Farm Animal Contact as Risk Factor for Transmission of Bovine-associated Salmonella Subtypes

Kevin J. Cummings

, Lorin D. Warnick, Margaret A. Davis, Kaye Eckmann, Yrjö T. Gröhn, Karin Hoelzer, Kathryn MacDonald, Timothy P. Root, Julie D. Siler, Suzanne M. McGuire, Martin Wiedmann, Emily M. Wright, Shelley M. Zansky, and Thomas E. Besser

Author affiliations: Author affiliations: Texas A&M University, College Station, Texas, USA (K.J. Cummings); Cornell University, Ithaca, New York, USA (K.J. Cummings, L.D. Warnick, Y.T. Gröhn, K. Hoelzer, J.D. Siler, M. Wiedmann, E.M. Wright); Washington State University, Pullman, Washington, USA (M.A. Davis, T.E. Besser); Washington State Department of Health, Olympia, Washington, USA (K. Eckmann, K. MacDonald); New York State Department of Health, Albany, New York, USA (T.P. Root, S.M. McGuire, S.M. Zansky)

Abstract

Salmonellosis is usually associated with foodborne transmission. To identify risk from animal contact, we compared animal exposures of case-patients infected with bovine-associated Salmonella subtypes with those of control-patients infected with non-bovine–associated subtypes. We used data collected in New York and Washington, USA, from March 1, 2008, through March 1, 2010. Contact with farm animals during the 5 days before illness onset was significantly associated with being a case-patient (odds ratio 3.2, p = 0.0008), after consumption of undercooked ground beef and unpasteurized milk were controlled for. Contact with cattle specifically was also significantly associated with being a case-patient (odds ratio 7.4, p = 0.0002), after food exposures were controlled for. More cases of bovine-associated salmonellosis in humans might result from direct contact with cattle, as opposed to ingestion of foods of bovine origin, than previously recognized. Efforts to control salmonellosis should include a focus on transmission routes other than foodborne.

Salmonella enterica remains a formidable public health challenge, resulting in ≈1.2 million illnesses and 400 deaths annually in the United States alone (1). Disease manifestations include diarrhea, fever, anorexia, abdominal pain, vomiting, and malaise. Although clinical disease generally resolves within 3–7 days, Salmonella spp. can also produce potentially fatal invasive infections. The incidence of human salmonellosis has not declined over the past 15 years and is significantly higher than it was during 2006–2008 (2). An estimated 94% of Salmonella infections are foodborne (1); common sources include undercooked eggs, poultry, beef, and pork; unpasteurized dairy products; and raw vegetables (3–7). Although some studies have shown that direct contact with infected animals is a risk factor for salmonellosis (8,9), the foodborne route is still regarded as the primary transmission route.
Dairy cattle are considered a key source of several Salmonella serovars that are a threat to human health, including multidrug-resistant S. enterica serovar Newport and S. enterica serovar Typhimurium (8–11). Foodborne transmission can occur through fecal contamination of beef carcasses at the time of slaughter (12) or through contamination of crops, either by manure used as fertilizer or by manure-contaminated irrigation water (13). Milk and other dairy products pose less of a public health threat because of commercial pasteurization, although consumption of unpasteurized dairy products persists. Infection by direct contact is an occupational risk for dairy farm workers and veterinarians. The most recent National Animal Health Monitoring System Dairy Study reports that there were >75,000 dairy operations in the United States in 2006, and the American Veterinary Medical Association reports that there were >5,000 veterinarians engaged either predominantly or exclusively in food animal practice as of 2010. Persons who interact with dairy cattle in public settings, such as open farms, petting zoos, and county or state fairs, are also at risk for salmonellosis through direct exposure (8,9,14,15).
Our objective was to identify significant risk factors for salmonellosis caused by bovine-associated Salmonella subtypes (including those within the Newport and Typhimurium serovars) by using the case–case study design (16). We specifically evaluated the role of direct animal contact as a potential route of transmission.