Prevalence and characterization of Salmonella in pigs from conventional and organic farms and first report of S. serovar 1,4,[5],12:i:- from Korea
Introduction
Salmonella enterica is a major foodborne zoonotic pathogen in humans causing life threatening infections mostly among young children, elderly, or immunocompromised individuals and poses significant threat to global public health (Weinberger and Keller, 2005). Approximately one million cases of nontyphoid Salmonella (NTS) illness, causing 20,000 hospitalizations and 370 deaths, occur each year in the United States (Scallan et al., 2011). Moreover, Salmonella was the second most commonly reported zoonoses in the European Union with a total of 91,034 confirmed cases of human salmonellosis in 2012 (EFSA and ECDC, 2014). In Korea, NTS strains are the third most common causative agents of water- and foodborne diseases (Gwack et al., 2010) and the serovar Enteritidis and Typhimurium are the two most prevalent serovars causing salmonellosis in humans as well as livestock (Tamang et al., 2011b).
Salmonella 1,4,[5],12:i:- is one of the most common Salmonella serovars responsible for human infections in many countries, including the second and sixth most prevalent serovar in Germany (EFSA, 2008) and the United States (CDC, 2008), respectively. Large outbreaks caused by this serovar have been reported in humans in the United States (CDC, 2007) and in the European Union (Bone et al., 2010). Pork and pigs are considered to be the main vectors in the spread of S. 1,4,[5],12:i:- strains (Wasyl and Hoszowski, 2012).
Increasing antimicrobial resistance has become a worldwide public health problem. Although antimicrobial therapy is not necessary for uncomplicated infections, severe Salmonella infections often require effective chemotherapy (Hohmann, 2001). Thus, Salmonella strains resistant to multiple antimicrobial agents may compromise the effective treatment of infections in humans. Moreover, reduced susceptibility to fluoroquinolones in Salmonella has been associated with clinical treatment failure causing significant therapeutic problems in human medicine (Aarestrup et al., 2003).
In Salmonella, resistance to cephalosporins is largely due to production of extended-spectrum β-lactamases (ESBLs) or AmpC-type enzymes. Among them, CTX-M β-lactamases have emerged worldwide over the last decade and have progressively replaced classical TEM and SHV-type ESBLs. Currently, CTX-M β-lactamases are the most prevalent type of ESBL in most areas of the world (Rossolini et al., 2008) including Korea. Furthermore, plasmid-mediated quinolone resistance (PMQR) has emerged in Salmonella and in other Enterobacteriaceae, and the prevalence of PMQR is increasing worldwide (Strahilevitz et al., 2009). Todate, three different transferable PMQR mechanisms have been described: Qnr proteins (QnrA, QnrB, QnrC, QnrD, and QnrS), AAC(6′)-Ib-cr (a variant of aminoglycoside acetyltransferase), and quinolone specific QepA-type or multi-drug resistance OqxAB-type efflux pumps (Strahilevitz et al., 2009).
Despite the importance of Salmonella infections in humans and swine and the role of pigs in the spread of S. 1,4,[5],12:i:- isolates, data on the prevalence and characteristics of various Salmonella serovars in pigs from organic farms in Korea have been lacking. Therefore, in the present study, the prevalence of Salmonella spp. including S. 1,4,[5],12:i:- and their antimicrobial susceptibilities in pigs from conventional and organic farms were compared. The Salmonella isolates showing resistance to ceftiofur or nalidixic acid were further characterized using phenotypic and molecular methods. In addition, the genetic diversity of S. Typhimurium and S. 1,4,[5],12:i:- strains was determined by multilocus variable number of tandem repeats analysis (MLVA).
Section snippets
Salmonella strains
A total of 1965 fecal samples from pigs from 44 farms nationwide were investigated during 2012–2013 in Korea. Three to four farms per province were randomly selected from all nine provinces of Korea. Altogether, 30 conventional farms and 14 organic farms were studied. Conventional farms were characterized by unrestricted use of antimicrobials for prevention and treatment of diseased pigs at the farm level. Whereas, the organic farms used organic feed and used antimicrobials only on prescription
Prevalence of Salmonella
A total of 100 Salmonella were isolated from 1965 pig fecal samples in this study: 47 isolates from 1324 pigs (3.5%) from conventional farms and 53 isolates from 641 pigs (8.3%) from organic farms (Table 1). Salmonella was detected in 53.3% and 78.6% of the conventional and organic farms investigated, respectively. Overall, the highest prevalence of Salmonella was observed among weaning group pigs followed by growers, finishers, and piglets. Altogether, seven different Salmonella serovars were
Discussion
In this study, the prevalence of Salmonella was higher among the pigs from organic farms compared to conventional farms with regard to both sample-wise (8.3% vs 3.5%) and farm-wise (78.6% vs 53.3%) distribution. While serovars Panama, Derby, Virchow, and Enteritidis were observed only in pigs from organic farms, the prevalence of Typhimurium was significantly higher in pigs from conventional than those from organic farms. This discrepancy may be owing to the difference in farm management
Conflict of interest
Nothing to declare.
Acknowledgement
This work was supported by a grant from the Animal and Plant Quarantine Agency, Ministry of Agriculture, Food, and Rural Affairs, Republic of Korea.
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