LITERATURE REVIEWS

Salmonella spp. in the pork supply chain: a risk approach^¤

Salmonella spp. en la cadena de producción porcícola: un enfoque de riesgo

Salmonella spp. na cadeia de produção de carne de porco: uma abordagem de risco

Diego M Rodríguez, MV, MSc; Martha C Suárez*, MV, MSc.

Grupo Genética Molecular de Patógenos GEMPA, Facultad de Medicina Veterinaria y de Zootecnia, Universidad Nacional de Colombia, Sede Bogotá.

(Received: November 19, 2012; accepted: December 11, 2013)

Summary

The genus Salmonella contains approximately 2,579 serovars, most of which are zoonotic and transmitted by foods of animal origin, such as fresh pork and further processed by-products. Non-typhoid salmonellosis in humans manifests as gastroenteritis, septicemia, or can be asymptomatic during the carrier state. Salmonella spp. has a considerable impact in the pork industry due to economic losses resulting from diagnosis, treatment, reduced production, and because this pathogen constitutes a non-tariff barrier to food trade and a serious public health problem. The microorganism is usually introduced to farms through incoming breeding stock or pig feed and is subsequently spread by sick animals or asymptomatic carriers. Infection and/or dissemination of the microorganism may increase particularly during pre-slaughtering due to contaminated trucks, long periods of time spent in transit, stress during handling and fasting, or high animal density or time spent in corrals. Contamination during slaughtering is commonly associated with carcass de-hairing and polishing, evisceration and rectum separation, or from Salmonella present in skin, oral cavity, feces or lymphatic nodes. Pork contamination may also occur through contact with equipment or tools, handling, storage, or improper preservation during slaughter, post-slaughter, marketing, sale, or consumption. For this reason, Salmonella control, with a focus on the supply chain and risk assessment is fundamental for guaranteeing quality and food safety of pork products in Colombia, thereby contributing to public health and improving competitiveness. Studies directed at establishing baselines for the disease and the microorganism in each of the stages of the supply chain should be conducted, including identification of differential risks and establishing measures for monitoring, prevention and control.

Key words: cross-contamination, farm, pigs, pork, slaughter.

Resumen

El género Salmonella agrupa alrededor de 2.579 serovariedades, en su mayoría zoonóticas, transmitidas por alimentos de origen animal, como la carne de cerdo y sus derivados. La salmonelosis no tifoidea en humanos puede manifestarse como gastroenteritis, septicemia o estado portador asintomático. La presencia de Salmonella spp. es de gran impacto para la industria porcícola, por las pérdidas económicas por diagnóstico, tratamiento y disminución de la producción, y por constituir una barrera no arancelaria para la comercialización de alimentos y un grave problema de salud pública. El microorganismo se introduce en las granjas a través del alimento, el pie de cría o los cerdos para levante, y se disemina a través de enfermos o portadores asintomáticos. En el prebeneficio la contaminación de camiones, el tiempo de transporte, el estrés por manipulación, el ayuno, la alta densidad animal, y la permanencia en corrales pueden incrementar la infección y/o diseminación del microorganismo. Durante el beneficio la contaminación se asocia al depilado, pulido de los animales, a la evisceración y corte de recto o a la presencia del microorganismo en piel, cavidad bucal, heces o ganglios linfáticos. La contaminación de la carne también puede ocurrir por contacto con equipos o utensilios, por manipulación, almacenamiento o conservación inapropiada de los productos en etapas del beneficio, posbeneficio, comercialización, venta o consumo. Por tal razón el control de Salmonella bajo un enfoque de cadena productiva y evaluación de riesgo es un aspecto fundamental para garantizar la calidad y la inocuidad de los alimentos de origen porcino en Colombia, contribuyendo a la salud pública y a mejorar la competitividad de la cadena. Se deben realizar estudios orientados a establecer las líneas base de la enfermedad y del microorganismo en cada una de las etapas, identificando el riesgo diferencial y estableciendo medidas de monitoreo, prevención y control.

Resumo

O gênero Salmonella agrupa ao redor de 2579 sorovariedades, a maioria delas zoonóticas, transmitidas por alimentos de origem animal, como a carne suína e seus derivados. Em humanos, a salmonelose não tifoide pode se manifestar como gastroenterite, septicemia ou pode ser assintomática. A presença de Salmonella spp. é de grande impacto na indústria produtora de carne suína pelas perdas econômicas por diagnóstico, tratamento e diminuição da produção. Esta doença constitui também uma barreira não alfandegária para a comercialização de alimentos, sendo também um grave problema de saúde pública. O microrganismo é introduzido nas granjas pelas matrizes e reprodutores, animais na fase de crescimento ou a través do alimento. Tanto os animais doentes quanto os portadores assintomáticos podem ser fontes de contaminação. Na fase prévia ao abate podem ser citados alguns fatores que podem favorecer a infecção e disseminação do microrganismo: contaminação dos caminhões somado ao tempo de transporte em veículos com alta densidade animal, jejum e estresse. Durante o processamento da carcaça, a contaminação está associada à depilação e polimento dos animais, assim como evisceração, presença de microrganismos na pele, cavidade oral, ampola retal, fezes ou linfonodos. A contaminação da carne pode acontecer pelo contato com equipamentos ou implementos, manuseio, armazenamento e conservação inadequada dos produtos nas etapas do abate e após do abate, comercialização, venda ou consumo. Diante do anteriormente exposto, na Colômbia é de fundamental importância direcionar o controle da Salmonella considerando um enfoque abrangente da cadeia produtiva, incluindo a avaliação do risco. Este enfoque permitirá garantir a qualidade e inocuidade dos alimentos de origem suíno, redundado em benefícios para a saúde pública e o aprimoramento da competitividade da cadeia. Devem ser realizados estudos orientados ao estabelecimento dos indicadores da presença e impacto da doença em cada uma das etapas produtivas, identificando o risco diferencial, para sentar as bases de medidas de monitoramento, prevenção e controle.

Palavras chave: abate, carne suína, contaminação cruzada, granjas.

Introduction

Foodborne disease can be caused by a wide variety of biological, chemical and physical hazards (CDC, 2007). The main cause of foodborne diseases of bacterial origin is Salmonella spp., E. coli O157:H7, Campylobacter spp., among others (Swartz, 2002; CDC, 2005).

Prevention and control of pathogens that cause foodborne diseases should take place in each stage of the supply chain; that is, all actors should guarantee food safety according to the concept of ''stable-totable'' or ''farm-to-fork'', preventing or controlling infection and/or contamination to protect the health of the consumer.

Non-typhoid serovars of Salmonella spp. decrease pig production yield and increase production costs. Contaminated finished products (carcass, fresh pork and further processed by-products) are considered a public health risk and are restricted for international trade (non-tariff barrier), affecting the industry competitiveness. The negative impact of Salmonellosis in humans is related to diagnostic, treatment, cost of cases and outbreaks, and reduced productivity due to absence from work.

This review discusses Salmonella focusing on the supply chain. Colombian law regulated the supply chain in this country in 2003. It was stated that the primary production sector should set up monitoring, prevention and control programs. The harvest (slaughter) and postharvest (deboning and meat products) should implement specific control measures regarding quality concepts and food safety. In pre-slaughter, pigs may become infected during the lairage and the carcass may become contaminated in different stages of the slaughter process. Unsuitable manipulation and cross contamination are the main sources of contamination risk during deboning.

The genus Salmonella spp. comprises gramnegative coccobacilli of the Enterobacteriaceae family, which are flagellated, non-spore forming, and facultative anaerobes. The pathogen can be found in the gastrointestinal tract of homeothermic and poikilothermic animals. This microorganism grows at temperatures between 6 °C and 45 °C and can survive freezing and drying, and persists even for years in organic substrates. They are inactivated by heat, direct sunlight, and disinfectants such as phenols, chlorates and iodines (Schwartz, 1999; Grimont et al., 2000).

The genus Salmonella includes two species: S. enterica (pathogenic) and S. bongori, (considered non-pathogenic). The first of these species comprises six subspecies designated by Roman numerals or numbers where I. is Salmonella enterica subspecies enterica, II. S. enterica subsp. salamae, IIIa. S. enterica subsp. arizonae, IIIb. S. enterica subsp. diarizonae, IV. S. enterica subsp. houtenae and VI. S. enterica subsp. indica. For nomenclature purposes, serovars may be designated only by genus and serovar. For example, Salmonella enterica subspecies enterica serovar Typhimurium may be designated as Salmonella Typhimurium (Brenner et al., 2000; Heyndrickx et al., 2005).

The WHO Collaborating Center for Reference and Research on Salmonella's last report generated by the Pasteur Institute in 2007 includes 2,579 Salmonella spp. serovars in a broad range of hosts (Grimont and Weill, 2007). Certain serovars are better adapted to a single host, as in the case of typhoidal S. Typhi and S. Paratyphi in humans, and non-typhoidals, such as S. Dublin in cattle, S. Enteritidis in poultry, and S. Choleraesuis in swine. These serovars may be opportunistic in other species. In this regard, pigs may be infected by a broad range of non-typhoid serovars, constituting a source of contamination for pork (Schwartz, 1999).

Salmonellosis in humans

Non-typhoid salmonellosis in humans may manifest as gastroenteritis, bacteremia or a carrier state. The main signs are nausea, vomit, and light to moderate diarrhea. Among the non-typhoid serovars involved are S. Enteritidis, S. Typhimurium, S. Newport, S. Hadar, S. Derby, S. Heidelberg, S. Agona, S. Infantis and, on rare occasions, S. Choleraesuis (Gebreyes et al., 2004; Boyle et al., 2007; Foley et al., 2008; Schwartz, 1999). Mortality is lower than 1%, and usually occurs in children younger than five years old, older adults or immuno-compromised people (CDC, 2006). For Salmonella Choleraesuis, mortality may exceed 20% (CFSPH, 2005), although there is little association with contamination of carcasses and pork products (Schwartz, 1999).

Studies performed in recent years have estimated salmonellosis rates (per 100,000 people) of up to 23 in European countries, 17.7 to 28.1 in the United States (Swartz, 2002), 12.7 in Asia, 17.2 in Brazil (Helms et al., 2005) and almost 200 in Mexico (Gutiérrez-Cogco, Montiel-Vázquez et al., 2000). In general, it is thought that 22% of patients with salmonellosis are hospitalized and per each reported case there may be 38 unreported cases (Mead et al., 1999).

In the United States, the annual economic impact of the disease is estimated to be US $365 million in direct medical costs (CDC, 2011) and in US $3.3 billion in illness costs (Batz et al., 2011).

Salmonellosis in pigs

In pigs, the disease generates economic losses represented by morbidity and mortality, increase in the time needed to reach slaughter weight (90 Kg to 95 Kg), non-uniform batches, diagnostic expenditures and medications. In addition, the microorganism may persist in the farm environment due to continuous transmission between animals of all age groups (Schwartz, 1999). Regarding international trade, the presence of the microorganism represents a nontariff barrier that restricts proper marketing and/or negotiation of pork products (Davies, 1997).

Salmonellosis is caused by numerous serovars, including Choleraesuis, Typhimurium, Derby, Saint Paul, Infantis, Heidelberg and Agona (Schwartz, 1999). The first serovar has been related primarily to septicemia in pigs (Gray et al., 1996; Chiu et al., 2004), while S. Typhimurium can cause enteritis, although it may also manifest in septicemia (Fedorka- Cray et al., 2000; Rostagno et al., 2003).

Most infected animals are asymptomatic carriers of various serovars (Giovannacci et al., 2001; Lo Fo Wong et al., 2002), meaning that the microorganisms may be transmitted constantly, thus making its control difficult and representing a potential source of indirect contamination of pork and pork products (Schwartz, 1999).

Epidemiology focuses on microorganism introduction into the farm and transmission within the farm (Lo Fo Wong et al., 2002). The most important sources of infection are breeding stock and other pigs entering from other farms, followed by feed (Fedorka-Cray et al., 1997; Sauli et al., 2005; Österberg et al., 2010), water (Davies et al., 2004; Jensen et al., 2006), and other animals such as bovines, rodents, birds, insects, and pets (Fedorka-Cray et al., 2000; Hurd et al., 2002, Langvad et al., 2006; Fosse et al., 2009). The most important source of infection is the asymptomatic carrier pig (Schwartz, 1999), with fecal-oral route being the main form of transmission (Schwartz, 1999; Fedorka-Cray et al., 2000). S. Typhimurium has been isolated in feces up to 5 weeks after nose-nose contact with infected pigs (Proux et al., 2001).

Infection occurs rather quickly; Salmonella Typhimurium at a concentration of 1.5 x 10³ UFC in feces can invade the gastrointestinal tract and the lymphatic nodes associated with the intestine (GALT: gut-associated lymphoid tissue) of exposed pigs in as little as 2 hours (Boughton et al., 2007). Three hours after experimental nasal inoculation, S. Typhimurium was detected in the cecum, and it was detected in mesenteric lymph nodes and tonsils after 6 hours (Fedorka-Cray et al., 1995).

The main source of contamination in slaughterhouses is pigs from infected farms. However, the microorganism's ability to quickly infect animals allows for infection during transport and/or lairage.

Salmonella spp. can persist in the intestinal mucosa, mesenteric lymphatic nodes or tonsils (Berends et al., 1998; Vieira-Pinto et al., 2005, Methner et al., 2011). In studies of groups of pigs, researchers isolated S. Typhimurium daily from feces during the 10 days post-infection and frequently during the following 4 to 5 months. At 5 to 7 months, approximately 90% of pigs were positive for the microorganism in mesenteric lymph nodes, tonsils, cecum or feces (Dickson et al., 2002; Jensen et al., 2006). S. Newport was isolated from mesenteric lymph nodes for up to 28 weeks and S. Choleraesuis for at least 12 weeks (Gray et al., 1995). In moist feces, this microorganism survives for 3 months, and in dry feces between 6 and 13 months (Schwartz, 1999; Dickson et al., 2002). S. Typhimurium and S. Dublin were isolated after almost a year in a moist and warm environment (CFSPH, 2005).

Pigs can acquire the carrier state with 10⁴ CFU of S. Typhimurium (Dickson et al., 2002), and with 10⁸ CFU, pigs may develop persistent infection lasting 12 weeks (Fedorka-Cray et al., 1995). Ingestion of more than 10³ CFU of Salmonella per gram of feces may cause acute infection in pigs (Loynachan and Harris, 2005). Pigs can excrete 10⁶ S. Choleraesuis/g of feces or 10⁷ in the case of S. Typhimurium (Wood and Rose, 1992; Schwartz, 1999).

Transportation time, stress due to handling, fasting, high animal density, environmental contamination, social regrouping, and time spent in pre-slaughter pens (lairage) can increase infection and/or dissemination of the microorganism among pig batches (Lo Fo Wong et al., 2002, Bolton et al., 2013, Kich et al., 2011, Hernández et al., 2013).

Contamination of trucks and pens during and after pig transport increases the probability of infection (Hurd et al., 2002; Mannion et al., 2008 and 2011; Swanenburg et al., 2001, Lo Fo Wong et al., 2002, Oliveira et al., 2005). The longer the pigs remain in lairage, the greater the risk of infection. Accordingly, one strategy could be to reduce lairage time. However, it is necessary for the pigs to rest for at least 2 hours to avoid affecting the organoleptic quality of pork.

Contamination with S. enterica has been found in lairage and drinking water offered to pigs (Rostagno et al., 2003; Hurd et al., 2002; Arguello et al., 2012). In one study, among the sampled pens, there was at least one positive sample; all pig groups tested positive for S. enterica in ileocecal lymph nodes and cecal contents. From 586 pigs, truck, and pen isolations, 36 different Salmonella spp. serovars were isolated. From 353 isolations in pigs (109 of ileocecal lymph nodes and 244 of cecal nodes), 27% corresponded to the same serovars isolated in the trucks, and 19% were related to those from pens (Rostagno et al., 2003).

With regard to stress, when animals are transported in trucks for 2 to 4 hours, increased levels of circulating cortisol or beta-endorphins and neutrophils are found (McGlone et al., 1993; Geverink et al., 1998). Stress may influence the outcome of many bacterial infections. Exposure to various stressors increases fecal shedding of these pathogens. Theoretically, the relationship between animal welfare and food safety is an effect that should not be overlooked (Verbrugghe et al., 2012).

Pigs can carry the microorganism in their skin, oral cavity, feces or lymph nodes (Lo Fo Wong et al., 2002), meaning that cross-contamination of carcasses occurs mainly through bacteria redistribution originating from positive pigs during the various slaughter stages (Berends et al., 1997; Botteldoorn et al., 2004; Busser et al., 2011).

In the initial stage of the process, during scalding, water can enter the lungs and contaminate the oral cavity and the pharynx; later, during the removal of the lungs, this liquid can contaminate the carcass. The dehairing equipment can continuously become contaminated with feces due to the movement of the pigs by the equipment. After flaming and during polishing, knives may favor distribution of microorganisms that were not eliminated by flaming. Additionally, knives may become contaminated if left undisinfected between carcasses. Contact of gastric contents with abdominal and thoracic cavities should be avoided during evisceration. The highest risk of contamination occurs upon separating the rectum and removing the viscera which may be perforated, their contents being able to contaminate the carcass, utensils and/or gloves of the workers (Borch et al., 1996; Fedorka-Cray et al., 2000; van Hoek et al., 2012).

With regard to carcass contamination, 5 to 15% occur during polishing, 55 to 90% during removal of viscera and 5 to 35% during other processes, such as rectum separation, ventral opening of the carcass, and meat inspection (Hald et al., 2003; Botteldoorn et al., 2004).

During the slaughter process, Salmonella spp prevalence was 6.3% (Zerby et al., 1998), 10.5% (Bouvet et al., 2003), 12.9% (Vieira-Pinto et al., 2005), 30% (Berends et al., 1997), and even as much as 37% (Botteldoorn et al., 2003) in carcass samples, and 24% (Bouvet et al., 2003) and as much as 53% (Botteldoorn et al., 2003) in environmental samples. These values may have resulted from increased infected animals during extended lairage. It is thought that as much as 30% positivity for Salmonella spp. may be due to cross-contamination during slaughter (Berends et al., 1997) and meat cutting (Lo Fo Wong et al., 2002). A prevalence of 18.8% has been found in mesenteric lymph nodes and in ileum, 13.9% (Vieira- Pinto et al., 2005).

Pigs from farms with higher positivity in fecal samples become the most contaminated carcass in the slaughterhouse (Foley et al., 2008). Thus, an initial strategy that can be implemented in plants is slaughtering first the animals from sero-negative farms to reduce the cross-contamination risk (Swanenburg et al., 2001). It is also possible to improve carcass decontamination processes by using products based on organic acids (Buncic, 2011).

The most influential factors in meat crosscontamination with human pathogens are handling, storage, and product preservation when sufficient precautions and correct hygiene (e.g. washing and disinfecting hands, clothes and utensils) have not been taken. It should be assumed that carcasses do not conclude the process with absolute food safety in the slaughterhouse; so one or more carcasses may have a higher load of pathogenic bacteria with respect to the others and thus increase the probability of crosscontamination occurring (Berends et al., 1997; Gomez et al., 2012).

A study of Belgian cutting plants, which process 48% of the pig production in the country, found presence of Salmonella in 0% to 50% of meat samples in a single plant (Delhalle et al., 2009). In Ireland, prevalence reached up to 2.6%, with S. Typhimurium being the most common serovar (Prendergast et al., 2009), and in a study from New Zealand, the prevalence was 3.6% (Wong et al., 2009).

Salmonella can remain in the submaxillary lymph nodes or tonsils of living animals; therefore, when the head is separated from the carcass, microorganisms can come into direct contact with utensils or gloves, which subsequently represent a contamination risk (Borch et al., 1996; Scherer et. al., 2008; Vieira- Pinto et al., 2005). European studies reported that microorganism prevalence in these tissues was 9.3% to 12.9% in nodes and 9.9% to 19.6% in tonsils (Swanenburg et al., 2001; Vieira-Pinto et al., 2005).

Ready-to-eat pork products commonly contain low price cuts such as meat of the arms and neck, and back fat. Such materials undergo considerable handling during transport and cutting, increasing the risk of crosscontamination. In spite of the fact that cutting plants and plants that elaborate ready-to-eat pork products depend to a certain degree on the microbial quality of the raw material, they also have responsibility for assuring the quality of their end-products.

The thermal process should eliminate the presence of Salmonella spp. during preparation of ready-toeat products; so, theoretically, such products would be free of the pathogen. In spite of this process, evidence of S. Typhimurium prevalence has been reported in sausages in Ireland (Boughton et al., 2004).

The proportion of wholesale market for pork in Colombia; that is, hypermarkets and supermarkets, is smaller than that of small pork distributors. Some wholesalers have their own cutting plants and distribute the meat directly to the sale points. Some large distributors supply smaller ones, and they cut or sell pieces to small butchers. In addition, not all slaughtered animals at a plant are destined for consumption in the same city or region, meaning that the product may be transported long distances, increasing the risk of contamination due to improper handling and preservation.

There is always a risk of contamination during food handling. Cross-contamination can occur when using contaminated kitchen implements in foods that do not require cooking before consumption, for example, when the meat is cut on a board with a knife and the knife is later used to cut vegetables that will be consumed as salad. In addition, proper cooking time and temperature should be used. The supply chain ends when the product is consumed.

The presence of non-typhoid Salmonella spp. serovars in food affects its safety and thus its international trade. The WTO (World Trade Organization) considers food safety a fundamental subject integrated into commerce to protect consumers in any part of the world where the product may be marketed. The FAO (Food and Agriculture Organization) and the WHO (World Health Organization) establish directives through the Codex Alimentarius to guarantee the marketing of safe foods. Likewise, the WTO recognizes OIE (currently World Organization for Animal Health) guidelines as the international reference.

The SPS agreement (Sanitary and Phytosanitary Measures) of the WTO establishes the guiding principles to protect the health and life of people and animals and to preserve plants for international trade. The CONPES 3458 framework of 2007 established the political guidelines on animal health and food safety for the pork supply chain in Colombia.

Although studies toward establishing a baseline for this microorganism have been conducted, health status regarding Salmonella spp. is still not known in Colombia. Therefore, future studies and projects should investigate non-typhoid Salmonella prevalence in each stage of the supply chain. In addition, further molecular and genomic studies are needed for epidemiological purposes to determine the current serovars present in the country and the clonal relationships among stages.

A productive approach would include inspection, surveillance, and control by official agencies in each stage of the chain, and voluntary programs should be established for monitoring, controlling, and implementing quality and safety systems (Good Practices, HACCP, ISO Standards) to ensure production of safe food under the concept of ''stable to table''. This way, consumer health would be protected, generating confidence in the product and improving market competitiveness.

In 2007 the Ministry of Health and Social Protection of Colombia issued Decree 1500 (normalized by resolution 4282 of the same year), which regulates inspection, monitoring and control of fresh pork and further processed by-products. Article 51 describes the performance standard for Salmonella spp.

As a part of the policy framework mentioned in the CONPES document, the College of Veterinary Medicine and Animal Science of the Universidad Nacional de Colombia completed in 2011 the project entitled ''Isolation and molecular characterization of Salmonella strains, antimicrobial susceptibility and microbiological risk assessment of contamination in carcass, cuts and pork products, strategies for prevention and control in slaughterhouse and processing plants''. This project was funded by the Colombian Ministry of Agriculture and Rural Development to establish the presence of the organism in pre-slaughter, slaughter and post-slaughter stages in Colombia. The results are currently in publication process.

Perspectives

Studies should be conducted to establish baselines for Salmonella contamination in each stage of the pork supply chain in Colombia, identifying the differential risks and establishing measures to monitor prevention and reduction in the relevant processes. Controlling the microorganism will require the coordinated actions of each actor in every stage of the supply chain. It also requires implementing quality and food safety systems, official and voluntary adoption, and also the integrated participation of industry with the official and academic sectors.

Salmonella results obtained in the pork supply chain could be related to isolates from human cases in our country, which would allow more targeted and specific strategies.

Achieving these goals should allow improving scientific, technical and operational capacity of official laboratories. It would also help improving diagnostic and university laboratories to develop research projects by implementing reference techniques.

Validation and transfer of research results will enable authorities to focus on national programs aimed at discussing food safety issues on international trade and public health.

Prevention and control of Salmonella in foods of animal origin requires participation and interaction of all actors in the production chain: the official, the production, and academic sectors. This will contribute to improved competitiveness of the chain and encourage the opening of new markets under the Sanitary and Phytosanitary Measures framework agreement.

¤ To cite this article: Rodríguez DM, Suárez MC. Salmonella spp. in the pork supply chain: a risk approach. Rev Colomb Cienc Pecu 2014; 27:65-75

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