Characterization and whole genome sequencing of closely related multidrug-resistant Salmonella enterica serovar Heidelberg isolates from imported poultry meat in the Netherlands
Abstract:Multidrug-resistant
Salmonella enterica
serovar Heidelberg isolates are frequently recovered in the Netherlands from poultry meat imported from South America. Our aim was to retrospectively assess the characteristics of the antimicrobial determinants, gene content and the clonal relatedness of 122 unique
S
. Heidelberg isolates from chicken meat from Brazil (n = 119) and Argentina (n = 3) that were imported between 2010 and 2015. These isolates were subjected to an… Show more
“…The four identified resistomes (Table 1) revealed a high level of resistance to amoxicillin, ampicillin and/or ceftriaxone. Although the bla CTX−M gene is reported with a higher incidence of Salmonella in poultry products (Moura et al, 2018;Perin et al, 2020), our study shows that its frequency was low (2/20-10%) and corroborates with recent studies carried out with samples Brazilian samples (van den Berg et al, 2019;Souza et al, 2020). Gram-negative ESBL-producing and hyper-producing AmpC bacteria have also stood out for their resistance to carbapenems, such as meropenem, identified in 20% (4/20) of our strains, when associated with other mechanisms, such as hyper expressed efflux systems (Andrade and Darini, 2017).…”
“…The presence of the bla CMY−2 gene is consistent with this phenotype, due to the overproduction of AmpC induced by the presence of cephalosporin and cephamycin that exhibit resistance to extended-spectrum cephalosporins, such as ceftriaxone, and to cefoxitin (identified in four of the 20 strains -data not shown) (De Angelis et al, 2020). The high prevalence of SH AmpC strains highlights the endemic occurrence of β-lactam resistance in North and South America (Edirmanasinghe et al, 2017;Monte et al, 2019;van den Berg et al, 2019;Souza et al, 2020).…”
The aim of the study was to evaluate the genotypic and phenotypic characteristics of 20 strains of S. Heidelberg (SH) isolated from broilers produced in southern Brazil. The similarity and presence of genetic determinants linked to virulence, antimicrobial resistance, biofilm formation, and in silico-predicted metabolic interactions revealed this serovar as a threat to public health. The presence of the ompC, invA, sodC, avrA, lpfA, and agfA genes was detected in 100% of the strains and the luxS gene in 70% of them. None of the strains carries the blaSHV, mcr-1, qnrA, qnrB, and qnrS genes. All strains showed a multidrug-resistant profile to at least three non-β-lactam drugs, which include colistin, sulfamethoxazole, and tetracycline. Resistance to penicillin, ceftriaxone (90%), meropenem (25%), and cefoxitin (25%) were associated with the presence of blaCTX–M and blaCMY–2 genes. Biofilm formation reached a mature stage at 25 and 37°C, especially with chicken juice (CJ) addition. The sodium hypochlorite 1% was the least efficient in controlling the sessile cells. Genomic analysis of two strains identified more than 100 virulence genes and the presence of resistance to 24 classes of antibiotics correlated to phenotypic tests. Protein-protein interaction (PPI) prediction shows two metabolic pathways correlation with biofilm formation. Virulence, resistance, and biofilm determinants must be constant monitoring in SH, due to the possibility of occurring infections extremely difficult to cure and due risk of the maintenance of the bacterium in production environments.
“…The four identified resistomes (Table 1) revealed a high level of resistance to amoxicillin, ampicillin and/or ceftriaxone. Although the bla CTX−M gene is reported with a higher incidence of Salmonella in poultry products (Moura et al, 2018;Perin et al, 2020), our study shows that its frequency was low (2/20-10%) and corroborates with recent studies carried out with samples Brazilian samples (van den Berg et al, 2019;Souza et al, 2020). Gram-negative ESBL-producing and hyper-producing AmpC bacteria have also stood out for their resistance to carbapenems, such as meropenem, identified in 20% (4/20) of our strains, when associated with other mechanisms, such as hyper expressed efflux systems (Andrade and Darini, 2017).…”
“…The presence of the bla CMY−2 gene is consistent with this phenotype, due to the overproduction of AmpC induced by the presence of cephalosporin and cephamycin that exhibit resistance to extended-spectrum cephalosporins, such as ceftriaxone, and to cefoxitin (identified in four of the 20 strains -data not shown) (De Angelis et al, 2020). The high prevalence of SH AmpC strains highlights the endemic occurrence of β-lactam resistance in North and South America (Edirmanasinghe et al, 2017;Monte et al, 2019;van den Berg et al, 2019;Souza et al, 2020).…”
The aim of the study was to evaluate the genotypic and phenotypic characteristics of 20 strains of S. Heidelberg (SH) isolated from broilers produced in southern Brazil. The similarity and presence of genetic determinants linked to virulence, antimicrobial resistance, biofilm formation, and in silico-predicted metabolic interactions revealed this serovar as a threat to public health. The presence of the ompC, invA, sodC, avrA, lpfA, and agfA genes was detected in 100% of the strains and the luxS gene in 70% of them. None of the strains carries the blaSHV, mcr-1, qnrA, qnrB, and qnrS genes. All strains showed a multidrug-resistant profile to at least three non-β-lactam drugs, which include colistin, sulfamethoxazole, and tetracycline. Resistance to penicillin, ceftriaxone (90%), meropenem (25%), and cefoxitin (25%) were associated with the presence of blaCTX–M and blaCMY–2 genes. Biofilm formation reached a mature stage at 25 and 37°C, especially with chicken juice (CJ) addition. The sodium hypochlorite 1% was the least efficient in controlling the sessile cells. Genomic analysis of two strains identified more than 100 virulence genes and the presence of resistance to 24 classes of antibiotics correlated to phenotypic tests. Protein-protein interaction (PPI) prediction shows two metabolic pathways correlation with biofilm formation. Virulence, resistance, and biofilm determinants must be constant monitoring in SH, due to the possibility of occurring infections extremely difficult to cure and due risk of the maintenance of the bacterium in production environments.
“…Similar results have been reported in S. Heidelberg isolates from humans (Cejas et al, 2014) and poultry (Castellanos et al, 2018;Souza et al, 2020). Moreover, the isolates show high prevalence of resistance to nalidixic acid and ciprofloxacin (FQ), a fact also observed by other authors in isolates from poultry (Casas et al, 2016;van den Berg et al, 2019). Similarly, an increasing number of isolates have been characterized as MDR to many antimicrobials by several authors (Giuriatti et al, 2017).…”
Non-typhoidal Salmonella (NTS) are one of the main causes of foodborne diseases worldwide, historically associated with the consumption of eggs and chicken meat (Campos et al., 2019;Jajere, 2019). The epidemiology of NTS has been the subject of numerous studies. (Wajid et al., 2019). The results of these studies have shown that S. Typhimurium and S. Enteritidis have historically
“…This combination of replicons, together with an IncN replicon, has also been found in E. coli. This plasmid carried an mcr-gene encoding colistin resistance [41]. A plasmid with exactly the same sequences was found in S. Brandenburg and S. Ohio from two different farms, indicating its spread amongst Salmonella in Suriname.…”
Salmonella is one of the most important food borne zoonotic pathogens. While mainly associated with poultry, it has also been associated with pigs. Compared to the high-income countries, there is much less known on the prevalence of Salmonella in low- and middle-income countries, especially in the Caribbean area. Therefore, we investigated the prevalence of Salmonella in pigs and pig meat in Suriname. A total of 53 farms and 53 meat samples were included, and Salmonella was isolated using standard protocols. Strains were subjected to whole genome sequencing. No Salmonella was found on pig meat. Five farms were found to be positive for Salmonella, and a total of eight different strains were obtained. Serotypes were S. Anatum (n = 1), S. Ohio (n = 2), a monophasic variant of S. Typhimurium (n = 3), one S. Brandenburg, and one S. Javaniana. The monophasic variant of S. Typhimurium belonged to the ST34 pandemic clone, and the three strains were very similar. A few resistance genes, located on mobile genetic elements, were found. Several plasmids were detected, though only one was carrying resistance genes. This is the first study on the prevalence of Salmonella in pigs in the Caribbean and that used whole genome sequencing for characterization. The strains were rather susceptible. Local comparison of similar serotypes showed a mainly clonal spread of certain serotypes.
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