1887

Abstract

We investigated the ability of isolated from septic patients with urinary tract infection (UTI) to translocate through the gastrointestinal (GI) tract of the same patients using cell-culture models. Forty-seven hospitalized patients with urosepsis were included in this study. was isolated from their urine and blood (total 94 isolates) and investigated for genetic relatedness and interaction with the cell lines A-498 and HT-29. An initial comparison of the strains isolated from urine and blood showed that 44 out of 47 patients (94 %) had identical strains in their blood and urine. The blood isolates adhered to both cell lines, although their rate of adherence to A-498 cells was significantly higher than that to HT-29 cells (5.8±3.8 per cell vs 2.8±1.9; <0.0001). The rate of translocation in A-498 cells was also significantly higher after 120 min (8.7×10 vs 2.9×10;  = 0.0006). Three non-identical blood isolates were unable to translocate in HT-29 cells, indicating that host immune factors might be more important than bacterial ability to translocate the GI epithelium in these patients. Our data showed that blood isolates from uroseptic patients are able to adhere to and translocate through both cell lines. This suggests that in patients with UTI may translocate from either the GI tract or the urinary tract, hence questioning the assumption that the urinary tract is the only source of septicaemia in these patients.

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2014-12-01
2019-12-07
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References

  1. Alexander J. W., Boyce S. T., Babcock G. F., Gianotti L., Peck M. D., Dunn D. L., Pyles T., Childress C. P., Ash S. K.. ( 1990;). The process of microbial translocation. . Ann Surg 212:, 496–510, discussion 511–512. [CrossRef][PubMed]
    [Google Scholar]
  2. Ansaruzzaman M., Albert M. J., Nahar S., Byun R., Katouli M., Kühn I., Möllby R.. ( 2000;). Clonal groups of enteropathogenic Escherichia coli isolated in case–control studies of diarrhoea in Bangladesh. . J Med Microbiol 49:, 177–185.[PubMed]
    [Google Scholar]
  3. Arthur M., Johnson C. E., Rubin R. H., Arbeit R. D., Campanelli C., Kim C., Steinbach S., Agarwal M., Wilkinson R., Goldstein R.. ( 1989;). Molecular epidemiology of adhesin and hemolysin virulence factors among uropathogenic Escherichia coli.. Infect Immun 57:, 303–313.[PubMed]
    [Google Scholar]
  4. Berg R. D.. ( 1980;). Mechanisms confining indigenous bacteria to the gastrointestinal tract. . Am J Clin Nutr 33: (Suppl), 2472–2484.[PubMed]
    [Google Scholar]
  5. Berg R. D.. ( 1981;). Promotion of the translocation of enteric bacteria from the gastrointestinal tracts of mice by oral treatment with penicillin, clindamycin, or metronidazole. . Infect Immun 33:, 854–861.[PubMed]
    [Google Scholar]
  6. Berg R. D., Garlington A. W.. ( 1979;). Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. . Infect Immun 23:, 403–411.[PubMed]
    [Google Scholar]
  7. Berry R. E., Klumpp D. J., Schaeffer A. J.. ( 2009;). Urothelial cultures support intracellular bacterial community formation by uropathogenic Escherichia coli. . Infect Immun 77:, 2762–2772. [CrossRef][PubMed]
    [Google Scholar]
  8. Brauner A., Kaijser B., Wretlind B., Kühn I.. ( 1991;). Characterization of Escherichia coli isolated in blood, urine and faeces from bacteraemic patients and possible spread of infection. . APMIS 99:, 381–386. [CrossRef][PubMed]
    [Google Scholar]
  9. Chen J., Griffiths M. W.. ( 1998;). PCR differentiation of Escherichia coli from other Gram-negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. . Lett Appl Microbiol 27:, 369–371. [CrossRef][PubMed]
    [Google Scholar]
  10. Clermont O., Bonacorsi S., Bingen E.. ( 2000;). Rapid and simple determination of the Escherichia coli phylogenetic group. . Appl Environ Microbiol 66:, 4555–4558. [CrossRef][PubMed]
    [Google Scholar]
  11. Couto C. R., Oliveira S. S., Queiroz M. L., Freitas-Almeida A. C.. ( 2007;). Interactions of clinical and environmental Aeromonas isolates with Caco-2 and HT29 intestinal epithelial cells. . Lett Appl Microbiol 45:, 405–410. [CrossRef][PubMed]
    [Google Scholar]
  12. Eto D. S., Jones T. A., Sundsbak J. L., Mulvey M. A.. ( 2007;). Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli.. PLoS Pathog 3:, e100. [CrossRef][PubMed]
    [Google Scholar]
  13. Gransden W. R., Eykyn S. J., Phillips I., Rowe B.. ( 1990;). Bacteremia due to Escherichia coli: a study of 861 episodes. . Rev Infect Dis 12:, 1008–1018. [CrossRef][PubMed]
    [Google Scholar]
  14. Grey P. A., Kirov S. M.. ( 1993;). Adherence to HEp-2 cells and enteropathogenic potential of Aeromonas spp. . Epidemiol Infect 110:, 279–287. [CrossRef][PubMed]
    [Google Scholar]
  15. Grubeck-Loebenstein B.. ( 1997;). Changes in the aging immune system. . Biologicals 25:, 205–208. [CrossRef][PubMed]
    [Google Scholar]
  16. Guarner C., Runyon B. A., Young S., Heck M., Sheikh M. Y.. ( 1997;). Intestinal bacterial overgrowth and bacterial translocation in cirrhotic rats with ascites. . J Hepatol 26:, 1372–1378. [CrossRef][PubMed]
    [Google Scholar]
  17. Hedlund M., Duan R. D., Nilsson Å., Svensson M., Karpman D., Svanborg C.. ( 2001;). Fimbriae, transmembrane signaling, and cell activation. . J Infect Dis 183: (Suppl 1), S47–S50. [CrossRef][PubMed]
    [Google Scholar]
  18. Holden N. J., Gally D. L.. ( 2004;). Switches, cross-talk and memory in Escherichia coli adherence. . J Med Microbiol 53:, 585–593. [CrossRef][PubMed]
    [Google Scholar]
  19. Johnson J. R.. ( 1991;). Virulence factors in Escherichia coli urinary tract infection. . Clin Microbiol Rev 4:, 80–128.[PubMed]
    [Google Scholar]
  20. Johnson J. R., Stell A. L.. ( 2000;). Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. . J Infect Dis 181:, 261–272. [CrossRef][PubMed]
    [Google Scholar]
  21. Kai-Larsen Y., Lüthje P., Chromek M., Peters V., Wang X., Holm Å., Kádas L., Hedlund K. O., Johansson J.. & other authors ( 2010;). Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. . PLoS Pathog 6:, e1001010. [CrossRef][PubMed]
    [Google Scholar]
  22. Katayama M., Xu D., Specian R. D., Deitch E. A.. ( 1997;). Role of bacterial adherence and the mucus barrier on bacterial translocation: effects of protein malnutrition and endotoxin in rats. . Ann Surg 225:, 317–326. [CrossRef][PubMed]
    [Google Scholar]
  23. Katouli M., Bark T., Ljungqvist O., Svenberg T., Möllby R.. ( 1994;). Composition and diversity of intestinal coliform flora influence bacterial translocation in rats after hemorrhagic stress. . Infect Immun 62:, 4768–4774.[PubMed]
    [Google Scholar]
  24. Katouli M., Nettebladt C. G., Muratov V., Ljungqvist O., Bark T., Svenberg T., Möllby R.. ( 1997;). Selective translocation of coliform bacteria adhering to caecal epithelium of rats during catabolic stress. . J Med Microbiol 46:, 571–578. [CrossRef][PubMed]
    [Google Scholar]
  25. Kühn I., Möllby R.. ( 1993;). The PhP-RS-System: a simple microplate method for studying coliform bacterial population. . J Microbiol Methods 17:, 255–259. [CrossRef]
    [Google Scholar]
  26. Leblebicioglu H., Esen S..Turkish Nosocomial Urinary Tract Infection Study Group ( 2003;). Hospital-acquired urinary tract infections in Turkey: a nationwide multicenter point prevalence study. . J Hosp Infect 53:, 207–210. [CrossRef][PubMed]
    [Google Scholar]
  27. Levert M., Zamfir O., Clermont O., Bouvet O., Lespinats S., Hipeaux M. C., Branger C., Picard B., Saint-Ruf C.. & other authors ( 2010;). Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. . PLoS Pathog 6:, e1001125. [CrossRef][PubMed]
    [Google Scholar]
  28. Ljungdahl M., Lundholm M., Katouli M., Rasmussen I., Engstrand L., Haglund U.. ( 2000;). Bacterial translocation in experimental shock is dependent on the strains in the intestinal flora. . Scand J Gastroenterol 35:, 389–397. [CrossRef][PubMed]
    [Google Scholar]
  29. MacFie J.. ( 2004;). Current status of bacterial translocation as a cause of surgical sepsis. . Br Med Bull 71:, 1–11. [CrossRef][PubMed]
    [Google Scholar]
  30. MacFie J., O’Boyle C., Mitchell C. J., Buckley P. M., Johnstone D., Sudworth P.. ( 1999;). Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. . Gut 45:, 223–228. [CrossRef][PubMed]
    [Google Scholar]
  31. MacFie J., Reddy B. S., Gatt M., Jain P. K., Sowdi R., Mitchell C. J.. ( 2006;). Bacterial translocation studied in 927 patients over 13 years. . Br J Surg 93:, 87–93. [CrossRef][PubMed]
    [Google Scholar]
  32. Macutkiewicz C., Carlson G., Clark E., Dobrindt U., Roberts I., Warhurst G.. ( 2008;). Characterisation of Escherichia coli strains involved in transcytosis across gut epithelial cells exposed to metabolic and inflammatory stress. . Microbes Infect 10:, 424–431. [CrossRef][PubMed]
    [Google Scholar]
  33. Maher S., McClean S.. ( 2006;). Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro.. Biochem Pharmacol 71:, 1289–1298. [CrossRef][PubMed]
    [Google Scholar]
  34. McNally A., Alhashash F., Collins M., Alqasim A., Paszckiewicz K., Weston V., Diggle M.. ( 2013;). Genomic analysis of extra-intestinal pathogenic Escherichia coli urosepsis. . Clin Microbiol Infect 19:, E328–E334. [CrossRef][PubMed]
    [Google Scholar]
  35. Moreno E., Andreu A., Pigrau C., Kuskowski M. A., Johnson J. R., Prats G.. ( 2008;). Relationship between Escherichia coli strains causing acute cystitis in women and the fecal E. coli population of the host. . J Clin Microbiol 46:, 2529–2534. [CrossRef][PubMed]
    [Google Scholar]
  36. Moss M.. ( 2005;). Epidemiology of sepsis: race, sex, and chronic alcohol abuse. . Clin Infect Dis 41: (Suppl. 7), S490–S497. [CrossRef][PubMed]
    [Google Scholar]
  37. Nettelbladt C. G., Katouli M., Volpe A., Bark T., Muratov V., Svenberg T., Möllby R., Ljungqvist O.. ( 1997;). Starvation increases the number of coliform bacteria in the caecum and induces bacterial adherence to caecal epithelium in rats. . Eur J Surg 163:, 135–142.[PubMed]
    [Google Scholar]
  38. Nettelbladt C. G., Katouli M., Bark T., Svenberg T., Möllby R., Ljungqvist O.. ( 2000;). Evidence of bacterial translocation in fatal hemorrhagic pancreatitis. . J Trauma 48:, 314–315. [CrossRef][PubMed]
    [Google Scholar]
  39. O’Boyle C. J., MacFie J., Mitchell C. J., Johnstone D., Sagar P. M., Sedman P. C.. ( 1998;). Microbiology of bacterial translocation in humans. . Gut 42:, 29–35. [CrossRef][PubMed]
    [Google Scholar]
  40. Parks R. W., Stuart Cameron C. H., Gannon C. D., Pope C., Diamond T., Rowlands B. J.. ( 2000;). Changes in gastrointestinal morphology associated with obstructive jaundice. . J Pathol 192:, 526–532. [CrossRef][PubMed]
    [Google Scholar]
  41. Ramos N. L., Saayman M. L., Chapman T. A., Tucker J. R., Smith H. V., Faoagali J., Chin J. C., Brauner A., Katouli M.. ( 2010;). Genetic relatedness and virulence gene profiles of Escherichia coli strains isolated from septicaemic and uroseptic patients. . Eur J Clin Microbiol Infect Dis 29:, 15–23. [CrossRef][PubMed]
    [Google Scholar]
  42. Saeedi B., Tärnberg M., Gill H., Hällgren A., Jonasson J., Nilsson L. E., Isaksson B., Kühn I., Hanberger H.. ( 2005;). Phene Plate (PhP) biochemical fingerprinting. A screening method for epidemiological typing of enterococcal isolates. . APMIS 113:, 603–612. [CrossRef][PubMed]
    [Google Scholar]
  43. Sedman P. C., Macfie J., Sagar P., Mitchell C. J., May J., Mancey-Jones B., Johnstone D.. ( 1994;). The prevalence of gut translocation in humans. . Gastroenterology 107:, 643–649. [CrossRef][PubMed]
    [Google Scholar]
  44. Sneath P. H. A., Sokal R. R.. (editors) ( 1973;). Numerical Taxonomy: the Principles and Practice of Numerical Classification. San Francisco:: W. H. Freeman & Co;.
    [Google Scholar]
  45. Snowden L., Wernbacher L., Stenzel D., Tucker J. R., McKay D., O’Brien M., Katouli M.. ( 2006;). Prevalence of environmental Aeromonas in South East Queensland, Australia: a study of their interactions with human monolayer Caco-2 cells. . J Appl Microbiol 101:, 964–975. [CrossRef][PubMed]
    [Google Scholar]
  46. Troeger H., Richter J. F., Beutin L., Günzel D., Dobrindt U., Epple H. J., Gitter A. H., Zeitz M., Fromm M., Schulzke J. D.. ( 2007;). Escherichia coli α-haemolysin induces focal leaks in colonic epithelium: a novel mechanism of bacterial translocation. . Cell Microbiol 9:, 2530–2540. [CrossRef][PubMed]
    [Google Scholar]
  47. Tullus K., Kühn I., Ørskov I., Ørskov F., Möllby R.. ( 1992;). The importance of P and type 1 fimbriae for the persistence of Escherichia coli in the human gut. . Epidemiol Infect 108:, 415–421. [CrossRef][PubMed]
    [Google Scholar]
  48. Vollmerhausen T. L., Ramos N. L., Gündogdu A., Robinson W., Brauner A., Katouli M.. ( 2011;). Population structure and uropathogenic virulence-associated genes of faecal Escherichia coli from healthy young and elderly adults. . J Med Microbiol 60:, 574–581. [CrossRef][PubMed]
    [Google Scholar]
  49. Wilson K. H., Blitchington R. B.. ( 1996;). Human colonic biota studied by ribosomal DNA sequence analysis. . Appl Environ Microbiol 62:, 2273–2278.[PubMed]
    [Google Scholar]
  50. Wold A. E., Caugant D. A., Lidin-Janson G., de Man P., Svanborg C.. ( 1992;). Resident colonic Escherichia coli strains frequently display uropathogenic characteristics. . J Infect Dis 165:, 46–52. [CrossRef][PubMed]
    [Google Scholar]
  51. Xu D., Lu Q., Deitch E. A.. ( 1998;). Elemental diet-induced bacterial translocation associated with systemic and intestinal immune suppression. . J Parenter Enteral Nutr 22:, 37–41. [CrossRef][PubMed]
    [Google Scholar]
  52. Yamamoto S., Tsukamoto T., Terai A., Kurazono H., Takeda Y., Yoshida O.. ( 1997;). Genetic evidence supporting the fecal-perineal-urethral hypothesis in cystitis caused by Escherichia coli. . J Urol 157:, 1127–1129. [CrossRef][PubMed]
    [Google Scholar]
  53. Yu P., Martin C. M.. ( 2000;). Increased gut permeability and bacterial translocation in Pseudomonas pneumonia-induced sepsis. . Crit Care Med 28:, 2573–2577. [CrossRef][PubMed]
    [Google Scholar]
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