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Cronobacter spp.—Opportunistic Foodborne Pathogens: an Update on Evolution, Osmotic Adaptation and Pathogenesis

  • Foodborne Pathogens (S Johler, Section Editor)
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Abstract

Purpose of Review

Cronobacter spp. are opportunistic, foodborne pathogens capable of causing severe illnesses predominantly in premature and low-birth-weight infants. These organisms have evolved features, which aid them to survive under harsh environmental conditions but may also contribute to pathogenesis during infection. In this review, we highlight efforts to study genetic diversity and evolutionary aspects, osmotic adaptation and pathogenesis of these pathogens.

Recent Findings

Next-generation genome sequencing-based techniques elucidated a species-level bidirectional divergence driven by niche adaptation in Cronobacter spp. Whole genome comparisons and proteomics revealed genes and pathways contributing to the survival and persistence phenotype in low-moisture environments. In silico genome comparisons and application of suitable in vivo models provided answers to pathogenesis-related questions.

Summary

Development and application of innovative molecular techniques and in vivo infection models have shed light on how Cronobacter spp. adapt to challenges experienced in natural, food processing and host-related environments.

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References

Recently published papers of particular interest have been highlighted as: • Of importance •• Of major importance

  1. Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, Fanning S, et al. 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. 2008;58:1442–7.

    Article  CAS  PubMed  Google Scholar 

  2. Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe SJ. Cronobacter condimenti sp. nov., isolated from spiced meat and Cronobacter universalis sp. nov., a novel species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water, and food ingredients. Int J Syst Evol Microbiol. 2012;62:1277–83.

    Article  CAS  PubMed  Google Scholar 

  3. Lai KK. Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine (Baltimore). 2001;80:113–22.

    Article  CAS  Google Scholar 

  4. Stoll BJ, Hansen N, Fanaroff AA, Lemons JA. Enterobacter sakazakii is a rare cause of neonatal septicemia or meningitis in VLBW infants. J Pediatr. 2004;144:821–3.

    PubMed  Google Scholar 

  5. Cruz-Cordova A, Rocha-Ramırez LM, Ochoa SA, Gonzalez-Pedrajo B, Espinosa N, et al. Flagella from five Cronobacter species induce pro-inflammatory cytokines in macrophage derivatives from human monocytes. PLoS One. 2012;7:e52091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Healy B, Cooney S, O’Brien S, Iversen C, Whyte P, Nally J, et al. Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. Foodborne Pathog Dis. 2010;7:339–50.

    Article  CAS  PubMed  Google Scholar 

  7. Food and Agriculture Organization of the United Nations/ World Health Organization (FAO/WHO), Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae. 2008 Microbiological Risk Assessment Series 15. Rome.

  8. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO), Enterobacter sakazakii and Salmonella in powdered infant formula (Meeting Report). 2006 Microbiological Risk AssessmentSeries 10. Rome.

  9. Bowen AB, Braden CR. Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis. 2006;12:1185–9.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Friedemann M. Enterobacter sakazakii in food and beverages (other than infant formula and milk powder). Int J Food Microbiol. 2007;116:1–10.

    Article  CAS  PubMed  Google Scholar 

  11. Schmid M, Iversen C, Gontia I, Stephan R, Hofmann A, Jha B, et al. Evidence for a plant-associated natural habitat for Cronobacter spp. Res Microbiol. 2009;160:608–14.

    Article  PubMed  Google Scholar 

  12. Hochel I, Ruzickova H, Krasny L, Demnerova K. Occurrence of Cronobacter spp. in retail foods. J Appl Microbiol. 2012;112:1257–65.

    Article  CAS  PubMed  Google Scholar 

  13. Himelright I, Harris E, Lorch V, Anderson M, Jones T, Craig A, et al. Enterobacter sakazakii infections associated with the use of powdered infant formula—Tennessee, 2001. MMWR Morb Mortal Wkly Rep. 2002;51:297–300.

    Google Scholar 

  14. Hunter CJ, Bean JF. Cronobacter: an emerging opportunistic pathogen associated with neonatal meningitis, sepsis and necrotizing enterocolitis. J Perinatol. 2013;33:581–5.

    Article  CAS  PubMed  Google Scholar 

  15. Jaradat ZW, Al Mousa W, Elbetieha A, Al Nabulsi A, Tall BT. Cronobacter spp.—opportunistic food-borne pathogens. A review of their virulence and environmental-adaptive traits. J Med Microbiol. 2014;63:1023–37.

    Article  CAS  PubMed  Google Scholar 

  16. Seo KH, Brackett RE. Rapid, specific detection of Enterobacter sakazakii in infant formula using a real-time PCR assay. J Food Prot. 2005;68:59–63.

    Article  CAS  PubMed  Google Scholar 

  17. Lehner A, Nitzsche S, Breeuwer P, Diep B, Thelen K, Stephan R. Comparison of two chromogenic media and evaluation of two molecular based identification systems for Enterobacter sakazakii detection. BMC Microbiol. 2006;6:15.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Stoop B, Lehner A, Iversen C, Fanning S, Stephan R. Development and evaluation of rpoB based PCR systems to differentiate the six proposed species within the genus Cronobacter. Int J Food Microbiol. 2009;136:165–8.

    Article  CAS  PubMed  Google Scholar 

  19. Lehner A, Fricker Feer C, Stephan R. Identification of the recently described Cronobacter condimenti by an rpoB-gene-based PCR system. J Med Microbiol. 2012;61:1034–5.

    Article  CAS  PubMed  Google Scholar 

  20. Jarvis KG, Grim CJ, Franco AA, Gopinath G, Sathyarmoorthy V, Hu L, et al. Molecular caracterization of Cronobacter lipopolysaccharide O-antigen gene clusters and development of serotype-specific PCR assays. Appl Environ Microbiol. 2011;77:4017–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sun Y, Wang M, Wang Q, Cao B, He X, Li K, et al. Genetic analysis of the Cronobacter sakazakii O4 to O7 O-antigen gene clusters and development of a PCR assay for identification of all C. sakazakii serotypes. Appl Environ Microbiol. 2012;78:3966–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Yan Q, Fanning S. Pulsed-field gel electrophoresis (PFGE) for pathogenic Cronobacter species. Methods Mol Biol. 2015;1301:55–69.

    Article  CAS  PubMed  Google Scholar 

  23. Mueller A, Stephan R, Fricker-Feer C, Lehner A. Genetic diversity of Cronobacter sakazakii isolates collected from a Swiss infant formula production facility. J Food Prot. 2013;76:883–7.

    Article  Google Scholar 

  24. Stoller A, Stephan R, Fricker-Feer C, Lehner A. Epidemiological investigation of a powdered infant formula product batch contaminated with Cronobacter in a Swiss infant formula production facility. Austin Food Sci. 2016;1:1028.

    Google Scholar 

  25. Baldwin A, Loughlin M, Caubilla-Barron J, Kucerova E, Manning G, Dawson C, et al. Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. BMC Microbiol. 2009;9:223.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Joseph S, Forsythe SJ. Insights into the emergent bacterial pathogen Cronobacter spp., generated by multilocus seqeunce typing and analysis. Front Microbiol. 2012;3:397.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Joseph S, Sonbol H, Hariri S, Desai P, McClelland M, Forsythe SJ. Diversity of the Cronobacter genus as revealed by multilocus sequence typing. J Clin Microbiol. 2012;50:3031–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yan Q, Wang J, Gangiredla J, Cao Y, Martins M, Gopinath GR, et al. Comparative genotypic and phenotypic analysis of Cronobacter species cultured from four powdered infant formula production facilities: indication of pathoadaptation along the food chain. Appl Environ Microbiol. 2015;81:4388–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Joseph S, Forsythe SJ. Predominance of Cronobacter sakazakii sequence type 4 in neonatal infections. Emerg Infect Dis. 2011;7:1713–5.

    Article  Google Scholar 

  30. Hariri S, Joseph S, Forsythe SJ. Predominance of Cronobacter sakazakii ST4 strains in Cronobacter neonatal meningitis United States. Emerg Infect Dis. 2013;19:175–7.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Mramba F, Broce A, Zurek L. Isolation of Enterobacter sakazakii from stable flies, Stomoxys calcitrans L. (Diptera: Muscidae). J Food Prot. 2006;69:671–3.

    Article  CAS  PubMed  Google Scholar 

  32. Pava-Ripoll M, Pearson REG, Miller AK, Ziobro GC. Prevalence and relative risk of Cronobacter spp., Salmonella spp., and Listeria monocytogenes associated with the body surfaces and guts of individual filth flies. App Environ Microbiol. 2012;78:7891–902.

    Article  CAS  Google Scholar 

  33. Forsythe SJ, Dickins B, Jolley KA. Cronobacter, the emergent bacterial pathogen Enterobacter sakazakii comes of age; MLST and whole genome sequence analysis. BMC Genomics. 2014;15:1121.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kucerova E, Clifton SW, Xia XQ, Long F, Porwolnik S, Fulton L, et al. Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS One. 2010;5:e9556.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Grim CJ, Kotewicz ML, Power KA, Gopinath G, Franco AA, Jarvis KG, et al. Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation. BMC Genomics. 2013;14:366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Franco AA, Hu L, Grim CJ, Gopinath G, Sathyamoorthy V, Jarvis KG, et al. Characterization of putative virulence genes on the related RepFIB plasmids harbored by Cronobacter spp. Appl Environ Microbiol. 2011;77:3255–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. • Eshwar AK, Tall BD, Gangiredla J, Gopinath GR, Patel IR, Neuhauss SCF, et al. Linking genomo- and pathotype: exploiting the zebrafish embryo model to investigate the divergent virulence potential among Cronobacter spp. PLoS One. 2016;11:e0158428. In this study, the potential of the zebrafish embryo model to study pathogenesis in Cronobacter spp. is discussed.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Chase HR, Gopinath GR, Eshwar AK, Stoller A, Fricker-Feer C, Gangiredla J, et al. Comparative genomic characterization of the highly persistent and potentially virulent Cronobacter sakazakii ST83, CC65 strain H322 and other ST83 strains. Front Microbiol. 2017;8:1136.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Tall BD, Gangiredla J, Gopinath GR, Yan Q, Chase HR, Lee B, et al. Development of a custom-designed, pan genomic DNA microarray to characterize strain-level diversity among Cronobacter spp. Front Pediatr. 2015;3:36.

    Article  PubMed  PubMed Central  Google Scholar 

  40. • Tall BD, Gangiredla J, Grim CJ, Patel IR, Jackson SA, Mammel MK, et al. Use of a pan-genomic DNA microarray in determination of the phylogenetic relatedness among Cronobacter spp. and its use as a data mining tool to understand Cronobacter biology. Microarrays. 2017;4:6. This study demonstates the application possibilities of the Cronobacter microarray.

    Article  Google Scholar 

  41. Yan Q, Power KA, Cooney S, Fox E, Gopinath GR, et al. Complete genome sequence and phenotype microarray analysis of Cronobacter sakazakii SP291: a persistent isolate cultured from a powdered infant formula production facility. Front Microbiol. 2013;4:256.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Gurtler JB, Beuchat LR. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. J Food Prot. 2007;70:1579–86.

    Article  PubMed  Google Scholar 

  43. Beuchat LR, Komitopoulou E, Beckers H, Betts RP, Bourdichon F, et al. Low water activity foods: increased concern as vehicles of foodborne pathogens. J Food Prot. 2013;76:150–72.

    Article  PubMed  Google Scholar 

  44. Podolak R, Enache E, Stone W, Black DG, Elliott PH. Sources and risk factors for contamination, survival, persistence, and heat resistance of Salmonella in low-moisture foods. J Food Prot. 2010;73:1919–36.

    Article  PubMed  Google Scholar 

  45. Breeuwer P, Lardeau A, Peterz M, Joosten HM. Desiccation and heat tolerance of Enterobacter sakazakii. J Appl Microbiol. 2003;95:967–73.

    Article  CAS  PubMed  Google Scholar 

  46. Barron JC, Forsythe SJ. Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J Food Prot. 2007;70:2111–7.

    Article  PubMed  Google Scholar 

  47. Drudy D, O’Rourke M, Murphy M, Mullane NR, O’Mahony R, Kelly L, et al. Characterization of a collection of Enterobacter sakazakii isolates from environmental and food sources. Int J Food Microbiol. 2006;110:127–34.

    Article  CAS  PubMed  Google Scholar 

  48. Mullane NR, Ryan M, Iversen C, Murphy M, O’Gaora P, Quinn T, et al. Development of multiple-locus variable-number tandem-repeat analysis for the molecular subtyping of Enterobacter sakazakii. Appl Environ Microbiol. 2008;74:1223–31.

    Article  CAS  PubMed  Google Scholar 

  49. Mullane NR, Whyte P, Wall PG, Quinn T, Fanning S. Application of pulsed-field gel electrophoresis to characterise and trace the prevalence of Enterobacter sakazakii in an infant formula processing facility. Int J Food Microbiol. 2007;116:73–81.

    Article  CAS  PubMed  Google Scholar 

  50. Feeney A, Sleator RD. An in silico analysis of osmotolerance in the emerging gastrointestinal pathogen Cronobacter sakazakii. Bioeng Bugs. 2011;2:260–70.

    Article  PubMed  Google Scholar 

  51. Power KA, Yan Q, Fox EM, Cooney S, Fanning S. Genome sequence of Cronobacter sakazakii SP291, a persistent thermotolerant isolate derived from a factory producing powdered infant formula. Genome Announc. 2013;1:e0008213.

    Article  PubMed  Google Scholar 

  52. Riedel K, Lehner A. Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics. 2007;7:1217–31.

    Article  CAS  PubMed  Google Scholar 

  53. •• Hu S, Yu Y, Wu X, Xia X, Xiao X, Wu H. Comparative proteomic analysis of Cronobacter sakazakii by iTRAQ provides insights into response to desiccation. Food Res Int. 2017;100:631–9. In this study, the most actual information on Cronobacter desiccation stress response is given.

    Article  CAS  PubMed  Google Scholar 

  54. Cayley S, Lewis BA, Guttman HJ, Record MT Jr. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. J Mol Biol. 1991;222:281–300.

    Article  CAS  PubMed  Google Scholar 

  55. Dosch DC, Helmer GL, Sutton SH, Salvacion FF, Epstein W. Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake potassium. J Bacteriol. 1991;173:687–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sleator RD, Wouters J, Gahan CG, Abee T, Hill C. Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl Environ Microbiol. 2001;67:2692–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nakamura T, Yamamuro N, Stumpe S, Unemoto T, Bakker EP. Cloning of the trkAH gene cluster and characterization of the Trk K(+)-uptake system of Vibrio alginolyticus. Microbiology. 1998;144:2281–9.

    Article  CAS  PubMed  Google Scholar 

  58. Roe AJ, McLaggan D, O’Byrne CP, Booth IR. Rapid inactivation of the Escherichia coli Kdp K+ uptake system by high potassium concentrations. Mol Microbiol. 2000;35:1235–43.

    Article  CAS  PubMed  Google Scholar 

  59. Gralla JD, Vargas DR. Potassium glutamate as a transcriptional inhibitor during bacterial osmoregulation. EMBO J. 2006;25:1515–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dinnbier U, Limpinsel E, Schmid R, Bakker EP. Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Arch Microbiol. 1988;150:348–57.

    Article  CAS  PubMed  Google Scholar 

  61. Wood JM. Proline porters effect the utilization of proline as nutrient or osmoprotectant for bacteria. J Membr Biol. 1988;106:183–202.

    Article  CAS  PubMed  Google Scholar 

  62. Finn S, Handler K, Condell O, Colgan A, Cooney S, McClure P, et al. ProP is required for the survival of desiccated Salmonella enterica serovar Typhimurium cells on a stainless steel surface. Appl Environ Microbiol. 2013;79:4376–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sola-Penna M, Meyer-Fernandes JR. Stabilization against thermal inactivation promoted by sugars on enzyme structure and function: why is trehalose more effective than other sugars? Arch Biochem Biophys. 1998;360:10–4.

    Article  CAS  PubMed  Google Scholar 

  64. Purvis JE, Yomano LP, Ingram LO. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol. 2005;71:3761–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Hunter CJ, Williams M, Petrosyan M, Guner Y, Mittal R, Mock D, et al. 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. 2009;77:1031–43.

    Article  CAS  PubMed  Google Scholar 

  66. Liu Q, Mittal R, Emami CN, Iversen C, Ford HR, Prasadarao NV. Human isolates of Cronobacter sakazakii bind efficiently to intestinal epithelial cells in vitro to induce monolayer permeability and apoptosis. J Surg Res. 2012;176:437–47.

    Article  CAS  PubMed  Google Scholar 

  67. Grishin A, Papillon S, Bell B, Wang J, Ford H. The role of the intestinal microbiota in the pathogenesis of necrotizing enterocolitis. Semin Pediatr Surg. 2013;22:69–75.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Mange JP, Stephan R, Borel N, Wild P, Kim KS, Pospischil A, et al. Adhesive properties of Enterobacter sakazakii to human epithelial and brain microvascular endothelial cells. BMC Microbiol. 2006;6:58.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Kim KP, Loessner MJ. Enterobacter sakazakii invasion in human intestinal Caco-2 cells requires the host cell cytoskeleton and is enhanced by disruption of tight junction. Infect Immun. 2008;76:562–70.

    Article  CAS  PubMed  Google Scholar 

  70. Nair MK, Venkitanarayanan K. Role of bacterial OmpA and host cytoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii. Pediatr Res. 2007;62:664–9.

    Article  CAS  Google Scholar 

  71. Mittal R, Wang Y, Hunter CJ, Gonzalez-Gomez I, Prasadarao NV. Brain damage in newborn rat model of meningitis by Enterobacter sakazakii: a role for outer membrane protein A. Lab Investig. 2009;89:263–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Mittal R, Bulgheresi S, Emami C, Prasadarao NV. Enterobacter sakazakii targets DC-SIGN to induce immunosuppressive responses in cultured human intestinal epithelial cells and human brain microvascular endothelial cells. Microb Pathog. 2009;52:140–7.

    Google Scholar 

  73. Nair MK, Venkitanarayanan K, Silbart LK, Kim KS. Outer membrane protein A (OmpA) of Cronobacter sakazakii binds fibronectin and contributes to invasion of human brain microvascular endothelial cells. Foodborne Pathog Dis. 2009;6:495–501.

    Article  PubMed  Google Scholar 

  74. Giri CP, Shima K, Tall BD, Curtis S, Sathyamoorthy V, Hanisch B, et al. Cronobacter spp.(previously Enterobacter sakazakii) invade and translocate across both cultured human intestinal epithelial cells and human brain microvascular endothelial cells. Microb Pathog. 2012;52:140–7.

    Article  CAS  PubMed  Google Scholar 

  75. Kim K, Kim KP, Choi J, Lim JA, Lee J, Hwang H, et al. Outer membrane proteins A (OmpA) and X (OmpX) are essential for basolateral invasion of Cronobacter sakazakii. Appl Environ Microbiol. 2010;76:5188–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Emami CN, Mittal R, Wang L, Ford HR, Prasadarao NV. Recruitment of dendritic cells is responsible for intestinal epithelial damage in the pathogenesis of necrotizing enterocolitis by Cronobacter sakazakii. J Immunol. 2011;186:7067–79.

    Article  CAS  PubMed  Google Scholar 

  77. Emami CN, Mittal R, Wang L, Ford HR, Prasadarao NV. Role of neutrophils and macrophages in the pathogenesis of necrotizing enterocolitis caused by Cronobacter sakazakii. J Surg Res. 2012;172:18–28.

    Article  CAS  PubMed  Google Scholar 

  78. Hunter CJ, Singamsetty VK, Chokshi NK, Boyle P, Camerini V, Grishin AV, et al. Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J Infect Dis. 2008;198:586–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Moriez R, Salvador-Cartier C, Theodorou V, Fioramonti J, Eutamene H, Bueno L. Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am J Pathol. 2005;167:1071–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Townsend S, Caubilla Barron J, Loc-Carrillo C, Forsythe S. 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. 2007;24:67–74.

    Article  CAS  PubMed  Google Scholar 

  81. Townsend SM, Hurrell E, Gonzalez-Gomez I, Lowe J, Frye JG, Forsythe S, et al. Enterobacter sakazakii invades brain capillary endothelial cells, persists in human macrophages influencing cytokine secretion and induces severe brain pathology in the neonatal rat. Microbiology. 2007;153:3538–47.

    Article  CAS  PubMed  Google Scholar 

  82. Townsend S, Hurrell E, Forsythe S. Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. BMC Microbiol. 2008;8:64.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Eshwar AK, Tasara T, Stephan R, Lehner A. Influence of FkpA variants on survival and replication of Cronobacter spp. in human macrophages. Res Microbiol. 2015;166:186–95.

    Article  CAS  PubMed  Google Scholar 

  84. Schwizer S, Tasara T, Zurfluh K, Stephan R, Lehner A. Identification of genes involved in serum tolerance in the clinical strain Cronobacter sakazakii ES5. BMC Microbiol. 2013;13:38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Franco AA, Kothary MH, Gopinath G, Jarvis KG, Grim CJ, Hu L, et al. Cpa, the outer membrane protease of Cronobacter sakazakii, activates plasminogen and mediates resistance to serum bactericidal activity. Infect Immun. 2011;79:1578–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Yan QQ, Condell O, Power K, Butler F, Tall BD, Fanning S. 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. 2012;113:1–15.

    Article  CAS  PubMed  Google Scholar 

  87. Singamsetty VK, Wang Y, Shimada H, Prasadarao NV. Outer membrane protein A expression in Enterobacter sakazakii is required to induce microtubule condensation in human brain microvascular endothelial cells for invasion. Microb Pathog. 2008;45:181–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Liu DX, Zhao WD, Fang WG, Chen YH. cPLA2a mediated actin rearrangements downstream of the Akt signaling is required for Cronobacter sakazakii invasion into brain endothelial cells. Biochem Biophys Res Commun. 2012;417:925–30.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Angelika Lehner.

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Dr. Lehner reports grants from Swiss National Science Foundation, during the conduct of the study.

Ben Davis Tall, Seamus Fanning and Shabarinath Srikumar declare that they have no conflict of interest.

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All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards and international/national/institutional guidelines).

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This article is part of the Topical Collection on Foodborne Pathogens

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Lehner, A., Tall, B.D., Fanning, S. et al. Cronobacter spp.—Opportunistic Foodborne Pathogens: an Update on Evolution, Osmotic Adaptation and Pathogenesis. Curr Clin Micro Rpt 5, 97–105 (2018). https://doi.org/10.1007/s40588-018-0089-7

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  • DOI: https://doi.org/10.1007/s40588-018-0089-7

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