Air Pollution and Domestic Animals: Dogs, Cats, and Horses

Production Animals

Pigs, poultry, cattle, goats and to a far lesser extend sheep are kept in indoor facilities for a variable part of their life, often for all of their life. For dairy cattle, goats and sheep these facilities are quite open and air quality is to a certain degree comparable with the outdoor air quality. The quality of this air is still much better than that of the closed facilities for swine and poultry (Wathes et al., 1998). These buildings are rather closed and the natural or mechanically ventilation is via small air inlets and outlets. Indoor temperature is regulated to create optimal growing conditions, whereby heat loss via ventilation is kept to a level that is just on the boundary of what is still physiologically tolerable. The other reasons for closing these types of buildings as much as possible are the strict bio security procedures applied in order to avoid or reduce introduction of potential infectious material via air or fomites. The temperature in the facilities for optimal growth can be quite high. For instance, one day-old broiler chicks are kept at a room temperature of 34°C the first days of the raising period. Thereafter, ambient temperature will be lowered daily by 1 °C. The high temperatures facilitate growth of fungi and bacteria especially around the drinkers where water is spilled by the animals. The most common used litter for broilers is wood shavings. Sometimes alternatives such as shredded paper, chopped straw and pulverised bark or peat may be used. The bird’s respiratory tracts are challenged by dust coming off the litter. Up to 40,000 broilers may be raised in a single house, on littered floors. A production cycle of broilers only takes 42 days on average. In this period the chicks will growth from about 60 grams to about 2000 grams. Thus, by the end of the raising period, the houses are well filled with animals and their activities increase dust levels in the air. In laying birds, although stocking density is lower, this beneficial effect on pollution, however, is offset by the longer housing period. The result is a larger accumulation of manure, usually in pits, which are only emptied infrequently (Harry, 1978). Hence, it is not surprising that especially in poultry houses high concentrations of ammonia, airborne dust, endotoxin and micro organisms can be measured (Wathes et al., 1998).

Fattening pigs are kept in grid floored pens and thus are exposed to fumes of their own faeces and urine for their entire existence, which is of not more than 6-7 month. Also in many piggeries high levels ammonia, airborne dust, endotoxin and micro organisms can be found (Wathes et al., 1998).

The indoor atmosphere in swine and poultry confinement buildings thus contains toxic gases, dusts and endotoxin in much higher concentrations than those in outdoor environments. Apart from minimal ventilation, poor stable design leading to poor homogeneity of ventilation causes locally stagnant air pockets. According to Donham (1991), recommended maximal concentrations of gases or contaminants in piggeries are: 2.4 mg dust /m³; 7 ppm ammonia, 0.08 mg endotoxin/m³, 10⁵ colony-forming units (cfu) of total microbes/m³; and 1,540 ppm. carbon dioxide. Concentrations of bacteria up to 1.1 x10⁶cfu/m^3, inhalable dust content of 0.26 mg/m³ and ammonia concentration of 27 ppm have been reported to occur in facilities during winter, while at summer lower concentrations were measured (Scherer & Unshelm, 1995). Less difference between in- and outdoor temperature in summer allows better ventilation of the buildings.

A fraction of the smallest and most respirable particles are manure particles containing enteric bacteria and endotoxin (Pickrell, 1991). The concentration of these airborne bacteria and endotoxin, of course, is related to the level of pen cleanliness. Regarding generated toxic gasses, ammonia concentrations in the air are primarily affected by level of pen hygiene, but also by volume of the building, pig density and pig flow management (Scherer & Unshelm, 1995). Furthermore, season plays a role as well as was shown by Scherer & Unshelm (1995). Similar factors on ammonia levels are known to play a role in farrowing units and poultry houses (Harry, 1978). Ammonia is considered as one of the most important inhaled toxicant in agriculture. Dodd & Gross (1980) reported that 1000 ppm for less than 24 hour caused mucosal damage, impaired ciliary activity, and secondary infections in laboratory animals. Since this level is nearly never achieved, it is rather the long-term, low level exposure to ammonia that seems to be related to its ability to cause mucosal dysfunction with subsequent disrupting of innate immunity to inhaled pathogenic micro organisms (Davis & Foster, 2002). Generally, the toxic effects of chronic ammonia exposure do not extend into the lower respiratory tract (Davis & Foster, 2002).

In pigs this combined effects of ammonia and endotoxin predispose the animals to infections with viruses and bacteria, both primary pathogenic and opportunistic species. Although food producing animals appear to be capable of maintaining a high level of efficient growth in spite of marked degrees of respiratory disease (Wilson et al., 1986), at a certain level of respiratory insufficiency rapid growth can no longer be attained. In that case the production results will be uneconomically. Ventilation is often at a just acceptable level. In their overview, Brockmeier et al., (2002) summarized the facts on porcine respiratory diseases. They are the most important health problem for the industrial pork production today. Data collected from 1990 to 1994 revealed a 58% prevalence of pneumonia at slaughter in pigs kept in high-health herds. These animals originate from better farms and thus incidence of pneumonia in less well managed farms is higher. Respiratory disease in swine is mostly the result of a combination of primary and opportunistic infectious agents, whereby adverse environmental and management conditions are the triggers. Primary respiratory infectious agents can cause serious disease on their own, however, often uncomplicated infections are observed. More serious respiratory disease will occur if these primary infections become complicated with opportunistic bacteria. Common agents are porcine reproductive and respiratory syndrome virus (PRRSV), swine influenza virus (SIV), pseudorabies virus (PRV), possibly porcine respiratory coronavirus (PRCV) and porcine circovirus type 2 (PCV2) and Mycoplasma hyopneumoniae, Bordetella bronchiseptica, and Actinobacillus pleuropneumoniae. Pasteurella multocida, is the most common opportunistic bacteria, other common opportunists are Haemophilus parasuis, Streptococcus suis, Actinobacillus suis, and Arcanobacterium pyogenes.

Workers in pig or poultry facilities are exposed to the same increased levels of carbon monoxide, ammonia, hydrogen sulphide, or the dust particles from feed and manure as the animals (Pickrell, 1991). As a result, workers in swine production tend to have higher rates of asthma and respiratory symptoms than any other occupational group. Mc Donnell et al. (2008) studied Irish swine farm workers in concentrated animal feeding operations and measured their occupational exposure to various respiratory hazards. It appeared that swine workers were exposed to high concentrations of inhalable (0.25–7.6 mg/m3) and respirable (0.01–3.4 mg/m3) swine dust and airborne endotoxin (166,660 EU/m3). Furthermore, the 8 hour time weighted average ammonia and peak carbon dioxide exposures ranged from 0.01–3 ppm and 430–4780 ppm, respectively.

Lesions caused by air pollution in production animals mainly include inflammatory processes. Neoplastic diseases are rather uncommon. This holds true for animals such as swine that are mainly kept indoors, as well as for cattle and sheep that are kept a variable part of their lives outdoors. This was shown in an abattoir survey some 5 decades ago performed in 100 abattoirs throughout Great Britain during one year (Anderson et al., 1969). All tumours found in a total of 1.3 million cattle, 4.5 million sheep and 3.7 million pigs were recorded and histologically typed. Just 302 neoplasias were found in cattle, 107 in sheep and 133 in pigs. Lymphosarcoma was the commonest malignancy in all three species. Lymphosacoma was considered as entirely sporadic, since herds with multiple cases were not found in the UK. The other form, a lentivirus infection that causes outbreaks of enzootic bovine leukaemia was not present in the UK at those days. The 25 primary lung carcinomas in cattle were well-differentiated adenocarcinomas of acinar and papillary structure, squamous and oat-cell forms and several anaplastic carcinomas of polygonal-cell and pleomorphic types. They represented only 8.3 % of all neoplasms, occurring at a rate of 19 per million cattle slaughtered. No primary lung cancers were encountered in sheep or pigs.

Outdoor air pollution could affect farm animals kept at pastures in urban and peri-urban areas. In the past (1952), a severe smog disaster in London was reported to have caused respiratory distress of prize cattle that were housed in the city for a cattle exhibition (Catcott, 1961). It was likely the high level of sulphur dioxide that was responsible for acute bronchiolitis and the accompanying emphysema and right-sided heart failure. Since some of the city farms are located rather in the periphery of cities than in the centre, the inhaled concentrations of pollutants by production animals is likely less than the concentrations inhaled by pet animals living in the city centres or close to industrial estates.

Companion Animals: Dogs and Cats

Bukowski & Wartenberg (1997) described clearly the importance of pathological findings in domestic animals with respect to analysis of the effects of indoor air pollution in a review. Radon and tobacco smoke are believed to be the most important respiratory indoor carcinogens. Already 42 years ago Ragland & Gorham (1967) reported that dogs in Philadelphia had an eight times higher risk developing tonsillar carcinoma than dogs from rural areas. Bladder cancer (Hayes et al., 1981), mesothelioma (Harbison & Godleski, 1983), lung and nasal cancer (Reif et al., 1992, 1998) in dogs are strongly associated with carcinogens released by human in-door activities. In cats, passive smoking increased the incidence of malignant lymphoma (Bertone et al., 2002). By measuring urinary cotinine, passive smoking of the cats can be quantified. However, the late Catherine Vondráková (unpublished results) observed that there was no direct association with the amount of cigarettes that were smoked in a household and the level of cotinine in the urine of the family cat. Nevertheless, there was evidence that exposed cats showed reduced lung function. Measurement of lung function in small animals and in cats particularly, is difficult and usually only possible with whole body plethysmography (Hirt et al., 2007). For this purpose the cat is placed in a Perspex plethysmography box. Whether this method has sufficient accuracy is still to be proven (van den Hoven, 2007).

The effect of outdoor air pollution on companion animals, so far, has not been studied extensively. Catcott (1961) however described that in the smog incident of 1954 in Donora, Pennsylvania about 15% of the cities dogs were reported to have experienced illness. A few died. Diseased dog were mostly less than 1 year old. Symptoms were mostly mild respiratory problems lasting for of 3-4 days. Also some cats had been reported ill. Further indirect evidence exsists provided by observations made during the smog disaster of 1950 in Poza Rica Mexico. Many pets were reported ill or died. Especially canary birds appeared sensitive, since 100% of the population died (Catcott, 1961). The cause of mortality in the dogs and cats, however, was not professionally established; the information was merely that what the owners had reported, when asked on the incident.

Recently, Manzo et al. (2010) reported that dogs with chronic bronchitis and cats with airways inflammatory disease are at increased risk of exacerbating their conditions if exposed to prolonged urban air pollutants. In this respect they respond similar to man. The authors advise to suppress ongoing inflammatory processes by medical therapy and avoid exercising pets outdoors in urban areas during peak pollutant periods.

Horses

The reason for the domestication of the horse must be attributed to its athletic ability. The quieter donkey and the ox had been domesticated earlier as draft animals. The horse is one of the mammals with the highest relative oxygen uptake and therefore capable of covering long distances at high speed. The tidal volume of a 500 kg horse at rest is 6-7 L and at racing gallops 12-15 L. At rest a horse breathes 60-70 L of air per minute, which corresponds to about 100,000 L/day. During a race, the ventilation rate increases up to 1800 L /min. With this huge amount of air moving in and out the respiratory track, large quantities of dust particles are inhaled and may sediment in the airways. This on its term could have adverse consequences for lung function. Any decrease of lung function could affect the horse’s performance over any distance that is longer than 400 meters. Respiratory problems have a direct impact on the racing career of racehorses, if not successfully treated. Horses that are submitted to less intensive exercise, however, can perform up to expectation for quite a long time, if they are only affected by a small decrease of lung function. This can easily be understood if one considers the huge capacity of the equine cardiopulmonary system. An overview of the physiological aspects of the sport horse is given by van den Hoven (2006).

Horses are not exposed to the negative effects of tobacco smoke or radiation, because stables and the living rooms of man mostly do not share common air spaces. Yet, this does not automatically imply that there is a healthy atmosphere in a horse stable. In those countries where horses are kept in stalls, subacute and chronic respiratory diseases are serious and common problems. In countries like New Zealand, where horses live almost exclusively outdoors, these diseases are less well known. Many equestrian enterprises are situated in the periphery of urbanized areas. Thus urban air pollution must be considered next to the health challenge by poor indoor air quality. In the suburban and urban enterprises mostly adult animals are employed. Riding schools, racehorse training yards and fiacre horse enterprises are examples of yards that may be located in or near city parks or urban green zones. Horses on these yards are either housed in barns or in individual open-fronted loose boxes. The latter have top doors that are mostly left open (Jones et al., 1987) in order to optimize air circulation. Nevertheless, in many of these boxes due to their small doors, the minimal air change rate of 4/ hour is hardly attained (Jones et al., 1987).

The younger animals mainly are kept in rural areas, mostly at stud farms. Here they are kept out-doors partly or continuously. In winter and prior to horse auctions the youngsters will be stabled for longer periods, just to the moment that many of them will be shipped to suburban or urban enterprises. Other young animals will remain in the countryside. A special category of animals are the breeding animals. After having served in sporting events for short or longer periods in the (sub)urban environment, these animals return to the countryside. Mares are bred to stallions and are mostly kept at pasture for all day, or at least a part of the day. If housed, stables are not necessarily well designed and are as traditional as those of racehorses. Thus, exposure to poor air quality is not uncommon in broodmares. Breeding stallions, have only limited freedom, and yet remain large parts of the day in the barn. Stallion barns are mostly better designed than those for mares; often the more valuable stallions have open-front boxes.

Principally almost all horses will be exposed during a variable period of their life to air of poor quality. The sports and working horses stabled and exercised in (sub)urban regions are exposed to the air pollution caused by traffic and industrial activities too (Fig.1.). Indoor and outdoor air pollution must have an impact on the lung health of our horses. Therefore it is not unexpected that respiratory disease is a major problem for horse industries worldwide (Bailey et al., 1999).

Traditional stable design for horses is based on non-empirical recommendations extrapolated from studies of other agricultural species (Clarke, 1987), ignoring fundamental differences in requirements of the equine athlete. Even now in 2010, only a fraction of the horses are housed in modern well designed stables. But even in the traditional stables, with a median floor space of about 12 m² (Jones et al., 1987) stocking density is much less than with production animals. Moreover, many horses have their individual living area, but often still share a common airspace with poor air quality.

Organic dust in the common or individual air space, released by moving of bedding and hay is the main pollutant in horse stables (Ghio et al., 2006). Sometimes dust levels in stalls are less than 3 mg/m³, but during mucking out, the amount increased to 10-15 mg/m³, of which 20 - 60% is of respirable particles. Measured at the level of the breathing zone, during eating of hay, dust levels may be 20-fold higher than those measured in the stable corridor (Woods et al., 1993). Dust concentrations of 10 mg/m³ are known to be associated with a high prevalence of bronchitis in humans. Apart from hay and bedding, cereal food may contain considerable levels of dust. It has been shown that dry rolled grains may contain 30 – 60-fold more respirable dust than whole grains or grains mixed with molasses (Vandenput et al., 1997). Respirable dust is defined as particles smaller than 7 μm (McGorum et al., 1998). Respirable particles are capable of reaching the alveolar membrane (Clarke, 1987) and interact with alveolar cells and Clara cells. In this respect current findings by Snyder et al., (2011) in chemical and genetic mouse models of Clara cell and Clara cell secretory protein (CCSP) deficiency coupled with Pseudomonas aeruginosa LPS elicited inflammation provide new understanding on the pathophysiology of chronic lung damage. In this study, the authors reported evidence for anti-inflammatory roles of the airway epithelium and elucidated a mechanism whereby Clara cells likely regulate this process. Injured airway epithelium and mice deficient in expression of CCSP respond more robustly to inhaled LPS, leading to increased recruitment of PMNs.

Kaup et al. (1990b) mention that their ultrastructural study suggests that Clara cells are the main target for antigens and various mediators of inflammation during bronchial changes that occur in horses with recurrent airway obstruction (RAO).

The main constituents of stable dust are mould spores (Clarke, 1987) and it may contain at least 70 known species of fungi and Actinomycetes. Most of these micro organisms are not considered as primary pathogens. Occasionally infection of the guttural pouch with Aspergilles fumigatus may occur (Church et al., 1986). The guttural pouch is a 300 mL diverticulum of the Eustachian tube (Fig 2).

The walls of the guttural pouches are in contact with the base of the skull, some cranial nerves and the internal carotic artery. In case of a fungal infection of the air sac, the fungal plaque is commonly located at the dorsal roof, but may occupy the other walls as well (Fig.3). The fungus may invade and erode the wall of the adjacent artery. The resulting haemorrhage is not easily controlled and the horse may die due to blood loss.

A special infection associated with inhalation of bacteria present in the dust generated by dried faeces is the pneumonia caused by Rhodococcus equi of young foals (Hillidge, 1986). R.equi is a conditional pathogen causing disease in immunologically immature or immune-deficient horses. It can even cause disease in immuno compromised man. The key to the pathogenesis of R. equipneumonia is the ability of the organism to survive and replicate within alveolar macrophages by inhibiting phagosome-lysosome fusion after phagocytosis. Only the virulent strains of R. equi having virulence-associated plasmid-encoded 15–17 kDa proteins (VapA) cause the disease in foals (Byrne et al., 2001; Wada et al, 1997). This large plasmid is required for intracellular survival within macrophages. Next to VapA an antigenically related 20-kDa protein, VapB is known. These two proteins however are not expressed by the same R. equi isolate. Additional genes carring virulence plasmids e.g. VapC, -D and –E are known. These are co-ordinately regulated by temperature with VapA (Byrne et al., 2001). Expression of the first occurs when R. equi is cultured at 37 °C, but not at 30° C. Thus it is plausible that the majority of cases of R. equi pneumonia are seen during the summer months. The prevalence of R. equi pneumonia is further associated with the airborne burden of virulent R. equi, but unexpectedly it seems not directly to be associated with the burden of virulent R. equi in the soil (Muscatello et al., 2006). Only under special conditions of the soil, the virulent organisms may be a thread to foals. Dry soil and little grass and holding pens and lanes which are sandy, dry, and lack sufficient grass cover are associated with elevated airborne concentrations of virulent R. equi. Hence, Muscatello et al. (2006) consider that environmental management strategies aiming to reduce the level of exposure of susceptible foals to airborne virulent R. equi likely will reduce the impact of R. equi pneumonia on endemically affected farms.

If contaminated dust is inhaled by foals of less than 5 month, pulmonary abscesses will develop (Fig. 4). Faecal contamination of pasture and stalls are a prerequisite for the bacteria to establish. Other dust-born bacterial infections are not known in the horse. The non viable components of dust appear to play a major role in the airway diseases of mature horses.

Any threshold limiting value (TLV) for exposure to mould spores or dust are yet not known in horses (Whittaker et al., 2009). In man working for 40 h/week in a dusty environment, the TLV is 10 mg/m³ (Anonymous, 1972). However, chronical exposure of 5 mg/m³ caused serious loss of pulmonary function in operators of grain elevators (Enarson et al., 1985). Also Khan & Nachal, 2007 showed that long-term exposure to dust or endotoxin is important for the development of occupational pulmonary diseases in man. In this respect long periods of stabling causing a cumulative exposure effect of dust and endotoxins could result in the development of pulmonary disease in both horses that are susceptible to respiratory disorders and horses that are otherwise healthy (Whittaker et al., 2009).

Generally, horses that are exposed to excess organic dust will develop mild, often subclinical lower airway inflammation. This may contribute to poor performance (see IAD). The symptoms initially seem to share common aspects with the organic dust toxic syndrome in man (van den Hoven, 2006). Some horses could show severe hyperreactivity to organic dust and will display asthma-like attacks after exposure (see RAO). Especially the feeding of mouldy hay is a well-known risk factor for this (McPherson et al., 1979). Commonly incriminated allergens for such sensitive horses are the spores of Aspergillus fumigatus and endotoxins. The specific role of β-glucans is still in discussion.

The origin of the moulds may be found in the feedstuff offered to horses. Buckley et al. (2007) analysed Canadian and Irish forage, oats and commercially available equine concentrate feed and found pathogenic fungi and mycotoxins. The most notable fungal species were Aspergillus and Fusarium. Fifty per cent of Irish hay, 37% of haylage and 13% of Canadian hay contained pathogenic fungi. Apart from problems by inhalation, these fungi may produce mycotoxins that are rather ingested with the feed than inhaled. T2 and zearalenone appeared to be the most prominent. Twenty-one per cent of Irish hay and 16% of pelleted feed contained zearalenone, while 45% of oats and 54% of pelleted feed contained T2 toxins.

Next to fungal antigens, inhaled endotoxins induce a dose dependent airway inflammatory response in horses (Pirie et al., 2001) and even a systemic response on blood leucocytes can be observed (Pirie et al., 2001; van den Hoven et al., 2006). Inhaled endotoxins in horses suffering RAO are likely not the only determinants of disease severity, but do contribute to the induction of airway inflammation and dysfunction (Pirie et al., 2003).

Whittaker et al. (2009) measured total dust and endotoxin concentrations in the breathing zone of horses in stables. Dust was collected for six hours with an IOM MultiDust Personal Sampler (SKC) positioned within the breathing zone of the horse and linked to a Sidekick sampling pump. The study confirmed earlier studies that forage has a greater effect on the total and respirable dust and endotoxin concentrations in the breathing zone of horses than the type of bedding.

Due to absence of slurry pits under their living area and the low stocking density, noxious gases generated indoors generally play a less important role in development of equine airway disease. Nevertheless, with poor stable hygiene, ammonia released from the urine by urease producing faecal bacteria may contribute to airway disease too.

The effect of air pollution on horses working in the open air has not been extensively studied, but the few studies performed on ozone showed that horses appear less susceptible to the acute effects of ozone compared to humans or laboratory animals (Tyler et al., 1991; Mills et al., 1996). Marlin et al. 2001 found that the anti-oxidant activity of glutathione in the pulmonary lining fluid is likely a highly efficient protective mechanism in the horse. Although it is not likely that ozone is a significant risk factor for the development of respiratory disease in horses, the ability of ozone to act in an either additive or synergistic way with other agents or with already existing disease can not be neglected. Foster (1999) described that this occurs in humans. Diseases associated with poor air quality are follicular pharyngitis, equine inflammatory airway disease and recurrent airway obstruction.

In man exposed to air pollution in large cities, respirable particles and toxic gas levels appear to be associated with acute and subacute cardiopulmonary mortality (Neuberger et al., 2007). Such effects have not been noticed in horse exposed to urban air pollution.