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Characterization of Salmonella enterica serovars recovered from meat products legally and illegally imported into the EU reveals the presence of multiresistant and AmpC-producing isolates.

ABSTRACT: Background:Food products of animal origin brought into the EU from third countries, both legally and illegally, can harbor foodborne pathogens such as Salmonella enterica. In this study, we examined five S. enterica isolates recovered either from legally imported chicken meat (n?=?3) or from meat products confiscated from air travel passengers arriving in Germany (n?=?2). The isolates were serotyped and further characterized by antimicrobial susceptibility testing, PCR-detection and sequencing of genes associated with antimicrobial resistances, and macrorestriction analysis. Transferability of resistance to third-generation cephalosporins was assessed by conjugation experiments and the plasmids tested for their incompatibility groups. Results:The three isolates from legal imports were identified as S. Heidelberg or as non-flagellated. All three isolates were identified as AmpC producers carrying bla CMY-2 and as non-susceptible to ciprofloxacin. They were additionally resistant to tetracycline and sulfamethoxazole. The bla CMY-2-carrying plasmids were transferable by conjugation and belonged to incompatibility groups IncI1 or IncA/C. The two isolates from illegally imported meat belonged to the serovars Infantis or Weltevreden. The former was phenotypically resistant to five classes of antimicrobial agents while the S. Weltevreden isolate was fully susceptible to all agents tested. Conclusion:The results of this study demonstrate that meat products imported from third countries, both legally and illegally, can harbor multiresistant Salmonella enterica. Consequently, these imports could constitute a source for the dissemination of antimicrobial resistant isolates, including those resistant to third-generation cephalosporins and fluoroquinolones.

PROVIDER: S-EPMC6151051 | BioStudies |

REPOSITORIES: biostudies

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Project description:Salmonella enterica is one of the most common causes of foodborne illness in the United States. Although salmonellosis is usually self-limiting, severe infections typically require antimicrobial treatment, and ceftriaxone, an extended-spectrum cephalosporin (ESC), is commonly used in both adults and children. Surveillance conducted by the National Antimicrobial Resistance Monitoring System (NARMS) has shown a recent increase in ESC resistance among Salmonella Heidelberg isolated from food animals at slaughter, retail meat, and humans. ESC resistance among Salmonella in the United States is usually mediated by a plasmid-encoded bla(CMY) ?-lactamase. In 2009, we identified 47 ESC-resistant bla(CMY)-positive Heidelberg isolates from humans (n=18), food animals at slaughter (n=16), and retail meats (n=13) associated with a spike in the prevalence of this serovar. Almost 90% (26/29) of the animal and meat isolates were isolated from chicken carcasses or retail chicken meat. We screened NARMS isolates for the presence of bla(CMY), determined whether the gene was plasmid-encoded, examined pulsed-field gel electrophoresis patterns to assess the genetic diversities of the isolates, and categorized the bla(CMY) plasmids by plasmid incompatibility groups and plasmid multi-locus sequence typing (pMLST). All 47 bla(CMY) genes were found to be plasmid encoded. Incompatibility/replicon typing demonstrated that 41 were IncI1 plasmids, 40 of which only conferred bla(CMY)-associated resistance. Six were IncA/C plasmids that carried additional resistance genes. pMLST of the IncI1-bla(CMY) plasmids showed that 27 (65.8%) were sequence type (ST) 12, the most common ST among bla(CMY)-IncI1 plasmids from Heidelberg isolated from humans. Ten plasmids had a new ST profile, ST66, a type very similar to ST12. This work showed that the 2009 increase in ESC resistance among Salmonella Heidelberg was caused mainly by the dissemination of bla(CMY) on IncI1 and IncA/C plasmids in a variety of genetic backgrounds, and is likely not the result of clonal expansion.

Project description:Salmonella remains the leading cause of reported bacterial foodborne disease in China. Meat products are recognized as one of the major sources of human salmonellosis; however, there is a lack of comprehensive, quantitative data concerning Salmonella contamination of these foods. Therefore, the objectives of this study were to investigate the prevalence, bacterial load, and antimicrobial resistance profiles of various Salmonella serovars in retail meat across the whole of China. Between July 2011 and June 2016, a total of 807 retail meat samples were collected, covering most provincial capitals in China. Overall, 159 (19.7%) samples tested positive for Salmonella. The highest contamination rate occurred in pork (37.3%, n = 287), followed by beef (16.1%, n = 161), mutton (10.9%, n = 92), dumplings (6.6%, n = 212), and smoked pork (3.6%, n = 55). Most probable number (MPN) analysis revealed that contamination was mainly in the range of 0.3-10 MPN/g among those samples testing positive using this method (n = 83), with eight samples exceeding 110 MPN/g. Among the 456 Salmonella enterica subsp. enterica isolates obtained in this study, 29 serovars and 33 multilocus sequence typing patterns were identified, with S. Derby, S. Typhimurium, S. London, S. Rissen, S. 1,4,[5],12:i:-, S. Weltevreden, and S. Enteritidis being the most prevalent. Among the 218 non-duplicate isolates, 181 (83.0%) were resistant to at least one class of antimicrobials and 128 (58.7%) were resistant to at least three classes. High rates of resistance were observed for tetracycline (65.6%), ampicillin (45.4%), trimethoprim-sulfamethoxazole (40.8%), streptomycin (40.4%), and nalidixic acid (35.8%), with the seven most prevalent serovars, except S. Weltevreden, showing higher rates of resistance and multidrug resistance compared with the less dominant serovars. Of note, all S. Indiana isolates exhibited resistance to extended-spectrum cephalosporins (including ceftriaxone and cefepime), ciprofloxacin, and multiple other classes of antibiotics. Further, two S. 1,4,[5],12:i:- isolates showed resistance to imipenem. This study provides systematic and comprehensive data on the prevalence and antimicrobial resistance profiles of various Salmonella serovars isolated from meat products in China, indicating their potential risk to public health.

Project description:Ampicillin-resistant (Amp(r)) Salmonella enterica isolates (n = 344) representing 32 serotypes isolated from retail meats from 2002 to 2006 were tested for susceptibility to 21 other antimicrobial agents and screened for the presence of five beta-lactamase gene families (bla(CMY), bla(TEM), bla(SHV), bla(OXA), and bla(CTX-M)) and class 1 integrons. Among the Amp(r) isolates, 66.9% were resistant to five or more antimicrobials and 4.9% were resistant to 10 or more antimicrobials. Coresistance to other beta-lactams was noted for amoxicillin-clavulanic acid (55.5%), ceftiofur (50%), cefoxitin (50%), and ceftazidime (24.7%), whereas less than 5% of isolates were resistant to piperacillin-tazobactam (4.9%), cefotaxime (3.5%), ceftriaxone (2%), and aztreonam (1.2%). All isolates were susceptible to cefepime, imipenem, and cefquinome. No Salmonella producing extended-spectrum beta-lactamases was found in this study. Approximately 7% of the isolates displayed a typical multidrug-resistant (MDR)-AmpC phenotype, with resistance to ampicillin, chloramphenicol, streptomycin, sulfonamide, tetracycline, plus resistance to amoxicillin-clavulanic acid, cefoxitin, and ceftiofur and with decreased susceptibility to ceftriaxone (MIC > or = 4 microg/ml). Pulsed-field gel electrophoresis results showed that several MDR clones were geographically dispersed in different types of meats throughout the five sampling years. Additionally, 50% of the isolates contained bla(CMY), 47% carried bla(TEM-1), and 2.6% carried both genes. Only 15% of the isolates harbored class I integrons carrying various combinations of aadA, aadB, and dfrA gene cassettes. The bla(CMY), bla(TEM), and class 1 integrons were transferable through conjugation and/or transformation. Our findings indicate that a varied spectrum of coresistance traits is present in Amp(r) Salmonella strains in the meat supply of the United States, with a continued predominance of bla(CMY) and bla(TEM) genes in beta-lactam-resistant isolates.

Project description:Colistin is a last-resort antibiotic in fighting severe infections caused by multidrug resistant Gram negative pathogens in hospitals. Zoonotic bacteria acquire colistin resistance in animal reservoirs and mediate its spread along the food chain. This is the case of non-typhoid serovars of Salmonella enterica. Colistin-resistant S. enterica in foods represents a threat to human health. Here, we assessed the prevalence of colistin-resistance in food-borne isolates of S. enterica (2014-2019; Asturias, Spain), and established the genetic basis and transferability of this resistance. Five out of 231 isolates tested (2.2%) were resistant to colistin. Four of them, belonging to the European monophasic ST34 clone of S. Typhimurium, were characterized in the present study. They were collected from pork or pork and beef meat-derived products, either in 2015 (three isolates) or 2019 (one isolate). Molecular typing with XbaI-PFGE and plasmid profiling revealed distinct patterns for each isolate, even though two of the 2015 isolates derived from the same sample. The MICs of colistin ranged from 8 to 16 mg/L. All isolates carried the mcr-1.1 gene located on conjugative plasmids of the incompatibility groups IncX4 (2015 isolates) or IncHI2 (2019 isolate). Apart from colistin resistance, the four isolates carried chromosomal genes conferring resistance to ampicillin, streptomycin, sulfonamides and tetracycline [bla TEM-1, strA-strB, sul2, and tet(B)] and heavy metals, including copper and silver (silESRCFBAGP and pcoGE1ABCDRSE2), arsenic (arsRSD2A2BCA1D1) ± mercury (merEDACPTR), which are characteristically associated with the European ST34 monophasic clone. The 2019 isolate was also resistant to other antibiotics, comprising third generation cephalosporins and cephamycins. The latter phenotype was conferred by the bla CMY-2 gene located on an IncI1-I(α)-ST2 plasmid. Results in the present study identified meat-derived products as a reservoir of a highly successful clone harboring transferable plasmids which confer resistance to colistin and other clinically important antibiotics. An important reduction in the number of food-borne S. enterica detected during the period of the study, together with the low frequency of colistin resistance, underlines the success of One Health initiatives, such as those implemented at the UE, to control zoonotic bacteria along the food chain and to halt the spread of antimicrobial resistance.

Project description:The use of antibiotics in food animals is of public health concern, because resistant zoonotic pathogens can be transmitted to humans. Furthermore, global trade with food may rapidly spread multi-resistant pathogens between countries and even continents. The purpose of the study was to investigate whether imported chicken meat and meat from locally reared chicken are potential sources for human exposure to multi resistant Escherichia coli isolates. 188 samples from imported and locally produced chicken meat were sampled and analyzed. 153 bacteria isolates were successfully cultured and identified as E. coli using MALDI-ToF. Of these 109 isolates were from meat whereas the remaining 44 were isolated from the cloaca of locally reared live chickens. Antimicrobial susceptibility test was done on the identified E. coli isolates. Additionally, beta-lactamases production (ESBL and/or AmpC) were phenotypically confirmed on all isolates showing resistance to cefpodoxime. Beta-lactamase producing (BLP) E. coli meat isolates were further genotyped. Antimicrobial resistance to four antibiotic markers with highest resistance was detected more frequently in isolates from local chickens compared to imported chickens (tetracycline 88.9% vs. 57.5%, sulphonamide 75.0% vs. 46.6%, ampicillin 69.4% vs. 61.6% and trimethoprim 66.7% vs. 38.4%). Beta-lactamase production was found in 29 E. coli meat isolates, with 56.9% of them being multiple drug resistant (? 3). The predominant phylogroup identified was B1 followed by A and D, with similar distribution among the isolates from meat of locally reared chickens and imported chickens. Beta-lactamase producing genotype blaCTX-M-15 (50%; 10/20) was the most frequently drug resistant gene detected. More BLP E. coli isolates were found in imported chicken meat compared to locally reared chickens, demonstrating that these isolates may be spreading through food trade. In conclusion, both imported and locally produced chicken meats are potential sources for human exposure to BLP E. coli.

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Characterization of Salmonella enterica serovars recovered from meat products legally and illegally imported into the EU reveals the presence of multiresistant and AmpC-producing isolates.

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