Salmonella spp. is still the second most common zoonosis within the EU with over 91 000 cases reported in 2017 (European Food Safety Authority (EFSA), 2018). In pig meat, S. enterica ser. Typhimurium was the commonest reported serovar and accounted for 161 (27%) out of the 595 Salmonella spp. isolates serotyped. The group of monophasic variants of Salmonella Typhimurium was the commonest reported serovar from pigs and pig meat accounting for, respectively, 167 (37.4%) and 129 (22%) isolates. These results confirm that pigs are the main animal reservoir for monophasic variants of Salmonella Typhimurium. Farm animals are an important source of infections to humans, with risk of contamination of the food chain when infected animals are transported to slaughter facilities. Salmonella Typhimurium prevalence in UK and Irish herds in both breeding and slaughter pigs have historically been the highest in the EU, with figures of 19.4% and 17.5% respectively (EFSA, 2009) (Figure 1).
Salmonella — a zoonotic pathogen
The genus Salmonella is divided into two species: Salmonella enterica and Salmonella bongori. S. enterica is further divided into six subspecies, and most zoonotic Salmonella belong to the subspecies enterica. S. enterica ser. Typhimurium is one serovar within the subspecies and is categorised by the antigens present (Figure 2). Salmonella is a Gram-negative facultative anaerobe and is usually mobile due to the long flagella on the bacteria's surface.
Salmonella is a continuous problem on pig farms and the bacteria are transmitted through breeding pyramids which eventually supply finishing pigs. Subclinical infections are common in pigs and the organism may easily spread between animals in a herd without detection and animals may become intermittent or persistent carriers. Transmission between animals occurs through two main routes, airborne and oral (Figure 3). The oral route is the most common and occurs when animals come into contact with faeces from infected animals which is then ingested. However, dust and aerosols can also cause infection via the airborne route. Both infection routes result in the bacteria invading the animal where it can then thrive and continue to spread when it is shed in the faeces. It is for this reason that cleaning and disinfection measures are extremely important in the control of Salmonella spp. on pig farms.
Diagnosis
Sampling on farm is important to determine the areas of the unit which have high environmental Salmonella spp. contamination. The most common samples include individual pig faeces, pooled faeces collected using the sock method (Figure 4) and environmental samples collected using swabs. At least one of each sample type should be taken at each stage of production on the farm to get the full picture of all the Salmonella spp. involved. These samples are used for microbiology to determine the types of Salmonella spp. on the farm. The resultant colonies may also be used for poly-merase chain reaction (PCR). However, it is important to note that bacteriological examinations on environmental swabs do not illustrate the real prevalence of each serovar on the farm, especially if several serovars are present.
It may be important to be able to distinguish between the vaccine strain and field strains when testing for Salmonella spp. Therefore, the Biotecon Vetproof STM Vaccine Detection 1 Kit, which is a real-time PCR kit, was developed which can differentiate the vaccine strain in Salmoporc (the only commercial vaccine available) from Salmonella field strains. Although pigs are not under a national control programme, it is important to remember that Salmonella spp. is a reportable pathogen and therefore notification of Salmonella spp. detection should be given.
Implementing a sustainable control programme
A sustainable control programme is multi-factorial and involves three pillars which hold up the overall success of Salmonella spp. control (Figure 5). Hygiene, biosecurity and vaccination are these three pillars and they should all be given equal attention.
Environmental contamination
The environment can be contaminated via various routes including staff, visitors, wildlife and pigs themselves. Pigs shedding Salmonella spp. in faeces results in birds and rodents becoming contaminated also. Outdoor farms are generally at greater risk of environmental contamination due to increased exposure to wildlife and difficulty in applying biosecurity measures for both staff and members of the public who may come into contact with the farm perimeter when using public footpaths. Once an outdoor farm has been contaminated with Salmonella spp., it is extremely difficult to eradicate, as supported by De Lucia et al (2018) reporting that Salmonella spp. infection persisted in a field left empty of pigs for more than 2 years, most probably due to the role of wild birds. The difficulty of cleaning and disinfecting outdoor units also contributes to increased environmental contamination as well as the design of the huts for example, where faeces is kept in the environment for longer due to straw bedding (Smith et al, 2017).
Cleaning and disinfection
Salmonella spp. can survive on almost any surface for long periods of time due to a strong ability to form a biofilm. A baseline study carried out in 2008 showed that over 50% of all breeding holdings were Salmonella spp. positive (EFSA, 2009), but some types, like S. enterica ser. Typhimurium and monophasic Salmonella Typhimurium are more hazardous than others. Monophasic Salmonella Typhimurium strains can spread rapidly in pig farms and are difficult to eliminate (Martelli et al, 2018). Therefore, it is extremely important to put management and hygiene measures in place to reduce the environmental pressure as much as possible. This can be particularly difficult on outdoor units as the bacteria can survive in soil for 1 year, dried faeces for 2 1/2 years, and has been detected in fields 2 years after being vacated by pigs (SchÖning, 1999; De Lucia et al, 2018). However, management practices could help, supported by studies reporting that increased frequency of change of location (more than the average every 2–3 years) for outdoor herds could help to reduce on-farm prevalence of Salmonella spp. (Smith et al, 2017).
In the cleaning stage, the removal of dust and organic matter is extremely important as, already mentioned, the bacteria can survive for a long period of time in these materials and therefore their removal is essential to eliminating Salmonella spp. in the buildings. It is important to remember feeders and drinkers, as well as enrichment materials, which should be also thoroughly cleaned before moving new animals into the pens. Cleaning is most effective when surfaces and equipment are left to soak for 6 hours or more, as this helps to loosen any dried faeces. A detergent should be used to foam the walls, floors and fixtures. After cleaning, ensuring sufficient drying time before application of disinfectant is imperative, as the bacteria multiply in moisture. Putting the heating on in the farrowing pens helps with the drying process. The category and concentration of disinfectant used are also very important, as some disinfectants are more effective than others, and Salmonella spp. elimination requires a higher concentration of disinfectant than most other viruses and bacteria.
A study has been completed which clearly demonstrates the importance of this cleaning and disinfection process. A number of farms implemented a strict hygiene programme and this was compared with control farms which continued their normal programme. The Salmonella prevalence in intervention buildings was significantly lower (p<0.001) than in control buildings (Martelli et al, 2017).
Vaccination
Vaccine development
Monophasic Salmonella Typhimurium has already been shown to be highly resistant to ampicillin, sulfonamides and tetracycline, which is a concern for human health (EFSA, 2019). In addition, with the planned removal of zinc oxide at therapeutic levels from the feed in the EU in 2022, enteric diseases are likely to become more clinically apparent. Therefore, a different route needs to be taken in controlling Salmonella spp. on farm. Vaccinating pigs can help farmers to substantially reduce their use of antibiotics, reduce the prevalence of Salmonella spp. on the farm, and reduce subclinical infection.
Salmoporc, a live, attenuated, vaccine from Ceva, is the only vaccine licensed for use in pigs (both piglets and sows) in the UK and Ireland. It is administered orally to piglets and through subcutaneous injection in sows, and it provides protection against Salmonella Typhimurium and its monophasic variants. Development of the vaccine required isolation and testing of the field strain to result in a strain which was avirulent, immunogenic, genetically stable and had reduced persistence in the environment. The vaccine is for the active immunisation of gilts to reduce the excretion of Salmonella Typhimurium wild type strain during lactation; and the oral administration in pigs is for the active immunisation of suckling and weaned piglets to reduce bacterial colonisation, as well as clinical symptoms due to an infection with Salmonella Typhimurium.
Vaccination strategies
Different vaccination strategies were evaluated in a recent study (Peeters et al, 2019) and the impact on excretion of Salmonella Typhimurium and the number of positive pigs (ileocaecal lymph nodes) was evaluated. The study reported that vaccination of sows and piglets resulted in the most consistent reduction of Salmonella Typhimurium field strain positive lymph nodes at slaughter vs vaccination of just sows, for example. The vaccination of sows and their offspring prevents or impedes the vertical and/or horizontal transmission of Salmonella Typhimurium.
Another possible control strategy that could be implemented by the large companies is to vaccinate the top layers of the breeding pyramid and then evaluate the effect that this has further down the production pyramid (Figure 6). Previous experience shows significant reduction of the prevalence of Salmonella Typhimurium and its monophasic variant at the bottom of the production pyramid when this is implemented (Animal and Plant Health Agency (APHA), 2019). In farms where Salmonella spp. challenge is very high, vaccination of sows and piglets at the bottom of the production pyramid may be necessary.
Gilts
Increasing Salmonella spp. pressure is all the more serious because previously infected animals are reintegrated into the sow herd as potential carriers and further raise the pressure of infection there. Under stress (e.g. regrouping, farrowing), these animals excrete higher levels of Salmonella spp. Once Salmonella spp. infection has entered the production chain, the pressure rises very rapidly, especially in closed systems breeding their own animals for restocking. Because gilts are often reared in finishing, this exacerbates the situation further. Therefore, it is important to ensure replacement gilts are not shedding the bacteria when entering the farm.
Vaccination success
A study on outdoor breeding units reported substantially and significantly reduced prevalence of Salmonella spp. following vaccination with Salmoporc, from 45 to 6% in individual samples and 91 to 7% in pooled samples (Davies et al, 2016). A reduction in prevalence post-vaccination was reported for all three of the farms in the study, and there was a large improvement in the clinical disease observed on the two indoor units.
Another study has shown that when immunising pigs against Salmonella Typhimurium farmers will experience economic benefits due to lowered mortality and improved daily live weight gain (DLWG) among their pigs. Trials at the University of Ghent in Belgium showed that, between 3 and 29 weeks, vaccinated piglets from three herds gained between 30 g and 39 g, significantly (p<0.01) more per day than unvaccinated controls (De Ridder et al, 2014).
Ultimately vaccination, combined with hygiene measures, is an effective way of protecting infected pig farms against clinical disease and reducing the excretion dynamics of Salmonella spp. step-by-step. For closed-system breeding farms, it is important to establish a vaccination chain starting with the nucleus facility and ending with Salmonella-free finishing animals.
A long-term approach
Successful Salmonella spp. control requires a long-term approach. Interim setbacks are possible and should be taken into account, especially on farms with several associated sections and complicated movements of people and animals. Before implementing any Salmonella spp. control measure, it is important to conduct a detailed herd inventory by pathogen detection at all stages of production. This is also important to gauge the success of the measures implemented. All staff should be informed and made aware of the measures to be taken. The current status should be checked regularly (at least every 6 months) and the strategies adjusted if necessary. At least once a year, the sow unit should conduct a status survey using sock and environmental samples at all stages of production. This will provide information on the environmental burden and allow prompt action to be taken in the event of suspicious results.
Conclusion
Salmonella spp. are zoonotic bacteria that can survive on almost any surface for long periods of time, with Salmonella Typhimurium, and monophasic Salmonella Typhimurium in particular being of greatest importance in pigs. Transmission of the bacteria into the food chain is of public importance and multi-resistant strains are a risk for humans. Vaccination alone is not enough to eliminate Salmonella spp. infection on farm, but can play a key role in the reduction of prevalence and management of clinical symptoms. Controlling Salmonella spp. infection through a combination of interventions is of great importance, as is the avoidance of the long-term use of antimicrobial treatment.
KEY POINTS
- Salmonella spp. is an important pathogen for both human and animal health.
- Correct diagnosis is very important in ensuring the correct control measures can be actioned on farm.
- Successful Salmonella spp. control is multi-factorial and involves three pillars: hygiene, biosecurity and vaccination, all of which should be given equal attention.
- Cleaning and disinfection have large roles in reducing environmental pressure and therefore spread of Salmonella spp. through the farm.
- Vaccination forms one of the pillars of Salmonella spp. control and has been shown to be effective in reducing prevalence of Salmonella spp. and increasing economic benefit.