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United States Department of Agriculture

Agricultural Research Service

Research Project: MONITORING OF ANTIMICROBIAL RESISTANCE IN FOOD ANIMAL PRODUCTION

Location: Bacterial Epidemiology and Antimicrobial Resistance

Title: Characterization of multidrug-resistant Salmonella enterica serovar Heidelberg from a ground turkey-associated outbreak in the United States in 2011

Authors
item Folster, Jason -
item Pecic, Gary -
item Rickert, Regan -
item Taylor, Jason -
item Zhao, Shaohua -
item Cray, Paula
item Whichard, Jean -
item Mcdermott, Patrick -

Submitted to: Antimicrobial Agents and Chemotherapy
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 19, 2012
Publication Date: June 1, 2012
Citation: Folster, J.P., Pecic, G., Rickert, R., Taylor, J., Zhao, S., Cray, P.J., Whichard, J., Mcdermott, P. 2012. Characterization of multidrug-resistant Salmonella enterica serovar Heidelberg from a ground turkey-associated outbreak in the United States in 2011. Antimicrobial Agents and Chemotherapy. 56(6):3465-3466.

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 gel electrophoresis which assets in determining if strains originating from food at retail, ill humans, and animals at slaughter are related to each other. In March 2011 a multi-state outbreak of Salmonella serotype Heidelberg infections in humans was investigated. Using Pulsed field gel electrophoresis, Salmonella Heidelberg isolates closely matched Salmonella Heidelberg isolates originating from ground turkey product at retail. Antimicrobial resistance patterns also matched between these isolates. The antimicrobial resistance genes were located on a small piece of DNA called a plasmid which can move from bacterial cell to bacterial cells conferring resistance. These Salmonella isolates from humans and ground turkey at retail also closely matched isolates originating from ground turkey isolates at slaughter. NARMS has identified several isolates from past routine surveillance of isolates from ground turkey at retail, ground turkey at slaughter, and human clinical samples that match the observed characteristics of the isolates from the March 2011 outbreak. 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: In March 2011, a multi-state outbreak of Salmonella enterica ser. Heidelberg infections was investigated. Pulsed-field gel electrophoresis (PFGE) analysis of isolates from suspected cases and an epidemiologic investigation identified 136 case patients from 34 states from February to September. Two closely related XbaI PFGE patterns were identified among the outbreak isolates. Additional information was available on 94 ill-persons. Their ages ranged from <1 to 90 years of age, and the median age was 23. Thirty-nine percent of patients were hospitalized. One death was reported. A collaborative effort by national, state, and local agencies identified ground turkey as the source of infection. Serotype Heidelberg isolates matching the outbreak pattern were identified among ground turkey products from retail establishments, and these products originated from a common food production establishment. Nineteen outbreak isolates from ill persons or retail meat samples were sent to the National Antimicrobial Resistance Monitoring System (NARMS) at CDC for antimicrobial susceptibility testing (AST). Minimum inhibitory concentrations (MIC) were determined for amikacin, ampicillin, amoxicillin-clavulanic acid, cefoxitin, ceftiofur, ceftriaxone, chloramphenicol, ciprofloxacin, gentamicin, kanamycin, nalidixic acid, streptomycin, sulfisoxazole, tetracycline, and trimethoprim-sulfamethoxazole by broth microdilution (Sensititre®, Trek Diagnostics, Westlake, OH). Resistance was defined by the Clinical and Laboratory Standards Institute (CLSI) interpretive standards, when available. For streptomycin, where no CLSI interpretive criteria for human isolates exist, the resistance breakpoint is 64 mg/L. All of the isolates were resistant to ampicillin, gentamicin, streptomycin, and tetracycline. Two isolates with different XbaI PFGE patterns (JF6X01.0058 and JF6X01.0032) but the same BlnI pattern (JF6A26.0076) from patients in Ohio were analyzed for antimicrobial resistance genes by polymerase chain reaction and DNA sequencing. Both isolates were positive for blaTEM-1, aac(3)-IIa, aadA1, ant(3”)-Ia, and tetA genes. Plasmid DNA was electroporated into E. coli DH10B cells and Polymerase Chain Reaction (PCR)-analysis and AST demonstrated the transfer of all five genes, confirming that they were plasmid-encoded. PCR-based replicon typing identified the plasmid as type IncI1 which is a common poultry associated plasmid. Plasmid PFGE confirmed plasmids of approximately 100 kb in size in both transformants, and plasmid multi-locus sequence typing (pMLST) identified them as ST26. Most ST26 plasmids submitted to the pMLST database are cephalosporin resistance plasmids in E. coli isolated from porcine and human sources in Europe. Conjugation experiments demonstrated that both plasmids were transferred to E. coli J53 (sodium azide resistant) cells with high efficiency (2.8 x 10-1 and 9.0 x 10-2), similar to IncI1 plasmids from other studies (9, 12). While these isolates do not match previously studied Heidelberg isolates in our lab by PFGE, resistance gene content, and plasmid type, NARMS has identified several isolates from past routine surveillance of isolates from ground turkey, turkey, and human clinical samples that match the observed characteristics including XbaI PFGE pattern, AST pattern, and plasmid characteristics.

Last Modified: 4/23/2014