the heterogeneity of the experimental design, the lack of standardized sampling methods, analysis, and valid standard quantitative exposure assessment methods among studies. Although a Dutch Expert Committee has recommended health-based limits of 104 cfu/m³ for bacteria in air and 90 EU/m³ (5 ng/m3) for endotoxins (Swan et al. 2003).

The 53rd Annual A&WMA Critical Review offers a comprehensive knowledge of the bioaerosol analytical Techniques with their limiting factors critical in determining the efficiency and reliability of bioaerosol sampling. The purpose of this review is to give a summary on: i) recent advances or applications of aerosol sampling technology, and to provide an overview of wastewater and surface sampling techniques; ii) to create a framework to design infectious disease sampling that may use multiple sampling modalities; iii) to propose a straightforward guideline for sampling infectious aerosols; and iv) to identify areas of future research. This paper offers a guide to better selections of bioaerosol sampling based on various conditions and needs. The authors examine the current practices and recent advances in technology that are used for environmental sampling of infectious diseases, note limitations, and recommend best practices and directions for future research.2013

The authors, Dr. Joshua L. Santarpia, Ms. Elizabeth Klug, Ms. Ashley Ravnholdt, and Mr. Sean M. Kinahan, explore the topic by giving a historical background on bioaerosols, its discovery by Louis Pasteur and John Tyndall in the 1860s and 1870s; its application in the sampling of sewage water in 1885. The continuation and the acknowledgment of the role of microorganism in human disease by routine, random sampling especially in hospital environment, and its usage in biological attack necessitate the needs for advancement of technologies that monitor potential threats in real-time, as well as collection of aerosol samples for offline analyses.

This review presents a framework for developing an environmental sampling plan based on the responses to three main questions: a) what is the purpose?; b) what actions will be taken?; and c) what are the potential hazards? The purpose of the sampling might fall into the following categories: i) outbreak investigation, ii) risk assessment, iii) disease surveillance, iv) biodefense, and v) environmental characterization. Environmental sampling plan must address what is known about the disease, and its routes of transmission. The actions taken based on the data collected can have implications on: i) scientific advancement, ii) remediation, iii) protection from exposure, and iv) medical interventions.

The techniques used for aerosol collection and its biological analysis and characterization can be categorized as filtration, impaction, impingement, cyclonic collection, and electrostatic deposition. Optical spectroscopy, mass spectrometry, and atomic spectroscopy are used for instantaneously (seconds to minutes) detection and classification of biological aerosols. Wiping methods with moistened swabs, sponge sticks, or gauze pads are used for sampling of surfaces contaminants of inanimate especially in hospitals environment. The choice of eluant has an impact on the detection sensitivity.

Several techniques that are used for identification of an infectious agent with high accuracy are: polymerase chain reaction (PCR) or loop-mediated isothermal amplification (LAMP), where a unique fragment of the organism’s DNA or RNA is recognized by short RNA or DNA strands; ii) immunoassay, where antigenic proteins of the organism are recognized by antibodies; iii) sequencing, where all or large fragments of the organism’s genome are read and recognized; iv) clustered regularly interspaced short palindromic repeats (CRISPR) based assays, where guide-RNAs recognize specific segments of the organisms genome and an engineered enzyme reports binding of the guides; and v) digital droplet PCR (ddPCR).

Covid-19 has tremendously alleviated the environmental monitoring and sampling in hospitals and in public spaces such as public schools, airplanes, cruise ships, transportation, quarantine facilities, homes, and wastewater. The authors highlight the importance of having common guidelines for measurement and identification of infectious aerosols by the research and public health communities as it improves the acceptance of new information. The skepticism of acceptance by public health organizations, including the U.S. Centers for Disease Control (CDC) and the World Health Organisation (WHO) of published letters from the scientific community (Morawska and Milton 2020) that suggested the role of aerosols containing SARS-CoV-2 RNA in COVID-19 pandemic further marks the need.

A&WMA appreciates the leadership of Dr. Joshua L. Santarpia in preparing this review. Dr. Santarpia is an Associate Professor of Microbiology and Pathology and Program Director for Biodefense and Health Security Degree Program at the University of Nebraska Medical Center. He is also the Science and Technology Advisor for the National Strategic Research Institute at the University of Nebraska. His research interest is in the field of aerobiology, and the study of airborne microorganisms. He has worked extensively on biological sensors, optical, building, and facility sensing networks, and has developed aerosol measurement tools, including those for unmanned aerial vehicles and for biodetection/collection activities for both U.S. Department of Defense (DOD) and U.S. Department of Homeland Security (DHS). He has developed novel methods to study bioaerosol hazards in medical environments such as characterizing SARS-CoV-2 aerosol in the patient environment and characterizing aerosol risk in public spaces.

A&WMA members and interested parties are invited to read, attend, and comment on the 53rd Annual Critical Review, which will be held as part of A&WMA’s 2023 Annual Conference & Exhibition in Orlando, FL, on Thursday, June 8, 2023, 8:00 to 10:00 am EDT (https://www.awma.org/ace2023registration). Following the review presentation, a commentary from a panel of invited experts will critique the review, address additional issues, and offer alternative perspectives. This year’s invited discussants are: Gary S. Casuccio, Vice President and Senior Scientist, RJ Lee Group; Dr. John A. Lednicky, a Research Professor of Environmental and Global Health with the College of Public Health and Health Professions at the University of Florida, Gainesville; and Dr. John G. Watson, a Research Professor at the Desert Research Institute of the Nevada System of Higher Education.

The authors and discussants will also accept and answer comments from the floor and from written submissions to the Critical Review Committee (CRC) Chair. The chair will condense and summarize these points in the October issue of JA&WMA. Comments should be submitted in writing to CRC Chair Susan S. Wierman at [email protected] by July 13, 2023. Members are encouraged to suggest topics and authors for future critical reviews and to volunteer for membership on the Critical Review Committee to assist with the process.

Disclosure statement

No potential conflict of interest was reported by the author.

Additional information

Notes on contributors

Roya Mortazavi

Roya Mortazavi, PhD, is a Research Associate in the Department of Atmospheric and Oceanic Sciences, McGill University, Montreal, Quebec, Canada. Dr. Mortazavi is a member of the A&WMA Critical Review Committee and was the coordinator of this year’s Critical Review.