Edited by: Artur Summerfield, Institute of Virology and Immunology, Switzerland
Reviewed by: Alejandro Ramirez, Iowa State University, United States; Caroline Duchaine, Laval University, Canada
Specialty section: This article was submitted to Veterinary Infectious Diseases, a section of the journal Frontiers in Veterinary Science
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Modern swine production facilities typically house dense populations of pigs and may harbor a variety of potentially zoonotic viruses that can pass from one pig generation to another and periodically infect human caretakers. Bioaerosol sampling is a common technique that has been used to conduct microbial risk assessments in swine production, and other similar settings, for a number of years. However, much of this work seems to have been focused on the detection of non-viral microbial agents (i.e., bacteria, fungi, endotoxins, etc.), and efforts to detect viral aerosols in pig farms seem sparse. Data generated by such studies would be particularly useful for assessments of virus transmission and ecology. Here, we summarize the results of a literature review conducted to identify published articles related to bioaerosol generation and detection within swine production facilities, with a focus on airborne viruses. We identified 73 scientific reports, published between 1991 and 2017, which were included in this review. Of these, 19 (26.7%) used sampling methodology for the detection of viruses. Our findings show that bioaerosol sampling methodologies in swine production settings have predominately focused on the detection of bacteria and fungi, with no apparent standardization between different approaches. Information, specifically regarding virus aerosol burden in swine production settings, appears to be limited. However, the number of viral aerosol studies has markedly increased in the past 5 years. With the advent of new sampling technologies and improved diagnostics, viral bioaerosol sampling could be a promising way to conduct non-invasive viral surveillance among swine farms.
Bioaerosols can be defined as fine particles ranging in size and composition that are suspended in the air and considered to be derived from a biological source or to affect a biological target (
This literature review was conducted to better understand the source and types of viral bioaerosols within and around swine production facilities, the scope of sampling methodologies, and the current state of research. The information summarized from this review may also serve as a collated resource for other researchers.
Following PRISMA guidelines, a systematic online search of three scientific abstract indexing databases (PubMed, Web of Science, and CAB Abstracts), with no restriction on year of publication, was performed using the following structured query: (bioaerosol* or bio-aerosol*) and (swine or pig* or hog* or barrow* or gilt* or sow or sows or boar or boars or porcine or pork or suidae or sus scrofa). Given that PubMed is a database specific to biomedical and life science research, Web of Science and CAB Abstract databases were included to capture a broader range of disciplines and information sources, including engineering, agriculture, and other technical journals. Search results were manually reviewed and abstracts meeting the following inclusion criteria were retained: (1) peer-reviewed and published scientific report, (2) research occurred in an experimental swine unit, swine production facility, or market, and (3) a bioaerosol sampling strategy was utilized. Articles that were reviews, comments to editor, perspectives, personal opinions, did not present sampling result data, did not have a full-text article available in English, or did not meet the inclusion criteria listed above were excluded. Full reports were reviewed and summarized according to their date of publication.
From a search conducted April 5, 2017, results yielded 68 publications from PubMed, 180 publications from Web of Science, and 90 publications from CAB Abstracts. After 128 duplicates were removed, 210 publications remained. These were screened, and 114 articles that did not meet the initial inclusion criteria were removed leaving 96 articles. Finally, 23 full-text articles that did not present sufficient data, were not available in English, or did not sufficiently describe the methods were also removed, resulting in a final article count of 73 (Figure S1 in Supplementary Material).
After the selection and screening procedures were completed, 73 scientific reports that met the inclusion criteria for this review remained (Table S1 in Supplementary Material) (
In this literature review, articles were searched and summarized to better understand the source and types of bioaerosols detected in and around swine production facilities, as well as the sampling methods used to detect them. Based on the articles evaluated, different bacteria were the predominantly sampled bioaerosol targets, with several studies identifying elevated levels of both Gram-positive and Gram-negative bacteria, including
Seasonal variation was assessed in multiple studies identifying trends in the rates of bioaerosol detection between seasons, which also varied based on the type of target being sampled (
One of the first studies to assess bioaerosol transmission of viruses between swine was conducted in 1997 by Torremorell et al., which evaluated the airborne transmission of porcine reproductive and respiratory syndrome virus (PRRSV) under experimental conditions among nursery pigs (
These seminal works were followed by 16 additional studies (
Evaluation of reviewed bioaerosol studies assessing viruses (
Reference | Target virus(es) | Strength(s) |
---|---|---|
Torremorell et al. ( |
Porcine reproductive and respiratory syndrome virus (PRRSV) | Evaluated virus viability Confirmation of source population infection using virus isolation and serology Assessed strain differences Robust controls |
Otake et al. ( |
PRRSV | Evaluated virus viability Confirmation of source population infection using virus isolation and serology Assessed strain differences Robust controls Evaluated long-distance transport |
Pitkin et al. ( |
PRRSV | Evaluated virus viability Confirmation of source population infection Robust sampling strategy Year-long sampling |
Dee et al. ( |
PRRSV | Evaluated virus viability Confirmation of source population infection Robust controls Evaluated long-distance transport |
Otake et al. ( |
PRRSV | Evaluated virus viability Confirmation of source population infection Robust controls Evaluated long-distance transport |
Verreault et al. ( |
Porcine circovirus type 2 (PCV2) | Multi-year sampling Sensitivity of detection assay explored |
Linhares et al. ( |
PRRSV | Evaluated virus viability Confirmation of source population infection Robust controls Pigs sampled concomitantly with air |
Corzo et al. ( |
Influenza A virus (IAV) | Evaluated virus viability Confirmation of source population infection Subtyping conducted Evaluated long-distance transport |
Corzo et al. ( |
IAV | Bioaerosol detection and viral secretion in pigs directly compared |
de Evgrafov et al. ( |
PCV2 | Used controls to rule out contamination Used advanced genomic methods |
Alonso et al. ( |
Porcine epidemic diarrhea virus (PEDV) | Evaluated virus viability Confirmation of source population infection Evaluated long-distance transport |
Brito et al. ( |
PRRSV | Used controls to rule out contamination Used GIS modeling to correlate sampling with farm density Used sequencing techniques and phylogenetic analysis |
Corzo et al. ( |
IAV | Evaluated virus viability Confirmation of source population infection Robust controls Viral shedding assessed over time |
Alonso et al. ( |
IAV PRRSV PEDV |
Multiple viruses concomitantly assessed Particle size evaluated Evaluated virus viability Confirmation of source population infection Robust controls Pigs sampled concomitantly with air Infectivity of air samples assessed using swine bioassay |
Choi et al. ( |
IAV | Human, animal, and environmental sampling conducted concomitantly Evaluated virus viability Documented possible aerosol transmission of swine-sourced virus to humans Sequencing used to compare detected virus RNA gene segments |
Anderson et al. ( |
IAV | Human, animal, and environmental sampling conducted concomitantly Seasonal comparisons made Risk factors evaluated Sampling types statistically compared |
Neira et al. ( |
IAV | Sampling captured during outbreaks under field settings Animal, environmental, and air sampling conducted concomitantly Evaluated virus viability Sampling types statistically compared |
O’Brien and Nonnenmann ( |
IAV | Human exposure directly assessed Two samplers compared Confirmation of source population infection Physical conditions of farms assessed |
Alonso et al. ( |
PRRSV PEDV |
Particle size evaluated Confirmation of source population infection Sampling types statistically compared |
Several studies have documented detection of PRRSV, IAV, and PEDV virus genomic RNAs at various distances downwind from swine barns with infected source populations (
Graphical depiction of influenza A virus (IAV), porcine reproductive and respiratory syndrome virus (PRRSV), and porcine epidemic diarrhea virus (PEDV) RNA detection downwind from farms with infected source populations: (A) PRRSV RNA detected up to 9.1 km away from infected source population; (B) PRRSV RNA detected 4.7 km away from infected source population; (C) PRRSV infects naïve pigs 120 m away from infected source population; (D) IAV RNA detected up to 2.1 km away from infected source population; and (E) PEDV RNA detected up to 16.1 km away from infected source population.
Despite the increase in the number of studies that have been conducted using bioaerosol sampling for the detection of viruses, such approaches may have some limitations given the difficulty of determining the correct sampling parameters (i.e., flow rate, collection media, volume, etc.). Optimization is essential to capture aerosolized viruses and to maintain their viability throughout the collection process. Identifying viable virus is important because it allows for a more informed risk assessment in the environments being sampled. A viable virus carries a greater transmission risk to exposed humans or animals. In contrast, if the virus is already inactivated (by UV light or drying or other means) when it is detected, it likely poses minimal risk in terms of airborne transmission. This emphasizes the need for additional field-based studies that focus on the optimization of collection parameters to improve the recovery of viable virus.
Another important factor that contributes to the viability of aerosolized viruses is particle size. In a study conducted by Zuo et al., the authors demonstrated a close relationship between particle size of three different animal viruses (gastroenteritis virus, swine IAV, and avian IAV) and the infectivity and survivability of those viruses after collection using a bioaerosol sampling device (
A further challenge to using bioaerosol sampling as a method for virus surveillance and risk assessment is that commercially available air samplers are not optimally designed for the collection of submicron particles (<1 μm), for which the collection efficiencies tend to be low. Samplers are instead designed for the collection of micrometer-sized particles such as fungal spores and bacteria (
Overall, the bioaerosol sampling research studies evaluated in this review were predominately focused on the detection of bacteria and fungi and relied on broad-spectrum microbial detection as an indicator for overall bioaerosol burden. In addition, sampling strategies were found to utilize a wide variety of methodologies, with no apparent consistency between research groups, suggesting a lack of standard methods for performing bioaerosol studies in swine production settings. Many of the researchers in the reviewed studies agreed that there are insufficient data regarding virus aerosol burdens in swine production facilities to assess their potential impact upon human and animal health. Furthermore, only a few studies have since been conducted using multi-faceted strategies to sample animals, humans, and the environment. This approach will be critical in future studies to better understand transmission pathways and virus ecology. Finally, only one study was conducted in Mainland China, a region with the largest and fastest growing swine industry in the world (
Recent breaches in animal production biosecurity in the United States, resulting in the incursion of H5N2 avian IAV (
BA conducted the literature review and wrote the manuscript; JL and MT helped revise the manuscript to add important scientific content and refine the interpretation of the results; GG conceived of the idea of the review and helped revise the manuscript to add important scientific content and refine the interpretation of the results. All the authors reviewed the final version of the manuscript and agreed to its submission.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors would like to thank Drs. Tara Sabo-Attwood, Song Liang, and Maureen Long for their scientific advice during the early stages of developing this manuscript. The authors would also like to thank Kristine Alpi for her help in optimizing the database search query. This research was supported with GG’s discretionary funding at Duke University and through a grant from the National Institute of Allergy and Infectious Diseases (grant number R01-AI108993 to GG). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
The Supplementary Material for this article can be found online at