Emerging Infectious Diseases

Address for correspondence: Andreas J. Bäumler, Department of Medical Microbiology and Immunology, Texas A&M University, 407 Reynolds Medical Building, College Station, TX 77843-1114; fax: (979) 845-3479; e-mail: [email protected]. The avian-adapted serovar Salmonella Gallinarum, which includes two biovars, Gallinarum and Pullorum, was endemic in poultry flocks in Europe and the Americas in the early 20th century (1). To reduce economic losses to the poultry industry, national surveillance programs were established in the United States (National Poultry Improvement Plan, 1935) and England and Wales (Poultry Stock Improvement Plan, 1939). Since S. Gallinarum (antigen formula O9,12:-:-) has no animal reservoir other than domestic and aquatic fowl, the test-andslaughter method of disease control under these surveillance programs led to its eradication from commercial poultry flocks in the United States, England, and Wales by the 1970s (1,2). At that time, the number of human cases of infection with serovar S. Enteritidis (antigen formula O9,12:g,m:1,7) began to increase in these countries (3,4). By the 1980s, S. Enteritidis had emerged as a major concern for food safety in Europe and the Americas (5); by 1990 it was the most frequently reported Salmonella serovar in the United States (6). Most S. Enteritidis outbreaks in Europe and the United States are associated with foods containing undercooked eggs (7-10). Eggs can become contaminated with S. Enteritidis through cracks in the shell after contact with chicken feces or by transovarian infection (11). Thus, laying hens were the likely source of the S. Enteritidis epidemic in Europe and the Americas. The inverse relationship between the incidence of S. Gallinarum infection in chickens and egg-associated S. Enteritidis infections in humans prompted the hypothesis that S. Enteritidis filled the ecologic niche vacated by eradication of S. Gallinarum from domestic fowl (12). The hypothesis suggests that the epidemic increase in human S. Enteritidis cases in several geographic areas can be traced to the same origin, accounting for the simultaneous emergence of S. Enteritidis as a major egg-associated pathogen on three continents (5). A connection between the epidemics in Western Europe and the United States was not apparent from analysis of epidemic isolates. Although most human cases from England and Wales result from infection with S. Enteritidis phage type 4 (PT4), most cases in the United States are due to infections with PT8 and PT13a (13,14). The PT4 clone is genetically distinct from PT8 and 13a, as shown Competitive Exclusion of Salmonella Enteritidis by Salmonella Gallinarum in Poultry