1887

Abstract

The genus consists of a diverse group of Gram-negative bacilli and comprises seven species: , , , , and are regarded as opportunistic pathogens, and have been implicated in newborn and infant infections, causing meningitis, necrotizing enterocolitis and bacteraemia or sepsis. virulence is believed to be due to multiple factors. Some strains were found to produce diarrhoea or cause significant fluid accumulation in suckling mice. Two iron acquisition systems ( and /), plasminogen activator gene (), a 17 kb type VI secretion system (T6SS), and a 27 kb filamentous haemagglutinin gene () and associated putative adhesins locus are harboured on a family of RepFIB-related plasmids (pESA3 and pCTU1), suggesting that these are common virulence plasmids; 98 % of 229 tested strains possessed these plasmids. Even though pESA3 and pCTU1 share a common backbone composed of the gene and and gene clusters, the presence of , T6SS and FHA loci depended on species, demonstrating a strong correlation with the presence of virulence traits, plasmid type and species. Other factors were observed, in that form biofilms, and show unusual resistance to heat, dry and acid stress growth conditions. The outer-membrane protein A is probably one of the best-characterized virulence markers of . Furthermore, it was reported that employ phosphatidylinositide 3-kinase/Akt signalling, which activates protein kinase C-α and impairs the host cell’s mitogen-activated protein kinase pathway, in order to invade cells. can also use immature dendritic cells and macrophages to escape the immune response. This review addresses the various virulence and environmental-adaptive characteristics possessed by members of the genus .

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.073742-0
2014-08-01
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/8/1023.html?itemId=/content/journal/jmm/10.1099/jmm.0.073742-0&mimeType=html&fmt=ahah

References

  1. Al-Nabulsi A. A. , Osaili T. M. , Elabedeen N. A. , Jaradat Z. W. , Shaker R. R. , Kheirallah K. A. , Tarazi Y. H. , Holley R. A. . ( 2011; ). Impact of environmental stress desiccation, acidity, alkalinity, heat or cold on antibiotic susceptibility of Cronobacter sakazakii . . Int J Food Microbiol 146:, 137–143. [CrossRef] [PubMed]
    [Google Scholar]
  2. Álvarez-Ordóñez A. , Begely M. , Clifford T. , Deasy T. , Coolins B. , Hill C. . ( 2014; ). Transposon mutagenesis reveals genes involved in osmotic stress and drying in Cronobacter sakazakii . . Food Res Int 55:, 45–54. [CrossRef]
    [Google Scholar]
  3. Arbatsky N. P. , Wang M. , Shashkov A. S. , Chizhov A. O. , Feng L. , Knirel Y. A. , Wang L. . ( 2010; ). Structure of the O-polysaccharide of Cronobacter sakazakii O2 with a randomly O-acetylated l-rhamnose residue. . Carbohydr Res 345:, 2090–2094. [CrossRef] [PubMed]
    [Google Scholar]
  4. Arbatsky N. P. , Wang M. , Daeva E. D. , Shashkov A. S. , Feng L. , Knirel Y. A. , Wang L. . ( 2011; ). Elucidation of the structure and characterization of the gene cluster of the O-antigen of Cronobacter sakazakii G2592, the reference strain of C. sakazakii O7 serotype. . Carbohydr Res 346:, 1169–1172. [CrossRef] [PubMed]
    [Google Scholar]
  5. Arroyo C. , Condón S. , Pagán R. . ( 2009; ). Thermobacteriological characterization of Enterobacter sakazakii . . Int J Food Microbiol 136:, 110–118. [CrossRef] [PubMed]
    [Google Scholar]
  6. Baldwin A. , Loughlin M. , Caubilla-Barron J. , Kucerova E. , Manning G. , Dowson C. , Forsythe S. . ( 2009; ). Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. . BMC Microbiol 9:, 223.[CrossRef]
    [Google Scholar]
  7. Bar-Oz B. , Preminger A. , Peleg O. , Block C. , Arad I. . ( 2001; ). Enterobacter sakazakii infection in the newborn. . Acta Paediatr 90:, 356–358. [CrossRef] [PubMed]
    [Google Scholar]
  8. Barron J. C. , Forsythe S. J. . ( 2007; ). Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. . J Food Prot 70:, 2111–2117.[PubMed]
    [Google Scholar]
  9. Baumgartner A. , Grand M. , Liniger M. , Iversen C. . ( 2009; ). Detection and frequency of Cronobacter spp. (Enterobacter sakazakii) in different categories of ready-to-eat foods other than infant formula. . Int J Food Microbiol 136:, 189–192.[CrossRef]
    [Google Scholar]
  10. Beuchat L. R. , Kim H. , Gurtler J. B. , Lin L. C. , Ryu J. H. , Richards G. M. . ( 2009; ). Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. . Int J Food Microbiol 136:, 204–213.[CrossRef]
    [Google Scholar]
  11. Biering G. , Karlsson S. , Clark N. C. , Jónsdóttir K. E. , Lúdvígsson P. , Steingrímsson O. . ( 1989; ). Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. . J Clin Microbiol 27:, 2054–2056.[PubMed]
    [Google Scholar]
  12. Bowen A. B. , Braden C. R. . ( 2006; ). Invasive Enterobacter sakazakii disease in infants. . Emerg Infect Dis 12:, 1185–1189. [CrossRef] [PubMed]
    [Google Scholar]
  13. Brady C. , Cleenwerck I. , Venter S. , Coutinho T. , De Vos P. . ( 2013; ). Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): Proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter . . Syst Appl Microbiol 36:, 309–319.[CrossRef]
    [Google Scholar]
  14. Breeuwer P. , Lardeau A. , Peterz M. , Joosten H. M. . ( 2003; ). Desiccation and heat tolerance of Enterobacter sakazakii . . J Appl Microbiol 95:, 967–973. [CrossRef] [PubMed]
    [Google Scholar]
  15. Burgos J. , Varela M. . ( 2002; ). Multiple antibiotic resistant dairy soil bacteria. Abstracts of the 102nd General Meeting of the American Society for Microbiology; Salt Palace Convention Center, May 19–23, 2002, Session 25, Paper A-31. American Society for Microbiology. .
    [Google Scholar]
  16. Carter L. , Lindsey L. A. , Grim C. J. , Sathyamoorthy V. , Jarvis K. G. , Gopinath G. , Lee C. , Sadowski J. A. , Trach L. et al. ( 2013; ). Multiplex PCR assay targeting a diguanylate cyclase-encoding gene, cgcA, to differentiate species within the genus Cronobacter . . Appl Environ Microbiol 79:, 734–737. [CrossRef] [PubMed]
    [Google Scholar]
  17. Caubilla-Barron J. , Hurrell E. , Townsend S. , Cheetham P. , Loc-Carrillo C. , Fayet O. , Prère M. F. , Forsythe S. J. . ( 2007; ). Genotypic and phenotypic analysis of Enterobacter sakazakii strains from an outbreak resulting in fatalities in a neonatal intensive care unit in France. . J Clin Microbiol 45:, 3979–3985. [CrossRef] [PubMed]
    [Google Scholar]
  18. CDC ( 2009; ). Cronobacter species isolation in two infants – New Mexico, 2008. . MMWR Morb Mortal Wkly Rep 58:, 1179–1183.[PubMed]
    [Google Scholar]
  19. Cetin S. , Ford H. R. , Sysko L. R. , Agarwal C. , Wang J. , Neal M. D. , Baty C. , Apodaca G. , Hackam D. J. . ( 2004; ). Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. . J Biol Chem 279:, 24592–24600. [CrossRef] [PubMed]
    [Google Scholar]
  20. Cetinkaya E. , Joseph S. , Ayhan K. , Forsythe S. J. . ( 2013; ). Comparison of methods for the microbiological identification and profiling of Cronobacter species from ingredients used in the preparation of infant formula. . Mol Cell Probes 27:, 60–64. [CrossRef] [PubMed]
    [Google Scholar]
  21. Chap J. , Jackson P. , Siqueira R. , Gaspar N. , Quintas C. , Park J. , Osaili T. , Shaker R. , Jaradat Z. . & other authors ( 2009; ). International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. . Int J Food Microbiol 136:, 185–188. [CrossRef]
    [Google Scholar]
  22. Chenu J. W. , Cox J. M. . ( 2009; ). Cronobacter (‘Enterobacter sakazakii’): current status and future prospects. . Lett Appl Microbiol 49:, 153–159. [CrossRef] [PubMed]
    [Google Scholar]
  23. Cruz A. , Xicohtencatl-Cortes J. , González-Pedrajo B. , Bobadilla M. , Eslava C. , Rosas I. . ( 2011; ). Virulence traits in Cronobacter species isolated from different sources. . Can J Microbiol 57:, 735–744. [CrossRef] [PubMed]
    [Google Scholar]
  24. Cruz-Córdova A. , Rocha-Ramírez L. M. , Ochoa S. A. , González-Pedrajo B. , Espinosa N. , Eslava C. , Hernández-Chiñas U. , Mendoza-Hernández G. , Rodríguez-Leviz A. et al. ( 2012; ). Flagella from five Cronobacter species induce pro-inflammatory cytokines in macrophage derivatives from human monocytes. . PLoS ONE 7:, e52091. [CrossRef] [PubMed]
    [Google Scholar]
  25. Dancer G. I. , Mah J. H. , Rhee M. S. , Hwang I. G. , Kang D. H. . ( 2009; ). Resistance of Enterobacter sakazakii (Cronobacter spp.) to environmental stresses. . J Appl Microbiol 107:, 1606–1614. [CrossRef] [PubMed]
    [Google Scholar]
  26. Edelson-Mammel S. G. , Porteous M. K. , Buchanan R. L. . ( 2005; ). Survival of Enterobacter sakazakii in a dehydrated powdered infant formula. . J Food Prot 68:, 1900–1902.[PubMed]
    [Google Scholar]
  27. Edelson-Mammel S. , Porteous M. , Buchanan R. . ( 2006; ). Acid resistance of twelve strains of Enterobacter sakazakii, and the impact of habituating the cells to an acidic environment. . J Food Sci 71:, 201–207. [CrossRef]
    [Google Scholar]
  28. Emami C. N. , Mittal R. , Wang L. , Ford H. R. , Prasadarao N. V. . ( 2011; ). Recruitment of dendritic cells is responsible for intestinal epithelial damage in the pathogenesis of necrotizing enterocolitis by Cronobacter sakazakii . . J Immunol 186:, 7067–7079. [CrossRef] [PubMed]
    [Google Scholar]
  29. Emami C. N. , Mittal R. , Wang L. , Ford H. R. , Prasadarao N. V. . ( 2012; ). Role of neutrophils and macrophages in the pathogenesis of necrotizing enterocolitis caused by Cronobacter sakazakii . . J Surg Res 172:, 18–28. [CrossRef] [PubMed]
    [Google Scholar]
  30. FAO/WHO ( 2006; ). Enterobacter sakazakii and Salmonella in Powdered Infant Formula (Meeting Report). Microbiological Risk Assessment Series 10. Rome:: Food and Agriculture Organization of the United Nations/World Health Organization;.
    [Google Scholar]
  31. FAO/WHO ( 2008; ). Enterobacter sakazakii (Cronobacter spp.) in Powdered Follow-Up Formulae. Microbiological Risk Assessment Series 15. Rome:: Food and Agriculture Organization of the United Nations/World Health Organization;.
    [Google Scholar]
  32. Feeney A. , Sleator R. D. . ( 2011; ). An in silico analysis of osmotolerance in the emerging gastrointestinal pathogen Cronobacter sakazakii . . Bioeng Bugs 2:, 260–270. [CrossRef] [PubMed]
    [Google Scholar]
  33. Flores J. P. , Medrano S. A. , Sánchez J. S. , Fernández-Escartín E. . ( 2011; ). Two cases of hemorrhagic diarrhea caused by Cronobacter sakazakii in hospitalized nursing infants associated with the consumption of powdered infant formula. . J Food Prot 74:, 2177–2181. [CrossRef] [PubMed]
    [Google Scholar]
  34. Franco A. A. , Kothary M. H. , Gopinath G. , Jarvis K. G. , Grim C. J. , Hu L. , Datta A. R. , McCardell B. A. , Tall B. D. . ( 2011a; ). Cpa, the outer membrane protease of Cronobacter sakazakii, activates plasminogen and mediates resistance to serum bactericidal activity. . Infect Immun 79:, 1578–1587. [CrossRef] [PubMed]
    [Google Scholar]
  35. Franco A. A. , Hu L. , Grim C. J. , Gopinath G. , Sathyamoorthy V. , Jarvis K. G. , Lee C. , Sadowski J. , Kim J. et al. ( 2011b; ). Characterization of putative virulence genes on the related RepFIB plasmids harbored by Cronobacter spp. . Appl Environ Microbiol 77:, 3255–3267. [CrossRef] [PubMed]
    [Google Scholar]
  36. Friedemann M. . ( 2007; ). Enterobacter sakazakii in food and beverages (other than infant formula and milk powder). . Int J Food Microbiol 116:, 1–10. [CrossRef] [PubMed]
    [Google Scholar]
  37. Friedemann M. . ( 2009; ). Epidemiology of invasive neonatal Cronobacter (Enterobacter sakazakii) infections. . Eur J Clin Microbiol Infect Dis 28:, 1297–1304. [CrossRef] [PubMed]
    [Google Scholar]
  38. Gajdosova J. , Benedikovicova K. , Kamodyova N. , Tothova L. , Kaclikova E. , Stuchlik S. , Turna J. , Drahovska H. . ( 2011; ). Analysis of the DNA region mediating increased thermotolerance at 58°C in Cronobacter sp. and other enterobacterial strains. . Antonie van Leeuwenhoek 100:, 279–289. [CrossRef] [PubMed]
    [Google Scholar]
  39. Giri C. P. , Shima K. , Tall B. D. , Curtis S. , Sathyamoorthy V. , Hanisch B. , Kim K. S. , Kopecko D. J. . ( 2012; ). Cronobacter spp. (previously Enterobacter sakazakii) invade and translocate across both cultured human intestinal epithelial cells and human brain microvascular endothelial cells. . Microb Pathog 52:, 140–147. [CrossRef] [PubMed]
    [Google Scholar]
  40. Gosney M. A. , Martin M. V. , Wright A. E. , Gallagher M. . ( 2006; ). Enterobacter sakazakii in the mouths of stroke patients and its association with aspiration pneumonia. . Eur J Intern Med 17:, 185–188. [CrossRef] [PubMed]
    [Google Scholar]
  41. Grim C. J. , Kotewicz M. L. , Power K. A. , Gopinath G. , Franco A. A. , Jarvis K. G. , Yan Q. Q. , Jackson S. A. , Sathyamoorthy V. et al. ( 2013; ). Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation. . BMC Genomics 14:, 366. [CrossRef] [PubMed]
    [Google Scholar]
  42. Grishin A. , Papillon S. , Bell B. , Wang J. , Ford H. R. . ( 2013; ). The role of the intestinal microbiota in the pathogenesis of necrotizing enterocolitis. . Semin Pediatr Surg 22:, 69–75. [CrossRef] [PubMed]
    [Google Scholar]
  43. Gurtler J. B. , Beuchat L. R. . ( 2007; ). Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. . J Food Prot 70:, 1579–1586.[PubMed]
    [Google Scholar]
  44. Hamby S. E. , Joseph S. , Forsythe S. J. , Chuzhanova N. . ( 2011; ). In silico identification of pathogenic strains of Cronobacter from biochemical data reveals association of inositol fermentation with pathogenicity. . BMC Microbiol 11:, 204. [CrossRef] [PubMed]
    [Google Scholar]
  45. Hariri S. , Joseph S. , Forsythe S. J. . ( 2013; ). Cronobacter sakazakii ST4 strains and neonatal meningitis, United States. . Emerg Infect Dis 19:, 175–177. [CrossRef] [PubMed]
    [Google Scholar]
  46. Hartmann I. , Carranza P. , Lehner A. , Stephan R. , Eberl L. , Riedel K. . ( 2010; ). Genes involved in Cronobacter sakazakii biofilm formation. . Appl Environ Microbiol 76:, 2251–2261. [CrossRef] [PubMed]
    [Google Scholar]
  47. Healy B. , Cooney S. , O’Brien S. , Iversen C. , Whyte P. , Nally J. , Callanan J. J. , Fanning S. . ( 2010; ). Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. . Foodborne Pathog Dis 7:, 339–350. [CrossRef] [PubMed]
    [Google Scholar]
  48. Himelright I. , Harris E. , Lorch V. , Anderson M. , Jones T. , Craig A. , Kuehnert M. , Forster T. , Arduino M. . Centers for Disease Control and Prevention ( 2002; ). Enterobacter sakazakii infections associated with the use of powdered infant formula – Tennessee, 2001. . MMWR Morb Mortal Wkly Rep 51:, 297–300.[PubMed]
    [Google Scholar]
  49. Hochel I. , Růžičková H. , Krásný L. , Demnerová K. . ( 2012; ). Occurrence of Cronobacter spp. in retail foods. . J Appl Microbiol 112:, 1257–1265. [CrossRef] [PubMed]
    [Google Scholar]
  50. Holý O. , Forsythe S. . ( 2014; ). Cronobacter spp. as emerging causes of healthcare-associated infection. . J Hosp Infect 86:, 169–177. [CrossRef] [PubMed]
    [Google Scholar]
  51. Hunter C. J. , Bean J. F. . ( 2013; ). Cronobacter: an emerging opportunistic pathogen associated with neonatal meningitis, sepsis and necrotizing enterocolitis. . J Perinatol 33:, 581–585. [CrossRef] [PubMed]
    [Google Scholar]
  52. Hunter C. J. , Williams M. , Petrosyan M. , Guner Y. , Mittal R. , Mock D. , Upperman J. S. , Ford H. R. , Prasadarao N. V. . ( 2009; ). Lactobacillus bulgaricus prevents intestinal epithelial cell injury caused by Enterobacter sakazakii-induced nitric oxide both in vitro and in the newborn rat model of necrotizing enterocolitis. . Infect Immun 77:, 1031–1043. [CrossRef] [PubMed]
    [Google Scholar]
  53. Iversen C. , Lane M. , Forsythe S. J. . ( 2004; ). The growth profile, thermotolerance and biofilm formation of Enterobacter sakazakii grown in infant formula milk. . Lett Appl Microbiol 38:, 378–382. [CrossRef] [PubMed]
    [Google Scholar]
  54. Iversen C. , Lehner A. , Mullane N. , Bidlas E. , Cleenwerck I. , Marugg J. , Fanning S. , Stephan R. , Joosten H. . ( 2007; ). The taxonomy of Enterobacter sakazakii: proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov., Cronobacter sakazakii subsp. sakazakii comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies 1. . BMC Evol Biol 7:, 64. [CrossRef] [PubMed]
    [Google Scholar]
  55. Iversen C. , Mullane N. , McCardell B. , Tall B. D. , Lehner A. , Fanning S. , Stephan R. , Joosten H. . ( 2008a; ). Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov. and Cronobacter dublinensis subsp. lactaridi subsp. nov.. Int J Syst Evol Microbiol 58:, 1442–1447. [CrossRef] [PubMed]
    [Google Scholar]
  56. Iversen C. , Druggan P. , Schumacher S. , Lehner A. , Feer C. , Gschwend K. , Joosten H. , Stephan R. . ( 2008b; ). Development of a novel screening method for the isolation of “Cronobacter” spp. (Enterobacter sakazakii). . Appl Environ Microbiol 74:, 2550–2553. [CrossRef] [PubMed]
    [Google Scholar]
  57. Jaradat Z. W. , Bhunia A. K. . ( 2003; ). Adhesion, invasion, and translocation characteristics of Listeria monocytogenes serotypes in Caco-2 cell and mouse models. . Appl Environ Microbiol 69:, 3640–3645. [CrossRef] [PubMed]
    [Google Scholar]
  58. Jaradat Z. W. , Ababneh Q. O. , Saadoun I. M. , Samara N. A. , Rashdan A. M. . ( 2009; ). Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from infant food, herbs and environmental samples and the subsequent identification and confirmation of the isolates using biochemical, chromogenic assays, PCR and 16S rRNA sequencing. . BMC Microbiol 9:, 225. [CrossRef] [PubMed]
    [Google Scholar]
  59. Jaradat Z. W. , Rashdan A. M. , Ababneh Q. O. , Jaradat S. A. , Bhunia A. K. . ( 2011; ). Characterization of surface proteins of Cronobacter muytjensii using monoclonal antibodies and MALDI-TOF mass spectrometry. . BMC Microbiol 11:, 148. [CrossRef] [PubMed]
    [Google Scholar]
  60. Jarvis K. G. , Grim C. J. , Franco A. A. , Gopinath G. , Sathyamoorthy V. , Hu L. , Sadowski J. A. , Lee C. S. , Tall B. D. . ( 2011; ). Molecular characterization of Cronobacter lipopolysaccharide O-antigen gene clusters and development of serotype-specific PCR assays. . Appl Environ Microbiol 77:, 4017–4026. [CrossRef] [PubMed]
    [Google Scholar]
  61. Jarvis K. G. , Yan Q. Q. , Grim C. J. , Power K. A. , Franco A. A. , Hu L. , Gopinath G. , Sathyamoorthy V. , Kotewicz M. L. et al. ( 2013; ). Identification and characterization of five new molecular serogroups of Cronobacter spp. . Foodborne Pathog Dis 10:, 343–352. [CrossRef] [PubMed]
    [Google Scholar]
  62. Jo S. H. , Baek S. B. , Ha J. H. , Ha S. D. . ( 2010; ). Maturation and survival of Cronobacter biofilms on silicone, polycarbonate, and stainless steel after UV light and ethanol immersion treatments. . J Food Prot 73:, 952–956.[PubMed]
    [Google Scholar]
  63. Johler S. , Stephan R. , Hartmann I. , Kuehner K. A. , Lehner A. . ( 2010; ). Genes involved in yellow pigmentation of Cronobacter sakazakii ES5 and influence of pigmentation on persistence and growth under environmental stress. . Appl Environ Microbiol 76:, 1053–1061. [CrossRef] [PubMed]
    [Google Scholar]
  64. Joseph S. , Forsythe S. J. . ( 2011; ). Predominance of Cronobacter sakazakii sequence type 4 in neonatal infections. . Emerg Infect Dis 17:, 1713–1715. [CrossRef] [PubMed]
    [Google Scholar]
  65. Joseph S. , Sonbol H. , Hariri S. , Desai P. , McClelland M. , Forsythe S. J. . ( 2012a; ). Diversity of the Cronobacter genus as revealed by multilocus sequence typing. . J Clin Microbiol 50:, 3031–3039. [CrossRef] [PubMed]
    [Google Scholar]
  66. Joseph S. , Cetinkaya E. , Drahovska H. , Levican A. , Figueras M. J. , Forsythe S. J. . ( 2012b; ). Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. . Int J Syst Evol Microbiol 62:, 1277–1283. [CrossRef] [PubMed]
    [Google Scholar]
  67. Joseph S. , Desai P. , Ji Y. , Cummings C. A. , Shih R. , Degoricija L. , Rico A. , Brzoska P. , Hamby S. E. et al. ( 2012c; ). Comparative analysis of genome sequences covering the seven Cronobacter species. . PLoS ONE 7:, e49455. [CrossRef] [PubMed]
    [Google Scholar]
  68. Joseph S. , Hariri S. , Forsythe S. J. . ( 2013a; ). Lack of continuity between Cronobacter biotypes and species as determined using multilocus sequence typing. . Mol Cell Probes 27:, 137–139. [CrossRef] [PubMed]
    [Google Scholar]
  69. Joseph S. , Hariri S. , Masood N. , Forsythe S. J. . ( 2013b; ). Sialic acid utilization by Cronobacter sakazakii. . Microb Inform Exp 3:, 3. [CrossRef] [PubMed]
    [Google Scholar]
  70. Kandhai M. C. , Reij M. W. , Gorris L. G. M. , Guillaume-Gentil O. , van Schothorst M. . ( 2004; ). Occurrence of Enterobacter sakazakii in food production environments and households. . Lancet 363:, 39–40. [CrossRef] [PubMed]
    [Google Scholar]
  71. Kilonzo-Nthenge A. , Chen F. C. , Godwin S. L. . ( 2008; ). Occurrence of Listeria and Enterobacteriaceae in domestic refrigerators. . J Food Prot 71:, 608–612. [CrossRef] [PubMed]
    [Google Scholar]
  72. Kim K. P. , Loessner M. J. . ( 2008; ). Enterobacter sakazakii invasion in human intestinal Caco-2 cells requires the host cell cytoskeleton and is enhanced by disruption of tight junction. . Infect Immun 76:, 562–570. [CrossRef] [PubMed]
    [Google Scholar]
  73. Kim H. , Ryu J. H. , Beuchat L. R. . ( 2006; ). Attachment of and biofilm formation by Enterobacter sakazakii on stainless steel and enteral feeding tubes. . Appl Environ Microbiol 72:, 5846–5856. [CrossRef] [PubMed]
    [Google Scholar]
  74. Kim H. , Ryu J. H. , Beuchat L. R. . ( 2007; ). Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm. . Appl Environ Microbiol 73:, 1256–1265. [CrossRef] [PubMed]
    [Google Scholar]
  75. Kim K. , Jang S. S. , Kim S. K. , Park J. H. , Heu S. , Ryu S. . ( 2008; ). Prevalence and genetic diversity of Enterobacter sakazakii in ingredients of infant foods. . Int J Food Microbiol 122:, 196–203. [CrossRef] [PubMed]
    [Google Scholar]
  76. Kim K. , Kim K. P. , Choi J. , Lim J. A. , Lee J. , Hwang S. , Ryu S. . ( 2010; ). Outer membrane proteins A (OmpA) and X (OmpX) are essential for basolateral invasion of Cronobacter sakazakii . . Appl Environ Microbiol 76:, 5188–5198. [CrossRef] [PubMed]
    [Google Scholar]
  77. Kotewicz M. L. , Tall B. D. . ( 2009; ). Optical maps of subgroups of Cronobacter (formerly Enterobacter sakazakii) show large chromosomal regions of homology and differences among isolates. 1st International Conference on Cronobacter . , Poster Abstract 60, Dublin, Ireland:.
  78. Kothary M. H. , McCardell B. A. , Frazar C. D. , Deer D. , Tall B. D. . ( 2007; ). Characterization of the zinc-containing metalloprotease encoded by zpx and development of a species-specific detection method for Enterobacter sakazakii . . Appl Environ Microbiol 73:, 4142–4151. [CrossRef] [PubMed]
    [Google Scholar]
  79. Kucerova E. , Clifton S. W. , Xia X. Q. , Long F. , Porwollik S. , Fulton L. , Fronick C. , Minx P. , Kyung K. et al. ( 2010; ). Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. . PLoS ONE 5:, e9556. [CrossRef] [PubMed]
    [Google Scholar]
  80. Lai K. K. . ( 2001; ). Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. . Medicine (Baltimore) 80:, 113–122. [CrossRef] [PubMed]
    [Google Scholar]
  81. Lampel K. A. , Chen Y. . ( 2009; ). Method for the isolation and detection of Enterobacter sakazakii (Cronobacter) from powdered infant formula. . Int J Food Microbiol 136:, 179–184.[CrossRef]
    [Google Scholar]
  82. Lee Y. , Parka J. , Chang H. . ( 2012; ). Detection, antibiotic susceptibility and biofilm formation of Cronobacter spp. from various foods in Korea. . Food Contr 24:, 225–230. [CrossRef]
    [Google Scholar]
  83. Lehner A. , Riedel K. , Eberl L. , Breeuwer P. , Diep B. , Stephan R. . ( 2005; ). Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. . J Food Prot 68:, 2287–2294.[PubMed]
    [Google Scholar]
  84. Li Q. , Zhao W. D. , Zhang K. , Fang W. G. , Hu Y. , Wu S. H. , Chen Y. H. . ( 2010; ). PI3K-dependent host cell actin rearrangements are required for Cronobacter sakazakii invasion of human brain microvascular endothelial cells. . Med Microbiol Immunol (Berl) 199:, 333–340. [CrossRef] [PubMed]
    [Google Scholar]
  85. Lin L. C. , Beuchat L. R. . ( 2007; ). Survival of Enterobacter sakazakii in infant cereal as affected by composition, water activity, and temperature. . Food Microbiol 24:, 767–777. [CrossRef] [PubMed]
    [Google Scholar]
  86. Liu D. X. , Zhao W. D. , Fang W. G. , Chen Y. H. . ( 2012a; ). cPLA2α-mediated actin rearrangements downstream of the Akt signaling is required for Cronobacter sakazakii invasion into brain endothelial cells. . Biochem Biophys Res Commun 417:, 925–930. [CrossRef] [PubMed]
    [Google Scholar]
  87. Liu Q. , Mittal R. , Emami C. N. , Iversen C. , Ford H. R. , Prasadarao N. V. . ( 2012b; ). Human isolates of Cronobacter sakazakii bind efficiently to intestinal epithelial cells in vitro to induce monolayer permeability and apoptosis. . J Surg Res 176:, 437–447. [CrossRef] [PubMed]
    [Google Scholar]
  88. Liu L. , Yang Y. , Cui J. , Liu L. , Liu H. , Hu G. , Shi Y. , Li J. . ( 2013; ). Evaluation and implementation of a membrane filter method for Cronobacter detection in drinking water. . FEMS Microbiol Lett 344:, 60–68. [CrossRef]
    [Google Scholar]
  89. MacLean L. L. , Pagotto F. , Farber J. M. , Perry M. B. . ( 2009; ). Structure of the antigenic repeating pentasaccharide unit of the LPS O-polysaccharide of Cronobacter sakazakii implicated in the Tennessee outbreak. . Biochem Cell Biol 87:, 459–465. [CrossRef] [PubMed]
    [Google Scholar]
  90. Mange J. P. , Stephan R. , Borel N. , Wild P. , Kim K. S. , Pospischil A. , Lehner A. . ( 2006; ). Adhesive properties of Enterobacter sakazakii to human epithelial and brain microvascular endothelial cells. . BMC Microbiol 6:, 58. [CrossRef] [PubMed]
    [Google Scholar]
  91. Masood N. , Moore K. , Farbos A. , Hariri S. , Paszkiewicz K. , Dickins B. , McNally A. , Forsythe S. , Forsythe S. . ( 2013a; ). Draft genome sequence of earliest Cronobacter sakazakii sequence type 4 strain, NCIMB 8272. . Genome Announc 1:, e00782-13. [CrossRef] [PubMed]
    [Google Scholar]
  92. Masood N. , Moore K. , Farbos A. , Hariri S. , Block C. , Paszkiewicz K. , Dickins B. , McNally A. , Forsythe S. . ( 2013b; ). Draft genome sequence of a meningitic isolate of Cronobacter sakazakii clonal complex 4 strain 8399. . Genome Announc 1:, e00833-13. [CrossRef] [PubMed]
    [Google Scholar]
  93. Masood N. , Moore K. , Farbos A. , Hariri S. , Paszkiewicz K. , Dickins B. , McNally A. , Forsythe S. . ( 2013c; ). Draft genome sequences of three newly identified species in the genus Cronobacter, C. helveticus LMG23732, C. pulveris LMG24059, and C. zurichensis LMG23730. . Genome Announc 1:, e00783-13. [CrossRef] [PubMed]
    [Google Scholar]
  94. Mittal R. , Wang Y. , Hunter C. J. , Gonzalez-Gomez I. , Prasadarao N. V. . ( 2009a; ). Brain damage in newborn rat model of meningitis by Enterobacter sakazakii: a role for outer membrane protein A. . Lab Invest 89:, 263–277. [CrossRef] [PubMed]
    [Google Scholar]
  95. Mittal R. , Bulgheresi S. , Emami C. , Prasadarao N. V. . ( 2009b; ). Enterobacter sakazakii targets DC-SIGN to induce immunosuppressive responses in dendritic cells by modulating MAPKs. . J Immunol 183:, 6588–6599. [CrossRef] [PubMed]
    [Google Scholar]
  96. Molloy C. , Cagney C. , O’Brien S. , Iversen C. , Fanning S. , Duffy G. . ( 2009; ). Surveillance and characterisation by Pulsed-Field Gel Electrophoresis of Cronobacter spp. in farming and domestic environments, food production animals and retail foods. . Int J Food Microbiol 136:, 198–203.[CrossRef]
    [Google Scholar]
  97. Mullane N. R. , O’Gaora P. , Nally J. E. , Iversen C. , Whyte P. , Wall P. G. , Fanning S. . ( 2008; ). Molecular analysis of the Enterobacter sakazakii O-antigen gene locus. . Appl Environ Microbiol 74:, 3783–3794. [CrossRef] [PubMed]
    [Google Scholar]
  98. Müller A. , Stephan R. , Fricker-Feer C. , Lehner A. G. . ( 2013; ). Genetic diversity of Cronobacter sakazakii isolates collected from a Swiss infant formula production facility. . J Food Prot 76:, 883–887. [CrossRef] [PubMed]
    [Google Scholar]
  99. Muytjens H. L. , van der Ros-van de Repe J. . ( 1986; ). Comparative in vitro susceptibilities of eight Enterobacter species, with special reference to Enterobacter sakazakii . . Antimicrob Agents Chemother 29:, 367–370. [CrossRef] [PubMed]
    [Google Scholar]
  100. Nair M. K. , Venkitanarayanan K. . ( 2007; ). Role of bacterial OmpA and host cytoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii . . Pediatr Res 62:, 664–669. [CrossRef] [PubMed]
    [Google Scholar]
  101. Nair M. K. , Venkitanarayanan K. , Silbart L. K. , Kim K. S. . ( 2009; ). Outer membrane protein A (OmpA) of Cronobacter sakazakii binds fibronectin and contributes to invasion of human brain microvascular endothelial cells. . Foodborne Pathog Dis 6:, 495–501. [CrossRef] [PubMed]
    [Google Scholar]
  102. Nazarowec-White M. , Farber J. M. . ( 1997; ). Thermal resistance of Enterobacter sakazakii in reconstituted dried-infant formula. . Lett Appl Microbiol 24:, 9–13. [CrossRef] [PubMed]
    [Google Scholar]
  103. Nazarowec-White M. , Farber J. M. . ( 1999; ). Phenotypic and genotypic typing of food and clinical isolates of Enterobacter sakazakii . . J Med Microbiol 48:, 559–567. [CrossRef] [PubMed]
    [Google Scholar]
  104. Noriega F. R. , Kotloff K. L. , Martin M. A. , Schwalbe R. S. . ( 1990; ). Nosocomial bacteremia caused by Enterobacter sakazakii and Leuconostoc mesenteroides resulting from extrinsic contamination of infant formula. . Pediatr Infect Dis J 9:, 447–449. [CrossRef] [PubMed]
    [Google Scholar]
  105. Osaili T. , Forsythe S. . ( 2009; ). Desiccation resistance and persistence of Cronobacter species in infant formula. . Int J Food Microbiol 136:, 214–220.[CrossRef]
    [Google Scholar]
  106. Osaili T. M. , Shaker R. R. , Al-Haddaq M. S. , Al-Nabulsi A. A. , Holley R. A. . ( 2009; ). Heat resistance of Cronobacter species (Enterobacter sakazakii) in milk and special feeding formula. . J Appl Microbiol 107:, 928–935. [CrossRef] [PubMed]
    [Google Scholar]
  107. Pagotto F. J. , Nazarowec-White M. , Bidawid S. , Farber J. M. . ( 2003; ). Enterobacter sakazakii: infectivity and enterotoxin production in vitro and in vivo . . J Food Prot 66:, 370–375.[PubMed]
    [Google Scholar]
  108. Pitout J. D. , Moland E. S. , Sanders C. C. , Thomson K. S. , Fitzsimmons S. R. . ( 1997; ). Beta-lactamases and detection of beta-lactam resistance in Enterobacter spp. . Antimicrob Agents Chemother 41:, 35–39.[PubMed]
    [Google Scholar]
  109. Raghav M. , Aggarwal P. K. . ( 2007; ). Purification and characterization of Enterobacter sakazakii enterotoxin. . Can J Microbiol 53:, 750–755. [CrossRef] [PubMed]
    [Google Scholar]
  110. Ravishankar S. , Juneja V. K. . ( 2003; ). Adaptation or resistance responses of microorganisms to stresses in the food processing environment. . In Microbial Stress Adaptation and Food Safety, pp. 105–158. Edited by Yousef A. E. , Juneja V. K. . . Boca Raton, FL:: CRC Press;.
    [Google Scholar]
  111. Schmid M. , Iversen C. , Gontia I. , Stephan R. , Hofmann A. , Hartmann A. , Jha B. , Eberl L. , Riedel K. , Lehner A. . ( 2009; ). Evidence for a plant-associated natural habitat for Cronobacter spp.. Res Microbiol 160:, 608–614. [CrossRef] [PubMed]
    [Google Scholar]
  112. Schwizer S. , Tasara T. , Zurfluh K. , Stephan R. , Lehner A. . ( 2013; ). Identification of genes involved in serum tolerance in the clinical strain Cronobacter sakazakii ES5. . BMC Microbiol 13:, 38. [CrossRef] [PubMed]
    [Google Scholar]
  113. See K. C. , Than H. A. , Tang T. . ( 2007; ). Enterobacter sakazakii bacteraemia with multiple splenic abscesses in a 75-year-old woman: a case report. . Age Ageing 36:, 595–596. [CrossRef] [PubMed]
    [Google Scholar]
  114. Shashkov A. S. , Arbatsky N. P. , Knirel Y. A. . ( 2011; ). Structures and genetics of Kdo-containing O-antigens of Cronobacter sakazakii G2706 and G2704, the reference strains of serotypes O5 and O6. . Carbohydr Res 346:, 1924–1929. [CrossRef] [PubMed]
    [Google Scholar]
  115. Singamsetty V. K. , Wang Y. , Shimada H. , Prasadarao N. V. . ( 2008; ). Outer membrane protein A expression in Enterobacter sakazakii is required to induce microtubule condensation in human brain microvascular endothelial cells for invasion. . Microb Pathog 45:, 181–191. [CrossRef] [PubMed]
    [Google Scholar]
  116. Siqueira Santos R. F. , da Silva N. , Amstalden Junqueira V. C. , Kajsik M. , Forsythe S. J. , Pereira J. L. . ( 2013; ). Screening for Cronobacter species in powdered and reconstituted infant formulas and from equipment used in formula preparation in maternity hospitals. . Ann Nutr Metab 63:, 62–68. [CrossRef] [PubMed]
    [Google Scholar]
  117. Sonbol H. , Joseph S. , McAuley C. M. , Craven H. M. , Forsythe S. J. . ( 2013; ). Multilocus sequence typing of Cronobacter spp. from powedered infant formula and milk powder production factories. . Int Dairy J 30:, 1–7. [CrossRef]
    [Google Scholar]
  118. Stephan R. , Lehner A. , Tischler P. , Rattei T. . ( 2011; ). Complete genome sequence of Cronobacter turicensis LMG 23827, a food-borne pathogen causing deaths in neonates. . J Bacteriol 193:, 309–310. [CrossRef] [PubMed]
    [Google Scholar]
  119. Stock I. , Wiedemann B. . ( 2002; ). Natural antibiotic susceptibility of Enterobacter amnigenus, Enterobacter cancerogenus, Enterobacter gergoviae and Enterobacter sakazakii strains. . Clin Microbiol Infect 8:, 564–578. [CrossRef] [PubMed]
    [Google Scholar]
  120. Stoll B. J. , Hansen N. , Fanaroff A. A. , Lemons J. A. . ( 2004; ). Enterobacter sakazakii is a rare cause of neonatal septicemia or meningitis in VLBW infants. . J Pediatr 144:, 821–823.[PubMed]
    [Google Scholar]
  121. Stoop B. , Lehner A. , Iversen C. , Fanning S. , Stephan R. . ( 2009; ). Development and evaluation of rpoB based PCR systems to differentiate the six proposed species within the genus Cronobacter . . Int J Food Microbiol 136:, 165–168. [CrossRef] [PubMed]
    [Google Scholar]
  122. Sun Y. M. , Wang M. , Liu H. B. , Wang J. J. , He X. , Zeng J. , Guo X. , Li K. , Cao B. Y. , Wang L. . ( 2011; ). Development of an O-antigen serotyping scheme for Cronobacter sakazakii . . Appl Environ Microbiol 77:, 2209–2214. [CrossRef] [PubMed]
    [Google Scholar]
  123. Teramoto S. , Tanabe Y. , Okano E. , Nagashima T. , Kobayashi M. , Etoh Y. . ( 2010; ). A first fatal neonatal case of Enterobacter sakazakii infection in Japan. . Pediatr Int 52:, 312–313. [CrossRef] [PubMed]
    [Google Scholar]
  124. Townsend S. , Caubilla Barron J. , Loc-Carrillo C. , Forsythe S. . ( 2007a; ). The presence of endotoxin in powdered infant formula milk and the influence of endotoxin and Enterobacter sakazakii on bacterial translocation in the infant rat. . Food Microbiol 24:, 67–74. [CrossRef] [PubMed]
    [Google Scholar]
  125. Townsend S. M. , Hurrell E. , Gonzalez-Gomez I. , Lowe J. , Frye J. G. , Forsythe S. , Badger J. L. . ( 2007b; ). Enterobacter sakazakii invades brain capillary endothelial cells, persists in human macrophages influencing cytokine secretion and induces severe brain pathology in the neonatal rat. . Microbiology 153:, 3538–3547. [CrossRef] [PubMed]
    [Google Scholar]
  126. Townsend S. , Hurrell E. , Forsythe S. . ( 2008; ). Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. . BMC Microbiol 8:, 64. [CrossRef] [PubMed]
    [Google Scholar]
  127. Tsai H.-Y. , Liao C. H. , Huang Y.-T. , Lee P.-I. , Hsueh P.-R. . ( 2013; ). Cronobacter infections not from infant formula, Taiwan. . Emerg Infect Dis 19:, 167–169. [CrossRef] [PubMed]
    [Google Scholar]
  128. van Acker J. , de Smet F. , Muyldermans G. , Bougatef A. , Naessens A. , Lauwers S. . ( 2001; ). Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. . J Clin Microbiol 39:, 293–297. [CrossRef] [PubMed]
    [Google Scholar]
  129. Walsh D. , Molloy C. , Iversen C. , Carroll J. , Cagney C. , Fanning S. , Duffy G. . ( 2011; ). Survival characteristics of environmental and clinically derived strains of Cronobacter sakazakii in infant milk formula (IMF) and ingredients. . J Appl Microbiol 110:, 697–703. [CrossRef] [PubMed]
    [Google Scholar]
  130. Willis J. , Robinson J. E. . ( 1988; ). Enterobacter sakazakii meningitis in neonates. . Pediatr Infect Dis J 7:, 196–199. [CrossRef] [PubMed]
    [Google Scholar]
  131. Yan Q. Q. , Condell O. , Power K. , Butler F. , Tall B. D. , Fanning S. . ( 2012; ). Cronobacter species (formerly known as Enterobacter sakazakii) in powdered infant formula: a review of our current understanding of the biology of this bacterium. . J Appl Microbiol 113:, 1–15. [CrossRef] [PubMed]
    [Google Scholar]
  132. Yang J. , Wei L. , Gu M. , Fang X. , Yang P. . ( 2009; ). Identification of proteins involved in infectivity and enterotoxin production in Enterobacter sakazakii . . J Rapid Methods Autom Microbiol 17:, 164–181. [CrossRef]
    [Google Scholar]
  133. Zhou X. , Gao J. , Huang Y. , Fu S. , Chen H. . ( 2011; ). Antibiotic resistance pattern of Klebsiella pneumoniae and Enterobacter sakazakii isolates from powdered infant formula. . Afr J Microbiol Res 5:, 3073–3077.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.073742-0
Loading
/content/journal/jmm/10.1099/jmm.0.073742-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error