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Title: Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from food animals, retail meat, and humans in the United States 2009

Author
item FOLSTER, JASON - Centers For Disease Control And Prevention (CDC) - United States
item PECIC, GARY - Centers For Disease Control And Prevention (CDC) - United States
item SINGH, ANDREA - Food And Drug Administration(FDA)
item DUVAL, BREA - Former ARS Employee
item RICKERT, REGAN - Centers For Disease Control And Prevention (CDC) - United States
item AYERS, SHARI - Food And Drug Administration(FDA)
item ABBOTT, JASON - Food And Drug Administration(FDA)
item MCGLINCHEY, BETH - Centers For Disease Control And Prevention (CDC) - United States
item BAUER-TURPIN, JENNIFER - Former ARS Employee
item Haro, Jovita
item HISE, K - Food And Drug Administration(FDA)
item ZHAO, SHAOHUA - Food And Drug Administration(FDA)
item Cray, Paula
item WHICHARD, JEAN - Centers For Disease Control And Prevention (CDC) - United States
item MCDERMOTT, PATRICK - Food And Drug Administration(FDA)

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/28/2012
Publication Date: 7/2/2012
Citation: Folster, J.P., Pecic, G., Singh, A., Duval, B., Rickert, R., Ayers, S., Abbott, J., Mcglinchey, B., Bauer-Turpin, J., Haro, J.H., Hise, K., Zhao, S., Cray, P.J., Whichard, J., Mcdermott, P.F. 2012. Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from food animals, retail meat, and humans in the United States 2009. Foodborne Pathogens and Disease. 9(7):638-645.

Interpretive Summary: Salmonella is an important food borne pathogens which can be transferred from contaminated foods to human resulting in gastroenteritis. Of particular concern is the development of resistance to antimicrobials important in both human and veterinary medicine. Typically, treatment of uncomplicated gastrointestinal illness resulting from Salmonella is not needed as the infection resolves within five to seven days. However, if the infection warrants treatment, particularly in the young, the elderly, and the immunocompromised, the presence of resistant Salmonella may compromise treatment. In order to track the development of resistance among Salmonella, isolates from food at retail, ill humans, and animals at slaughter are tested for resistance to a panel of antimicrobials as part of the National Antimicrobial Resistance Monitoring System (NARMS). Isolates may be further characterized using pulsed field gel electrophoresis which assets in determining if strains originating from food at retail, ill humans, and animals at slaughter are related to each other. Surveillance conducted by NARMS has shown a recent increase in extended-spectrum cephalosporin (ESC) resistance among Salmonella Heidelberg isolated from food animals at slaughter, retail meat, and ill humans. ESC resistance among Salmonella in the United States is usually mediated by a plasmid encoded gene identified as blaCMY. A plasmids is a small piece of DNA which can move from bacterial cell to bacterial cell conferring resistance if resistance genes are encoded on the plasmid. In 2009, we identified 47 ESC resistant blaCMY-positive Heidelberg isolates from humans (n=18), food animals at slaughter (n=16), and retail meats (n=13). Almost 90% (26/29) of the animal and meat isolates were isolated from chicken carcasses at slaughter or retail chicken meat. We screened NARMS isolates for the presence of the blaCMY gene, determined whether the gene was plasmid-encoded, examined pulsed-field gel electrophoresis patterns to assess the genetic diversities of the isolates, and categorized the blaCMY plasmids two different methods. All 47 blaCMY genes were found to be plasmid encoded. One plasmid typing method demonstrated that 41 plasmids belonged to a group called IncI1 plasmids, 40 of which only conferred blaCMY associated resistance. Six were of the plasmid group IncA/C that carried additional resistance genes. Plasmid multi-locus sequence typing (pMLST) of the IncI1-blaCMY plasmids showed that 27 (65.8%) were sequence type (ST) 12, the most common ST among blaCMY-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 blaCMY on IncI1 and IncA/C plasmids in a variety of genetic backgrounds, and likely not the result of clonal expansion. This data is critical for public and veterinary health officials and regulatory agencies as they investigate food borne illness outbreaks. This data is also critical for scientists studying the development of antimicrobial resistance and in the development of mitigation strategies.

Technical Abstract: 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, is commonly used in both adults and children. Surveillance conducted by the National Antimicrobial Resistance Monitoring System (NARMS) has shown a recent increase in extended-spectrum cephalosporin (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 blaCMY '-lactamase. In 2009, we identified 47 ESC resistant blaCMY-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 blaCMY, determined whether the gene was plasmid-encoded, examined pulsed-field gel electrophoresis patterns to assess the genetic diversities of the isolates, and categorized the blaCMY plasmids by plasmid incompatibility groups and plasmid multi-locus sequence typing. All 47 blaCMY genes were found to be plasmid encoded. Incompatibility/replicon typing demonstrated that 41 were IncI1 plasmids, 40 of which only conferred blaCMY associated resistance. Six were IncA/C plasmids that carried additional resistance genes. Plasmid multi-locus sequence typing (pMLST) of the IncI1-blaCMY plasmids showed that 27 (65.8%) were sequence type (ST) 12, the most common ST among blaCMY-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 blaCMY on IncI1 and IncA/C plasmids in a variety of genetic backgrounds, and likely not the result of clonal expansion.