Chapter 12 : The Genus Citrobacter

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

The Genus Citrobacter, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817541/9781555813420_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555817541/9781555813420_Chap12-2.gif


By the late 1960s and early 1970s, three major groups of biochemically defined citrobacteria were recognized, namely, , which dated back to the original work of Braak in 1928; , described by Frederiksen in 1970; and , an organism which was originally placed in the genus by Young and coworkers. A recently identified new subspecies or possibly even a new species was given the general name of Centers for Disease Control and Prevention (CDC) enteric group 137 because of uncertainty regarding the taxonomic (genus) status of named species within this group, based upon 16S rRNA analysis. species are not common agents of human disease. Although they are resident commensal flora in the gastrointestinal tract, they are infrequently implicated as primary pathogens. A study performed by researchers at the CDC since the recent taxonomic revisions within the genus suggests that many commercial systems should be able to identify these newly described species with only minor adjustments to their current algorithms. Biotyping is a technique primarily used for epidemiologic purposes. Two biotypes of are distinguished in the older literature, based upon the ability of citrobacteria to produce HS on triple sugar iron (TSI) slants.

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12

Key Concept Ranking

Type III Secretion System
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Clustering of species into distinct groups, based upon phylogenetic analysis of 16S rRNA sequences (158).

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Aldová, E.,, J. Schindler,, J. šourek,, A. Nemec,, and P. Urbášková. 1997. Detection and identification of Citrobacter sedlakiiin the Czech republic. Zentbl. Bakteriol. 285:389396.
2. Arens, S.,, J. Verhaegen,, and L. Verbist. 1997. Differentiation and susceptibility of Citrobacter isolates from patients in a university hospital. Clin. Microbiol. Infect. 3:5357.
3. Badger, J. L.,, M. F. Stins,, and K. S. Kim. 1999. Citrobacter freundii invades and replicates in human brain microvascular endothelial cells. Infect. Immun. 67:42084215.
4. Bangert, R. L.,, A. C. S. Ward,, E. H. Stauber,, B. R. Cho,, and P. R. Widders. 1988. A survey of the aerobic bacteria in the feces of captive raptors. Avian Dis. 32:5362.
5. Bascomb, S.,, S. L. Abbott,, J. D. Bobolis,, D. A. Bruckner,, S. J. Connell,, S. K. Cullen,, M. Daugherty,, D. Glenn,, J. M. Janda,, S. J. Lentsch,, D. Lindquist,, P. B. Mayhew,, D. M. Nothaft,, J. R. Skinner,, G. B. Williams,, J. Wong,, and B. L. Zimmer. 1997. Multicenter evaluation of the MicroScan rapid gram-negative identification type 3 panel. J. Clin. Microbiol. 35:25312536.
6. Bennett, A. R.,, S. MacPhee,, R. Betts,, and D. Post. 1999. Use of pyrrolidonyl peptidase to distinguish Citrobacter from Salmonella. Lett. Appl. Microbiol. 28:175178.
7. Bettelheim, K. A.,, H. Evangelidis,, J. L. Pearce,, E. Sowers,, and N. A. Strockbine. 1993. Isolation of a Citrobacter freundii strain which carries the Escherichia coli O157 antigen. J. Clin. Microbiol. 31:760761.
8. Bishara, J.,, B. Gabay,, Z. Samra,, E. Hodak,, and S. Pitlik. 1998. Cellulitis caused by Citrobacter diversus in a patient with multiple myeloma. Cutis 61:158159.
9. Blaylock, R. S. M. 2001. Normal oral bacterial flora from some southern African snakes. Onderstepoort J. Vet. Res. 68:175182.
10. Booth, L. V.,, J. D. Palmer,, J. Pateman,, and A. C Tuck. 1993. Citrobacter diversus ventriculitis and brain abscesses in an adult. J. Infect. 26:207209.
11. Brenner, D. J.,, P. A. D. Grimont,, A. G. Steigerwalt,, G. R. Fanning,, E. Ageron,, and C. F. Riddle. 1993. Classification of citrobacteria by DNA hybridization: designation of Citrobacter farmeri sp. nov., Citrobacter youngae sp. nov., Citrobacter braakii sp. nov., Citrobacter werkmanii sp. nov., Citrobacter sedlakii sp. nov., and three unnamed Citrobacter genomospecies. Int. J. Syst. Bacteriol. 43:645658.
12. Brenner, D. J.,, C. M. O’Hara,, P. A. D. Grimont,, J. M. Janda,, E. Falsen,, E. Aldova,, E. Ageron,, J. Schindler,, S. L. Abbott,, and A. G. Steigerwalt. 1999. Biochemical identification of Citrobacter species defined by DNA hybridization and description of Citrobacter gillenii sp. nov. (formerly Citrobacter genomospecies 10) and Citrobacter murliniae sp. nov. (formerly Citrobacter genomospecies 11). J. Clin. Microbiol. 37:26192624.
13. Brooks, D. E.,, E. R. Jacobson,, E. D. Wolf,, S. Clubb,, and J. M. Gaskin. 1983. Panophthalmitis and otitis interna in fire-bellied toads. J. Am. Vet. Med. Assoc. 183:11981201.
14. Bruckner, D. A.,, P. Colonna,, D. Glenn,, S. L. Abbott,, and J. M. Janda. 1997. Citrobacter farmeri bacteremia in a child with short-bowel syndrome. J. Clin. Microbiol. 35:33533354.
15. Bruehl, C. L.,, and R. Listernick. 1992. Citrobacter freundii septic arthritis. J. Paediatr. Child Health 28:402403.
16. Chart, H.,, G. A. Willshaw,, T. Cheasty,, and B. Rowe. 1993. Structure and antigenic properties of Citrobacter freundii lipolysaccharides. J. Appl. Bacteriol. 74:583587.
17. Chen, H.,, P. Gollnick,, and R. S. Phillips. 1995. Site-directed mutagenesis of His3436Ala in Citrobacter freundii tyrosine phenol-lyase. Effects on the kinetic mechanism and rate determining step. Eur. J. Biochem. 229:540549.
18. Chen, Y.-S.,, W.-W. Wong,, C.-P. Fung,, K.-W. Yu,, and C.-Y. Liu. 2002. Clinical features and antimicrobial susceptibility trends in Citrobacter freundii bacteremia. J. Microbiol. Immunol. Infect. 35:109114.
19. Chuang, A. W.,, J. B. Lewis,, E. B. Golden,, and S. K. Bhaskar. 1998. Citrobacter freundii empyema in a patient with occult pulmonary histoplasmosis. Am. J. Med. Sci. 315:314316.
20. Christo, G. G.,, J. Mathai,, B. Nalini,, M. Baliga,, and A. Venkatesh. 1990. Neonatal Citrobacter sepsis: clinical and epidemiological aspects. Ind. J. Pediatr. 57:781784.
21. Cockerill, F. R.III,, J. G. Hughes,, E. A. Vetter,, R. A. Mueller,, A. L. Weaver,, D. M. Ilstrup,, J. E. Rosenblatt,, and W. R. Wilson. 1997. Analysis of 281,797 consecutive blood cultures performed over an eight-year period: trends in microorganisms isolated and the value of anaerobic culture of blood. Clin. Infect. Dis. 24:403418.
22. Crosa, J. H.,, A. G. Steigerwalt,, G. R. Fanning,, and D. J. Brenner. 1974. Polynucleotide sequence divergence in the genus Citrobacter. J. Gen. Microbiol. 83:271282.
23. Dauga, C. 2002. Evolution of the gyrB gene and the molecular phylogeny of Enterobacteriaceae: a model molecule for molecular systematic studies. Int. J. Syst. Evol. Microbiol. 52:531547.
24. de la Puente-Redondo, V. A.,, C. B. Gutiérrez-Martin,, C. Pérez-Martínez,, N. García del Blanco,, M. J. García-Iglesias,, C. C. Pérez-García,, and E. F. Rodríguez-Ferri. 1999. Epidemic infection caused by Citrobacter rodentium in a gerbil colony. Vet. Rec. 145:400403.
25. Deng, W.,, B. A. Vallance,, Y. Li,, J. L. Puente,, and B. B. Finlay. 2003. Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol. Microbiol. 48:95115.
26. Doran, T. I. 1999. The role of Citrobacter in clinical disease of children: review. Clin. Infect. Dis. 28:384394.
27. Draper, C. S.,, R. D. Walker,, and H. E. Lawler. 1981. Patterns of oral bacterial infection in captive snakes. J. Am. Vet. Med. Assoc. 179:12231226.
28. Drelichman, V.,, and J. D. Band. 1985. Bacteremias due to Citrobacter diversus and Citrobacter freundii. Arch. Intern. Med. 145:18081810.
29. Dyer, J.,, K. C. Hayani,, W. M. Janda,, and P. C. Schreckenberger. 1997. Citrobacter sedlakii meningitis and brain abscess in a premature infant. J. Clin. Microbiol. 35:26862688.
30. El Harrif-Heraud, C. Arpin, S. Benliman, and C. Quentin. 1997. Molecular epidemiology of a nosocomial outbreak due to SHV-4-producing strains of Citrobacter diversus. J. Clin. Microbiol. 35:25612567.
31. Eppes, S. C.,, C. R. Woods,, A. S. Mayer,, and J. D. Klein. 1993. Recurring ventriculitis due to Citrobacter diversus: clinical and bacteriologic analysis. Clin. Infect. Dis. 17:437440.
32. Ewing, W. H.,, and B. R. Davis. 1972. Biochemical characterization of Citrobacter diversus (Burkey) Werkman and Gillen and designation of the neotype strain. Int. J. Syst. Bacteriol. 22:1218.
33. Farmer, J. J., III, 1981.The genus Citrobacter, p. 11401147. In M. P. Starr,, H. Stolp,, H. G. Trüper,, and H. G. Schlegel (ed.), The Prokaryotes: a Handbook on Habitats, Isolation, and Identification of Bacteria. Springer-Verlag, Berlin, Germany.
34. Farmer, J. J.III, 2003. Enterobacteriaceae: introduction and identification, p. 636653. In P. R. Murray,, E. J. Baron,, J. H. Jorgensen,, M. A. Pfaller,, and R. H. Yolken (ed.), Manual of Clinical Microbiology, 8th ed. American Society for Microbiology, Washington, D.C.
35. Farmer, J. J.III,, B. R. Davis,, F. W. Hickman-Brenner,, A. McWhorter,, G. P. Huntley-Carter,, M. A. Asbury,, C. Riddle,, H. G. Wathen-Grady,, C. Elias,, G. R. Fanning,, A. G. Steigerwalt,, C. M. O’Hara,, G. K. Morris,, P. B. Smith,, and D. J. Brenner. 1985. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. J. Clin. Microbiol. 21:4676.
36. Farr, R. W.,, R. A. Khakoo,, L. P. Maxwell,, and R. C. Hill. 1994. Citrobacter pericarditis secondary to a subphrenic abscess. Clin. Infect. Dis. 18:838839.
37. Ferrer, F. A.,, C. D. A. Herndon,, and P. H. McKenna. 1999. Citrobacter diversus urosepsis and cerebral abscess in a child with antenatal hydronephrosis. Urology 54:1097v1097vii.
38. Fields, B. N.,, M. M. Uwaydah,, L. J. Kunz,, and M. N. Swartz. 1967. The so-called “paracolon” bacteria. Am. J. Med. 42:89106.
39. Fincher, R.-M. E.,, M. W. Jackson,, and A. Q. Fischer. 1990. Case report: Citrobacter freundii: a newly reported cause of pyomyositis. Am. J. Med. Sci. 299:331333.
40. Finn, A.,, G. H. Talbot,, E. Anday,, M. Skros,, M. Provencher,, and C. Hoegg. 1988. Vertical transmission of Citrobacter diversus from mother to infant. Pediatr. Infect. Dis. J. 7:293294.
41. Fischer, C.,, M. Kallerhoff,, W. Weidner,, and R. H. Ringert. 1996. Citrobacter emphysematous pyelonephritis in a tuberculous kidney caused by Citrobacter. A case report in a diabetic patient. Ann. Urol. (Paris) 30:108111.
42. Flaherty, J. P.,, S. Garcia-Houchins,, S. Chudy,, and P. M. Arnow. 1993.An outbreak of gram-negative bacteremia traced to contaminated O-rings in reprocessed dialyzers. Ann. Intern. Med. 119:10721078.
43. Flegg, P. J.,, and B. K. Mandal. 1989. Citrobacter freundii bacteraemia presenting as typhoid fever. J. Infect. 18:171173.
44. Fluit, A. C.,, F. J. Schmitz,, J. Verhoef, and the European SENTRY Participant Group. 2001. Frequency of isolation of pathogens from bloodstream, nosocomial pneumonia, skin and soft tissue, and urinary tract infections occurring in European patients. Eur. J. Clin. Microbiol. Infect. Dis. 20:188191.
45. Frederiksen, W. 1970. Citrobacter koseri (n. sp.) a new species within the genus Citrobacter, with a comment on the taxonomic position of Citrobacter intermedium (Werkman and Gillen). Publ. Fac. Sci. Univ. J. E. Purkyne Brno 47:8994.
46. Frederiksen, W. 1990. Correct names of the species Citrobacter koseri, Levinea malonatica, and Citrobacter diversus. Request for an opinion. Int. J. Syst. Bacteriol. 40:107108.
47. Frederiksen, W.,, and P. Søgaard,. 1991. The genus Citrobacter, p. 27442753. In A. Balows,, H. G. Trüper,, M. Dworkin,, W. Harder,, and K.-H. Schleifer (ed.), The Prokaryotes: a Handbook on the Biology of Bacteria. Ecophysiology, Isolation, Identification, Applications, 2nd ed. Springer-Verlag, Berlin, Germany.
48. Funke, G.,, D. Monnet,, C. deBernardis,, A. von Graevenitz,, and J. Freney. 1998. Evaluation of the VITEK 2 system for rapid identification of medically relevant gram-negative rods. J. Clin. Microbiol. 36:19481952.
49. Galarneau, J. R.,, M. Fortin,, J. M. Lapointe,, and C. Girard. 2003. Citrobacter freundii septicemia in two dogs. J. Vet. Diagn. Investig. 15:297299.
50. Garcia, D. C.,, G. M. Woloj,, S. Piñeiro,, D. O. Sordelli,, and S. Kaufman. 1995. An 8-year study of resistance in gramnegative bacilli isolates from patients with nosocomial infection at one hospital in Argentina. J. Med. Microbiol. 42:283290.
51. Garcia-Bustinduy, M.,, M. Lecuona,, F. Guimera,, M. Saez,, S. Dorta,, R. Sanchez,, A. Noda,, and R. Garcia-Montelongo. 2002. Citrobacter koseri in scalp folliculitis. Cutis 69:393394.
52. Gill, M. A.,, and G. E. Schutze. 1999. Citrobacter urinary tract infections in children. Pediatr. Infect. Dis. J. 18:889892.
53. Goering, R. V.,, J. Ehrenkranz,, C. C. Sanders,, and W. E. Sanders, Jr. 1992. Long term epidemiological analysis of Citrobacter diversus in a neonatal intensive care unit. Pediatr. Infect. Dis. J. 11:99104.
54. Goldstein, E. J. C.,, E. O. Agyare,, A. E. Vagvolgyi,, and M. Halpern. 1981. Aerobic bacterial oral flora of garter snakes: development of normal flora and pathogenic potential for snakes and humans. J. Clin. Microbiol. 13:954956.
55. Gordon, D. M.,, and F. FitzGibbon. 1999. The distribution of enteric bacteria from Australian mammals: host and geographical effects. Microbiology 145:26632671.
56. Graham, D. R.,, R. L. Anderson,, F. E. Ariel,, N. J. Ehrenkranz,, B. Rowe,, H. R. Boer,, and R. E. Dixon. 1981. Epidemic nosocomial meningitis due to Citrobacter diversus in neonates. J. Infect. Dis. 144:203209.
57. Graham, D. R.,, and J. D. Band. 1981. Citrobacter diversus brain abscess and meningitis in neonates. JAMA 245:19231925.
58. Gross, R. J.,, and B. Rowe. 1975. Citrobacter koseri. I. An extended antigenic scheme for Citrobacter koseri (syn. C. diversus, Levinea malonatica). J. Hyg. Camb. 75:121127.
59. Gross, R. J.,, and B. Rowe. 1983. Citrobacter koseri (syn. C. diversus): biotype, serogroup and drug resistance patterns of 517 strains. J. Hyg. Camb. 90:233239.
60. Gross, R. J.,, B. Rowe,, I. Sechter,, D. Cahan,, and G. Altman. 1981. Antigenic scheme for Citrobacter koseri (syn. C. diversus, Levinea malonatica): three new antigens recognized in strains from Israel. J. Hyg. Lond. 86:111115.
61. Guarino, A.,, G. Capano,, B. Malamisura,, M. Alessio,, S. Guandalini,, and A. Rubino. 1987. Production of Escherichia coli STa-like heat-stable enterotoxin by Citrobacter freundii isolated from humans. J. Clin. Microbiol. 25:110114.
62. Guarino, A.,, R. Giannella,, and M. R. Thompson. 1989. Citrobacter freundii produces an 18-amino-acid heat-stable enterotoxin identical to the 18-amino-acid Escherichia coli heat-stable enterotoxin (ST Ia). Infect. Immun. 57:649652.
63. Guerrant, R. L.,, M. D. Dickens,, R. P. Wenzel,, and A. Z. Kapikian. 1976. Toxigenic bacterial diarrhea: nursery outbreak involving multiple bacterial strains. J. Pediatr. 89:885891.
64. Harvey, B. S.,, T. Koeuth,, J. Versalovic,, C. R. Woods,, and J. R. Lupski. 1995. Vertical transmission of Citrobacter diversus documented by DNA fingerprinting. Infect. Control Hosp. Epidemiol. 16:564569.
65. Hess, P.,, N. Daryab,, K. Michaelis,, A. Reisenauer,, and T. A. Oelschlaeger. 2000. Type 1 pili of Citrobacter freundii mediate invasion into host cells. Adv. Exp. Med. Biol. 485: 225235.
66. Hoban, D. J.,, S. K. Bouchillon,, J. L. Johnson,, G. G. Zhanel,, D. L. Butler,, L. A. Miller,, J. A. Poupard, and the Gemifloxacin Surveillance Study Research Group. 2001. Comparative in vitro activity of gemifloxacin, ciprofloxacin, levofloxacin and ofloxacin in a North American surveillance study. Diagn. Microbiol. Infect. Dis. 40:5157.
67. Hodges, G. R.,, C. E. Degener,, and W. G. Barnes. 1978. Clinical significance of Citrobacter isolates. Am. J. Clin. Pathol. 70:3740.
68. Holmes, B.,, M. Costas,, M. Ganner,, S. L. W. On,, and M. Stevens. 1994. Evaluation of Biolog system for identification of some gram-negative bacteria of clinical importance. J. Clin. Microbiol. 32:19701975.
69. Holmes, B.,, M. Costas,, T. Thaker,, and M. Stevens. 1994. Evaluation of two BBL Crystal systems for identification of some clinically important gram-negative bacteria. J. Clin. Microbiol. 32:22212224.
70. Inoue, K.,, K. Miki,, K. Tamura,, and R. Sakazaki. 1996. Evaluation of L-pyrrolidonyl peptidase paper strip test for differentiation of members of the family Enterobacteriaceae, particularly Salmonella spp. J. Clin. Microbiol. 34:18111812.
71. Jacoby, G. A.,, and G. L. Archer. 1991. New mechanisms of bacterial resistance to antimicrobial agents. N. Engl. J. Med. 324:601612.
72. Janda, J. M.,, S. L. Abbott,, W. K. W. Cheung,, and D. F. Hanson. 1994. Biochemical identification of citrobacteria in the clinical laboratory. J. Clin. Microbiol. 32:18501854.
73. Joaquin, A.,, S. Khan,, N. Russell,, and N. Al Fayez. 1991. Neonatal meningitis and bilateral cerebellar abscesses due to Citrobacter freundii. Pediatr. Neurosurg. 17:2324.
74. Jolivet-Gougeon, A.,, Z. Tamanai-Shacoori,, F. Sauvager,, and M. Cormier. 1997. Production of Escherichia coli group I-like heat-labile enterotoxin by Enterobacteriaceae isolated from environmental water. Microbios 90:209218.
75. Jones, R. N.,, E. N. Kehrberg,, M. E. Erwin,, S. C. Anderson, and the Fluoroquinolone Resistance Surveillance Group. 1994. Prevalence of important pathogens and antimicrobial activity of parenteral drugs at numerous medical centers in the United States. I. Study on the threat of emerging resistances: real or perceived? Diagn. Microbiol. Infect. Dis. 19:203215.
76. Jossart, M.-F.,, and R. J. Courcol. 1999. Evaluation of an automated system for identification of Enterobacteriaceae and nonfermenting bacilli. Eur. J. Clin. Microbiol. Infect. Dis. 18:902907.
77. Karasawa, T.,, H. Ito,, T. Tsukamoto,, S. Yamasaki,, H. Kurazono,, S. M. Faruque,, G. B. Nair,, M. Nishibuchi,, and Y. Takeda. 2002. Cloning and characterization of genes encoding homologues of the B subunit of cholera toxin and the Escherichia coli heat-labile enterotoxin from clinical isolates of Citrobacter freundii and E. coli. Infect. Immun. 70:71537155.
78. Karlowsky, J. A.,, M. E. Jones,, C. Thornsberry,, I. R. Friedland,, and D. F. Sahm. 2003. Trends in antimicrobial susceptibilities among Enterobacteriaceae isolated from hospitalized patients in the United States from 1998 to 2001. Antimicrob. Agents Chemother. 47:16721680.
79. Kelly, M. T.,, and C. Leicester. 1992. Evaluation of the Autoscan Walkaway system for rapid identification and susceptibility testing of gram-negative bacilli. J. Clin. Microbiol. 30:15681571.
80. Khan, A.,, R. K. Nandi,, S. C. Das,, T. Ramamurthy,, J. Khanam,, T. Shimizu,, S. Yamasaki,, S. K. Bhattacharya,, W. Chaicumpa,, Y. Takeda,, and G. B. Nair. 2003. Environmental isolates of Citrobacter braakii that agglutinate with Escherichia coli O157 antiserum but do not possess the genes responsible for the biosynthesis of O157 somatic antigen. Epidemiol. Infect. 130:179186.
81. Khashe, S.,, and J. M. Janda. 1996. Iron utilization studies in Citrobacter species. FEMS Microbiol. Lett. 137:141146.
82. Kitch, T. T.,, M. R. Jacobs,, and P. C. Appelbaum. 1994. Evaluation of RapID onE system for identification of 379 strains in the family Enterobacteriaceae and oxidase-negative, gramnegative nonfermenters. J. Clin. Microbiol. 32:931934.
83. Kline, M. W. 1988. Citrobacter meningitis and brain abscess in infancy: epidemiology, pathogenesis, and treatment. J. Pediatr. 113:430434.
84. Kline, M. W.,, S. L. Kaplan,, E. P. Hawkins,, and E. O. Mason, Jr. 1988. Pathogenesis of brain abscess formation in an infant rat model of Citrobacter diversus bacteremia and meningitis. J. Infect. Dis.157:106112.
85. Kline, M. W.,, E. O. Mason, Jr.,, and S. L. Kaplan. 1988. Characterization of Citrobacter diversus strains causing neonatal meningitis. J. Infect. Dis. 157:101105.
86. Kline, M. W.,, E. O. Mason, Jr.,, and S. L. Kaplan. 1989. Epidemiologic marker system for Citrobacter diversus using outer membrane protein profiles. J. Clin. Microbiol. 27:17931796.
87. Kocharova, N. A.,, Y. A. Knirel,, E. S. Stanislavsky,, E. V. Kholodkova,, C. Lugowski,, W. Jachymek,, and E. Romanowska. 1996. Structural and serological studies of lipopolysaccharides of Citrobacter O35 and O38 antigenically related to Salmonella. FEMS Microbiol. Immunol. 13:18.
88. Kueh, C. S. W.,, P. Kutarski,, and M. Brunton. 1992. Contaminated marine wounds-the risk of acquiring acute bacterial infection from marine recreational beaches. J. Appl. Bacteriol. 73:412420.
89. Lew, P. D.,, A. S. Baker,, L. J. Kunz,, and R. C. Moellering, Jr. 1984. Intra-abdominal Citrobacter infections: association with biliary or upper gastrointestinal source. Surgery 95:398403.
90. Li, J.,, J. M. Musser,, P. Beltran,, M. W. Kline,, and R. K. Selander. 1990. Genotypic heterogeneity of strains of Citrobacter diversus expressing a 32-kilodalton outer membrane protein associated with neonatal meningitis. J. Clin. Microbiol. 28:17601763.
91. Lin, F.-Y. C.,, W. F. Devoe,, C. Morrison,, J. Libonati,, P. Powers,, R. J. Gross,, B. Rowe,, E. Israel,, and J. G. Morris. 1987. Outbreak of neonatal Citrobacter diversus meningitis in a suburban hospital. Pediatr. Infect. Dis. J. 6:5055.
92. Lipsky, B. A.,, E. W. Hook III,, A. A. Smith,, and J. J. Plorde. 1980. Citrobacter infections in humans experience at the Seattle Veterans Administration Medical Center and a review of the literature. Rev. Infect. Dis. 2:746760.
93. Luperchio, S. A.,, and D. B. Schauer. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3:333340.
94. Luperchio, S. A.,, J. V. Newman,, C. A. Dangler,, M. D. Schrenzel,, D. J. Brenner,, A. G. Steigerwalt,, and D. B. Schauer. 2000. Citrobacter rodentium, the causative agent of transmissable murine colonic hyperplasia, exhibits clonality: synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J. Clin. Microbiol. 38:43434350.
95. Mainardi, J.-L.,, P. Mugnier,, A. Coutrot,, A. Buu-Hoï,, E. Collatz,, and L. Gutmann. 1997. Carbapenem resistance in a clinical isolate of Citrobacter freundii. Antimicrob. Agents Chemother. 41:23522354.
96. Martinez, J. L.,, E. Cercenado,, F. Baquero,, J. C. Perez-Díaz,, and A. Delgado-Iribarren. 1987. Incidence of aerobactin production in gram-negative hospital isolates. FEMS Microbiol. Lett. 43:351353.
97. McDaniel, T. K.,, K. G. Jarvis,, M. S. Donnenberg,, and J. B. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92:16641668.
98. Miki, K.,, K. Tamura,, R. Sakazaki,, and Y. Kosako. 1996. Respeciation of the original reference strains of serovars in the Citrobacter freundii (Bethesda-Ballerup Group) antigenic scheme of West and Edwards. Microbiol. Immunol. 40:915921.
99. Miller, J. M.,, and P. Alachi. 1996. Evaluation of a new computer-enhanced identification program for microorganisms: adaptation of BioBASE for identification of members of the family Enterobacteriaceae. J. Clin. Microbiol. 34:179181.
100. Miller, J. M.,, and D. L. Rhoden. 1991. Preliminary evaluation of Biolog, a carbon source utilization method for bacterial identification. J. Clin. Microbiol. 29:11431147.
101. Morgan, M. G.,, C. Stuart,, A. T. Leanord,, M. Enright,, and G. F. Cole. 1992. Citrobacter diversus brain abscess: case report and molecular epidemiology. J. Med. Microbiol. 36: 273278.
102. Morris, J. G., Jr.,, F.-Y. C. Lin,, C. B. Morrison,, R. J. Gross,, R. Khabbaz,, K. O. Maher,, B. Rowe,, E. Israel,, and J. P. Libonati. 1986. Molecular epidemiology of neonatal meningitis due to Citrobacter diversus: a study of isolates from hospitals in Maryland. J. Infect. Dis. 154:409414.
103. Müller, H. E. 1986. Occurrence and clinical significance of tyrosine clearing positive Citrobacter freundii in human faecal specimens. Zentbl. Bakteriol. Hyg. A 262:412416.
104. Müller, G. F.,, and H. Keller. 1992. Spondylitis durch Citrobacter diversus. 1992. Schweiz. Med. Wochenschr. 122:11731177.
105. Mundy, R.,, D. Pickard,, R. K. Wilson,, C. P. Simmons,, G. Dougan,, and G. Frankel. 2003. Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol. Microbiol. 48:795809.
106. Murphey, D. K.,, E. J. Septimus,, and D. C. Waagner. 1992. Catfish-related injury and infection: report of two cases and review of the literature. Clin. Infect. Dis. 14:689693.
107. Naas, T.,, D. Aubert,, N. Fortineau,, and P. Nordmann. 2002. Cloning and sequencing of the β-lactamase gene and surrounding DNA sequences of Citrobacter braakii, Citrobacter murliniae, Citrobacter werkmanii, Escherichia fergusonii and Enterobacer cancerogenus. FEMS Microbiol. Lett. 215:8187.
108. Nicolle, L. E. 2001. Urinary tract pathogens in complicated infection and in elderly individuals. J. Infect. Dis. 183(Suppl. 1):S5S8.
109. Novak, S. S.,, and R. A. Seigel. 1986. Gram-negative septicemia in American alligators (Alligator mississippiensis). J. Wildl. Dis. 22:484487.
110. Oelschlaeger, T. A.,, P. Guerry,, and D. J. Kopecko. 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA 90:68846888.
111. O’Hara, C. M.,, and J. M. Miller. 2003. Evaluation of the Vitek 2 ID-GNB assay for identification of members of the family Enterobacteriaceae and other nonenteric gramnegative bacilli and comparison with the Vitek GNI+ card. J. Clin. Microbiol. 41:20962101.
112. O’Hara, C. M.,, D. L. Rhoden,, and J. M. Miller. 1992. Reevaluation of the API 20E identification system versus conventional biochemicals for identification of members of the family Enterobacteriaceae: a new look at an old product. J. Clin. Microbiol. 30:123125.
113. O’Hara, C. M.,, S. B. Roman,, and J. M. Miller. 1995. Ability of commercial identification systems to identify newly recognized species of Citrobacter. J. Clin. Microbiol. 33:242245.
114. O’Hara, C. M.,, F. C. Tenover,, and J. M. Miller. 1993. Parallel comparison of accuracy of API 20E, Vitek GNI, MicroScan Walk/Away Rapid ID, and Becton Dickinson Cobas Micro ID-E/NF for identification of members of the family Enterobacteriaceae and common gram-negative, nonglucose-fermenting bacilli. J. Clin. Microbiol. 31:31653169.
115. O’Hara, C. M.,, G. L. Westbrook,, and J. M. Miller. 1997. Evaluation of Vitek GNI+ and Becton Dickinson Microbiology Systems Crystal E/NF identification systems for identification of members of the family Enterobacteriaceae and other gram-negative, glucose-fermenting and non-glucosefermenting bacilli. J. Clin. Microbiol. 35:32693273.
116. Papasian, C. J.,, J. Kinney,, S. Coffman,, R. J. Hollis,, and M. A. Pfaller. 1996. Transmission of Citrobacter koseri from mother to infant documented by ribotyping and pulsed-field gel electrophoresis. Diagn. Microbiol. Infect. Dis. 26:6367.
117. Parry, M. F.,, J. H. Hutchinson,, N. A. Brown,, C.-H. Wu,, and L. Estreller. 1980. Gram-negative sepsis in neonates: a nursery outbreak due to hand carriage of Citrobacter diversus. Pediatrics 65:11051109.
118. Pepperell, C.,, J. V. Kus,, M. A. Gardam,, A. Humar,, and L. L. Burrows. 2002. Low-virulence Citrobacter species encode resistance to multiple antimicrobials. Antimicrob. Agents Chemother. 46:35553560.
119. Pfaller, M. A.,, D. Sahm,, C. O’Hara,, C. Ciaglia,, M. Yu,, N. Yamane,, G. Scharnweber,, and D. Rhoden. 1991. Comparison of the AutoSCAN-W/A rapid bacterial identification system and the Vitek AutoMicrobic system for identification of gram-negative bacilli. J. Clin. Microbiol. 29:14221428.
120. Philippon, A.,, J. Dusart,, B. Joris,, and J.-M. Frère. 1998. The diversity, structure, and regulation of β-lactamases. Cell. Mol. Life Sci. 54:341346.
121. Prais, D.,, M. Nussinovitch,, L. Harel,, and J. Amir. 2003. Citrobacter koseri (diversus) meningitis in an otherwise healthy adolescent. Scand. J. Infect. Dis. 35:202204.
122. Raidal, S. R.,, M. Ohara,, R. P. Hobbs,, and R. I. Prince. 1998. Gram-negative bacterial infections and cardiovascular parasitism in green sea turtles (Chelonia mydas). Aust. Vet. J. 76:415417.
123. Rais-Bahrami, K.,, and B. L. Short. 2000. Citrobacter sepsis and severe newborn respiratory failure supported with extracorporeal membrane oxygenation. J. Perinatol. 4:265266.
124. Ratner, A. J.,, R. S. Mosca,, and H. A. Zucker. 2002. Citrobacter mediastinitis following surgery in a neonate. J. Infect. 44:5258.
125. Richard, C.,, B. Brisou,, and J. Lioult. 1972. Étude taxonomique de Levinea, nouveau genre de la famille des Entérobacteréries. Ann. Inst. Pasteur 122:11371146.
126. Richards, M. J.,, J. R. Edwards,, D. H. Culver,, R. P. Gaynes, and the National Nosocomial Infectious Surveillance System. 1999. Nosocomial infections in pediatric intensive care units in the United States. Pediatrics 103:e39.
127. Richards, M. J.,, J. R. Edwards,, D. H. Culver,, R. P. Gaynes, and the National Nosocomial Infections Surveillance System. 2000. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect. Control Hosp. Epidemiol. 21:510515.
128. Robinson, A.,, Y. S. McCarter,, J. Tetreault. 1995. Comparison of Crystal Enteric/Nonfermenter system, API 20E system, and Vitek Automicrobic system for identification of gram-negative bacilli. J. Clin. Microbiol. 33:364370.
129. Roberts, F. J. 1980. A review of positive blood cultures: identification and source of microorganisms and patterns of sensitivity to antibiotics. Rev. Infect. Dis. 2:329339.
130. Sakazaki, R., 1984. Genus IV. Citrobacter Werkman and Gillen 1932, 173AL, p. 458461. In N. R. Krieg, and J. G. Holt (ed.), Bergey’s Manual of Systematic Bacteriology, vol. 1. Williams & Wilkins, Baltimore, Md.
131. Samonis, G.,, E. Anaissie,, L. Elting,, and G. P. Bodey. 1991. Review of Citrobacter bacteremia in cancer patients over a sixteen-year period. Eur. J. Clin. Microbiol. Infect. Dis. 10:479485.
132. Sanguinetti, M.,, B. Posteraro,, T. Spanu,, D. Ciccaglione,, L. Romano,, B. Fiori,, G. Nicoletti,, S. Zanetti,, and G. Fadda. 2003. Characterization of clinical isolates of Enterobacteriaceae from Italy by the BD Phoenix extended-spectrum β-lactamase detection method. J. Clin. Microbiol. 41:14631468.
133. Schaberg, D. R.,, D. H. Culver,, and R. P. Gaynes. 1991. Major trends in the microbial etiology of nosocomial infection. Am. J. Med. 91:3B72S3B75S.
134. Schauer, D. B.,, and S. Falkow. 1993. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect. Immun. 61:24862492.
135. Schauer, D. B.,, and S. Falkow. 1993.The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissable murine colonic hyperplasia. Infect. Immun. 61:46544661.
136. Schauer, D. B.,, B. A. Zabel,, I. F. Pedraza,, C. M. O’Hara,, A. G. Steigerwalt,, and D. J. Brenner. 1995. Genetic and biochemical characterization of Citrobacter rodentium sp. nov. J. Clin. Microbiol. 33:20642068.
137. Schmidt, H.,, M. Montag,, J. Bockemühl,, J. Heesemann,, and H. Karch. 1993. Shiga-like toxin II-related cytotoxins in Citrobacter freundii strains from humans and beef samples. Infect. Immun. 61:534543.
138. Schubert, S.,, S. Cuenca,, D. Fischer,, and J. Heesemann. 2000. High-pathogenicity island of Yersinia pestis in Enterobacteriaceae isolated from blood cultures and urine samples: prevalence and functional expression. J. Infect. Dis. 182:12681271.
139. Sechter, I.,, G. Altmann,, D. Cahan,, I. Braunstein,, and C. B. Gerichter. 1981. Antigenic scheme of Citrobacter koseri. J. Clin. Microbiol. 14:620622.
140. Sedlák, J. 1973. Present knowledge and aspects of Citrobacter. Curr. Top. Microbiol. Immunol. 62:4159.
141. Sherley, M.,, D. M. Gordon,, and P. J. Collignon. 2003. Species differences in plasmid carriage in the Enterobacteriaceae. Plasmid 49:7985.
142. Shih, C.-C.,, Y.-C. Chen,, S.-C. Chang,, K.-T. Luh,, and W.-C. Hsieh. 1996. Bacteremia due to Citrobacter species: significance of primary intraabdominal infection. Clin. Infect. Dis. 23:543549.
143. Soriano, A. L.,, R. G. Russell,, D. Johnson,, R. Lagos,, I. Sechter,, and J. G. Morris, Jr. 1991. Pathophysiology of Citrobacter diversus neonatal meningitis: comparative studies in an infant mouse model. Infect. Immun. 59:13521358.
144. Sotto, A.,, J. C. Bernard,, C. Brunschwig,, D. Blin,, F. M. Lopez,, and B. Combe. 1994. Bifocal cervical spondylodiscitis due to Citrobacter diversus. Infection 22:423424.
145. Šourek, J.,, and E. Aldová. 1988. Importance of serological tests in the diagnosis of Citrobacter diversus and Citrobacter amalonaticus. Syst. Appl. Microbiol. 11:6066.
146. Spröer, C.,, U. Mendrock,, J. Swiderski,, E. Lang,, and E. Stackebrandt. 1999. The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. Int. J. Syst. Bacteriol. 49:14331438.
147. Straussberg, R.,, L. Harel,, and J. Amir. 2001. Long-term outcome of neonatal Citrobacter koseri (diversus) meningitis treated with imipenem/meropenem and surgical drainage. Infection 29:280282.
148. Sugandhi, R. P.,, V. K. Beena,, P. G. Shivananda,, and M. Baliga. 1992. Citrobacter sepsis in infants. Ind. J. Pediatr. 59:309312.
149. Tang, L.-M.,, S.-T. Chen,, and T.-N. Lui. 1994. Citrobacter meningitis in adults. Clin. Neurol. Neurosurg. 96:5257.
150. Tellez, I.,, G. S. Chrysant,, I. Omer,, and W. E. Dismukes. 2000. Citrobacter diversus endocarditis. Am. J. Med. Sci. 320:408410.
151. Thornsberry, C. 1994. Susceptibility of clinical bacterial isolates to ciprofloxacin in the United States. Infection 22(Suppl. 2):S80S89.
152. Thornton, S. M.,, S. Nolan,, and F. M. D. Gulland. 1998. Bacterial isolates from California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and northern elephant seals (Mirounga angustirostris) admitted to a rehabilitation center along the central California coast, 1994-1995. J. Zoo Wildl. Med. 29:171176.
153. Thurm, V.,, and B. Gericke. 1994. Identification of infant food as a vehicle in a nosocomial outbreak of Citrobacter freundii: epidemiological subtyping by alloenzyme, wholecell protein and antibiotic resistance. J. Appl. Bacteriol. 76:553558.
154. Toranzo, A. E.,, J. M. Cutrín,, B. S. Roberson,, S. Núñez,, J. M. Abell,, F. M. Hetrick,, and A. M. Baya. 1994. Comparison of the taxonomy, serology, drug resistance transfer, and virulence of Citrobacter freundii strains from mammals and poikilothermic hosts. Appl. Environ. Microbiol. 60:17891797.
155. Tschäpe, H.,, R. Prager,, W. Streckel,, A. Fruth,, E. Tietze,, and G. Böhme. 1995. Verotoxinogenic Citrobacter freundii associated with severe gastroenteritis and cases of haemolytic uraemic syndrome in a nursery school: green butter as the infection source. Epidemiol. Infect. 114:441450.
156. Visser, M. R.,, L. Bogaards,, M. Rozenberg-Arska,, and J. Verhoef. 1992. Comparison of the autoSCAN-W/A and Vitek Automicrobic systems for identification and susceptibility testing of bacteria. Eur. J. Clin. Microbiol. Infect. Dis. 11:979984.
157. Wang, H.,, S. Kelkar,, W. Wu,, M. Chen,, and J. P. Quinn. 2003. Clinical isolates of Enterobacteriaceae producing extendedspectrum βlactamases: prevalence of CTX-M-3 at a hospital in China. Antimicrob. Agents Chemother. 47:790793.
158. Warren, J. R.,, J. J. Farmer III,, F. E. Dewhirst,, K. Birkhead,, T. Zembower,, L. R. Peterson,, L. Sims,, and M. Bhattacharya. 2000. Outbreak of nosocomial infections due to extendedspectrum β-lactamase-producing strains of Enteric Group 137, a new member of the family Enterobacteriaceae closely related to Citrobacter farmeri and Citrobacter amalonaticus. J. Clin. Microbiol. 38:39463952.
159. Wayne, L. G. 1994. Actions of the Judicial Commission of the International Committee on Systematic Bacteriology on requests for opinions published between January 1985 and July 1993. Int. J. Syst. Bacteriol. 44:177178.
160. Werkman, C. H.,, and G. F. Gillen. 1932. Bacteria producing trimethylene glycol. J. Bacteriol. 23:167182.
161. Widrow, C. A.,, S. M. Kellie,, B. R. Saltzman,, and U. Mathur-Wagh. 1991. Pyomyositis in patients with the human immunodeficiency virus: an unusual form of disseminated bacterial infection. Am. J. Med. 91:129136.
162. Williams, W. W.,, J. Mariano,, M. Spurrier,, H. D. Donnell, Jr.,, R. I. Beckenridge, Jr.,, R. L. Anderson,, I. K. Wachsmuth,, C. Thornsberry,, D. R. Graham,, D. W. Thibeault,, and J. R. Allen. 1984. Nosocomial meningitis due to Citrobacter diversus in neonates: new aspects of the epidemiology. J. Infect. Dis. 150:229235.
163. Woods, C. R., Jr.,, E. O. Mason, Jr.,, and S. L. Kaplan. 1992. Interaction of Citrobacter diversus strains with HEp-2 epithelial and human umbilical vein endothelial cells. J. Infect. Dis. 166:10351044.
164. Woods, C. R., Jr.,, J. Versalovic,, T. Koeuth,, and J. R. Lupski. 1992. Analysis of relationships among isolates of Citrobacter diversus by using DNA fingerprints generated by repetitive sequence-based primers in the polymerase chain reaction. J. Clin. Microbiol. 30:29212929.
165. Yan, J.-J.,, W.-C. Ko,, C.-L. Chuang,, and J.-J. Wu. 2002. Metallo-β-lactamase-producing Enterobaceriaceae isolates in a university hospital in Taiwan: prevalence of IMP-8 in Enterobacter cloacae and first identification of VIM-2 in Citrobacter freundii. J. Antimicrob. Chemother. 50:503511.
166. York, M. K.,, G. F. Brooks,, and E. H. Fiss. 1992. Evaluation of the autoSCAN-W/A rapid system for identification and susceptibility testing of gram-negative fermentative bacilli. J. Clin. Microbiol. 30:29032910.
167. Young, V. M.,, D. M. Kenton,, B. J. Hobbs,, and M. R. Moody. 1971. Levinea, a new genus of the family Enterobacteriaceae. Int. J. Syst. Bacteriol. 21:5863.


Generic image for table
Table 1

Current taxonomic composition of the genus

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 2

Distribution of recently described species

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 3

Clinical presentations associated with infection

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 4

Presentations of meningitis

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 5

. Identification of species by selected commercial systemsa

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 6

Distinguishing biochemical characteristics of major groups within the genus

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 8

Biotypes of

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 7

Relative distribution of former members within the complex

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 9

Distinguishing features of enteric group 137 from and

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 10

Potential virulence factors operative in the genus sensu lato

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12
Generic image for table
Table 11

Antimicrobial susceptibility of species

Citation: Janda J, Abbott S. 2006. The Genus Citrobacter, p 181-204. In The Enterobacteria, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817541.ch12

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error