Overview of Environment pressure of infection, Airborne Disease and Microbiota of Respiratory Tract and Airbiota in Pigs and Poultry.

Luis-Miguel Gomez-Osorio, Martin Masner, Andres Pio, William Serna, Laura Maccio

Abstract

This white paper comprehensively examines the influences of environmental pressures, airborne diseases, and microbiota on the respiratory tracts of pigs and poultry and their wider implications for animal production, public health and food security. The globalization of the livestock industry has escalated the risks associated with infectious diseases, demanding a shift towards improved pathogen prioritization and diagnostic tools. Notably, the air environment within animal housing is identified as a significant pathway for the transmission of antibiotic resistance genes (ARGs), especially under intensive farming conditions, poor ventilation, and during disease outbreaks. The paper highlights that pork and poultry are crucial for global food security, with Asia and Latin America being significant contributors to global production. The challenges of antimicrobial resistance and the need for sustainable practices are stressed, particularly in the context of rapidly growing poultry sectors in developing countries. The airborne transmission of pathogens and ARGs in livestock settings is underlined as a critical factor affecting animal and human health, necessitating advanced air diagnostic technologies and robust biosecurity measures.

Introduction

Pork and poultry production play a major role in global food security and trade worldwide, and infectious diseases pose a major threat to both productions. The globalization of the industry has facilitated the emergence and spread of pathogens. Animal epidemiology and food safety are highlighting that while the importance of zoonotic pathogens is increasing, the industry’s structural changes and intensive biosecurity production practices are shifting towards pathogen prioritization as well as the improvement in reliable tools of diagnostic (1).

Pork meat production

Pork follows as the second most consumed meat globally after chicken meat. This production has evolved significantly from traditional methods to more intensive and specialized systems aimed at meeting the global demands for food safety, animal welfare, and environmental sustainability. In Asia, pork consumption varies significantly by country, with some of the highest per capita consumption rates in the world. For instance, Hong Kong leads globally with a pork consumption of 55.24 kg per person per year, reflecting the strong cultural affinity for pork and its significant role in local cuisine. Mainland China and Macau are also highlighted as major consumers of pork, though specific quantitative details for these regions were not provided in the source (2).

This high level of consumption indicates the critical role pork plays in the diet and culinary practices across many Asian countries. In Latin America, pork meat production is a significant segment of the region’s agricultural economy. In 2020, Latin America and the Caribbean (LAC) produced 18% of the world’s meat, with pork accounting for 16% of the meat production in the region, following poultry and beef. Poultry meat was the most produced, while pork was third in terms of volume (3). By the end of 2021, the meat sector, including pork, in Latin America showed positive production figures, indicating a growing trend in several countries within the region.

Looking into the future, the USDA’s Livestock and Poultry report predicts a substantial increase in pork production for Latin America in 2024, with Brazil expected to lead in export growth. This indicates not just an increase in production but also a potential boost in the region’s economy due to the meat sector. Specifically, in 2021, Brazil’s swine meat production was forecasted to reach nearly 4.45 million metric tons carcass-weight equivalent (CWE), the highest in the region. However, meat production is also heavily influenced by external situations such as a globalized business influenced by politics, regulations and the pressure of disease outbreaks.

A more comprehensive view of the year 2022 shows that Brazil, Mexico, Argentina, Chile, and Colombia were the major contributors, accounting for 90% of the swine production in Latin America. There was a 4.2% increase in pork production from the previous year, rising from 8.4 million tons to 8.7 million tons. Interestingly, the import volumes also increased by 5.6%, which shows not just an internal growth in production but also a rising demand for pork imports into the region.

Thereby this indicates a robust and growing pork industry in Latin America, with Brazil being a significant player in both production and export. The overall positive outlook suggests that the region may continue to see growth in this sector, driven by both increased domestic demand and export opportunities.

Pork meat production and its contributions to both food security and food safety emphasizes that food safety is a complex issue that spans the entire pork production chain. According to the Canadian Food Inspection Agency, there are health risks associated with zoonotic diseases for both producers and consumers. They highlighted the importance of a food safety culture that includes awareness, surveillance, and traceability, as well as the implementation of science-based standards internationally. Food safety is not just about inspection but is a continuous process from farm to consumption, requiring prevention and response at every step (4).

Chicken meat production

As of 2021, poultry is the most consumed type of meat worldwide, with around 132.3 million tons consumed. Global chicken meat production points out that poultry, including chicken, also plays a pivotal role in food security and nutrition. It offers essential nutrients to humans with the advantages of short production cycles, at lower costs, as well as the ability to convert a wide range of by-products into meat and eggs. The poultry sub-sector is expanding rapidly, especially in developing countries, and is anticipated to continue growing due to factors such as population growth, rising incomes, and urbanization. However, this sector faces significant challenges related to food security, social issues, health, and environmental impact. Governmental authorities such as USDA, are increasing regulations in order to tackle ongoing problems and incipient subjects worth considering at large scale. These concerns include, high impact outbreaks, zoonotic diseases, antimicrobial resistance, and the environmental footprint of feed production, which contributes to climate change and resource consumption.

The global poultry industry has experienced remarkable growth in recent decades, largely driven by increasing demand for both meat and eggs. However, challenges such as the 2022 HPAI avian influenza wave have posed significant threats, resulting in bird culls and egg shortages. In terms of production, China has been the world’s largest producer of poultry meat since 2021, as a result of ASF, which dramatically reduced the pig population in China, and the government supported and incentivized chicken meat consumption, followed closely by the United States and Brazil. In 2022, an estimated 1,627 trillion eggs were produced worldwide, with China also leading as the top egg producer. The forecast for chicken meat production worldwide was set at 103.4 million metric tons for 2023, with Brazil and the United States driving this growth. Despite high feed costs, the industry benefits from low corn and soybean prices, which bolster production efforts across various countries. On a continental scale, Asia leads in chicken production, contributing to almost half of the global output. In 2021, Asia produced nearly 33 billion chickens, with significant contributions from Africa, North America, South America, Europe, and Oceania. At the country level, China and the United States are the biggest chicken producers. However, Brazil is projected to see a 3% increase in chicken meat production, reaching a record high and surpassing China’s output by a significant margin. The poultry industry’s expansion is integral to the worldwide meat market, affecting economies, food security, and trade. Continuous monitoring and adaptation to health and environmental challenges remain vital for sustaining this growth.

Airborne transmission

The air environment plays a crucial role in determining the health and productivity of poultry within poultry houses where the major components of the air, including gases, odors, and particulate matter in forms of dust or droplets which may carry pathogens on them. Airborne transmission of pathogens, particularly in poultry production and processing as well as laying hen environments, underline the significance of this route for the spread of diseases. Pathogens transmitted through the air can lead to harmful infections and spread over large distances via bioaerosols among flocks. The development of air diagnostic technologies is highlighted as a crucial measure to early detection and prevention to reduce the spread of airborne diseases. Advancements in these technologies are essential for reliable detecting tools and inactivating airborne pathogens which will improve health and performance in livestock animals. This highlights the importance of continued surveillance and advanced technological interventions to mitigate the risks associated with bioaerosols. These findings are crucial for public health and the poultry industry, emphasizing the need for robust biosecurity measures and air quality management in these settings.

The concentration and size distribution of airborne virus and bacteria are influenced by the type of poultry housing system (5). It was reported differences in floor versus cages in the total bacterial concentration being much higher in floor-type systems for laying hens (6). The size distribution of airborne virus and bacteria also change among size of housing systems, with a skew towards larger sizes in floor-type systems (7). However, bacterial and virus concentration and size distribution also differ among different poultry types, such as broilers and laying hens, which can be attributed to differences in virus and bacterial shedding as well as management practices, indoor and outdoor environmental conditions, and other factors affecting the physical and biological properties of airborne agents (8).

The indoor aerosol microbiome and resistome profiles are crucial for understanding the impact of airborne pathogens and drug resistance genes. The bacterial diversity and antibiotic resistance genes in layer hen houses’ aerosols can vary significantly with the laying period. Studies utilizing 16S rRNA gene sequencing and metagenomics have shown differences in bacterial communities and resistance genes across different laying periods, with a higher diversity observed during the peak laying period. Potential pathogenic bacterial genera have been identified carrying abundant antibiotic resistance genes (ARGs) of animal and human resistance including tetracyclines, β-lactams, and fluoroquinolones. The abundance of ARGs was higher in the late laying period, suggesting that the laying period significantly influences the bacterial community and resistome in layer house aerosols.

In the case of virus, avian influenza (AI) virus is one of the most studied in airborne transmission because of your spreading which is mainly by secretions including nasal, faeces, and saliva. The bird secretions can either be dried and suspended in the air for a long period of time or stay on the litter. This virus particles with AI re-aerosolized together with litter particles into the air by sand to clean the feathers as usual behaviour of birds. Droplets as well as dust particles carries AI may then be distributed into the poultry house environment and transmitted from barn to barn via ventilation system and transport of air (9).

The air environment in poultry houses is recognized as a significant pathway for the transmission of antibiotic resistance genes (ARGs) under several circumstances and conditions. These environments are complex, and the risk of ARG transmission through the air can be influenced by various factors including management practices, the use of antibiotics, and the physical setup of the facilities. Here’s a more detailed look at where and when the air environment becomes a crucial pathway for ARG transmission:

During high-density farming conditions, in intensive poultry farming operations where birds are kept in close proximity, often in large numbers. This is especially significant during peak production times when the density of birds increases the amount of fecal matter and the level of dust and bioaerosols in the air. High density conditions facilitate the rapid spread of microorganisms and ARGs through the air, as the close contact among birds increases the likelihood of transmission. Besides, the use of Antibiotics in poultry houses where antibiotics are used regularly, either as prophylactics, growth promoters, or therapeutics favour ARG transmission. Particularly, after the administration of antibiotics, when the microbial ecosystem is disturbed, and resistant bacteria can proliferate. Therefore, the use of antibiotics can create selective pressure, leading to the emergence and spread of resistant bacteria. These bacteria or their ARGs can become airborne and spread through the house. In addition, poor ventilation and air quality control in poultry houses with inadequate ventilation systems or those that lack proper air filtration and purification impair the environment with the accumulation of harmful gases, dust, and bioaerosols, including those carrying ARGs. This increases the risk of these genes being transmitted through the air. Indeed, during periods of extreme temperatures when ventilation systems may struggle to maintain optimal air quality.

During the later stages of production cycles when litter has accumulated and possibly become moist and heavily contaminated, litter management may be a concern. In poultry operations where litter is not regularly or properly managed leads to increased microbial activity and the generation of dust and bioaerosols that can carry ARGs, facilitating their airborne spread.

In the case of disease outbreaks, these often result in increased use of antibiotics and disruptions to the normal microbial environment, both of which can promote the spread of resistant bacteria and ARGs through the air. Also, an inadequate cleaning and disinfection in facilities where cleaning and disinfection protocols are insufficient or not rigorously followed, can leave residual bacteria and ARGs, which can be resuspended in the air of newly populated houses. Lastly but least, handling and movement of birds and materials, during handling, transport, and replacement operations can stir up dust and bioaerosols that contain microorganisms and ARGs, facilitating their spread through the air.

Airborne diseases in pigs

Airborne transmission of swine bacteria and viruses underscores the critical role of biosecurity in pig farming. Aerosol transmission presents significant challenges, especially with diseases like African swine fever (ASFV) in Asia, where traditional controls like vaccines are ineffective bioaerosols, small particles capable of carrying pathogens, are a primary concern, as swine respiratory activities can release viruses and bacteria into the air, leading to widespread disease dissemination.

Today, there is a great urgency to detect pathogens in the air in the production cycle as early as possible. For example, the risk of long-distance transmission (over 150m) of viruses like foot-and-mouth disease (FMDV) and short-distance transmission (up to 150m) of others like African Swine Fever Virus (ASFV), affecting both inter-farm and intra-farm biosecurity. Factors influencing aerosol transmission include particle size, viral strains, host sensitivity, weather, and environmental conditions.

Environmental pressure of infection. A new concept in veterinary epidemiology

The concept of environmental pressure of infection which can be defined as a quantity and to a lesser degree by the quality of an infectious agent in the proximity of a potential host, for example poultry and swine species. In endemic countries, infection pressure is greater than “0” however, differences in infection pressure occur among endemic countries. In livestock animals including poultry and swine species has gained attention as a critical component in understanding disease transmission. It also includes the impact of agricultural practices on the emergence and spread of diseases, and the role of microbiota in disease dynamics. A comprehensive literature review on the environmental pressure of infection and pathology in poultry and swine species would cover several aspects, including the pathogens affecting these species, the amount of pathogens in a define area, host immune response among others.

Microorganisms reside in the environment as remnants of agricultural activity, and they combine with the threats that come from the environment. To what extent these pathogens remain, are transmitted within the same environment and to others, multiplying in production animals or in hosts or in the environment, relates to the threat they pose. All these factors add to the environmental pressure of infection, which is greater the more readily each of these processes occurs. The residual levels of pathogens in the environment at a lot change, the threat of a shed contaminated with a transmissible pathogen in close geographical proximity, and the transmission of diseases by humans (zoonoses) and non-humans (vectors/pests) give us day-to-day examples of how this pressure is exerted on production animals.

This pressure is also multipathogenic, since it depends on all species and variants of microorganisms capable of threatening the health of a group of animals.  Therefore, specific and generic studies on viral and bacterial composition on farms bring us closer to their understanding, and the importance of their management.

Starting with poultry, the industry is heavily impacted by viral and bacterial infections, and there is a concern about multi drug-resistant (MDR) pathogens. However, and according to WHO, the principal cause of MDR in humans are the self-prescription and wrong prescription.  This has led to an exploration of novel antimicrobial strategies as a precaution principle in veterinary medicine and a market-driven trend, such as the use of natural alternatives to inhibit bacterial pathogens including essential oils, pre and probiotics, short and medium chain fatty acids, bacteriophages, etc. Research has focused on pathogens like C. perfringens, Salmonella spp. Mycoplasma sp. and E. coli as well as virus such as infectious bronchitis, which are major concerns due to production losses, animal mortality, and food safety issues. Studies have identified specific bacteriocins that can inhibit C. perfringens and potentially improve the health and growth performance of broiler chickens.

The review of lung microbiota in a broader context, although focusing on mice, offers insights into the possible effects of airbiota on livestock. The dysregulation of lung microbiota was linked to pulmonary fibrosis in mice, suggesting the lung-resident microbiota is a key driver of fibrotic disease. This could have implications for the management of livestock health, indicating that similar dysregulation may affect animals and pointing to potential treatment avenues.

The respiratory tract microbiota and Airbiota

The respiratory tract microbiota plays a crucial role in the health and performance of poultry and pigs. A study focusing on laying chickens and turkey breeders provides data on the microbial community in the respiratory organs, indicating the significance of these microbes for the poultry industry (10).

One study employing 16S rRNA gene analysis to study the respiratory microbiota of chickens noted that while many studies have been done on human respiratory microbiota, limited research has been published on the respiratory microbiota of healthy chickens. These microbial communities are essential for maintaining respiratory health (11).

Research has also explored how influenza infection affects the upper respiratory tract (URT) microbiota in chickens. It was found that the H9N2 avian influenza virus (AIV) infection reduces the alpha diversity indices in the URT microbiota during the acute phase of infection, with a significant increase in the family Lactobacillaceae within the respiratory microbiota (12).

Furthermore, there are age-related differences in the respiratory microbiota of chickens. Studies using culture-based methods have isolated a wide variety of bacteria and fungi from the respiratory tracts of healthy chickens. These studies have provided insight into the diverse microbial life that can influence respiratory health and disease resistance (11).

The type of breeding environment also affects the microbiota of the respiratory tract in chickens. In a study comparing isolator, floor, and cage breeding, 75 strains of Lactobacillus species were isolated from all respiratory organs and the intestine, demonstrating the impact of breeding conditions on respiratory tract microbiota (13).

It is worth noting that it can find microorganisms from the gut that end up in the respiratory tract (as it can also be found in the air), but the routes in this case could be self-inoculation due to the feather flying, or also the recirculation of dried feces through the air, or by another bird in the vicinity.

The microbiota of the respiratory tract in pigs reveals a growing interest in understanding the complex interplay between these microorganisms and porcine health. Interesting findings  indicates critical features that can influence porcine respiratory microbiota mainly in the lungs, nasal cavity, and tonsils (14). A study focusing on the upper respiratory tract microbiota showed that the use of antibiotics could alter its composition. However, by the finishing phase of the pigs’ growth, the bacterial populations tended to uniformity regardless of whether the pigs had respiratory diseases, suggesting a stabilizing effect over time (15).

The environmental complexity where pigs are reared also has an impact on the respiratory and gut microbiota. This relationship is not yet fully understood but is recognized as a significant factor in determining the optimal housing system to promote animal health and production (16).

The bacterial topography of the respiratory tract in pigs has been mapped for the first time, comparing different sites within the tract. It was found that the microbiota in the choana (part of the nasal cavity) closely resembles that of the trachea, implying that the posterior portion of the nasal cavity might be the primary source of bacteria for the lower respiratory tract (17). The respiratory microbiome is crucial for maintaining respiratory physiology and may influence the individual susceptibility to diseases in pigs. This has led to a focus on the role of microbiota in respiratory health, with many studies aiming to unravel the complexities of these microbial communities (14,18–21).

One study aimed to characterize the bacterial communities across various sites in both the upper (nostrils, choana, and tonsils) and lower (trachea and lungs) respiratory tract of pigs. Understanding these complex structures and interactions is still in the early stages but is crucial for developing strategies to manage respiratory health in pigs (17).

Moreover, there’s an interest in how the lower respiratory tract microbiota is associated with other tissues and environmental microbiomes. For example, one study described the microbiome of tracheal and oral fluids, air, and faeces in pigs during the late stage of Mycoplasma hyopneumoniae infection. This research assessed the association between the tracheal microbiome and those from other sources, which could have implications for understanding disease dynamics and transmission (22).

These studies collectively provide insight into the composition and role of the respiratory microbiota in poultry and pigs, influencing the understanding of animal health and disease, and informing future research directions and strategies for disease prevention and control in poultry and pig farming and highlights their implications for health management. The research indicates that factors such as age, disease, and breeding conditions can significantly influence the composition of respiratory microbiota, which in turn can impact animal health and productivity. Further research in this field is essential for developing better strategies to manage respiratory health in chickens.

Airbiota it is a new term which refers to the community of microorganisms present in the air. Particularly in relation to pig and poultry farming, indicates a complex interplay between these microorganisms and the health and growth of the animals, as well as potential impacts on human health. Airbiota may be related with the concept of intestinal microbiota which has been more studied in the past (23).  It was shown that the link between the porcine intestinal microbiota of pigs and their growth and feed efficiency, suggesting that microbiota-targeted strategies could improve productivity. Identifying reliable microbial predictors of host phenotype is challenging due to environmental factors and differences along the intestine. However, the scientific information about airbiota is scarce (24).

This is not only from the pig production and health standpoint, in terms of human health, studies have looked at how occupational exposure to microbes on pig farms may impact the microbial communities in human guts. However, the implications of this exposure are still not fully understood (25). Additionally, there’s an interest in understanding how the indoor-air microbiota of pig farms may influence the human nasal microbiota. Samples collected from pig farms indicate a potential influence, but the exact nature of this relationship requires further investigation (26).

Conclusions

Pork and poultry production are essential for global food security, with pork being the second most consumed meat worldwide and poultry the most consumed. The significant consumption rates in Asia and the growing production in Latin America highlight the global reliance on these sectors. The air environment in animal houses plays a pivotal role in the health and productivity of livestock.

Poor air quality can lead to the spread of pathogens and ARGs, impacting animal health and potentially transferring risks to humans. Reducing environmental pressure of infection through effective monitoring and management is essential to minimize these risks.

The transmission of ARGs through air in poultry houses is particularly concerning during high-density farming, when antibiotics are used, and where ventilation is inadequate. These conditions facilitate the rapid spread of ARGs, posing challenges to both animal welfare and public health.

To combat the spread of airborne diseases and ARGs, this paper advocates for enhanced biosecurity, prudent use of antibiotics, and improved air quality management. These strategies are vital to maintaining healthy livestock and safeguarding public health.

The adoption of advanced diagnostic technologies, air filtration systems, and rigorous biosecurity protocols is recommended to detect and control airborne pathogens and ARGs effectively. Monitoring and surveillance of air quality and microbial communities are crucial for timely interventions.

Further research is needed to understand the complex interactions between airbiota, respiratory microbiota, and external environmental factors. Policymakers are urged to support research and implement regulations that address the challenges highlighted, particularly concerning antibiotic use and air quality management.

Raising awareness about the importance of air quality in animal production settings and its impact on disease transmission and antibiotic resistance is essential. Training for farmers, veterinarians, and workers can enhance understanding and compliance with best practices.

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