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Buoio, E.; Cialini, C.; Costa, A. Pollutants Generated in Piggeries. Encyclopedia. Available online: https://encyclopedia.pub/entry/47174 (accessed on 18 June 2024).
Buoio E, Cialini C, Costa A. Pollutants Generated in Piggeries. Encyclopedia. Available at: https://encyclopedia.pub/entry/47174. Accessed June 18, 2024.
Buoio, Eleonora, Chiara Cialini, Annamaria Costa. "Pollutants Generated in Piggeries" Encyclopedia, https://encyclopedia.pub/entry/47174 (accessed June 18, 2024).
Buoio, E., Cialini, C., & Costa, A. (2023, July 24). Pollutants Generated in Piggeries. In Encyclopedia. https://encyclopedia.pub/entry/47174
Buoio, Eleonora, et al. "Pollutants Generated in Piggeries." Encyclopedia. Web. 24 July, 2023.
Pollutants Generated in Piggeries
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Reducing the sources of stress on farms allows for enhanced animal welfare and productivity. Aerial contaminants and pollutants that can be found in indoor animal houses are among these stressors. In Italy, the guidelines to assess animal welfare in pig farming are displayed in a protocol named “ClassyFarm”, based on European legislation. Specific indications are given on the microclimatic conditions of livestock indoor environments (temperature, relative humidity, dustiness) and air quality, especially regarding harmful gases such as ammonia (NH3) and carbon dioxide (CO2). Nevertheless, the recommended measurement techniques for dust and harmful gases are not satisfactory.

air quality assessment animal welfare pigs aerial pollutants pollutants measurements

1. Introduction 

In the UE and in the Italian legislation (D.L. 146/2001, all. 1, par. 10), the indication given about livestock air quality is to keep “the air circulation, the amount of dust, the temperature, the relative humidity, and the gas concentration within certain limits that are not harmful to animals”, but no limits are given. As mentioned above, defined maximum limits were provided by the Scientific Veterinary Committee (1997, Table 1).
Currently, different welfare protocols are available, but they are voluntary-certification systems whose aim is to make the farm more environmentally and animal-friendly.
Air pollutants generated by swine husbandry include gases such as ammonia, carbon dioxide, nitrous oxide, methane, and hydrogen sulfide, but also particulate matter and microbial by-products. Methane, in piggeries, is originated by anaerobic fermentation of slurry at high levels in deep pits, and it can be considered nontoxic. [1][2].
Pigs raised in inadequate air quality conditions have a lower feed intake, a worse feed conversion efficiency, and an increased cortisol concentration [3]. In addition, in polluted environments, animals may show less playful behavior [4] and be more prone to aggressivity and cannibalism phenomena [5][6], resulting from a sense of disorder.
Table 2 shows the possible outcomes of different pollutants at low concentrations on animal health.
There are several experimental studies on the effects of these gases on animal health, as well as recent reviews [1][7][8][9]. Experience shows that high concentrations of harmful gases mainly occur in housing systems with insufficient ventilation and high temperatures, while open environments have higher air circulation and do not present such problems.
In ClassyFarm, specific limits are present only for ammonia and carbon dioxide, the indicated reference for an appropriate condition of NH3 and CO2 must be 10–20 ppm and less than 3000 ppm, respectively; an NH3 concentration lower than 10 ppm is considered the acceptable one.

2. Carbon Dioxide

Carbon dioxide is a greenhouse gas and derives mainly from the respiration of animals that inhale air containing 0.035% CO2 and exhale it containing 5% CO2. Animal production of CO2 depends on the species, body weight, and diet. To a lesser extent, CO2 production is due to the degradation of organic substances [10], such as those contained in manure. Indeed, based on manure management and the type of barn, different concentrations can be found. In particular, on slatted floors with deep pits in which slurry is stored for a long period of time, the CO2 concentration can be up to 10% higher. Also, litter presence can contribute to CO2 production. Litter emissions are more difficult to calculate; however, it has been shown that bedding can produce the same quantities as animal CO2 production [8][11].
As indicated in ClassyFarm, the acceptable level of carbon dioxide in animal houses is below 3000 ppm [10], although in winter, with a minimal ventilation rate, it can reach 6000 ppm [7]. Its concentration strongly depends on the ventilation rate, and for this reason, there is an important diurnal variation to consider during CO2 measurements. Mainly during the night, with a reduction of the ventilation rate, the concentration of CO2 in animal husbandry can increase by about 20% [8].
At high concentrations, animals experience dizziness and unconsciousness, while at very high concentrations (30,000 ppm), it can cause death by asphyxiation.
One characteristic of CO2 is that, by being heavier than air, it tends to stratify downward. Therefore, during environmental measurements for its detection, it would be better to measure its concentrations at different heights.

3. Ammonia

Ammonia is the most studied livestock pollutant. It comes from the biological degradation of nitrogenous organic substances (urea and uric acid) contained in urine and feces [5]. It is a colorless gas that can cause a systemic inflammatory response [12].
Usually, in swine confinement, NH3 is present in different concentrations, as shown in Table 3.
In ClassyFarm, a restrictive range for ammonia is reported: 10 to 20 ppm. The first value is the maximum limit accepted for prolonged exposure in humans.
In most countries, the threshold limit concentration in piggeries is 25 ppm; as regards human health, the current recommended maximum exposure standards vary from 7 to 25 ppm depending on the country and the exposure time, short-term, 15 min, or workday, 8–10 h [5][13][14].
Preference studies have been conducted to understand whether pigs are able to discriminate a polluted place from a cleaner one, but the flaw in these studies is the pollutants concentration. For example, in Drummond [15], NH3 concentrations of 50, 100, and 150 ppm were tested, but those levels do not reflect real farm conditions. In fact, as indicated by De Boer and Morrison [16], the ammonia concentration in piggeries generally ranges from 1 ppm to 30 ppm.
In another study, the preference test was performed at 5–10 ppm versus 100 ppm, finding that animals have different tolerances to aerial ammonia. It was also noted that the choice of laying area is strongly related to the animal social hierarchy [17]. The first threshold (5–10 ppm) was chosen because these limits are not toxic for animals. However, researchers know from Jones [18] that 10 ppm is enough to create discomfort in pigs, and these values are also bothersome to humans. Exposure to ammonia, alone or in combination with other pollutants, has detrimental effects on animals, such as eye inflammation, coughing, sneezing, and dyspnea, depending on the duration of exposure and the amount of pollutant. It is a very dangerous gas, especially for young pigs, whereas in adults there may be less damage due to the animal’s major resistance.
As reported by Gustafsson [9], high NH3 concentrations have an important influence on animal growth performance since feed intake and nutrient utilization efficiency are reduced. This could also depend on changes in gut integrity that concern gut morphology, intestinal bacterial flora, metabolites, and gene networks [19]. However, a compensatory response has been shown following long-term ammonia exposure: while food intake decreased, food conversion efficiency increased [20]. This may indicate that animals have to work harder to deal with the environment and, as a result, may be an indicator of potentially compromised welfare. In Table 3, some ammonia values recorded in piggeries are reported.
Table 3. Some values of ammonia concentration measured in swine buildings.
All organisms exposed to NH3 undergo oxidative stress, which can cause a series of pathological damages to cells, inducing cell necroptosis and having further negative effects on animal immunity [5]. The high presence of oxidant radicals results in animals’ higher susceptibility to pathogens and diseases.
Moreover, the possible modification of epithelia due to the chronic inflammatory state may reduce the ability to absorb nutrients, resulting in a higher frequency of diarrhea.
In Li et al. [38], the effect of 90 mg of NH3 was studied, showing damage to the gut-brain axis through the induction of cell apoptosis. Moreover, some recent research has reported that ammonia exposure can interfere with lipid metabolism [39].
Another important aspect concerns the effects on the respiratory system.
Ammonia exposure can lead to respiratory symptoms such as coughing, rhinitis, and even pneumonia. Damage to the respiratory system may involve the upper airways and, under critical conditions and in the presence of fine particulate matter, may reach the lower compartment. The main symptom is mucus overproduction caused by nasal mucosa hyperplasia [12].
A critical respiratory condition involves the olfactory perception; the ability to recognize scents may be affected, with consequences such as feed palatability reduction [40]. Furthermore, it can have negative effects on pheromone reception and therefore on animal reproduction [6][41].
Recently, the effect on the liver has also been investigated since it is responsible for the detoxification activity of the organism. It has been shown that an excess of NH3 (approximately 90 ppm) can change the transcriptional profiles of pig liver, with consequent liver pathology and immune dysfunction [42].
Among many studies, NH3 toxicity on (in vitro) porcine oocytes was investigated to examine the negative implications in the reproduction sphere. The data suggest that factors such as actin disruption, ROS generation, early apoptosis, and autophagy could influence oocyte maturation [43]. Although it is an in vitro study, it could provide crucial information related to farrowing room biosafety.

5. Hydrogen Sulfide

In ClassyFarm, hydrogen sulfide is not reported among the noxious gases, probably because it results from the anaerobic digestion of slurry, it binds with water, and the greatest production comes from slurry agitation [1].
Nevertheless, hydrogen sulfide (H2S) can be very dangerous. It can cause inflammation of the respiratory system, irritation of the mucous membranes, reduced appetite, paralysis of the diaphragm, and be lethal at high concentrations [7]. The target organ is the central nervous system, so after acute exposure, animals can appear unconscious and in respiratory failure [1].
Reported incidents of poisoning or death are related to the closeness of slurry storage tanks during slurry agitation, from which high concentrations of H2S were released into the air [44]. So, in pig facilities, H2S is typically under the detection limit (approx. 1 ppm), but it can reach higher concentrations unless manure management is conducted in the correct way, especially when it comes to livestock with slatted floors and deep pits.

6. Particulate Matter

In animal buildings, dust can originate from both inorganic and organic sources, principally from feed [45] and bedding materials and less from animals (skin flaking, hair) and manure [37][46][47][48][49].
However, as well as ammonia, chronic exposure to high dust concentrations can lead to the development of diseases such as bronchitis, asthma, and chronic coughing due to its mechanically irritating effect. Therefore, further information about dust needs to be investigated.
Airborne dust represents a big risk both to farm operators and animals. Moreover, it can also pollute the surrounding area, increasing the risk of asthma and lung disease in nearby residents [50][51][52]. Particulate matter consists of coarse (PM 2.5–10), fine (PM 1–2.5), and ultrafine (PM < 1) particles.
Dust can be classified according to the aerodynamic size of the particles. Total Suspended Particles includes all the particle size fractions. Inhalable dust refers to the smallest airborne particles that can be breathed in, and it includes particles with an aerodynamic size up to 100 μm. Respirable dust is the larger particle that can move into the gas exchange lung area [53] and can carry harmful gases and microorganisms into the respiratory tract [54]. These particles can reach the lung area in an inversely proportional way to their size, since the smaller the particle diameter, the deeper the particles are deposited in the respiratory tract through different mechanisms with different negative effects: impaction, sedimentation, interception, and diffusion [6][48].
So, dust can be distinguished first for its particle size and morphology; it is determinant to know the transmission distance, the suspension time, and the location of deposition in the respiratory tract [52]. PM10 are particles smaller than 10 µm and they include dust, pollen, and spores. In contrast, PM2.5 refers to particles smaller than 2.5 µm, such as combustion particles, organic compounds, and metals.
In the ClassyFarm system, the topic of dust concentration is not examined in depth. They define an unsuitable condition as one in which dust does not allow one to see “the end of the shed”. Dust concentration is assessed on a black A4 sheet positioned at a height above the pigs and away from the feed dispensers. At the end of the evaluation, the dustiness level is assessed according to the amount of dust present (“none, little, a thin coating, a lot of dust, the color of the sheet is not recognizable”). The housing conditions are considered unsuitable when the color of the sheet is no longer recognizable.
This technique, proposed as a risk assessment for air pollution by dust in ClassyFarm, can present critical issues since the A4 sheet will be covered by Total Suspended Particles (TSP), which includes all particle size fractions, while the investigation may be directed to the finest fraction of dust, or at least to particles with an aerodynamic size less than 10 µm, using dust samplers, as reported in Table 4. The monitoring of fine particles could reveal potential high concentrations of dust having the capacity to penetrate deeply into the respiratory tract, triggering negative synergistic health effects in the lungs [5]. Moreover, particles with an aerodynamic size lower than 100 nm are captured by the blood stream in the zone of gas exchange in the alveoli, escaping the phagocytosis exerted by alveolar macrophages and thus initiating the formation of ROS [52], with adverse effects on animals and workers.
As reported in Table 4, particulate matter can be characterized under physical, chemical, and microbiological parameters.
Regarding the chemical composition, it is possible to investigate the particles’ origin (mineral or organic) and the potential presence of toxins and allergens. It is important to investigate not only the chemical composition of dust but also its morphological and aerodynamical characteristics in order to define the PM sources and their properties [48].
In the end, microorganisms contained in dust derive principally from animals’ excreta. This mixture forms the bioaerosol, which includes mostly bacteria and, to a lesser extent, viruses, fungi, and endotoxins. Moreover, ammonia and odors can bond with dust, and this is a problem considering that microorganisms can use ammonia as a source of nitrogen for their growth.
In addition, ultrafine particles (<1 μm) reacting with acidic gases, such as ammonium and nitrate sulfate, contribute to the formation of secondary particulates and may pose an additional health risk [52].
Pikridas [58] reported that relative humidity and ammonia play a fundamental role in the formation of new particles. Starting from ultrafine particles, through phase transformation, it is possible to obtain new and different ultrafine particles subjected to continual changes [5]. These molecules, being very small in size, can cause serious health damage.
Ammonia levels in dust can reach 0.9–7.2 μg mg−1 [59].
The threshold limit for organic dust varies; in many countries, the limit is 10 mg m−3 for total dust; in Denmark, it is only 3 mg m−3, although in barns that limit is often crossed. Wathes [57] indicated that 5 mg m−3 of dust can dramatically affect pigs’ performance, suggesting that the Danish threshold is probably more reliable.
In recent years, greater attention has been given to the evaluation of farm dust and airborne particles’ content and the possible risk to animals reared in enclosed buildings. The most important information is related to the difference in bonding compounds depending on the particulate dimension.
The hazardousness of PM is defined by its aerodynamic dimension: PM2.5 can directly reach the alveoli and the blood circulation, which makes it the most dangerous compound [52]. In swine confinement buildings, PM2.5 is the most prevalent [39].
High hygiene standards can help keep airborne particulate matter under control, but no limit regulation is provided for dust [60]. However, even if a limited value were given, it would not be enough because a deeper analysis of dust components is needed to understand its role in affecting animals.
Unlike other studies, Done et al. [53] found no statistical relation between air quality and clinical observations or animal performance. The authors realized a single, multifactorial study on ammonia and dust effects on weaned pigs, using nine hundred and sixty animals exposed for 5 weeks to different mean ammonia (0.6, 10.0, 18.8, or 37.0 ppm) and mean inhalable dust (1.2, 2.7, 5.1, or 9.9 mg m−3) concentrations to represent air quality in a commercial husbandry.
On the other hand, these results disagree with other studies, in which the exposure limits for inhalable dust and respirable dust were set at 3.7 mg/m3 (2.4 mg/m3 per human) and 0.23 mg/m3 [61][62].
As reported by several studies, high levels of NH3 and dust can increase the incidence of multifactorial respiratory diseases [53][62][63][64].
As said before, dust can contain dangerous substances for animal and human health, like gases, bacteria, fungi, viruses, and active endotoxins [48][65][66].
Endotoxins are implicated in hypersensitive pneumonia in humans and can also affect the immune system; they are sufficient to trigger an immune response and lead to a respiratory disease [65]. The levels of endotoxins can clearly represent a great hazard, both for workers and animals.
Seedorf [60] proposed a Livestock Burden Index (LBI) for airborne contaminants, to establish index classes indicating the magnitude of the burden to which the animals are exposed:
He was one of the first researchers to understand the necessity of defining the synergic effect between them. He defined a full equation to estimate LBI for pigs, in which he included ammonia (NH3), inhalable dust (ID), respirable dust (RD), and inhalable endotoxins (IEtox). The limit concentration was defined by the literature review.
Thresholds over which diseases and production problems can be developed are:
An amount of 10 ppm of ammonia, which is enough to create animal discomfort [18];
An amount of 3.7 mg m−3 of inhalable dust, 0.23 mg m−3 of respirable dust and 1.540 EU m−3 of endotoxins, that means 154 ng m−3 [67].
The equation of LBI for pigs is reported as follows in Equation (1):
 
LBIp = CNH 3 10   ppm + CID 3 . 7   mg   m 3 + CRD 0.23   mg   m 3 + CIEtox 154   ng   m 3
where C is the measured concentration related to the defined TLV (Threshold Limit Value, intended as the environmental concentrations of airborne substances below which workers can be repeatedly exposed for a working life without any adverse health effects) of a specific component.
Dust particles are affected by different forces that define their diffusion and deposition in animals’ rooms. According to Cambra-Lopez [48], PM sources can vary among different swine facilities. Most PM originates from manure; its contribution is 70–98% in fine particles and 41–94% in coarse particles.
The defecatory habits, the building structure, and the manure removal system can affect the presence of airborne bacteria in PM, with different percentages in summer and winter, 59.4% and 19.9%, respectively [51]. This difference can be due to several reasons: firstly, the different temperature; secondly, the practice of emptying the pit; and also parameters such as RH and ventilation. The potential of fattening pigs to release manure-derived particles is three times greater than that of sows and piglets and may depend on the metabolism and maturity of the digestive system, as well as the feeding ratio [52][67].
In addition, particulate matter can be rich in antimicrobial resistance genes (ARGs), known as resistome. Luiken [68] found out that about 63–73% of dust resistome derives from the aerosolization of animal faces. However, it is clear that the other part of the resistome is defined by bacteria from other body parts and substrates present in the farm (feed, soil, and instruments).
Since antimicrobial resistance is part of the One Health concept, it is necessary to investigate this aspect of farm reality in order to understand the transmission risk.
Recently, Van Gompel [69] used a metagenomic shotgun approach to investigate the relationship between pig resistance and risk factors at the farm level, across nine European countries. Results show a positive correspondence between antibiotics used in association with macrolides and tetracycline resistance. On the other hand, no association was found for β-lactam resistance.
This aspect is very important because it provides some new information about fecal ARGs that can affect animals and operators, causing problems with antibiotic resistance.
The greatest worry concerns the public health risk because the farm airborne resistome represents a problem not only for farm workers but also for the community living near the facility [70].
Cui et al. [71] established that the abundancy and the variability of the bacterial population in dust increase according to pigs age, so that at the beginning and at the end of the breeding cycle there are different risk conditions.
The microbic concentration in dust has seasonal variations; it has much more diversity during summer and autumn, strongly influenced by temperature and humidity but not by PM2.5 concentration [39]. The easiest explanation is the relation between the growth and survival of certain taxa and microclimate conditions.
In Song [51], the results of their study showed a positive correlation between airborne bacteria and temperature (p < 0.05); therefore, a high temperature creates a suitable environment for bacteria. In contrast, in less recent research, bacterial bioaerosol diversity was indicated to be significantly higher in winter [72]. Finally, a relative humidity (RH) above 80% seems to help with bacterial growth inhibition [51][73][74].
PM2.5 and ventilation have a seasonal influence on airborne contaminants. Air velocity can play a minor role in winter (when it is quite low), contributing to the ARGs increase, while in summer, the indoor speed velocity can push the spread of bioaerosol outside the buildings, constituting further risks for farmers and surrounding areas [51]. In winter, the absence of ventilation can contribute to the increase of NH3, dust, and pathogen concentrations in swine barns, increasing risks for pigs’ health [75].
Kumari [76] investigated fungi diversity and abundance in swine houses, finding that fungal OTU (operational taxonomic unit) composition is strongly related to RH, temperature, PM, NH3, and stocking density.
The community composition is wider and more heterogeneous in summer, when the major component is Ascomycota, thanks to its small dimensions, which make it more aerosolisable.
In addition, allergens related to fungi bound to PM2.5 are characterized by great variability among different structures. The abundance of these allergens depends on fungi genera, and it has been estimated to be around 13–25%. The most dangerous toxin is related to the Fusarium genera, which can cause infections in both animals and humans [76][77].
Each farm has its own dust composition depending on the breeding barn, farm buildings, management, and obviously the microclimatic conditions [71].
Since in recent decades limited importance has been given to the concentration of dust in livestock farms, it is necessary to introduce the habit of characterizing dust, and by deepening this aspect, it will be possible to ensure greater biosecurity and better animal and worker welfare.

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