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Volume 61, Issue 6

Shiga toxin-producing O157 : H7 shows an increased pathogenicity in mice after the passage through the gastrointestinal tract of the same host Free

Abstract

Haemolytic uraemic syndrome (HUS) is a rare but life-threatening complication of Shiga toxin (Stx)-producing (STEC) infections, characterized by acute renal failure, thrombocytopenia and haemolytic anaemia. Although the main infection route is the consumption of contaminated food or water, person-to-person transmission has been suggested in several situations. Moreover, epidemiological data indicate that the horizontal transmission of several pathogens, including STEC, among individuals of the same species requires significantly lower doses than those used in animal models infected with laboratory-cultured bacteria. Thus, the aim of this study was to evaluate whether the passage of a clinically isolated STEC strain through the gastrointestinal tract of mice affects its pathogenicity in mice. To test this, weaned mice were orally inoculated by gavage with either an O157 : H7 isolate from an HUS patient, or the same strain recovered from stools after one or two successive passages through the gastrointestinal tract of the mice. We show that stool-recovered strains are able to induce a more generalized and persistent colonization than the parent strain. Furthermore, a 10-fold-reduced inoculum of the stool-recovered strains still causes gut colonization and mouse mortality, which are not observed with the parent strain. These results indicate an increased pathogenicity in stool-recovered strains that may be associated with an increased ability to colonize the mouse intestine.

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© 2012 SGM
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2012-06-01
2024-05-01
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References

  1. Bell B. P., Goldoft M., Griffin P. M., Davis M. A., Gordon D. C., Tarr P. I., Bartleson C. A., Lewis J. H., Barrett T. J. other authors 1994; A multistate outbreak of Escherichia coli O157 : H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers. The Washington experience. JAMA 272:1349–1353 [View Article][PubMed]
     [Google Scholar]
  2. Besser T. E., Richards B. L., Rice D. H., Hancock D. D. 2001; Escherichia coli O157 : H7 infection of calves: infectious dose and direct contact transmission. Epidemiol Infect 127:555–560 [View Article][PubMed]
     [Google Scholar]
  3. Brando R. J., Miliwebsky E., Bentancor L., Deza N., Baschkier A., Ramos M. V., Fernández G. C., Meiss R., Rivas M., Palermo M. S. 2008; Renal damage and death in weaned mice after oral infection with Shiga toxin 2-producing Escherichia coli strains. Clin Exp Immunol 153:297–306 [View Article][PubMed]
     [Google Scholar]
  4. Cornick N. A., Helgerson A. F. 2004; Transmission and infectious dose of Escherichia coli O157 : H7 in swine. Appl Environ Microbiol 70:5331–5335 [View Article][PubMed]
     [Google Scholar]
  5. Cray W. C. Jr, Moon H. W. 1995; Experimental infection of calves and adult cattle with Escherichia coli O157 : H7. Appl Environ Microbiol 61:1586–1590[PubMed]
     [Google Scholar]
  6. Crump J. A., Sulka A. C., Langer A. J., Schaben C., Crielly A. S., Gage R., Baysinger M., Moll M., Withers G. other authors 2002; An outbreak of Escherichia coli O157 : H7 infections among visitors to a dairy farm. N Engl J Med 347:555–560 [View Article][PubMed]
     [Google Scholar]
  7. Dekker A., Moonen P., de Boer-Luijtze E. A., Terpstra C. 1995; Pathogenesis of swine vesicular disease after exposure of pigs to an infected environment. Vet Microbiol 45:243–250 [View Article][PubMed]
     [Google Scholar]
  8. Domingo S., Díaz R., Gamazo C. 1995; Antibiotic treatment induces an increase of the specific antibody levels in Brucella melitensis infected mice. FEMS Immunol Med Microbiol 12:91–95 [View Article][PubMed]
     [Google Scholar]
  9. Fedorka-Cray P. J., Whipp S. C., Isaacson R. E., Nord N., Lager K. 1994; Transmission of Salmonella Typhimurium to swine. Vet Microbiol 41:333–344 [View Article][PubMed]
     [Google Scholar]
  10. Fernandez M. I., Thuizat A., Pedron T., Neutra M., Phalipon A., Sansonetti P. J. 2003; A newborn mouse model for the study of intestinal pathogenesis of shigellosis. Cell Microbiol 5:481–491 [View Article][PubMed]
     [Google Scholar]
  11. Frankel G., Phillips A. D., Rosenshine I., Dougan G., Kaper J. B., Knutton S. 1998; Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30:911–921 [View Article][PubMed]
     [Google Scholar]
  12. Fujii J., Kita T., Yoshida S., Takeda T., Kobayashi H., Tanaka N., Ohsato K., Mizuguchi Y. 1994; Direct evidence of neuron impairment by oral infection with verotoxin-producing Escherichia coli O157 : H- in mitomycin-treated mice. Infect Immun 62:3447–3453[PubMed]
     [Google Scholar]
  13. Garber L. P., Wells S. J., Hancock D. D., Doyle M. P., Tuttle J., Shere J. A., Zhao T. 1995; Risk factors for fecal shedding of Escherichia coli O157 : H7 in dairy calves. J Am Vet Med Assoc 207:46–49[PubMed]
     [Google Scholar]
  14. Garmendia J., Frankel G., Crepin V. F. 2005; Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73:2573–2585 [View Article][PubMed]
     [Google Scholar]
  15. Gianantonio C. A., Vitacco M., Mendilaharzu F., Gallo G. E., Sojo E. T. 1973; The hemolytic-uremic syndrome. Nephron 11:174–192 [View Article][PubMed]
     [Google Scholar]
  16. Gray J. T., Fedorka-Cray P. J., Stabel T. J., Kramer T. T. 1996; Natural transmission of Salmonella Choleraesuis in swine. Appl Environ Microbiol 62:141–146[PubMed]
     [Google Scholar]
  17. Grif K., Dierich M. P., Karch H., Allerberger F. 1998; Strain-specific differences in the amount of Shiga toxin released from enterohemorrhagic Escherichia coli O157 following exposure to subinhibitory concentrations of antimicrobial agents. Eur J Clin Microbiol Infect Dis 17:761–766 [View Article][PubMed]
     [Google Scholar]
  18. Griffin P. M., Tauxe R. V. 1991; The epidemiology of infections caused by Escherichia coli O157 : H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 13:60–98[PubMed]
     [Google Scholar]
  19. Hancock D. D., Besser T. E., Rice D. H., Herriott D. E., Tarr P. I. 1997; A longitudinal study of Escherichia coli O157 in fourteen cattle herds. Epidemiol Infect 118:193–195 [View Article][PubMed]
     [Google Scholar]
  20. Karmali M. A. 1989; Infection by verocytotoxin-producing Escherichia coli . Clin Microbiol Rev 2:15–38[PubMed]
     [Google Scholar]
  21. Karmali M. A., Petric M., Lim C., Cheung R., Arbus G. S. 1985; Sensitive method for detecting low numbers of verotoxin-producing Escherichia coli in mixed cultures by use of colony sweeps and polymyxin extraction of verotoxin. J Clin Microbiol 22:614–619[PubMed]
     [Google Scholar]
  22. Keepers T. R., Psotka M. A., Gross L. K., Obrig T. G. 2006; A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J Am Soc Nephrol 17:3404–3414 [View Article][PubMed]
     [Google Scholar]
  23. Koitabashi T., Vuddhakul V., Radu S., Morigaki T., Asai N., Nakaguchi Y., Nishibuchi M. 2006; Genetic characterization of Escherichia coli O157 :  H7/− strains carrying the stx2 gene but not producing Shiga toxin 2. Microbiol Immunol 50:135–148[PubMed] [CrossRef]
     [Google Scholar]
  24. Leotta G. A., Chinen I., Epszteyn S., Miliwebsky E., Melamed I. C., Motter M., Ferrer M., Marey E., Rivas M. 2005; [Validation of a multiplex PCR for detection of Shiga toxin-producing Escherichia coli]. Rev Argent Microbiol 37:1–10 (in Spanish) [PubMed]
     [Google Scholar]
  25. Lindgren S. W., Melton A. R., O’Brien A. D. 1993; Virulence of enterohemorrhagic Escherichia coli O91 : H21 clinical isolates in an orally infected mouse model. Infect Immun 61:3832–3842[PubMed]
     [Google Scholar]
  26. Linton A. H., Al-Chalaby Z. A., Hinton M. H. 1985; Natural subclinical Salmonella infection in chickens: a potential model for testing the effects of various procedures on Salmonella shedding. Vet Rec 116:361–364 [View Article][PubMed]
     [Google Scholar]
  27. Lyte M., Arulanandam B. P., Frank C. D. 1996; Production of Shiga-like toxins by Escherichia coli O157 : H7 can be influenced by the neuroendocrine hormone norepinephrine. J Lab Clin Med 128:392–398 [View Article][PubMed]
     [Google Scholar]
  28. Merrell D. S., Butler S. M., Qadri F., Dolganov N. A., Alam A., Cohen M. B., Calderwood S. B., Schoolnik G. K., Camilli A. 2002; Host-induced epidemic spread of the cholera bacterium. Nature 417:642–645 [View Article][PubMed]
     [Google Scholar]
  29. Molyneux G., Gibson F. M., Gordon-Smith E. C., Pilling A. M., Liu K. C., Rizzo S., Sulsh S., Turton J. A. 2005; The haemotoxicity of mitomycin in a repeat dose study in the female CD-1 mouse. Int J Exp Pathol 86:415–430 [View Article][PubMed]
     [Google Scholar]
  30. Mühldorfer I., Hacker J., Keusch G. T., Acheson D. W., Tschäpe H., Kane A. V., Ritter A., Olschläger T., Donohue-Rolfe A. 1996; Regulation of the Shiga-like toxin II operon in Escherichia coli . Infect Immun 64:495–502[PubMed]
     [Google Scholar]
  31. Nagano K., Taguchi K., Hara T., Yokoyama S., Kawada K., Mori H. 2003; Adhesion and colonization of enterohemorrhagic Escherichia coli O157 : H7 in cecum of mice. Microbiol Immunol 47:125–132[PubMed] [CrossRef]
     [Google Scholar]
  32. Neely M. N., Friedman D. I. 1998; Functional and genetic analysis of regulatory regions of coliphage H-19B: location of Shiga-like toxin and lysis genes suggest a role for phage functions in toxin release. Mol Microbiol 28:1255–1267 [View Article][PubMed]
     [Google Scholar]
  33. Orskov F., Orskov L. 1984; Serotyping of Escherichia coli. In Methods in Microbiology pp. 43–112 Edited by Bergan T. E. London: Academic Press;
     [Google Scholar]
  34. Palermo M., Alves-Rosa F., Rubel C., Fernández G. C., Fernández-Alonso G., Alberto F., Rivas M., Isturiz M. 2000; Pretreatment of mice with lipopolysaccharide (LPS) or IL-1β exerts dose-dependent opposite effects on Shiga toxin-2 lethality. Clin Exp Immunol 119:77–83 [View Article][PubMed]
     [Google Scholar]
  35. Paton A. W., Ratcliff R. M., Doyle R. M., Seymour-Murray J., Davos D., Lanser J. A., Paton J. C. 1996; Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with Shiga-like toxin-producing Escherichia coli . J Clin Microbiol 34:1622–1627[PubMed]
     [Google Scholar]
  36. Proux K., Cariolet R., Fravalo P., Houdayer C., Keranflech A., Madec F. 2001; Contamination of pigs by nose-to-nose contact or airborne transmission of Salmonella Typhimurium. Vet Res 32:591–600 [View Article][PubMed]
     [Google Scholar]
  37. Ribot E. M., Fair M. A., Gautom R., Cameron D. N., Hunter S. B., Swaminathan B., Barrett T. J. 2006; Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157 : H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3:59–67 [View Article][PubMed]
     [Google Scholar]
  38. Sauter K. A., Melton-Celsa A. R., Larkin K., Troxell M. L., O’Brien A. D., Magun B. E. 2008; Mouse model of hemolytic-uremic syndrome caused by endotoxin-free Shiga toxin 2 (Stx2) and protection from lethal outcome by anti-Stx2 antibody. Infect Immun 76:4469–4478 [View Article][PubMed]
     [Google Scholar]
  39. Shere J. A., Kaspar C. W., Bartlett K. J., Linden S. E., Norell B., Francey S., Schaefer D. M. 2002; Shedding of Escherichia coli O157 : H7 in dairy cattle housed in a confined environment following waterborne inoculation. Appl Environ Microbiol 68:1947–1954 [View Article][PubMed]
     [Google Scholar]
  40. Snyder J. A., Haugen B. J., Buckles E. L., Lockatell C. V., Johnson D. E., Donnenberg M. S., Welch R. A., Mobley H. L. 2004; Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72:6373–6381 [View Article][PubMed]
     [Google Scholar]
  41. Sperandio V., Torres A. G., Jarvis B., Nataro J. P., Kaper J. B. 2003; Bacteria–host communication: the language of hormones. Proc Natl Acad Sci U S A 100:8951–8956 [View Article][PubMed]
     [Google Scholar]
  42. Tree J. J., Wolfson E. B., Wang D., Roe A. J., Gally D. L. 2009; Controlling injection: regulation of type III secretion in enterohaemorrhagic Escherichia coli . Trends Microbiol 17:361–370 [View Article][PubMed]
     [Google Scholar]
  43. Turner S. M., Scott-Tucker A., Cooper L. M., Henderson I. R. 2006; Weapons of mass destruction: virulence factors of the global killer enterotoxigenic Escherichia coli . FEMS Microbiol Lett 263:10–20 [View Article][PubMed]
     [Google Scholar]
  44. Wadolkowski E. A., Burris J. A., O’Brien A. D. 1990; Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157 : H7. Infect Immun 58:2438–2445[PubMed]
     [Google Scholar]
  45. Wagner P. L., Acheson D. W., Waldor M. K. 2001a; Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichia coli . Infect Immun 69:1934–1937 [View Article][PubMed]
     [Google Scholar]
  46. Wagner P. L., Neely M. N., Zhang X., Acheson D. W., Waldor M. K., Friedman D. I. 2001b; Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 183:2081–2085 [View Article][PubMed]
     [Google Scholar]
  47. Wiles S., Dougan G., Frankel G. 2005; Emergence of a ‘hyperinfectious’ bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol 7:1163–1172 [View Article][PubMed]
     [Google Scholar]
  48. Yoshimatsu T., Shirai M., Nagata K., Okita K., Nakazawa T. 2000; Transmission of Helicobacter pylori from challenged to nonchallenged nude mice kept in a single cage. Dig Dis Sci 45:1747–1753 [View Article][PubMed]
     [Google Scholar]
  49. Zhang Y., Laing C., Zhang Z., Hallewell J., You C., Ziebell K., Johnson R. P., Kropinski A. M., Thomas J. E. other authors 2010; Lineage and host source are both correlated with levels of Shiga toxin 2 production by Escherichia coli O157 : H7 strains. Appl Environ Microbiol 76:474–482 [View Article][PubMed]
     [Google Scholar]
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Shiga toxin-producing Escherichia coli O157 : H7 shows an increased pathogenicity in mice after the passage through the gastrointestinal tract of the same host
J. Med. Microbiol. 61, 852 (2012); https://doi.org/10.1099/jmm.0.041251-0
/content/journal/jmm/10.1099/jmm.0.041251-0
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