Salmonellosis is a major cause of bacterial enteric illness in both humans and animals. Each year an estimated 1.4 million cases of salmonellosis occur among humans in the United States (15). In approximately 35,000 of these cases, Salmonella isolates are serotyped by public health laboratories and the results are electronically transmitted to the Centers for Disease Control and Prevention (CDC). This information is used by local and state health departments and CDC to monitor local, regional, and national trends in human salmonellosis and to identify possible outbreaks of salmonellosis (1, 5). Over the past 25 years, the National Salmonella Surveillance System has provided valuable information on the incidence of human salmonellosis in the United States and trends in specific serotypes. The recently implemented Salmonella Outbreak Detection Algorithm, another valuable tool for the recognition of outbreaks (11), allows users to detect increases in human infections due to specific Salmonella serotypes. Salmonella surveillance activities depend upon the accuracy of serotype identification and are facilitated by standardized nomenclature. The National Salmonella Reference Laboratory at CDC assists public health laboratories in the United States in serotype identification by providing procedure manuals, training workshops, updates, and assistance with the identification of problem isolates.
There are currently 2,463 serotypes (serovars) of Salmonella (18). The antigenic formulae of Salmonella serotypes are defined and maintained by the World Health Organization (WHO) Collaborating Centre for Reference and Research on Salmonella at the Pasteur Institute, Paris, France (WHO Collaborating Centre), and new serotypes are listed in annual updates of the Kauffmann-White scheme (18, 19).
Salmonella nomenclature is complex, and scientists use different systems to refer to and communicate about this genus. However, uniformity in Salmonella nomenclature is necessary for communication between scientists, health officials, and the public. Unfortunately, current usage often combines several nomenclatural systems that inconsistently divide the genus into species, subspecies, subgenera, groups, subgroups, and serotypes (serovars), and this causes confusion. CDC receives many inquiries concerning the appropriate Salmonella nomenclature for the reporting of results and for use in scientific publications.
The nomenclature for the genus Salmonella has evolved from the initial one serotype-one species concept proposed by Kauffmann (12) on the basis of the serologic identification of O (somatic) and H (flagellar) antigens. Each serotype was considered a separate species (for example, S. paratyphi A, S. newport, and S. enteritidis); this concept, if used today, would result in 2,463 species of Salmonella. Other taxonomic proposals have been based on the clinical role of a strain, on the biochemical characteristics that divide the serotypes into subgenera, and ultimately, on genomic relatedness. The proposals for nomenclature changes in the genus have been summarized previously (8, 9, 14).
The defining development in Salmonella taxonomy occurred in 1973 when Crosa et al. (6) demonstrated by DNA-DNA hybridization that all serotypes and subgenera I, II, and IV of Salmonella and all serotypes of “Arizona” were related at the species level; thus, they belonged in a single species. The single exception, subsequently described, is S. bongori, previously known as subspecies V, which by DNA-DNA hybridization is a distinct species (21). Since S. choleraesuis appeared on the Approved List of Bacterial Names (23) as the type species of Salmonella, it had priority as the species name. The name “choleraesuis,” however, refers to both a species and a serotype, which causes confusion. In addition, the serotype Choleraesuis is not representative of the majority of serotypes because it is biochemically distinct, being arabinose and trehalose negative (4, 13).
In 1986 the Subcommittee of Enterobacteriaceae of the International Committee on Systematic Bacteriology at the XIV International Congress of Microbiology unanimously recommended that the type species for Salmonella be changed to S. enterica (17), a name coined by Kauffmann and Edwards in 1952 (13), because no serotype shares this name. In 1987, Le Minor and Popoff of the WHO Collaborating Centre formally made a proposal as a “Request for an Opinion” to the Judicial Commission of the International Committee of Systematic Bacteriology (14). The recommendation was adopted by CDC, by Ewing in 1986 in the 4th edition of Edward's and Ewing's Identification of Enterobactericeae (8), and by other laboratories (16).
Nonetheless, the request was denied by the Judicial Commission. Although the Judicial Commission was generally in favor of S. enterica as the type species of Salmonella, its members believed that the status of Salmonella serotype Typhi, the causative agent of typhoid fever, was not adequately addressed in this request for an opinion. They were concerned that if S. enterica were adopted as the type species, Salmonella serotype Typhi would be referred to as S. enterica subsp. enterica serotype Typhi and might be missed or overlooked by physicians in the same way that S. choleraesuis subsp. choleraesuis serotype Typhi might be overlooked. From this perspective, nothing would be gained by changing the type species name. The Judicial Commission therefore ruled that S. choleraesuis be retained as the legitimate type species pending an amended request for an opinion (24). To comply with this ruling, in 1999 Euzéby (7) made an amended request, which is pending, to adopt S. enterica as the type species of Salmonella while retaining the species “S. typhi” as an exception.
In 1987, Le Minor and Popoff (14) also proposed that the seven subgenera of Salmonella be referred to as subspecies (subspecies I, II, IIIa, IIIb, IV, V, and VI). Subgenus III was divided into IIIa and IIIb by genomic relatedness and biochemical reactions. Subspecies IIIa (S. enterica subsp. arizonae) includes the monophasic “Arizona” serotypes and subspecies IIIb (S. enterica subsp. diarizonae) contains the diphasic serotypes. All “Arizona” serotypes had been incorporated into the Kauffmann-White scheme by Rohde in 1979 (22).