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Human Salmonellosis Associated with Animal-Derived Pet Treats --- United States and Canada, 2005

During 2004--2005, contact with Salmonella-contaminated pet treats of beef and seafood origin resulted in nine culture-confirmed human Salmonella Thompson infections in western Canada and the state of Washington. This is the third published report (1,2) of an outbreak of human illness associated with pet treats in North America and the first to describe such an outbreak in the United States. This report highlights the investigation of the outbreak by U.S. and Canadian public health officials and provides recommendations for reducing the risk that Salmonella-contaminated pet treats pose to humans. Public health practitioners should consider pet treats a potential source for Salmonella transmission.

Case Reports

Case 1. In February 2005, a man aged 26 years in Alberta, Canada, sought medical care because of diarrheal illness. Stool culture yielded S. Thompson. The patient reportedly had fed his dog beef pet treats a few days before the onset of his illness. The dog was asymptomatic. A package of the same brand of pet treats fed to the dog was purchased and submitted for testing. The treats yielded S. Thompson, S. Cerro, and S. Meleagridis. The S. Thompson isolates from the patient and the treats were indistinguishable (i.e., defined as the outbreak strain) by pulsed-field gel electrophoresis (PFGE) using Xba1. The treats were packaged and distributed by a British Columbia (BC) manufacturing plant, but plant records were inadequate to determine where the treats had been produced.

Case 2. In February 2005, a woman aged 37 years in BC sought medical care because of diarrheal illness. Stool culture yielded S. Thompson. The patient reportedly had fed her dog salmon pet treats a few days before the onset of her illness. The dog also had a diarrheal illness, but specimens were not collected. The remaining pet treats were collected from the patient's house for testing. The treats yielded S. Thompson. Isolates of S. Thompson from the patient and treats were indistinguishable from each other and from the outbreak strain by PFGE. The salmon treats originated from a Washington manufacturing plant. The treats were imported into Canada, labeled, and distributed for sale in BC and Alberta by the same BC manufacturing plant identified in case 1.

Case 3. In March 2005, a woman aged 81 years in Washington sought medical care because of diarrheal illness, fever, and vomiting. The patient was hospitalized. Stool culture yielded S. Thompson indistinguishable from the outbreak strain by PFGE. The patient had purchased and fed beef pet treats to her dog before the onset of her illness. The patient reported frequent contact with her dog but reported no recent illness in the dog. The remaining treats were collected from the patient's house for testing. The treats yielded S. Thompson indistinguishable from the outbreak strain by PFGE. The treats originated from and were packaged by the Washington manufacturing plant that was the source of the treats in case 2.

Additional cases. In 2004 and 2005, six additional human cases of S. Thompson (three in BC, two in Washington, and one in Alberta), with isolates indistinguishable by PFGE from the outbreak strain, were identified by PulseNet USA and PulseNet Canada (national molecular subtyping networks for foodborne disease surveillance). Five of the six additional patients were interviewed. Three (60%) of them had handled pet treats from the Washington or BC manufacturing plants. The two other patients had pet dogs. Stool culture from an asymptomatic dog yielded S. Thompson indistinguishable from the outbreak strain by PFGE.

Source Investigation

The BC and Washington manufacturing plants were investigated by authorities. Both manufacturers processed frozen, raw beef and salmon into pet treats for cats and dogs by thawing the materials, cutting them into the desired shapes and sizes, dehydrating them, and then packaging the finished products for distribution. The manufacturers in BC and Washington received frozen, raw beef parts from slaughterhouses in Canada and the United States, respectively. The Washington manufacturer also received frozen, raw salmon from a Washington seafood company. Although the pet treats were dehydrated at the BC and Washington plants, the dehydration temperatures were not high enough to kill bacteria that might have been present. No processing step, such as irradiation, that would destroy Salmonella and other bacteria was used during the processing. Production code dates, lot numbers, and location of plants were not recorded on the finished product packaging. No labels instructing pet owners to wash their hands after handling the product were provided. The BC manufacturing plant received some of its processed beef treats and all of its processed salmon treats from the Washington manufacturing plant.

Cultures of salmon and beef pet treats manufactured at the Washington plant and collected at the BC plant by Canadian authorities, and cultures of salmon treats collected at the Washington plant by U.S. authorities, yielded S. Thompson indistinguishable by PFGE from the outbreak strain. The salmon treats contained up to 80,000 colony-forming units of Salmonella per gram. Pet treats from the BC and Washington plants also contained other Salmonella serotypes, including S. Montevideo, S. Newport, S. Give, S. Meleagridis, S. Cerro, S. Muenster, S. Agona, and S. Anatum. Both manufacturing companies issued voluntary recalls of the implicated products in June 2005.

Reported by: L Crowe, Calgary Health Region, Calgary; L Chui, PhD, Alberta Provincial Laboratory for Public Health (Microbiology); D Everett, Alberta Ministry of Health and Wellness. S Brisdon, L Gustafson, MD, Fraser Health Authority, Surrey; E Galanis, MD, L McIntyre, L MacDougall, MSc, L Wilcott, A Paccagnella, British Columbia Centre for Disease Control. D MacDonald, MHSc, A Ellis, DVM, Public Health Agency of Canada. A Drake, MPH, J Koepsell, MS, C DeBolt, MPH, S McKeirnan, MPH, J Duchin, MD, Public Health Seattle & King County, Seattle; R Baer, MPH, M Leslie, DVM, Washington State Dept of Health. ML Collins, JM Johnson, DE Farmer, CE Keys, H Ekperigin, DVM, PhD, Food and Drug Admin. F Angulo, DVM, PhD, Div of Foodborne, Bacterial and Mycotic Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases (proposed); RE Colindres, MD, EIS Officer, CDC.

Editorial Note:

In 2004, a total of 5,085 laboratory-confirmed cases of human Salmonella infections were reported in Canada, and 35,661 laboratory-confirmed cases were reported in the United States (3,4). Studies in the United States have demonstrated that for each laboratory-confirmed case of Salmonella infection, 38 Salmonella infections occur in the community, indicating that more than 1 million persons in Canada and the United States might be infected with Salmonella each year (5). Although salmonellosis generally is a self-limiting infection, it can result in serious illness in more vulnerable populations, such as the very young, older adults, and immunocompromised persons.

Most human Salmonella infections are acquired by handling or consuming contaminated food products, particularly foods of animal origin. Infections also are acquired by direct and indirect contact with farm animals, reptiles, chicks, and, occasionally, pets. Infected animals usually shed Salmonella organisms in their feces. Humans can become infected when they place contaminated food, hands, or other objects in their mouths; therefore, hand washing after contact with animals is an effective way to prevent Salmonella infection.

This report describes an outbreak of nine culture-confirmed cases of human S. Thompson infection associated with handling animal-derived pet treats in Washington and western Canada. Because laboratory-confirmed cases of Salmonella represent only a small proportion of cases in the community (5), this outbreak might have involved hundreds of infections. In recent years, an increasing variety of animal by-products, such as pig ears, have become available for purchase as animal-derived pet treats. Animal-derived pet treats have been associated with previous outbreaks of human Salmonella infection in Canada. In 1999, contaminated pig ear pet treats were confirmed as the source of an outbreak of human S. Infantis in several provinces (1,6). In 2002, contaminated pet treats imported from Texas were associated with human S. Newport infections in Calgary, Alberta (2). The S. Infantis isolates from the patients in Canada and from the pet treats in the United States were indistinguishable by PFGE. Follow-up investigations of those outbreaks indicated that pet treats are frequently contaminated with Salmonella organisms. In Canada, after the 1999 outbreak, Salmonella organisms were isolated from 48 (51%) of 94 samples of pig ear pet treats purchased from retail stores in Alberta (2). In the United States, Salmonella organisms, including S. Infantis, were isolated from 65 (41%) of 158 samples of pig ear and other animal-derived pet treats purchased from retail stores during 1999--2000 (7).

Detecting and controlling the transmission of Salmonella organisms through pet treats poses several challenges (8). Animal-derived pet treats often are contaminated with salmonellae, and the dehydration procedure used to make pet treats might not be effective at eliminating the organism. Aside from direct contact with contaminated pet treats, transmission of salmonellae to humans might also occur indirectly through infection in pets. Pets consuming contaminated treats might become colonized with salmonellae but remain asymptomatic, thus becoming unrecognized sources of contamination in the household. Young children, older adults, or immunocompromised persons in such households might have a higher risk for severe illness from Salmonella infection.

In Canada, pet treats are not regulated, but the Canadian Food Inspection Agency has used the Animal Health Act* to encourage product recalls. The Public Health Agency of Canada and the Pet Industry Joint Advisory Council are collaborating to improve the safety of these products.

In the United States, pet treats are regulated by the Food and Drug Administration (FDA). Salmonella-contaminated pet treats are considered adulterated under the Federal Food, Drug, and Cosmetic (FDC) Act. After the 1999 Canadian outbreak, FDA encouraged manufacturers to take voluntary steps to ensure the absence of salmonellae in pet treats. In addition, the American Pet Products Manufacturers Association published Guidelines for the Manufacturing of Natural Part Treats for Pets to educate its members about contamination risks (9). In 2004, FDA initiated annual nationwide testing of pet treats for salmonellae. Because results of this testing have shown that the prevalence of Salmonella organisms in pet treats in the United States has not decreased, FDA plans to broaden its use of enforcement actions to ensure compliance with the FDC Act.

Pet treat manufacturers, retailers, health-care providers, public health authorities, veterinarians, and consumers should be aware of the potential for animal-derived pet treats to serve as a source of Salmonella-related illness in humans. Public health authorities should routinely consider this possibility during their investigations of cases or outbreaks of human salmonellosis. In response to the public health hazard described in this and other reports, CDC and the Public Health Agency of Canada have issued recommendations (Box) to reduce the risk for transmission of salmonellae to humans from contaminated animal-derived pet treats.

References

  1. Laboratory Centre for Disease Control, Public Health Agency of Canada. Human health risk from exposure to natural dog treats. Can Commun Dis Rep 2000;26:41--2.
  2. Pitout JDD, Reisbig MD, Mulvey M, et al. Association between handling of pet treats and infection with Salmonella enterica serotype Newport expressing the AmpC ß-Lactamase, CMY-2. J Clin Microbiol 2003;39:538--42.
  3. Centre for Infectious Disease Prevention and Control. Notifiable Diseases Reporting System. Ottawa, Canada: Public Health Agency of Canada, Centre for Infectious Disease Prevention and Control; 2006. Available at http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/index_e.html.
  4. CDC. Salmonella surveillance: annual summary, 2004. Atlanta, GA: US Department of Health and Human Services, CDC; 2005.
  5. Voetsch AC, Van Gilder TJ, Angulo FJ, et al. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 2004; 38: S127--34.
  6. Clark C, Cunningham J, Ahmed R, et al. Characterization of Salmonella associated with pig ear dog treats in Canada. J Clin Microbiol 2001;39:3962--8.
  7. White DG, Datta A, McDermott P, et al. Antimicrobial susceptibility and genetic relatedness of Salmonella serovars isolated from animal-derived dog treats in the USA. J Antimicro Chem 2003;52:860--3.
  8. Finlay R, Reid-Smith R, Weese JS. Human health implications of Salmonella-contaminated natural pet treats and raw pet food. Clin Infect Dis 2006;42:686--91.
  9. American Pet Products Manufacturers Association, Inc. Guidelines for the manufacturing of natural part treats for pets. Greenwich, CT: American Pet Products Manufacturers Association, Inc.; 2006. Available at http://www.appma.org/lawlibrary_article.asp?topic=20.

* Available at http://www.fda.gov/opacom/laws/fdcact/fdcact4.htm.

Available at http://www.inspection.gc.ca/english/anima/heasan/heasane.shtml.

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