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Multidrug-Resistant Salmonella Serotype Typhimurium -- United States, 1996

A multidrug-resistant strain of Salmonella serotype Typhimurium known as Definitive Type 104 (DT104) has emerged as an increasing cause of Salmonella infections in the United Kingdom (UK). DT104 isolates in the UK are highly resistant to antimicrobial agents, frequently demonstrating a pattern of resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (R-type ACSSuT) (1). This report summarizes surveillance data documenting the rapid emergence of DT104 R-type ACSSuT in the United States and preliminary findings from the investigation of the first outbreak of DT104 infections in this country. U.S. Surveillance

S. Typhimurium was the second most commonly reported Salmonella serotype in 1995, accounting for 9702 (24%) of 41,222 Salmonella isolates reported that year. During July-August 1996, the algorithm used by the Public Health Laboratory Information System (PHLIS) to detect Salmonella outbreaks indicated that, in 29 states, the number of S. Typhimurium isolates had substantially increased when compared with a 5-year historical baseline. Although it is unknown whether these increases were associated with the emergence of DT104, the ACSSuT resistance pattern was present in 90 (32%) of the 282 human S. Typhimurium isolates tested at CDC in 1996. This pattern also was present in 273 (28%) of a national sample of 976 S. Typhimurium isolates tested during 1995, compared with 7% in 1990. In 1995, a total of 30 S. Typhimurium R-type ACSSuT isolates were obtained from 10 states and were sent to the UK for phage typing; of these, 25 (83%) were DT104. Nebraska Outbreak

During October 1996, the Nebraska Department of Health was notified about an outbreak of diarrheal illness among elementary school children in Cass County, a farming community in east central Nebraska. During October 12-14, a total of 19 (59%) of 32 children attending an elementary school developed diarrhea (100%), fever (89%), headache (89%), nausea (89%), and vomiting (58%); three reported bloody diarrhea. None required hospitalization, and all recovered.

On October 10, during lunch at the school, children had been served cold chocolate milk poured from cartons. Of the 22 children who drank the milk, 18 (82%) developed diarrhea, compared with one (10%) of 10 children who did not drink it (risk ratio {RR}=8.2; 95% confidence interval {CI}=1.3-53.1). Inspection of the school refrigerator detected numerous cartons of milk with expiration dates predating October 10, but cultures of samples obtained from these remaining cartons were negative for enteropathogens. In addition, some children had handled a turtle brought to the school for "show-and-tell" and a reportedly ill kitten during October 7-9. However, neither the turtle nor kitten were available for testing. Culture of stool samples obtained from seven children all yielded S. Typhimurium R-type ACSSuT. Phage-typing at CDC confirmed the isolates as DT104.

Reported by: G Hosek, D Leschinsky, S Irons, TJ Safranek, MD, State Epidemiologist, Nebraska Dept of Health. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: S. Typhimurium DT104 was first reported in the UK in 1984; this organism is now the second most prevalent strain of Salmonella isolated from humans in the UK after Salmonella serotype Enteritidis phage type 4 (1). Contact with ill farm animals and consumption of chicken, pork sausages, and meat paste were identified as risk factors for DT104 infection in England and Wales (2), and an outbreak investigation in 1995 implicated beef consumption (3). The organism has been isolated from several species (poultry, sheep, pigs {4}, cats, wild birds, rodents, foxes, and badgers {5}) and has been transmitted from cattle and sheep to humans (6). The ecology of this organism in the United States has not been well characterized, and efforts similar to those conducted in the UK (5) are needed to elucidate its distribution in the environment and human food chain. However, transmission of S. Typhimurium DT104 through food probably occurs through a complex route that may include wild animals, animal feed, farm animals, slaughterhouses, processing and distribution networks, retail outlets, and the consumer.

The clinical features associated with infection with this organism were severe in the UK study: 41% of patients were hospitalized (2), and of 295 patients with culture-confirmed illness, 10 (3%) died. In contrast, the case-fatality rate for nontyphoid Salmonella infections is approximately 0.1% (7).

Although R-type ACSSuT is the most common antimicrobial resistance pattern of DT104 isolates (present in 54%-67% of DT104 isolates in the UK during 1992-1995), resistance of DT104 isolates to trimethoprim and fluoroquinolones is emerging. In the UK, from 1993 to 1995, trimethoprim-resistant DT104 (R-type ACSSuTTm) increased from 1% to 27% of isolates, and ciprofloxacin-resistant DT104 (R-type ACSSuTCp) increased from 0 to 6% of isolates (1). Acquisition of trimethoprim resistance may have resulted from use of this agent to treat DT104 R-type ACSSuT infections in cattle (1). In addition, the emergence of fluoroquinolone resistance may be related to veterinary use: enrofloxacin was licensed for veterinary use in the UK in 1994, and the observed increased resistance of human isolates of DT104 to fluoroquinolones followed this introduction (1). In 1995, the Food and Drug Administration approved the fluoroquinolone sarafloxacin for treatment of Escherichia coli infections in poultry flocks. Fluoroquinolone resistance has not been detected in DT104 isolates from humans in the United States; however, ciprofloxacin is currently a treatment of choice for Salmonella infections in adult humans. The development of fluoroquinolone resistance in a strain of Salmonella that causes serious human illness could have serious public health implications.

Reservoirs for DT104 infection in the United States are not known. The outbreak of DT104 infections in Nebraska suggests possible associations with animal reservoirs (e.g., through milk or contact with animals). However, additional epidemiologic studies are needed to improve understanding of risk factors for and public health implications associated with this pathogen. CDC is conducting a national case-control study of S. Typhimurium infections through the Emerging Infectious Diseases Program's Foodborne Diseases Active Surveillance Network (FoodNet). Resistance to chloramphenicol in S. Typhimurium isolates is a highly specific marker for DT104. State health departments investigating clusters of infections of S. Typhimurium can measure chloramphenicol resistance and, if present, contact CDC's Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, to discuss more extensive antimicrobial testing and phage-typing of isolates.


  1. Threnlfal EJ, Frost JA, Ward LR, Rowe B. Increasing spectrum of resistance in multiresistant Salmonella Typhimurium. Lancet 1996;347:1053-4.

  2. Wall PG, Morgan D, Lamden K, et al. A case control study of infection with an epidemic strain of multiresistant Salmonella Typhimurium DT104 in England and Wales. Commun Dis Rep CDR Rev 1994;4:R130-R135.

  3. Davies A, O'Neill P, Towers L, Cooke M. An outbreak of Salmonella Typhimurium DT104 food poisoning associated with eating beef. Commun Dis Rep CDR Rev 1996;6:R159-R162.

  4. Anonymous. Salmonella in animal and poultry production, 1992. London: Ministry of Agriculture, Fisheries, and Food, Welsh Office, Agriculture Department, Scottish Office, Agriculture and Fisheries Department, 1993.

  5. Evans S, Davies R. Case control study of multiple resistant Salmonella typhimurium DT104 infection of cattle in Great Britain. Vet Rec 1996;139:557-8.

  6. Fone DL, Barker RM. Association between human and farm animal infections with Salmonella typhimurium DT104 in Herefordshire. Commun Dis Rep CDR Rev 1994;4:R136-R140.

  7. Council for Agricultural Science and Technology. Foodborne pathogens: risks and consequences. Ames, Iowa: Council for Agricultural Science and Technology, 1994; Task Force Report no. 122.

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