Salmonella enterica and enterobacteria in pig carcasses processed on different slaughter days

Salmonella enterica e enterobactérias em carcaças suínas processadas em diferentes dias de abate

Abstract

The objective of this work was to evaluate the contamination by Salmonella sp. and enterobacteria in pig carcasses from the first and last batches slaughtered in a same week, at different stages of the slaughtering line. Samples were collected from the first and last batches slaughtered on Monday and Friday of each week, respectively, during five weeks, totaling ten batches. From each batch, ten carcasses were collected in eight stages of the slaughter line: bleeding, scalding, singeing/evisceration, inspection, spinal cord removal, final washing, blast chilling, and after cooling. A total of 800 samples were analyzed for Salmonella sp. and enterobacteria quantification. The last batch of the week showed twice the chances of the pig carcasses being contaminated with Salmonella sp. and, consequently, a greater amount of enterobacteria (1.00 log₁₀ CFU per square centimeter) than the first batch (0.88 log₁₀ CFC per square centimeter). A higher count of enterobacteria was also observed in the stages of bleeding (2.37 log₁₀ CFU per square centimeter) and scalding (2.36 log₁₀ CFU per square centimeter). The last batches slaughtered in the week show a greater contamination than the first ones, and there is a greater contamination of carcasses by Salmonella sp. and enterobacteria in the initial stages of pig slaughter, i.e., at bleeding and scalding.

Index terms:
foodborne illnesses; fridge; pig batch

Resumo

O objetivo deste trabalho foi avaliar a contaminação por Salmonella sp. e enterobactérias em carcaças suínas do primeiro e do último lote abatido na mesma semana, em diferentes etapas da linha de abate. Foram coletadas amostras do primeiro e do último lote abatido na segunda e na sexta-feira de cada semana, respectivamente, durante cinco semanas, o que totalizou dez lotes. De cada lote, foram coletadas dez carcaças, em oito etapas da linha de abate: sangria, escaldagem, chamuscador/evisceração, inspeção, retirada da medula espinhal, lavagem final, choque térmico e refrigeração. Um total de 800 amostras foi analisado para quantificação de Salmonella sp. e enterobactérias. O último lote da semana apresentou duas vezes mais chances de as carcaças estarem contaminadas com Salmonella sp. e, consequentemente, maior quantidade de enterobactérias (1,00 log₁₀ UFC por centímetro quadrado) que o primeiro lote (0,88 log₁₀ UFC por centímetro quadrado). Uma quantidade maior de enterobactérias também foi observada nas etapas de sangria (2,37 log₁₀ UFC por centímetro quadrado) e escaldagem (2 , 36 log₁₀ UFC por centímetro quadrado). Os últimos lotes abatidos na semana apresentam contaminação maior do que os primeiros, e há maior contaminação das carcaças suínas por Salmonella sp. e enterobactérias nas etapas iniciais do abate de suínos, isto é, na sangria e na escaldagem.

Termos para indexação:
doenças transmitidas por alimentos; frigorífico; lote de suíno

Introduction

Several countries in Latin America are implementing national epidemiological surveillance systems for foodborne illnesses (FBIs). In Brazil, most FBIs are caused by bacteria, among which Samonella sp. is one of the most important (Brasil, 2018b).

Samonella sp. is a pathogen with a great zoonotic potential, as salmonellosis is one of the most commonly reported foodborne diseases worldwide. Outbreaks in humans are caused by the consumption of products derived from pigs, which represent an important source of contamination (Pires et al., 2014). This shows the need of assessing the hygiene conditions during the pig slaughtering process, which can be done using several groups of bacteria – such as, for example, Escherichia coli and Salmonella sp., both members of the Enterobacteriaceae family – as a quality standard (Milios et al., 2014).

A study carried out in Southern Brazil showed a high prevalence of Salmonella sp. in pigs at pre-slaughter, with values ranging from 8.7 to 24% in pre-cooled carcasses (Paim et al., 2019). In an exploratory research carried out by Ministério da Agricultura, Pecuária e Abastecimento (MAPA) on the presence of Salmonella sp. in pig carcasses in Brazil, Salmonella sp. was found in 10.3% (81 out of 788) of the carcass samples collected before cooling and in 5.5% (42 out of 756) of the samples collected after cooling (Anuário…, 2 016 ).

The surface of carcasses can carry different types and quantities of microorganisms, making the slaughter stages critical points in the process to prevent, reduce, or eliminate microbiological hazards (Choi et al., 2013). Some preventive actions to control this problem include the implementation of food safety programs, such as the Hazard Analysis and Critical Control Point, during the entire process of slaughter and meat processing, with monitoring through microbiological analysis (Fajardo-Guerrero et al., 2019).

Brazil is considered one of the main food producers worldwide (ABPA, 2021). For the increase in the consumption and rise in the market of pork or its byproducts, it is essential that the final product is within the current hygienic and sanitary standards and does not cause risks to consumer health, which requires minimizing, as much as possible, the presence of microorganisms that cause FBIs (Paim et al., 2019).

The objective of this work was to evaluate the contamination by Salmonella sp. and enterobacteria in pig carcasses from the first and last batches slaughtered in a same week, at different stages of the slaughtering line.

Materials and Methods

The experiment was carried out in a federally-inspected pig slaughterhouse, which is located in the state of Santa Catarina, Brazil, and where the average slaughter is of 4,630 pigs per day. The first and last batches slaughtered in a same week – on Monday and Friday, respectively – were sampled for a period of five consecutive weeks, from May to June 2018, totaling ten batches.

Upon their arrival at the slaughterhouse, the pigs were unloaded with the aid of mobile ramps and directed to the pens where they were separated by batch. There, they were cleaned with water jets and left to rest from 4 to 5 hours. After the animals were removed from the pens, these were cleaned with water and disinfectant for the arrival of the next batch.

The pigs were taken through corridors to the beginning of the slaughter line, being electrically stunned at the end. At this stage, the pigs whose carcasses would be sampled were identified by a cut in their ear. After bled on the mat, the pigs were hung on hooks of the conveyor for their blood to leak out. Then, the slaughtered pigs were released into a scalding tank at an average temperature of 62ºC and hung again on the conveyor for their carcasses to be scorched by flames in a continuous tunnel. After being scorched, the carcasses were cleaned (remaining hair was removed) and washed with water jets.

In the clean slaughter area, the rectum of the animals was occluded with an appropriate pistol and the carcasses were eviscerated for the removal of giblets and the head. Since the heads were removed, the initial identification of the carcasses for sampling was substituted by plastic tapes tied to the double chin. After this procedure, the carcass was divided into two parts (half carcasses) using an electric saw – sterilized in boiling water between one carcass cut and the other –, with the half carcasses still hanging from the same hook. Afterwards, the carcasses were inspected and taken on the transport rails for spinal cord removal and then washing with water jets. After all these procedures, the carcasses were placed in a cooling chamber at -7°C.

The evaluated samples were collected from ten carcasses from each batch, always from the first carcass of the batch, skipping four carcasses, and then from the next carcass. The same carcass was sampled after each stage of the entire slaughter line, i.e., bleeding, scalding, singeing/evisceration, inspection, spinal cord removal, final washing, blast chilling, and after cooling. The samples were specifically collected from the carcasses after thermal shock, in average 1 hour after the shower, and from the left carcass, at the cooling point, at -8°C, in average 12 hours later.

For enterobacteria quantification, 800 samples were collected by rubbing three 132 cm² areas of the belly, loin, and ham surfaces, totaling an area of 396 cm² per sample. A marker was used to indicate the pre-established areas for sample collection on the carcass. For Salmonella sp. collection, the entire area of each carcass was frictionized, forming a pool used to detect the presence or absence of the bacteria. Two sterile 3M sponges (3M United States, Saint Paul, MN, USA) – one for Salmonella sp. and the other for enterobacteria –, hydrated with 10 mL of 1.0% peptone water, free from biocides, were used for each carcass at each collection point. After sample collection, the sponges were placed in plastic bags and stored under refrigeration in isothermal boxes.

The samples were analyzed for the presence of Salmonella sp. and of enterobacteria quantified in colony forming units (CFU) in the microbiology sector of the slaughterhouse laboratory.

For enterobacteria, the ISO 21528-2:2017 method (ISO, 2017a) of plate count was used. For this 1.0% peptone water was added to the sample, homogenizing and removing the 1.0 mL aliquot. This volume was placed in a petri dish containing 15 mL of violet red bile agar. After agar solidification, the plates were incubated in the inverted position, at a temperature of 36±1°C, for 18 to 24 hours, and then CFU were counted.

For the analysis of Salmonella sp. in the samples, the MDS II 3M detection assay kit (3M United States, Saint Paul, MN, USA) was used, following the loop-mediated isothermal DNA amplification molecular technique, based on the isothermal amplification of specific DNA sequences and described by Domesle et a l . (2 017 ).

After screening, the positive samples underwent a confirmatory analysis using method ISO 6579-1:2017 (ISO, 2017b). First, the sample was enriched through a specific medium and then through a selective one. Afterwards, the samples were spread on agar plates to isolate the colonies. After the isolation of the characteristic colonies, biochemical tests were carried out and an antiserum was used for confirmation. If the sample presented a positive result, the isolates were serotyped on a plate with antisera using the microagglutination technique, as described by White-Kauffmann-Le (2007).

The data were tabulated in an Excel spreadsheet where the amount of Salmonella per stage and per day of slaughter was counted, transformed from mL to cm², and expressed as log₁₀ CFU per square centimeter. The normality of the enterobacteria data was verified with the Shapiro-Wilk (PROC UNIVARIATE) test. For the analysis of Salmonella, the logistic regression test and odds ratio (PROC LOGISTIC) were used. Enterobacteria were quantified by the Wilcoxon and Kruskall-Wallis (PROC NPAR1WAY) tests, and means were compared by the Dwass-Steel-Critchlow-Fligner test. Differences were considered significant at 5% probability. All analyzes were performed using the SAS software, version 9.4 (SAS Institute, Inc., Cary, NC, USA).

Results and Discussion

The contamination of pig carcasses, both by Salmonella sp. and by enterobacteria, was frequent but decreased significantly throughout the stages of pig slaughter and processing of the carcasses (Table 1).

Table 1
Characterization of pig carcasses regarding the amount of enterobacteria and the number and serovars of Salmonella sp. in the sampling points along the slaughter line during five weeks in a federally-inspected slaughterhouse in the state of Santa Catarina, Brazil.

Colletion point (slaughtering stage)	Average of enterobacteria (log10 CFU per cm-²)	Number of carcasses positive for Salmonella sp. on Monday and Friday	Serovar
Bleeding	11,380.31	57	Derby Monophasic (1,4, [5], 12: i :-) Infantis Schwarzengrund Infantis Braenderup Heidelberg Agona
Scalding	5,258.49	60	Schwarzengrund Rissen Panama Infantis Javiana Anatum Ohio Livingstone Typhimurium Bredeney Monophasic (1,4, [5], 12: i :-) Panama Derby
Singeing /evisceration	31.47	3	Infantis
Inspection	111.12	2	Infantis
Spinal cord removal	135.69	0	-
Final wash	653.83	1	Monophasic (1,4, [5], 12: i :-)
Blast chilling	1.46	0	-
After cooling	0.01	0	-

A greater contamination by enterobacteria was observed in the last batches of the week, slaughtered on Fridays (1.00 log₁₀ CFU per square centimeter), than in the first batches slaughtered on Mondays (0.88 log₁₀ CFU per square centimeter) (p<0.05) (Figure 1). In addition, higher enterobacteria counts were obtained in the stages of bleeding (2.37 log₁₀ CFU per square centimeter) and scalding (2.36 log₁₀ CFU per square centimeter) (p>0.05), which did not differ from each other (Figure 2).

Figure 1
Quantification of enterobacteria (log₁₀ CFU per cm²) in pig carcasses according to slaugther days (Monday and Friday) in the same week during fiive weeks in a federally-inspected slaughterhouse in the state of Santa Catarina, Brazil.

Figure 2
Quantification of enterobacteria (log₁₀ CFU per cm²) in pig carcasses in different stages of the slaughter line during five weeks in a federally-inspected slaughterhouse in the state of Santa Catarina, Brazil. Equal letters, on the bars, do not differ by the Dwass-Steel-Critchlow-Fligner test, at 5% probability.

Therefore, significant differences were found in the degree of contamination by enterobacteria in the samples collected in the first and last slaughtered batches of the week. This difference was approximately five-fold greater in the last batch slaughtered within the same week, i.e., bacterial counts were significantly higher in the last batches than in the first ones.

The presence of Salmonella sp. was detected in 123 of the 800 samples collected and analyzed throughout the study. Comparing the evaluated days of the week by logistic regression, the carcasses of the last batch of the week were twice as likely by the odds ratio to be contaminated with Salmonella sp. than those of the first batch of the week.

These data agree with the findings of Corbellini et al. (2016), who evaluated two sets of samples collected from pigs, considering sampling days. These authors reported more positive estimates for samples collected on Tuesday than on Monday.

Bleeding and scalding were the stages with the highest number of carcasses contaminated by Salmonella sp., with 57 and 60 contaminated samples out of 100. A large decrease was observed after the stages of singeing/evisceration (3/100), inspection (2/100), and final wash (1/100) (Figure 3).

Figure 3
Number of pig carcasses positive for Salmonella sp. at different stages of the slaughter line, with samples collected on Monday and Friday of the same week during five weeks, in a federally-inspected slaughterhouse in the state of Santa Catarina, Brazil.

During the pig raising process, several factors can cause contamination by Salmonella sp., making it difficult to completely eliminate this pathogen before the animals reach the slaughterhouses. Moreover, the volume of animals slaughtered throughout the day in the same slaughter line and without proper sanitation increases the chances of cross-contamination.

In the slaughtering line, cross-contamination can occur between carcasses due to handling by employees and direct contact with equipment and utensils. For this reason, proper hygiene is essential – as the greater the number of animals slaughtered per day, the greater the risk of contamination – and also avoiding the contact of the carcass with intestinal contents (Paim et al., 2019).

The reliability of data referring to Salmonella sp. was also verified, specifically the odds ratio of contamination along the slaughter line through the receiver operating characteristic curve. The results showed 92% reliability considering the variation of the curve – the further away from the central line, the greater the reliability of the data found. When evaluating the sampled points along the slaughter line, after scalding and bleeding, the probability of finding Salmonella sp. was of 60 and 55%, respectively.

The carcasses of all slaughtered batches were positive for Salmonella sp., and the presence of the pathogen was observed in 57 carcasses in the first stage of slaughter (Figure 3). According to Corbellini et al. (2016), pig batches delivered with a high level of this microorganism may result in a higher than average contamination of carcasses by Salmonella sp. on slaughter day. The data obtained in the present study confirm those of Paim et al. (2019), who found that all ten batches sampled after bleeding were positive for the bacteria, suggesting that the pigs already arrived contaminated at the slaughter line.

In Brazil, most farmed pigs are positive for Salmonella sp., as shown by Silva et al. (2012), who found, through ELISA’s technique, 80.6% seroprevalence in batches at finishing and 23.8% of cecal contents positive for the bacteria. In another study carried out in the province of Córdoba, Argentina, Vico et al. (2020) observed a prevalence of 41. 5 % Salmonella, strongly associated with infections of this microorganism in the pre-slaughter period (distance between the farm to the slaughterhouse and lairage time), with a possible dissemination to other animals exposed to the same environment. Baer et al. (2013) point out that Salmonella spp. have the ability of resisting in an environment for long periods of time, which can cause asymptomatic infections; the infected carrier animals can be a source of contamination for the healthy population of the herd, including in slaughterhouses.

Dang-Xuan et al. (2017) reported a prevalence of 45% Salmonella sp. in fresh pork meat in Vietnam and a 17.7% probability of human beings contracting the disease due to the consumption of boiled pork. These results are indicative of how important it is to collect data on the contamination of pork carcass and meat by Salmonella sp., which is prevalent in several parts of the world and may cause serious health problems to humans.

Contamination by enterobacteria did not differ significantly (p>0.05) at carcass inspection, final washing, singeing/evisceration, and spinal cord removal, with 0.81, 0.69, 0.65, and 0.49 log₁₀ CFU per square centimeter, respectively. However, a significant reduction in contamination was observed in the stage of blast chilling, followed by that of after cooling, with values of 0.11 and 0.00 log₁₀ CFU per square centimeter (p<0.05), respectively (Figure 3).

After the scalding process, there was no significant reduction in the enterobacterial contamination of pig carcasses. This was the stage with the greatest contamination by Salmonella sp., followed by bleeding. All sampled batches (60 carcasses) were positive for this bacteria. It is noteworthy that these two stages of slaughter take place in the dirty area of the slaughterhouse.

In 80% of the batches evaluated during scalding, the serovars of Salmonella sp. were different from those found in the bleeding stage, showing a possible cross-contamination between batches and that scalding is a critical stage for the occurrence of such contamination (Table 1). The water inside the scalding tank comes into contact with the organic matter released from the carcasses and can become highly contaminated, although water temperature during this process must be between 62 and 72°C (Brasil, 2018b). If the scalding water is at a temperature below 60°C or has a large amount of organic matter, microorganisms may survive and there may be cross-contamination between carcasses. Zeng et al. (2021) concluded that the recycled water used in the dehairing machine was the main source of carcass contamination in the slaughterhouse.

However, the alkalinization of the scalding water can contribute to the elimination of Salmonella sp. (Inagaki et al., 2018), which made irrelevant the accumulation of organic matter in the water at 62°C in the present study. Therefore, scalding can reduce bacteria in the carcasses (Buncic & Sofos, 2012) if these are clean when entering the slaughter line.

Another critical stage in pig slaughtering is evisceration, which involves the total removal of animal viscera, increasing the chances of contaminating not only the carcass but also the entire slaughter line due to the risk of perforation and leakage of contents during belly opening (Swart et al., 2016). However, in the present study, a low level of contamination by enterobacteria and Salmonella sp. was observed at this stage, since only three carcasses from the same batch were positive for the bacteria. Furthermore, the serotype found in the carcasses in the previous stages was the same as in singeing/evisceration, which does not even indicate cross-contamination between them.

Similar results were found by Zeng et al. (2021), who concluded that evisceration did not seem to be critical since the percentage of contamination of the carcasses was similar before (16.7%) and after (18.3%) this slaughter stage. Cardoso & Silva (2015) suggested that the main cause of reduction in contamination after evisceration was the scorching of the carcasses, in direct contact with the flames, at high temperatures that can exceed 700°C, which almost completely eliminate microorganisms.

The last batch of the week was positive for Salmonella sp. at the slaughter point after the inspection stage, right after the carcass was split into two. Carcass division is a critical step in terms of microbial contamination in the slaughter line, and the disinfection of the saw is recommended after processing each carcass (Cardoso & Silva, 2015). Despite this result, this stage showed a low contamination both by enterobacteria and Salmonella sp., as only two samples were positive for Salmonella sp., whose serovars were the same found in the previous stages.

The final wash can also be considered a critical control point, even though the obtained result does not differ from those found in singeing/evisceration, inspection, and spinal cord removal. At that stage, there still was contamination by enterobacteria and two samples in the last batch of the week were positive for Salmonella sp., with similar values to those of 1.25 and 3.9%, respectively, reported by Hernández et al. (2013) and Mannion et al. (2012). The action of water on the carcasses during final washing can contribute to the spread of bacteria on the surface of the carcasses and between them.

In the present study, the presence of Salmonella sp. was verified in the washing step in one of the evaluated batches, that is, in a single day. However, it is not possible to conclude there was cross-contamination between batches since a sample from a carcass from the first batch was contaminated and the same serotype was found in the scalding step in this same carcass. This result is indicative that there was a reduction and not the elimination of the bacteria throughout the slaughter stages.

Samples collected after thermal shock and after cooling showed different levels of contamination by enterobacteria, but not by Salmonella sp. This may be related to the use of controlled temperature, which reduces the microbiological load of the slaughtered carcasses, besides decreasing their pH. In the carcass blast chilling and cooling stages, the negative temperature – which must be below -8 and -7°C, respectively (Brasil, 2018b) – is one of the great contributors to the reduction of that microorganism. Arguello et al. (2012) found that the low temperature and reduction in water activity were two important factors to help reduce the concentration of Salmonella sp. in the cooling chamber due to a continuous air flow.

In the classification of Salmonella sp., 15 different serovars were found. The most frequent, in a decreasing order, were: 31 monophasic Typhimurium (1,4, [5], 12: i:-), 25 Infantis, 21 Derby, 20 Typhimurium, and 6 Schwarzengrund (Figure 4). Of the serotyped samples, a total of 39.7% were identified as Typhimurium and its variants.

Figure 4
Percentage of Salmonella sp. serovars in pig carcasses, whose samples were collected on Monday and Friday during five weeks throughout the slaughter process in a federally-inspected slaughterhouse in the state of Santa Catarina, Brazil.

The monophasic variant Salmonella T y p h i m u r i u m , which has swine as one of its main hosts, causes salmonellosis in humans who consume contaminated pork meat (Gonzales-Barron et al., 2012; Crump et al., 2015). Campos et al. (2019) mainly attributes the high percentage of the serovar Typhimurium clinically affecting humans to an intensified production chain and increased production of pigs and pork meat on an international scale.

Another 13 other serovars were also found, of which the most relevant, in a decreasing order, were: 25 Infants, 21 Derby, and 6 Schwarzengrund. When swabbing pig carcasses along the slaughter line, Paim et al. (2019) also observed the presence of several serovars of Salmonella sp., among them Typhimurium, Infantis, and Derby.

Considering the obtained results and Instrução Normativa N^o 60 of Agência Nacional de Vigilância Sanitária (Anvisa, 2019) and MA PA (Brasil, 2018a), in the present study, the pig slaughtering process followed, respectively, the microbiological standards for ready-to-eat foods for human consumption and the regulations for microbiological control in pig and cattle slaughterhouses.

Conclusions

1. The pig carcasses of the last batches of the week, slaughtered on Fridays, show a greater contamination by Salmonella sp. and enterobacteria than those of the first batches, slaughtered on Mondays.

2. There is a greater contamination of pig carcasses with both Salmonella sp. and enterobacteria in the initial stages of pig slaughter – bleeding and scalding –, regardless of the day of the week.

3. All actions taken along the slaughter line are effective in reducing the microbial load on the carcasses at the end of processing, making them suitable for commercialization.

Acknowledgments

To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for the scientific initiation scholarship granted to the second author.

References

• ABPA. Associação Brasileira de Proteína Animal. Relatório Anual 2021 2021. Available at: <https://abpa-br.org/wp-content/uploads/2021/04/ABPA_Relatorio_Anual_2021_web.pdf>. Accessed on: Apr. 14 2022.
  » https://abpa-br.org/wp-content/uploads/2021/04/ABPA_Relatorio_Anual_2021_web.pdf
• ANUÁRIO dos programas de controle de alimentos de origem animal do DIPOA. Brasília: Mapa, 2016. v.2. Available at: <https://www.gov.br/agricultura/pt-br/assuntos/inspecao/produtos-animal/arquivos-publicacoes-dipoa/anuario-dipoa-v2/view>. Accessed on: Apr. 14 2022.
  » https://www.gov.br/agricultura/pt-br/assuntos/inspecao/produtos-animal/arquivos-publicacoes-dipoa/anuario-dipoa-v2/view
• ANVISA. Agência Nacional de Vigilância Sanitária. Instrução Normativa nº 60, de 23 de dezembro de 2019. Estabelece as listas de padrões microbiológicos para alimentos. Diário Oficial da União, 26 dez. 2019. Seção1, p.133-139.
• ARGUELLO, H.; CARVAJAL, A.; COLLAZOS, J.A.; GARCÍA-FELIZ, C.; RUBIO, P. Prevalence and serovars of Salmonella enterica on pig carcasses, slaughtered pigs and the environment of four Spanish slaughterhouses. Food Research International, v.45, p.905-912, 2012. DOI: https://doi.org/10.1016/j.foodres.2011.04.017
  » https://doi.org/10.1016/j.foodres.2011.04.017
• BAER, A.A.; MILLER, M.J.; DILGER, A.C. Pathogens of interest to the pork industry: a review of research on interventions to assure food safety. Comprehensive Reviews in Food Science and Food Safety, v.12, p.183-217, 2013. DOI: https://doi.org/10.1111/1541-4337.12001
  » https://doi.org/10.1111/1541-4337.12001
• BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa nº 60, de 20 de dezembro de 2018. [Estabelece o controle microbiológico em carcaça de suínos e em carcaça e carne de bovinos em abatedouros frigoríficos, registrados no Departamento de Inspeção de Produtos de Origem Animal – DIPOA]. Diário Oficial da União, 24 dez. 2018a. Seção1, p.4-6.
• BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Portaria nº 1.304, de 7 de agosto de 2018. [Aprova as normas técnicas de instalações e equipamentos para abate e industrialização de suínos]. Diário Oficial da União, 22 ago. 2018b. Seção1, p.10.
• BUNCIC, S.; SOFOS, J. Interventions to control Salmonella contamination during poultry, cattle and pig slaughter. Food Research International, v.45, p.641-655, 2012. DOI: https://doi.org/10.1016/j.foodres.2011.10.018
  » https://doi.org/10.1016/j.foodres.2011.10.018
• CAMPOS, J.; MOURÃO, J.; PEIXE, L.; ANTUNES, P. Non-typhoidal Salmonella in the pig production chain: a comprehensive analysis of its impact on human health. Pathogens, v.8, art.19, 2019. DOI: https://doi.org/10.3390/pathogens8010019
  » https://doi.org/10.3390/pathogens8010019
• CARDOSO, M.R. de I.; SILVA, L.E. da. Controle de salmonela em matadouros-frigoríficos de suínos. In: KICH, J.D.; SOUZA, J.C.P.V.B. (Ed.). Salmonela na suinocultura brasileira: do problema ao controle. Brasília: Embrapa, 2015. p.115-154.
• CHOI, Y.M.; PARK , H.J.; JANG, H.I.; KIM, S.A.; IMM, J.Y.; HWANG, I.G.; RHEE, M.S. Changes in microbial contamination levels of porcine carcasses and fresh pork in slaughterhouses, processing lines, retail outlets, and local markets by commercial distribution. Research in Veterinary Science, v.94, p.413-418, 2013. DOI: https://doi.org/10.1016/j.rvsc.2012.11.015
  » https://doi.org/10.1016/j.rvsc.2012.11.015
• CORBELLINI, L.G.; BIANCO JÚNIOR, A.; COSTA, E. de F.; DUARTE, A.S.R.; ALBUQUERQUE, E.R.; KICH, J.D.; NAUTA, M. Effect of slaughterhouse and day of sample on the probability of a pig carcass being Salmonella-positive according to the Enterobacteriaceae count in the largest Brazilian pork production region. International Journal Food Microbiol, v.228, p.58-66, 2016. DOI: https://doi.org/10.1016/j.ijfoodmicro.2016.03.030
  » https://doi.org/10.1016/j.ijfoodmicro.2016.03.030
• CRUMP, J.A.; SJÖLUND-KARLSSON, M.; GORDON, M.A.; PARRY, C.M. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clinical Microbiology Reviews, v.28, p.901-937, 2015. DOI: https://doi.org/10.1128/CMR.00002-15
  » https://doi.org/10.1128/CMR.00002-15
• DANG-XUAN, S.; NGUYEN-VIET, H.; UNGER, F.; PHAM-DUC, P.; GRACE, D.; TRAN-THI, N.; BAROT, M.; PHAM-THI, N.; MAKITA, K. Quantitative risk assessment of human salmonellosis in the smallholder pig value chains in urban of Vietnam. International Journal of Public Health, v. 62 , p. 93-102, 2017. DOI: https://doi.org/10.1007/s00038-016-0921-x
  » https://doi.org/10.1007/s00038-016-0921-x
• DOMESLE, K.J.; YANG, Q.; HAMMACK, T.S.; GE, B. Validation of a Salmonella loop-mediated isothermal amplification assay in animal food. International Journal of Food Microbiology, v.264, p.63-76, 2017. DOI: https://doi.org/10.1016/j.ijfoodmicro.2017.10.020
  » https://doi.org/10.1016/j.ijfoodmicro.2017.10.020
• FAJARDO-GUERRERO, M.; ROJAS-QUINTERO, C.; CHAMORRO-TOBAR, I.; ZAMBRANO, C.; SAMPEDRO, F.; CARRASCAL-CAMACHO, A.K. Exposure assessment of Salmonella spp. in fresh pork meat from two abattoirs in Colombia. Food Science and Technology International, v.26, p.21-27, 2019. DOI: https://doi.org/10.1177/1082013219864746
  » https://doi.org/10.1177/1082013219864746
• GONZALES-BARRON, U.A.; REDMOND, G.; BUTLER, F. A risk characterization model of Salmonella Typhimurium in Irish fresh pork sausages. Food Research International, v.45, p.1184-1193, 2012. DOI: https://doi.org/10.1016/j.foodres.2010.04.036
  » https://doi.org/10.1016/j.foodres.2010.04.036
• HERNÁNDEZ, M.; GÓMEZ-LAGUNA, J.; LUQUE, I.; HERRERA-LEÓN, S.; MALDONADO, A.; REGUILLO, L.; ASTORGA, R.J. Salmonella prevalence and characterization in a free-range pig processing plant: tracking in trucks, lairage, slaughter line and quartering. International Journal of Food Microbiology, v.162, p.48-54, 2013. DOI: https://doi.org/10.1016/j.ijfoodmicro.2012.12.026
  » https://doi.org/10.1016/j.ijfoodmicro.2012.12.026
• INAGAKI, J.M.F.; SERENO, M.J.; PEGORARO, K.; WAZ, M.Z.; SOARES, V.M.; PEREIRA, J.G.; BERSOT, L. dos S. Effect of organic matter and pH on the resistance of Salmonella Typhimurium and Salmonella Derby in scalding water from pig slaughter. Journal of Food Safety, v.39, e12504, 2018. DOI: https://doi.org/10.1111/jfs.12504
  » https://doi.org/10.1111/jfs.12504
• ISO. International Organization for Standardization. ISO 21528-2:2017: Microbiology of the food chain: horizontal method for the detection and enumeration of Enterobacteriaceae – part 2: colony-count technique. 2^th ed. Geneva, 2017a.
• ISO. International Organization for Standardization. ISO 6579-1:2017: Microbiology of the food chain: horizontal method for the detection, enumeration and serotyping of Salmonella: part 1: detection of Salmonella spp. Geneva, 2017b.
• MANNION, C.; FANNING , J.; MCLERNON, J.; LENDRUM, L.; GUTIERREZ, M.; DUGGAN, S.; EGAN, J. The role of transport, lairage and slaughter processes in the dissemination of Salmonella spp. in pigs in Ireland. Food Research International, v.45, p.871-879, 2012. DOI: https://doi.org/10.1016/j.foodres.2011.02.001
  » https://doi.org/10.1016/j.foodres.2011.02.001
• MILIOS, K.T.; DROSINOS, E.H.; ZOIOPOULOS, P.E. Food safety management system validation and verification in meat industry: carcass sampling methods for microbiological hygiene criteria – a review. Food Control, v.43, p.74-81, 2014. DOI: https://doi.org/10.1016/j.foodcont.2014.02.041
  » https://doi.org/10.1016/j.foodcont.2014.02.041
• PAIM, S.D.; PISSETTI, C.; VIEIRA, T.R.; WERLANG, G.O.; COSTA, E. de F.; KICH, J.D.; CARDOSO, M. Enumeration, antimicrobial resistance and typing of Salmonella enterica: profile of strains carried in the intestinal contents of pigs at slaughter in Southern Brazil. Acta Scientiae Veterinariae, v.47, art.1636, 2019. DOI: https://doi.org/10.22456/1679-9216.89668
  » https://doi.org/10.22456/1679-9216.89668
• PIRES, S.M.; VIEIRA, A.R.; HALD, T.; COLE, D. Source attribution of human salmonellosis: an overview of methods and estimates. Foodborne Pathogens and Disease, v.11, p.667-676, 2014. DOI: https://doi.org/10.1089/fpd.2014.1744
  » https://doi.org/10.1089/fpd.2014.1744
• SILVA, L.E. da; DIAS, V.; FERRONATTO, A.; GUERRA, P.; BERNO, L.; TRICHES, N.; KICH, J.D.; CORBELLINI, L.G.; CARDOSO, M. Longitudinal dissemination of Salmonella enterica clonal groups through the slaughter process of Salmonella-positive pig batches. Journal of Food Protection, v.75, p.1580-1588, 2012. DOI: https://doi.org/10.4315/0362-028X.JFP-11-515
  » https://doi.org/10.4315/0362-028X.JFP-11-515
• SWART, A.N.; EVERS, E.G.; SIMONS, R.L.L.; SWANENBURG, M. Modeling of Salmonella contamination in the pig slaughterhouse. Risk Analysis, v.36, p.498-515, 2016. DOI: https://doi.org/10.1111/risa.12514
  » https://doi.org/10.1111/risa.12514
• VICO, J.P.; LORENZUTTI, A.M.; ZOGBI, A.P.; ALEU, G.; SÁNCHEZ, I.C.; CAFFER, M.I.; ROSMINI, M.R.; MAINAR-JAIME, R.C. Prevalence, associated risk factors, and antimicrobial resistance profiles of non-typhoidal Salmonella in large scale swine production in Córdoba, Argentina. Research in Veterinary Science, v.130, p.161-169, 2020. DOI: https://doi.org/10.1016/j.rvsc.2020.03.003
  » https://doi.org/10.1016/j.rvsc.2020.03.003
• WHITE-KUFFMANN-LE Minor scheme. In: GRIMONT, P.A.D.; WEILL, F.-X. Antigenic formulae of the Salmonella serovars 9^th ed. Paris: World Health Organization and Institute Pasteur, 2007.
• ZENG, H.; RASSCHAERT, G.; DE ZUTTER, L.; MATTHEUS, W.; DE REU, K. Identification of the source for Salmonella contamination of carcasses in a large pig slaughterhouse. Pathogens, v.10, art.77, 2021. DOI: https://doi.org/10.3390/pathogens10010077
  » https://doi.org/10.3390/pathogens10010077

Publication Dates

• Publication in this collection
  13 July 2022
• Date of issue
  2022

History

• Received
  21 Dec 2021
• Accepted
  26 Jan 2022