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).
THE CURRENT SYSTEM USED BY CDC
In this report we update the nomenclature used at CDC for members of the genus Salmonella. The nomenclatural system is based on recommendations from the WHO Collaborating Centre and is summarized in Tables 1, 2, and 3.
TABLE 1.
Salmonella species, subspecies, serotypes, and their usual habitats, Kauffmann-White schemea
| Salmonella species and subspecies | No. of serotypes within subspecies | Usual habitat |
|---|---|---|
| S. enterica subsp. enterica (I) | 1,454 | Warm-blooded animals |
| S. enterica subsp. salamae (II) | 489 | Cold-blooded animals and the environmentb |
| S. enterica subsp. arizonae (IIIa) | 94 | Cold-blooded animals and the environment |
| S. enterica subsp. diarizonae (IIIb) | 324 | Cold-blooded animals and the environment |
| S. enterica subsp. houtenae (IV) | 70 | Cold-blooded animals and the environment |
| S. enterica subsp. indica (VI) | 12 | Cold-blooded animals and the environment |
| S. bongori (V) | 20 | Cold-blooded animals and the environment |
| Total | 2,463 |
TABLE 2.
Salmonella nomenclature in use at CDC, 2000a
| Taxonomic position | Nomenclature |
|---|---|
| Genus (italics) | Salmonella |
| Species (italics) | • enterica, which includes subspecies I, II, IIIa, IIIb, IV, and VI |
| • bongori (formerly subspecies V) | |
| Serotype (capitalized, not italicized)b | • The first time a serotype is mentioned in the text; the name should be preceded by the word “serotype” or “ser.” |
| • Serotypes are named in subspecies I and designated by antigenic formulae in subspecies II to IV, and VI and S. bongori | |
| • Members of subspecies II, IV, and VI and S. bongori retain their names if named before 1966 |
In 1984 Farmer et al. (10) updated the reporting system used at CDC for Salmonella. The major changes that CDC made and that result in a difference from the 1984 reporting system are (i) capitalization of the serotype name, (ii) inclusion of subspecies VI and S. bongori, and (iii) adoption of the type species name S. enterica.
Examples of serotype designations are Salmonella serotype (ser.) Typhimurium, Salmonella II 50:b:z6, Salmonella IIIb 60:k:z, and Salmonella ser. Marina (IV 48:g,z51:−).
TABLE 3.
Examples of Salmonella nomenclature currently seen in the literature
| Complete name | CDC designation | Other designations |
|---|---|---|
| S. entericaa subsp. enterica ser. Typhi | Salmonella ser. Typhi | Salmonella typhi |
| S. entericaa subsp. enterica ser. Typhimurium | S. ser. Typhimurium | Salmonella typhimurium |
| S. entericaa subsp. salamae ser. Greenside | S. ser. Greenside | S. II 50:z:e,n,x, S. greenside |
| S. entericaa subsp. arizonae ser. 18:z4,z23:− | S. IIIa 18:z4,z23:− | “Arizona hinshawii” ser. 7a,7b:1,2,5:− |
| S. entericaa subsp. diarizonae ser. 60:k:z | S. IIIb 60:k:z | “A. hinshawii” ser. 24:29:31 |
| S. entericaa subsp. houtenae ser. Marina | S. ser. Marina | S. IV 48:g,z51:−, S. marina |
| S. bongori ser. Brookfield | S. ser. Brookfield | S. V 66:z41:−, S. brookfield |
| S. entericaa subsp. indica ser. Srinagar | S. ser. Srinagar | S. VI 11:b:e,n,x, S. srinagar |
S. choleraesuis and S. enteritidis are also used (8).
According to the CDC system, the genus Salmonella contains two species, each of which contains multiple serotypes (Table 1). The two species are S. enterica, the type species, and S. bongori, which was formerly subspecies V (19, 21). S. enterica is divided into six subspecies (4, 19), which are referred to by a Roman numeral and a name (I, S. enterica subsp. enterica; II, S. enterica subsp. salamae; IIIa, S. enterica subsp. arizonae; IIIb, S. enterica subsp. diarizonae; IV, S. enterica subsp. houtenae; and VI, S. enterica subsp. indica). S. enterica subspecies are differentiated biochemically (4, 19) and by genomic relatedness (6, 19, 21).
Serotypes.
CDC uses names for serotypes in subspecies I (for example, serotypes Enteritidis, Typhimurium, Typhi, and Choleraesuis) and uses antigenic formulas for unnamed serotypes described after 1966 in subspecies II, IV, and VI and in S. bongori (see discussion below). The name usually refers to the geographic location where the serotype was first isolated. For named serotypes, to emphasize that they are not separate species, the serotype name is not italicized and the first letter is capitalized (Table 2). At the first citation of a serotype the genus name is given followed by the word “serotype” or the abbreviation “ser.” and then the serotype name (for example, Salmonella serotype or ser. Typhimurium). Subsequently, the name may be written with the genus followed directly by the serotype name (for example, Salmonella Typhimurium or S. Typhimurium) (18, 19). CDC uses the format for formula designations used by the WHO Collaborating Centre. Both versions of the serotype name are listed as key words in manuscripts to facilitate the search and retrieval of information on Salmonella serotypes from electronic databases. Table 3 lists other serotype designations seen in the literature.
Serotype names designated by antigenic formulae include the following: (i) subspecies designation (subspecies I through VI), (ii) O (somatic) antigens followed by a colon, (iii) H (flagellar) antigens (phase 1) followed by a colon, and (iv) H antigens (phase 2, if present) (for example, Salmonella serotype IV 45:g,z51:−. For formulae of serotypes in S. bongori, V is still used for uniformity (for example, S. V 61:z35:−).
Before 1966 all serotypes in all subspecies except subspecies IIIa and IIIb were given names. In 1966 the WHO Collaborating Centre began naming serotypes only in subspecies I and dropped all existing serotype names in subspecies II, IV, and VI and S. bongori from the Kauffmann-White scheme. For surveillance purposes, i.e., for compatibility with old data, as stated above, CDC continues to use pre-1966 names for serotypes in subspecies II, IV, and VI and S. bongori (2, 3, 4). A common example of an old serotype name used at CDC and seen in the United States is S. ser. Marina (S. IV 48:g,z51:−).
The majority (59%) of the 2,463 Salmonella serotypes belong to S. enterica subsp. I (S. enterica subsp. enterica) (19). Within S. enterica subsp. I, the most common O-antigen serogroups are A, B, C1, C2, D and E. Strains in these serogroups cause approximately 99% of Salmonella infections in humans and warm-blooded animals (19). Serotypes in S. enterica subspecies II (S. enterica subsp. salamae), IIIa (S. enterica subsp. arizonae), IIIb (S. enterica subsp. diarizonae), IV (S. enterica subsp. houtenae), IV (S. enterica subsp. indica), and S. bongori are usually isolated from cold-blooded animals and the environment but rarely from humans (10).
CONCLUSIONS
The nomenclature for Salmonella is still evolving and the debate on the name for the type species is not likely to be settled any time soon. In the meantime, the work of isolating, identifying, and reporting on Salmonella serotypes must go on for diagnostic, therapeutic, and public health purposes. We believe that the nomenclature system used at CDC, essentially based on the recommendations established by the WHO Collaborating Centre, adequately addresses the concerns and requirements of clinical and public health microbiologists. Because the type species name has not been officially approved and in order to shorten reports, Salmonella enterica subsp. enterica serotype Typhimurium, for example, is shortened to Salmonella serotype (ser.) Typhimurium or Salmonella Typhimurium. To ensure backward compatibility with literature searches on Salmonella serotypes from electronic databases, both versions of the serotype name should be listed as key words in manuscripts. In 1999, at the American Society for Microbiology (ASM) Publications Board Meeting, a proposal that relevant ASM journals adopt the Salmonella nomenclature currently used at CDC was unanimously endorsed by the board, with plans to update 2000 ASM Instructions to the Authors (20).
ACKNOWLEDGMENTS
We acknowledge the helpful discussions and advice given by Don J. Brenner and J. J. Farmer III.
Footnotes
The views expressed in this Commentary do not necessarily reflect the views of the journal or of ASM.
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