Characterization of E. coli Isolates Producing Extended Spectrum Beta-Lactamase SHV-Variants from the Food Chain in Germany

Abstract

Resistance of bacteria to 3rd generation cephalosporins mediated by beta-lactamases (ESBL, pAmpC) is a public health concern. In this study, 1517 phenotypically cephalosporin-resistant E. coli were screened for the presence of blaSHV genes. Respective genes were detected in 161 isolates. Majority (91%) were obtained from poultry production and meat. The SHV-12 beta-lactamase was the predominant variant (n = 155), while the remaining isolates exhibited SHV-2 (n = 4) or SHV-2a (n = 2). A subset of the isolates (n = 51) was further characterized by PCR, PFGE, or whole-genome sequencing and bioinformatics analysis. The SHV-12-producing isolates showed low phylogenetic relationships, and dissemination of the blaSHV-12 genes seemed to be mainly driven by horizontal gene transfer. In most of the isolates, blaSHV-12 was located on transferable IncX3 (~43 kb) or IncI1 (~100 kb) plasmids. On IncX3, blaSHV-12 was part of a Tn6 composite transposon located next to a Tn3 transposon, which harbored the fluoroquinolone resistance gene qnrS1. On IncI1 plasmids, blaSHV-12 was located on an incomplete class 1 integron as part of a Tn21 transposon. In conclusion, SHV-12 is widely distributed in German poultry production and spreads via horizontal gene transfer. Consumers are at risk by handling raw poultry meat and should take care in appropriate kitchen hygiene.

Antimicrobial Resistance in Escherichia coli from the Broiler Farm Environment, with Detection of SHV-12-Producing Isolates

“…The F, FIB, K, and HI1 plasmids were frequently detected among the SHV-12-producing isolates in poultry in other studies [38,39]. Moreover, IncI1 plasmids are also found associated with bla SHV-12 in the human and animal environment [17,40] and even in food isolates [10,30], where IncK and IncX3 replicons were also detected, in lower proportions. The IncF, IncF1B, IncK, IncHI1, and IncI1 replicon types have also been detected among our ESBL-producing isolates.…”

“…In the present study, all the 23 ESBL producers carried the gene encoding the SHV-12 enzyme. This ESBL is the most widespread variant in European countries in the poultry sector [9,16,29,30] and has also been frequently detected in Spanish hospitals [14]. Never-theless, other ESBL variants (TEM-52, CTX-M-14, CTX-M-1, CTX-M-15, CTX-M-32, and CTX-M-9, among others) and pAmpC enzymes (CMY-2) have also been reported in the poultry sector, including slaughterhouse wastewater [9,15,[31][32][33][34].…”

Characterization of Extended Spectrum Cephalosporin-Resistant Escherichia coli Strains Isolated from Raw Poultry Carcasses in Catering Services in Northern Greece

“…Resistance to extended-spectrum cephalosporins in Enterobacterales is typically conferred by ESBL, AmpC, or carbapenemase enzymes [ 24 , 28 , 29 ]. ESBL-producing Enterobacterales have historically been more prevalent in Europe, whereas AmpC enzymes are also a serious concern, especially in southern America [ 23 , 25 , 30 ]. Both seem to have been detected in virtually every stage of chicken or turkey meat production (from farm to slaughterhouses and in the final retail), much like the undoubtedly most common Enterobacterales species, i.e., E. coli [ 21 , 22 ], with chicken and turkeys considered as a reservoir of extended-spectrum cephalosporin-resistant Enterobacteriaceae [ 14 , 31 ].…”

“…This finding was barely surprising as extended-spectrum cephalosporin-resistant E. coli isolates have been regularly known to express MDR patterns [ 20 , 23 , 28 ]. Díaz-Jiménez et al [ 24 ] examined 100 chicken and turkey breast samples in 2016–2017 and found that 136 out of the 137 E. coli isolates were MDR, whereas Egervärn et al [ 14 ], Moawad et al [ 29 ], Nüesch-Inderbinen et al [ 26 ], and Irrgang et al [ 30 ] also reported very high MDR rates in extended-spectrum cephalosporin-resistant E. coli isolated from chicken and turkey samples, as well as from poultry-containing raw meat-based diets. Particularly, resistance to fluoroquinolones, aminoglycosides, and trimethoprim-sulfonamide combinations is very frequent in MDR ESBL/AmpC-producing isolates and raises profound concerns about its implication in the treatment of severe infections in both animals and humans [ 14 , 34 , 35 ].…”

Molecular interaction of a putative inhibitor with bacterial SHV, an enzyme associated with antibiotic resistance

“…In the past, the SHV bacterial enzyme has been implicated in some notable outbreaks, like in Mexico [ 12 ]. Recent studies have also drawn attention to SHV mediated bacterial infections [ 13 ]. A 2021 study reported a high rate of multidrug resistance in Pseudomonas aeruginosa isolates, and bacterial SHV was among the significant resistance enzymes [ 14 ].…”