Detection and Zoonotic Potential of Trichinella spp. from Free-Range Pig Farming in Greece

Introduction

T richinellosis is a zoonosis that is broadly distributed throughout the world, and it is considered a re-emerging disease. The causative agent, nematodes of the genus Trichinella, mainly infects carnivorous or omnivorous mammals, including domestic pigs (Gamble et al., 2000; Sequeira et al., 2000; Gottstein et al., 2009). Trichinella infection in pigs can only result from the consumption of first-stage larvae found in the musculature of infected animals. For this reason, there are limited, but well- documented risk factors for exposure of pigs to Trichinella infection in the farm, including feeding of raw or undercooked waste products which contain infected meat, exposure of pigs to infected rodents, exposure to infected wildlife, and exposure to infected pig carcasses (Schad et al., 1987; Gamble et al., 1999; Malakauskas et al., 2007).

The emergence or re-emergence of a parasite like Trichinella spp. results from a change in either the ecology of the host, the parasite, or both, because zoonotic parasites exist in the natural environment of wild and domestic animals, as well as that of human populations (Daszak et al., 2000). Although the incidence of human trichinellosis appears to have stabilized, outbreaks were clearly observed during the 1990s both in the maiden European Union (EU) member states as well as the newly associated EU countries in central and eastern Europe, where the incidence was especially noted (Murrell and Pozio, 2000; Djordjevic et al., 2003). Moreover, the most important meat sources of infection in Europe have been horses, wild boar, and pigs bred on small farms or allowed to graze on open pasture (Murrell and Pozio, 2000). Recent outbreaks of trichinellosis in western and central Europe indicate that wherever indigenous pigs were involved, they originated from small farms with outdoor access where the meat is used for local or regional consumption, only. Surprisingly, animals for local and regional consumption do not require testing according to the present EU legislation. In addition, the illegal imports of infected pork meat and pork meat products have led to outbreaks of trichinellosis in Germany, Denmark, Italy, and the United Kingdom (Pozio and Marucci, 2003; Hansen and Kristensen, 2004).

In free-range pig farming systems (or organic pig farming), the animals are kept at lower stocking densities, having outdoor access and obligatory straw bedding, and are fed organic feed (EC, 2007). With free-range farming, it is possible that new risks will arise or old risks with be reintroduced to public health. Parasites are a major problem for the animals' health and welfare in many free-range pig production systems. Additionally, rodents represent an important risk factor for zoonoses, especially for trichinellosis, in livestock systems, both by contaminating animal feed or being hunted by free-range pigs (Schad et al., 1987; Smith and Kay, 1987; Gamble et al., 1999; Oivanen et al., 2000).

The aim of this study was to examine the impact of Trichinella spp. on free-range pig farming in Greece.

Free-Range Pig Farming in Greece

The National Greek projects of free-range pig farming started in 2002. The contribution of free-range pig farming in total Greek free-range livestock farming was very low until 2004, but since then, it has grown significantly, reaching a participation rate of 15%. According to the official statistical data of the Greek Ministry of Rural Development and Food (Table 1), the total number of free-range pigs was just 1,288 in 2002. From then until 2005 a steady increase was observed, while in 2006–2007 a significant increase led to a total of 175,000 free-range pigs. However, as shown in Table 1, since 2007 there has been a remarkable decrease of free-range pigs (Djordjevic et al., 2011).

Methods

Results

As shown in Table 2, in 2009 two positive samples were detected: one positive for T. britovi and one positive for Trichinella spp. (unspecified), which came from free-range pigs (Boutsini and Kontos, 2011). It is alarming that one of these cases was connected with clinical signs of trichinellosis in five persons of the same family in northeastern Greece, all of whom consumed undercooked pork meat from a free-range pig farm. The farm's capacity was 220 free-raised animals in 3600 acres. One person suffered severe symptoms and was hospitalized (Papadopoulos and Papadopoulos, 2011). During 2010, five positive samples for Trichinella spp. (unspecified) were detected from 4,159 free-range pigs tested by the Greek NRL (Table 2). Also, from a total of 363 serum samples that were serologically tested with the method of ELISA, 15 samples were found positive and they all came from free-range pigs (Table 3).

Discussion

According to data from the European Food Safety Authority (EFSA), during 2008 the only positive sample for Trichinella spp. in EU was from a free-range pig farmed in Bulgaria. Furthermore, in Bulgaria in 2008, 34 positive samples for Trichinella spp. were detected from non-farmed wild boars (EFSA, 2010), while during 2009 the number of positive samples increased to four in pigs from conventional farms and to 64 in pigs from free-range farms. The above findings are of high interest to Greek Veterinary Authorities and the scientific community because Bulgaria is a neighboring country to Greece. There might be a connection between the cases in Bulgaria and the trichinellosis outbreak in Greece during 2009, as the two positive samples for Trichinella spp. came from regions (Kavala and Evros) very close to the Greece-Bulgaria borderline (Fig. 1). Around this border line, a significant population of wild boars lives, and it is possible that they come in direct or indirect contact with the environment of local Greek free-range pig farms.

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FIG. 1.

Map of the regions (Kavala and Evros) with the positive samples for Trichinella spp. in 2009.

The present study is the first report of detection of T. britovi in Greece. It is remarkable that the T. britovi that was identified in a sample from a free-range pig farm in Greece also appears to have a geographic distribution in Bulgaria, including the southern and eastern parts of the country (Kurdova et al., 2004). T. britovi is the most widely distributed species within sylvatic life cycles of Europe, Asia, and Northern and Western Africa (Pozio et al., 2005, 2009). As is the case with T. spiralis, T. britovi can also affect domestic pig populations mainly via extensive grazing systems or feed with scraps or carrion originating from sylvatic carnivores. Zoonotically, T. britovi is the second-most common species of Trichinella spp. to affect human health (Gottstein et al., 2009).

Based on the results of the present study, Trichinella spp. is a high risk factor for free-range pig farming in Greece.

Conclusion

Free-range pig farming leads to meat products without residues (e.g., pesticides and veterinary drugs) while also originating from animals that grow under more welfare-friendly production conditions compared to animals growing in conventional livestock production systems (Blokhuis et al., 2003; Hermansen, 2003). Consumers expect that pork meat from free-range pig farms is better than conventional pork meat with respect to all quality parameters, including nutritional value and health (Grunert, 2002). However, this advantage could be questioned based on increased cases of swine and human trichinellosis. In Europe, during 2007–2008 the highest number of Trichinella-positive slaughtered pigs from conventional farms was reported by Romania, followed by Spain and Poland, although it was still at very low prevalence. Trichinella spp. has been detected more often in wild boars than in free-range pigs (EFSA, 2010).

The recent legislation of EC describes the requirements for certifying pigs as free from the risk of Trichinella spp. infection (EC, 2005). Most farmers are inexperienced in free-range pigs' production and need to develop suitable management routines. Good farm management practices, including rodent control and avoiding feeding waste to pigs, must be implemented at the farm level (Gajadhar and Gabmle, 2000). In order to exclude the risk of transmitting Trichinella spp. in free-range pig farms, a Hazard-Analysis-Critical-Control-Points (HACCP) system should be applied combined with strict rules of good veterinary practices (GVP) and good production practices (GPP) (Papatsiros, 2011). Under strict conditions, it is possible to guarantee Trichinella-free pig farming. Trichinella-free pig farming is a feasible option for controlling this zoonosis, even in endemic areas (Van Knapen, 2000). The main key points of a HACCP system for free-range pig farms are (i) architectural and environmental barriers, (ii) feed and feed storage, (iii) rodent control, (iv) farm hygiene including proper disposal of dead animals, and (v) introducing piglets from farms with controlled housing conditions.

Free-range pig production is a relatively new production concept with promising possibilities for further development. Modern consumers demand safer and higher quality pork meat products, and expect the meat from free-range pig farms to be healthier, with better nutritional value than conventional pork as far as all quality dimensions are concerned. However, proponents of free-range production methods must be aware that, if food safety issues are not properly communicated, a food crisis could develop that might be disastrous for free-range livestock farming. Risks should be reduced to the minimum possible (e.g., freezing meat), and authorities, producers, and processors should offer proper communication to consumers about the risks of outdoor animal production, including advice on how consumers should deal with these risks. All the above requires good interaction between the public health sector and the corresponding veterinary sector (Kapel, 2005; Gottstein et al., 2009).