CTX-M-27 Producing Salmonella enterica Serotypes Typhimurium and Indiana Are Prevalent among Food-Producing Animals in China

Abstract

Salmonella spp. is one of the most important food-borne pathogens causing digestive tract and invasive infections in both humans and animals. Extended-spectrum β-lactamases (ESBLs) especially the CTX-M-type ESBLs are increasingly being reported worldwide and in China. These studies seldom focused on Salmonella isolates from food-producing animals. The aim of this study was to characterize the antimicrobial resistance profiles, serotypes and ESBLs and in particular, CTX-M producing Salmonella isolates from chickens and pigs in China. Salmonella isolates were identified by API20E system and polymerase chain reaction (PCR) assay; serotypes were determined using slide agglutination with hyperimmune sera; antimicrobial susceptibility was tested using the ager dilution method; the prevalence of ESBLs and PMQR genes were screened by PCR; CTX-M-producing isolates were further characterized by conjugation along with genetic relatedness and plasmid replicon type. In total, 159 Salmonella strains were identified, among which 95 strains were Salmonella enterica serovar Typhimurium, 63 strains were S. enterica serovar Indiana, and 1 strain was S. enterica serovar Enteritidis. All of these isolates presented multi-drug resistant phenotypes. Forty-five isolates carried blaCTX-M genes, the most common subtype was CTX-M-27(34), followed by CTX-M-65(7) and CTX-M-14(4). Most blaCTX-M genes were transmitted by non-typeable or IncN/IncFIB/IncP/IncA/C/IncHI2 plasmids with sizes ranging from 80 to 280 kb. In particular, all the 14 non-typeable plasmids were carrying blaCTX-M-27 gene and had a similar size. PFGE profiles indicated that CTX-M-positive isolates were clonally related among the same serotype, whilst the isolates of different serotypes were genetically divergent. This suggested that both clonal spread of resistant strains and horizontal transmission of the resistance plasmids contributed to the dissemination of blaCTX-M-9G-positive Salmonella isolates. The presence and spread of CTX-M, especially the CTX-M-27 in S. enterica serovars Typhimurium and Indiana from food-producing animals poses a potential threat for public health. Control strategies to limit the dissemination of these strains through the food chain are necessary.

Characterization of a P1-like bacteriophage carrying CTX-M-27 in Salmonella spp. resistant to third generation cephalosporins isolated from pork in China

“…CTX-M-65, CTX-M-55 and CTX-M-14 used to be the most prevalent ESBLs detected in E. coli from food-producing animals, but CTX-M-27 was only sporadically detected in E. coli 27. There is little literature reporting the prevalence of CTX-M-27 in Salmonella strains in China until recent times when a study detected bla CTX-M-27 as the most dominant ESBL genes in Salmonella Typhimirium and Indiana isolated from pigs and Chicken28. The high prevalence of bla CTX-M-27 in Salmonella from pork meat should be a cause of concern which will be a potential threat to public health.…”

Comparative Analysis of Extended-Spectrum-β-Lactamase CTX-M-65-Producing Salmonella enterica Serovar Infantis Isolates from Humans, Food Animals, and Retail Chickens in the United States

“…We examined select bla CTX-M-65 -positive isolates with PFGE pattern JFXX01.0787. The bla CTX-M-65 gene has been well described in E. coli, Klebsiella pneumoniae, Salmonella enterica serovar Indiana, and Salmonella enterica serovar Typhimurium isolated from humans and healthy animals in China and Korea (12)(13)(14)(15)(16). It has also been found in commensal bacteria in pediatric populations in Bolivia (17) and produce imported to Switzerland from the Dominican Republic and Vietnam (18).…”

Clonal spread of mcr-1 in PMQR-carrying ST34 Salmonella isolates from animals in China

“…Unpublished data from the China CDC surveillance system indicated that the carriage rate of human salmonellosis is 549 per 100,000 people in 2013, which is higher than that in the USA in 2012 (16.4 per 100,000)3. Salmonella enterica , especially non-typhoidal Salmonella (NTS), is a leading cause of food-borne disease of humans and livestock worldwide34. Various animal species, such as poultry, pigs, cattle, and reptiles, are reservoirs for NTS.…”

“…By contrast, 30 millions of infections every year in China, approximately 75% of the food-borne diseases, are attributed to this bacterium2. Unpublished data from the China CDC surveillance system indicated that the carriage rate of human salmonellosis is 549 per 100,000 people in 2013, which is higher than that in the USA in 2012 (16.4 per 100,000)3. Salmonella enterica , especially non-typhoidal Salmonella (NTS), is a leading cause of food-borne disease of humans and livestock worldwide34.…”