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Differentiation between Shigella, enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichia coli

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Abstract

Shigella causes bacillary dysentery and is classified into four species based on their antigen characteristics. This classification does not reflect genetic relatedness; in fact, Shigella species are so related to Escherichia coli , they should be classified as one distinctive species in the genus Escherichia. The differentiation of Shigella and E. coli is even more complicated with the description of enteroinvasive E. coli (EIEC). EIEC are strains that possess some of the biochemical characteristics of E. coli and have the ability to cause dysentery using the same method of invasion as Shigella does. Sequencing of multiple housekeeping genes indicates that EIEC is more related to Shigella than to non-invasive E. coli. Shigella and EIEC evolved from the same ancestor and form a single pathovar within E. coli. Shigella and EIEC could be separated from other E. coli by a PCR targeting the ipaH-gene; this is a multicopy gene exclusively found in all Shigella and EIEC. It is possible to differentiate Shigella and all E. coli, including EIEC, by using multiple tests, including ipaH-gene PCR, physiological and biochemical typing and serological typing. Based on literature study, a key is designed for daily use in diagnostic laboratories to identify Shigella and all E. coli.

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References

  1. Hale TL (1991) Genetic basis of virulence in Shigella species. Microbiol Rev 55(2):206–224

    PubMed  CAS  Google Scholar 

  2. Pupo GM, Lan R, Reeves PR (2000) Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc Natl Acad Sci USA 97(19):10567–10572

    Article  PubMed  CAS  Google Scholar 

  3. Lan R, Alles MC, Donohoe K, Martinez MB, Reeves PR (2004) Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infect Immun 72(9):5080–5088

    Article  PubMed  CAS  Google Scholar 

  4. Fernandez-Prada CM, Hoover DL, Tall BD, Hartman AB, Kopelowitz J, Venkatesan MM (2000) Shigella flexneri IpaH(7.8) facilitates escape of virulent bacteria from the endocytic vacuoles of mouse and human macrophages. Infect Immun 68(6):3608–3619

    Article  PubMed  CAS  Google Scholar 

  5. Sereny B (1955) Experimental shigella keratoconjunctivitis; a preliminary report. Acta Microbiol Acad Sci Hung 2(3):293–296

    PubMed  CAS  Google Scholar 

  6. Venkatesan MM, Buysse JM, Kopecko DJ (1989) Use of Shigella flexneri ipaC and ipaH gene sequences for the general identification of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol 27(12):2687–2691

    PubMed  CAS  Google Scholar 

  7. Brenner DJ, Fanning GR, Steigerwalt AG, Orskov I, Orskov F (1972) Polynucleotide sequence relatedness among three groups of pathogenic Escherichia coli strains. Infect Immun 6(3):308–315

    PubMed  CAS  Google Scholar 

  8. Brenner DJ, Steigerwalt AG, Wathen HG, Gross RJ, Rowe B (1982) Confirmation of aerogenic strains of Shigella boydii 13 and further study of Shigella serotypes by DNA relatedness. J Clin Microbiol 16(3):432–436

    PubMed  CAS  Google Scholar 

  9. Christensen H, Nordentoft S, Elmerdahl Olsen J (1998) Phylogenetic relationships of Salmonella based on rRNA sequences. Int J Syst Bacteriol 48:605–610

    PubMed  CAS  Google Scholar 

  10. Murray RGE, Brenner DJ, Colwell RR et al (1990) International committee on systematic bacteriology. Report of the ad hoc committee on approaches to taxonomy within the Proteobacteria. Int J Syst Bacteriol 40:213–215

    Article  Google Scholar 

  11. Jin Q, Yuan Z, Xu J, Wang Y, Shen Y, Lu W, Wang J, Liu H, Yang J, Yang F, Zhang X, Zhang J, Yang G, Wu H, Qu D, Dong J, Sun L, Xue Y, Zhao A, Gao Y, Zhu J, Kan B, Ding K, Chen S, Cheng H, Yao Z, He B, Chen R, Ma D, Qiang B, Wen Y, Hou Y, Yu J (2002) Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 30(20):4432–4441

    Article  PubMed  CAS  Google Scholar 

  12. Lan R, Lumb B, Ryan D, Reeves PR (2001) Molecular evolution of large virulence plasmid in Shigella clones and enteroinvasive Escherichia coli. Infect Immun 69(10):6303–6309

    Article  PubMed  CAS  Google Scholar 

  13. Nhung PH, Ohkusu K, Mishima N, Noda M, Shah MM, Sun X, Hayashi M, Ezaki T (2007) Phylogeny and species identification of the family Enterobacteriaceae based on dnaJ sequences. Diagn Microbiol Inf Dis 58:153–161

    Article  CAS  Google Scholar 

  14. Yang F, Yang J, Zhang X, Chen L, Jiang Y, Yan Y, Tang X, Wang J, Xiong Z, Dong J, Xue Y, Zhu Y, Xu X, Sun L, Chen S, Nie H, Peng J, Xu J, Wang Y, Yuan Z, Wen Y, Yao Z, Shen Y, Qiang B, Hou Y, Yu J, Jin Q (2005) Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33(19):6445–6458

    Article  PubMed  Google Scholar 

  15. Scheutz F, Strockbine NA (2005) Genus I. Escherichia. In: Bergey’s Manual of Systematic Bacteriology, 2nd edn. Springer, USA, pp 207–624

  16. Bopp CA, Brenner FW, Fields PI, Wells JG, Strockbine NA (2003) Escherichia, Shigella, and Salmonella. In: Manual of Clinical Microbiology, 8th edn. ASM Press, Washington D.C., pp 655–663

  17. Ewing WH (1986) The genus Escherichia and the genus Shigella. In: Edwards and Ewing’s Identification of Enterobacteriaceae, 4th edn. Elsevier Science Publishing Co., Inc., New York, pp 93–172

  18. Silva RM, Toledo MR, Trabulsi LR (1980) Biochemical and cultural characteristics of invasive Escherichia coli. J Clin Microbiol 11(5):441–444

    PubMed  CAS  Google Scholar 

  19. Toledo MR, Trabulsi LR (1983) Correlation between biochemical and serological characteristics of Escherichia coli and results of the Sereny test. J Clin Microbiol 17(3):419–421

    PubMed  CAS  Google Scholar 

  20. Venkatesan MM, Goldberg MB, Rose DJ, Grotbeck EJ, Burland V, Blattner FR (2001) Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect Immun 69(5):3271–3285

    Article  PubMed  CAS  Google Scholar 

  21. Maurelli AT (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267(1):1–8

    Article  PubMed  CAS  Google Scholar 

  22. Kingombe CI, Cerqueira-Campos ML, Farber JM (2005) Molecular strategies for the detection, identification, and differentiation between enteroinvasive Escherichia coli and Shigella spp. J Food Prot 68(2):239–245

    PubMed  Google Scholar 

  23. Hale TL, Sansonetti PJ, Schad PA, Austin S, Formal SB (1983) Characterization of virulence plasmids and plasmid-associated outer membrane proteins in Shigella flexneri, Shigella sonnei, and Escherichia coli. Infect Immun 40(1):340–350

    PubMed  CAS  Google Scholar 

  24. Harris JR, Wachsmuth IK, Davis BR, Cohen ML (1982) High-molecular-weight plasmid correlates with Escherichia coli enteroinvasiveness. Infect Immun 37(3):1295–1298

    PubMed  CAS  Google Scholar 

  25. Sansonetti PJ, Kopecko DJ, Formal SB (1981) Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infect Immun 34(1):75–83

    PubMed  CAS  Google Scholar 

  26. Sansonetti PJ, Kopecko DJ, Formal SB (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35(3):852–860

    PubMed  CAS  Google Scholar 

  27. Boileau CR, d'Hauteville HM, Sansonetti PJ (1984) DNA hybridization technique to detect Shigella species and enteroinvasive Escherichia coli. J Clin Microbiol 20(5):959–961

    PubMed  CAS  Google Scholar 

  28. Adler B, Sasakawa C, Tobe T, Makino S, Komatsu K, Yoshikawa M (1989) A dual transcriptional activation system for the 230 kb plasmid genes coding for virulence-associated antigens of Shigella flexneri. Mol Microbiol 3(5):627–635

    Article  PubMed  CAS  Google Scholar 

  29. Kopecko DJ, Baron LS, Buysse J (1985) Genetic determinants of virulence in Shigella and dysenteric strains of Escherichia coli: their involvement in the pathogenesis of dysentery. Curr Top Microbiol Immunol 118:71–95

    Article  PubMed  CAS  Google Scholar 

  30. Croxen MA, Finlay BB (2010) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8(1):26–38

    Google Scholar 

  31. Buysse JM, Stover CK, Oaks EV, Venkatesan M, Kopecko DJ (1987) Molecular cloning of invasion plasmid antigen (ipa) genes from Shigella flexneri: analysis of ipa gene products and genetic mapping. J Bacteriol 169(6):2561–2569

    PubMed  CAS  Google Scholar 

  32. Venkatesan M, Buysse JM, Vandendries E, Kopecko DJ (1988) Development and testing of invasion-associated DNA probes for detection of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol 26(2):261–266

    PubMed  CAS  Google Scholar 

  33. Uchiya K, Tobe T, Komatsu K, Suzuki T, Watarai M, Fukuda I, Yoshikawa M, Sasakawa C (1995) Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading. Mol Microbiol 17(2):241–250

    Article  PubMed  CAS  Google Scholar 

  34. Hartman AB, Venkatesan M, Oaks EV, Buysse JM (1990) Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Shigella flexneri. J Bacteriol 172(4):1905–1915

    PubMed  CAS  Google Scholar 

  35. Venkatesan MM, Buysse JM, Hartman AB (1991) Sequence variation in two ipaH genes of Shigella flexneri 5 and homology to the LRG-like family of proteins. Mol Microbiol 5(10):2435–2445

    Article  PubMed  CAS  Google Scholar 

  36. Buysse JM, Hartman AB, Strockbine N, Venkatesan M (1995) Genetic polymorphism of the ipaH multicopy antigen gene in Shigella spps. and enteroinvasive Escherichia coli. Microb Pathog 19(5):335–349

    Article  PubMed  CAS  Google Scholar 

  37. Luscher D, Altwegg M (1994) Detection of shigellae, enteroinvasive and enterotoxigenic Escherichia coli using the polymerase chain reaction (PCR) in patients returning from tropical countries. Mol Cell Probes 8(4):285–290

    Article  PubMed  CAS  Google Scholar 

  38. Oberhelman RA, Kopecko DJ, Venkatesan MM, Salazar-Lindo E, Gotuzzo E, Yi A, Chea-Woo E, Ruiz R, Fernandez-Prada C, Leon-Barua R et al (1993) Evaluation of alkaline phosphatase-labelled ipaH probe for diagnosis of Shigella infections. J Clin Microbiol 31(8):2101–2104

    PubMed  CAS  Google Scholar 

  39. Persson S, Olsen KE, Scheutz F, Krogfelt KA, Gerner-Smidt P (2007) A method for fast and simple detection of major diarrhoeagenic Escherichia coli in the routine diagnostic laboratory. Clin Microbiol Infect 13(5):516–524

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Bacteriology, Laboratory for Infectious Diseases and Perinatal Screening, National Institute for Public Health and the Environment, PO Box 1, Postvak 22, 3720, BA, Bilthoven, The Netherlands

    M. J. C. van den Beld & F. A. G. Reubsaet

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  1. M. J. C. van den Beld
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  2. F. A. G. Reubsaet
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Correspondence to M. J. C. van den Beld.

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van den Beld, M.J.C., Reubsaet, F.A.G. Differentiation between Shigella, enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichia coli . Eur J Clin Microbiol Infect Dis 31, 899–904 (2012). https://doi.org/10.1007/s10096-011-1395-7

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  • DOI: https://doi.org/10.1007/s10096-011-1395-7

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