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Outbreaks of Multidrug-Resistant Salmonella Typhimurium Associated With Veterinary Facilities ---Idaho, Minnesota, and Washington, 1999

CDC received reports in 1999 from three state health departments of outbreaks of multidrug-resistant Salmonella serotype Typhimurium infections in employees and clients of small animal veterinary clinics and an animal shelter. Salmonella infections usually are acquired by eating contaminated food; however, direct contact with infected animals, including dogs and cats, also can result in exposure and infection (1). This report summarizes clinical and epidemiologic data about these outbreaks and reviews methods of reducing the likelihood of Salmonella transmission in veterinary settings by avoiding fecal-oral contact.

Idaho

During September--October, the Idaho Department of Health and Welfare identified through routine surveillance an outbreak of Salmonella infections among employees of a small animal veterinary clinic; 10 of 20 persons had abdominal cramps and diarrhea, and two of the 10 had bloody diarrhea. The median age of the ill persons was 31 years (range: 19--44 years), the median duration of illness was 7 days (range: 4--12 days), and four persons sought medical care. The index patient reported caring for several kittens with diarrhea 1 or 2 days before illness onset; stool specimens were not cultured and the kittens died. All 10 ill employees ate meals in the clinic and had no common exposures outside the clinic. Stool specimens from five ill employees yielded S. Typhimurium. All isolates were indistinguishable by pulsed-field gel electrophoresis (PFGE); reacted to phage but did not conform to a definitive phage type; and were resistant to ampicillin, ceftriaxone, cephalothin, chloramphenicol, clavulanic acid/amoxicillin, gentamicin, kanamycin, streptomycin, sulfamethoxazole, and tetracycline.

Minnesota

The Minnesota Department of Health (MDH) routinely receives animal S. Typhimurium isolates from the Minnesota Veterinary Diagnostic Laboratory. In 1999, MDH tested S. Typhimurium isolates from nine cats and seven humans that were indistinguishable by PFGE. All isolates were resistant to ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline (R-type ACSSuT). Three cat and two human isolates tested were definitive type (DT) 104. The cats had died in an animal shelter during September--October at age 6--14 weeks as a result of infection. The median age of ill persons was 6 years (range: 11 months--23 years), and the median duration of diarrhea was 8 days (range: 5--11 days); all persons sought medical care, and one was hospitalized for 4 days. An adult treated with ciprofloxacin shed S. Typhimurium in stool at least 214 days after illness onset.

A connection with the animal shelter was established for six of the seven human patients; four purchased cats from the shelter during August--October and two attended the same day-care center as an ill child who owned a cat from the shelter. One cat developed bloody diarrhea 1 day after adoption and onset of illness in the patient began 4 days later. Two cats remained asymptomatic; however, the owner became ill 77 days after adopting the cats. The outbreak strain of S. Typhimurium was recovered from one cat 115 days after adoption.

Washington

Through laboratory-based surveillance and patient interviews, the Washington State Department of Health detected in late 1999 an outbreak of Salmonella infections associated with a small animal veterinary clinic. Stool specimens from three ill persons yielded S. Typhimurium, all three sought medical care, but none was hospitalized. One ill person was a clinic employee and the two others recently had brought their cats to the clinic, one for elective surgery and the other for a urinary tract infection. The cats developed diarrhea after their discharge from the clinic and the owners subsequently became ill. The clinic was the only common exposure reported by the three ill persons. S. Typhimurium was isolated from 14 cats associated with this clinic; some of the cats initially presented with diarrhea. Isolates from ill persons and cats were indistinguishable by PFGE. All isolates were DT104 R-type ACSSuT.

Reported by: H Ezell, B Tramontin, Idaho District Health Dept; R Hudson, PhD, Idaho State Public Health Laboratory; L Tengelsen, DVM, C Hahn, MD, State Epidemiologist, Idaho Dept of Health and Welfare. K Smith, DVM, J Bender, DVM, D Boxrud, J Adams, Minnesota Dept of Health; R Frank, DVM, Univ of Minnesota College of Veterinary Medicine, Dept of Veterinary Diagnostic Medicine; K Culbertson, DVM, Animal Humane Society, Golden Valley, Minnesota. T Besser, DVM, D Rice, MS, Washington State Univ College of Veterinary Medicine, Pullman; R Gautom, PhD, R Pallipamu, M Goldoft, MD, J Grendon, DVM, J Kobayashi, MD, Washington Dept of Health. F Angulo, DVM, T Barrett, PhD, S Rossiter, MPH, S Sivapalasingam, MD, J Wright, DVM, Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note: Although most of the estimated 1.4 million Salmonella infections that occur each year in the United States are transmitted through food, Salmonella also is transmitted through exposure to contaminated water, reptiles, farm animals, and pets (1). It is unknown how the human patients in these outbreaks became infected with Salmonella; however, the inadvertent ingestion of animal feces or food contaminated with animal feces may have occurred as the result of suboptimal sanitation and hygienic practices in the veterinary facilities. Many cats in these facilities had a diarrheal illness that also may have contributed to Salmonella transmission. Even after recovery from an acute episode of Salmonella gastroenteritis, fecal shedding of Salmonella can occur and may last several months. In addition, the use of antimicrobial agents in veterinary facilities may have contributed to transmission of multidrug-resistant Salmonella by lowering the infectious dose needed for ingestion to cause illness in animals and increasing the likelihood of transmission to humans. Although outbreaks of multidrug-resistant Salmonella with human and animal illness have been reported in large animal veterinary facilities (e.g., horse clinics) (2,3), outbreaks associated with small animal facilities are rare. The outbreaks described in this report demonstrate that small animals shed Salmonella and that small animal facilities can serve as foci of transmission for Salmonella to other animals and humans.

In 1999, the most commonly isolated Salmonella serotype in the United States was S. Typhimurium, accounting for 23% of laboratory-confirmed Salmonella cases (4). Multidrug resistance among S. Typhimurium isolates is common; of human S. Typhimurium isolates received at CDC through the National Antimicrobial Resistance Monitoring System, 46% were multidrug-resistant; 61% of these were R-type ACSSuT and 23% were R-type AKSSuT (resistant to ampicillin, kanamycin, streptomycin, sulfamethoxazole, and tetracycline). R-type ACSSuT and R-type AKSSuT, the two most common multidrug-resistant Salmonella strains, accounted for 7% and 3% of non-Typhi Salmonella isolates, respectively (5). Investigations in the United States have found associations between human infections caused by R-type ACSSuT and R-type AKSSuT strains of S. Typhimurium and contact with cattle, including eating and drinking unpasteurized dairy products (6,7). S. Typhimurium DT104 R-type ACSSuT has been associated with contact with pets in the United Kingdom (8); outbreaks described in this report are the first to associate DT104 with pets in the United States.

To prevent salmonellosis, persons should wash their hands before eating and after handling food. Immunosuppressed persons should avoid animals aged <6 months and animals with diarrhea (9). Veterinary workers should wash their hands after handling pets, especially after handling feces. These workers can further reduce their exposure to feces by wearing rubber or disposable gloves, and by removing gloves and washing their hands immediately after finishing a task that involves contact with animal feces. Although there have been no reports of Salmonella transmission through splash exposures, workers might consider taking measures to reduce splashes of feces to the mouth when hosing or cleaning a kennel. All surfaces contaminated with feces should be cleaned and disinfected. No eating should be allowed in animal treatment or holding areas. Because use of antimicrobial agents contributes to increasing resistance and facilitates transmission of multidrug-resistant Salmonella, eliminating inappropriate use of antimicrobial agents may help to prevent outbreaks of multidrug-resistant Salmonella infections in veterinary facilities (10).

References*

  1. Angulo FJ, Johnson KR, Tauxe RV, Cohen ML. Origins and consequences of antimicrobial- resistant nontyphoidal Salmonella: implications for the use of fluoroquinolones in food animals. Microbial Drug Resist 2000;6:77--83.
  2. Tillotson K, Savage CJ, Salman MD, et al. Outbreak of Salmonella infantis infection in a large animal veterinary teaching hospital. J Am Vet Med Assoc 1997;211:1554--7.
  3. Hartmann FA, Callan RJ, McGuirk SM, et al. Control of an outbreak of salmonellosis caused by drug-resistant Salmonella anatum in horses at a veterinary hospital and measures to prevent future infections. J Am Vet Med Assoc 1996;209:629--31.
  4. CDC. Salmonella surveillance: annual tabulation summary, 1999. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2000. Available at <http://www.cdc.gov/ncidod/dbmd/narms/annuals.htm>. Accessed August 2001.
  5. CDC. National Antimicrobial Resistance Monitoring System 1999 annual report, Atlanta, Georgia: US Department of Health and Human Services, CDC, 1999.
  6. Villar RG, Macek MD, Simons S, et al. Investigation of multidrug-resistant Salmonella serotype Typhimurium DT 104 infections linked to raw-milk cheese in Washington state. JAMA 1999;281:1811--6.
  7. Fey PD, Safranek TJ, Rupp M, et al. Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N Engl J Med 2000;342:1242--9.
  8. 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 1994;4:R126--R131.
  9. CDC. 1999 USPHS/IDSA guidelines for the prevention of opportunistic infections in persons infected with human immunodeficiency virus. MMWR 1999;48(no. RR 10).
  10. American Veterinary Medical Association. Principles on judicious therapeutic use of antimicrobials. Available at <http://www.avma.org/scienact/jtua/default.asp>. Accessed August 2001.

*All MMWR references are available on the Internet at <http://www.cdc.gov/mmwr>. Use the search function to find specific articles.



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