Prevalence, distribution, and molecular characterization of Salmonella recovered from swine finishing herds and a slaughter facility in Santa Catarina, Brazil

https://doi.org/10.1016/j.ijfoodmicro.2011.09.024Get rights and content

Abstract

Swine can carry Salmonella strains that may be transmitted to humans by pork products. This investigation determined the distribution and types of Salmonella in 12 swine finishing herds and a slaughter facility in Santa Catarina, Brazil. A total of 1258 samples, consisting of environmental, feed, carcass, lymph node, and fecal material were collected and submitted to bacteriological isolation of Salmonella. From 487 positive samples, 1255 isolates were recovered and confirmed to be Salmonella. The distribution of positive samples was as follows: finishing pen floors 26% (16/61); feed 29% (42/143); feces 44% (52/119); pooled feces 59% (35/59); slaughter holding pens 90% (36/40); lymph nodes 46% (220/478); pre-chilled carcass surfaces 24% (24/98); and post-chilled carcass surfaces 24% (62/260). The most prevalent serovars were Typhimurium, Panama, Senftenberg, Derby, and Mbandaka. By pulsed-field gel electrophoresis, 1071 isolates were subtyped using XbaI, and duplicate isolates were removed. From the remaining 747 isolates, 163 macrorestriction profiles (pulsotypes) were identified. Six pulsotypes were considered very frequent, occurring in 33 isolates or more. The multiple correspondence analyses showed correlations between pulsotypes from shedding pigs (feces), herd environment (pen floors), and subiliac and prescapular lymph nodes and between lairage and carcass surface samples before and after chilling. All sources of Salmonella investigated contributed to the carrier state; however, pre-slaughter contamination at lairage was the variable most strongly associated with carcass contamination. A total of 59 different antimicrobial resistance profiles were observed in 572 Salmonella isolates. From these isolates, 17% (97/572) were susceptible to all 15 antibiotics tested, 83% (475/572) were resistant to at least one, and 43% (246/572) were resistant to four or more antibiotics (multi-resistant). The AmpGenKanTet profile was the most prevalent in carcass isolates and was associated with farm origin.

Highlights

Salmonella including drug-resistant strains are distributed in swine production. ► Salmonella from herds and pre-slaughter contribute to carcass contamination. ► Salmonella carcass contamination is strongly associated with lairage contamination.

Introduction

Most Salmonella serotypes are considered potential human pathogens (WHO, 2005), and Salmonella is recognized worldwide as a major human food-borne pathogen (CDC, 2008). Although eggs are considered an important vehicle of infection and associated with food-borne outbreaks, contaminated pork and pork products may be responsible for up to 25% of all Salmonella infections in humans (Borch et al., 1996). Swine was a primary source of human salmonellosis in 15% of the cases in Denmark and The Netherlands and 25% of the cases in the U.S. (Bean and Griffin, 1990).

The continuous entrance of animals carrying and shedding Salmonella in slaughterhouses is the main source of pork contamination (Berends et al., 1997). Thus, efforts have been taken to minimize Salmonella shedding in swine in order to lower the hazard of contamination at slaughterhouses. Good Manufacturing Practices reduce cross-contamination during slaughter and processing; however, the first critical control point involves the reduction of delivery of shedders to the slaughterhouse (Borch et al., 1996). In previous studies, the finishing stage was shown to be critical for Salmonella infection amplification in the swine production system (Funk et al., 2001, Silva et al., 2006). The spread of Salmonella from a number of sources and the variability in the serovars isolated from positive samples demonstrate the epidemiological complexity in the swine production chain. Thus, it is difficult to determine the epidemiological relationship between sources of Salmonella transmission throughout the production chain and pork contamination. There are several tools available for subtyping and discriminating Salmonella, and one commonly-used technique for this purpose is DNA macro-restriction associated with pulsed-field gel electrophoresis (PFGE). This method has been used routinely in food-borne outbreak investigations, as well as in epidemiological veterinary studies (CDC. Center for Disease Control and Prevention, 2004, Giovannacci et al., 2001, Wonderling et al., 2003, Botteldoorn et al., 2004, Vieira-Pinto et al., 2006, Vigo et al., 2009).

Another challenge for human health is the emergence of multi-drug resistant Salmonella strains (Duijkeren et al., 2003). Moreover, it has been demonstrated that the transmission of resistance genes among bacteria colonizing the human gut is possible (Trobos et al., 2008). Infection with multi-resistant strains limits the chances of effective treatment. Swine and other production animals are recognized as a primary reservoir of multi-resistant bacteria (Wedel et al., 2005). The emergence of multi-resistant Salmonella is often related to mobile genetic elements (Butaye et al., 2006) that have spreading capacity among the population.

The southern region of Brazil includes the most important swine producing areas in the country, accounting for almost 65% in the last trimester of 2010 (IBGE, 2011-http://www.ibge.gov.br/home/estatistica/indicadores/agropecuaria/producaoagropecuaria/abate-leite-couro-ovos_201004_publ_completa.pdf) of the national pork production, which reached 3.19 million tons in 2009 (ABIPECS, 2010). Salmonella infection in swine herds of southern Brazil has been demonstrated by isolation and serology surveys (Kich et al., 2007). Antimicrobial resistance among porcine Salmonella strains has been also reported and characterized (Michael et al., 2005a, Michael et al., 2005b, Michael et al., 2008). In Brazil, ongoing Salmonella surveillance programs are conducted in poultry and interventions have recently been started in pig herds.

The objectives of this study were to determine: (1) the distribution of serotypes and clonal groups of Salmonella in 12 swine finishing herds and a slaughter facility in Santa Catarina, Brazil; (2) the epidemiological relationship among Salmonella isolates from the herd environment (floor swabs), shedders (swine fecal samples), feed, the lairage environment, lymph nodes, and carcasses; and (3) antimicrobial resistance profiles and their relationship with clonal groups and origin of the strains.

Section snippets

Materials and methods

This longitudinal study was conducted in one swine Production Company that adopted a two-site pig management system in vertically integrated farms. This company represented 7% of the annual number of pigs slaughtered in Brazil in 2007 (ABIPECS, 2007 http://www.abipecs.org.br/uploads/relatorios/relatorios-associados/ABIPECS_relatorio_2007_pt.pdf). A total of 12 cohorts represented by finishing herds located in the state of Santa Catarina, Brazil, each with a holding capacity of 250 to 800

Results

On placement day (70-day-old pigs), the seroprevalence was 23% (ranging from 0 to 66%) and increased to 92% (83 to 100%) at the slaughter age (150-day-old pigs), demonstrating the exposure to Salmonella in all herds. Analysis of 1258 samples from twelve finishing herds, including those taken at the slaughterhouse revealed that 487 samples (39%) were positive for Salmonella. The distribution of positive samples among the 12 herds is shown in Table 1. Overall Salmonella was most found in swabs

Discussion

In Brazil, a number of studies have shown that the finishing step is responsible for enhancing Salmonella-transmission and delivery of pig batches with a high number of carriers at slaughterhouses (Bessa et al., 2004, Kich et al., 2007, Schwarz et al., 2009). The same scenario was observed in our study, since twelve cohorts of pigs, with a low seroprevalence at placement on the farm and followed throughout the finishing phase, presented an increase in the number of Salmonella-seropositive pigs.

Acknowledgments

We thank Jovita Haro at the Agricultural Research Service (ARS), Richard B. Russell Research Center, for performing the antimicrobial resistance tests. We are also grateful to Embrapa and the ARS, Eastern Regional Research Center for funding this study.

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