Abstract
The purpose of this paper is to investigate the rate of translocation of Escherichia coli strains in different experimental/animal models. Four proficient translocating E. coli strains isolated from mesenteric lymph nodes (MLNs) and/or the blood of rats (strains KIC-1 and KIC-2), from a fatal case of pancreatitis (HMLN-1) and from pigs (PC-1 isolated in this study) were tested for their ability to translocate across two host species and the Caco-2 cell line as a model of the human gut epithelium. HMLN-1 was found in the MLNs of all 15 pigs tested. This strain, however, did not translocate in any rats and only colonised the caecum of four rats in small numbers. HMLN-1 and PC-1 were the dominant translocating strains in Caco-2 cells compared to KIC-1 and KIC-2, which were found to translocate at a lower rate in pigs and in Caco-2 cells. The rate of translocation of PC-1 in rats was also very low compared to KIC-1 and KIC-2. We suggest that, in studies aiming to investigate the mechanism of translocation of E. coli strains isolated from humans, rats may not be an appropriate animal model and that the Caco-2 cells or pigs are more suitable in vitro and in vivo models, respectively.
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References
Berg RD, Garlington AW (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
MacFie J, Reddy BS, Gatt M, Jain PK, Sowdi R, Mitchell CJ (2006) Bacterial translocation studied in 927 patients over 13 years. Br J Surg 93:87–93. doi:10.1002/bjs.5184
Finfer S, Bellomo R, Lipman J, French C, Dobb G, Myburgh J (2004) Adult-population incidence of severe sepsis in Australian and New Zealand intensive care units. Intensive Care Med 30:589–596. doi:10.1007/s00134-004-2157-0
MacFie J, O’Boyle C, Mitchell CJ, Buckley PM, 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
O’Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC (1998) Microbiology of bacterial translocation in humans. Gut 42:29–35
Deitch EA (1992) Multiple organ failure. Pathophysiology and potential future therapy. Ann Surg 216:117–134. doi:10.1097/00000658-199208000-00002
Nettelbladt CG, Katouli M, Bark T, Svenberg T, Möllby R, Ljungqvist O (2000) Evidence of bacterial translocation in fatal hemorrhagic pancreatitis. J Trauma 48:314–315. doi:10.1097/00005373-200002000-00021
Bark T, Katouli M, Ljungqvist O, Möllby R, Svenberg T (1993) Bacterial translocation after non-lethal hemorrhage in the rat. Circ Shock 41:60–65
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
Nettelbladt CG, Katouli M, Bark T, Svenberg T, Möllby R, Ljungqvist O (2003) Orally inoculated Escherichia coli strains colonize the gut and increase bacterial translocation after stress in rats. Shock 20:251–256. doi:10.1097/01.shk.0000068324.41183.c2
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. doi:10.1080/003655200750023958
Ljungdahl M, Rasmussen I, Haglund U (1999) Intestinal blood flow and intramucosal pH in experimental peritonitis. Shock 11:44–50
Kühn I, Burman LG, Haeggman S, Tullus K, Murray BE (1995) Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J Clin Microbiol 33:2812–2817
Sneath PHA, Sokal RR (1973) Numerical taxonomy. Freeman, San Francisco
Katouli M, Nettebladt CG, 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
Nettelbladt CG, Alibergovic A, Ljungqvist O (1996) Pre-stress carbohydrate solution prevents fatal outcome after hemorrhage in 24-hour food-deprived rats. Nutrition 12:696–699. doi:10.1016/S0899-9007(96)00165-7
Cruz N, Lu Q, Alvarez X, Deitch EA (1994) Bacterial translocation is bacterial species dependent: results using the human Caco-2 intestinal cell line. J Trauma 36:612–616. doi:10.1097/00005373-199405000-00002
Snowden L, Wernbacher L, Stenzel D, Tucker J, 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. doi:10.1111/j.1365-2672.2006.02919.x
Hidalgo IJ, Raub TJ, Borchardt RT (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96:736–749
Wells CL, Jechorek RP, Kinneberg KM, Debol SM, Erlandsen SL (1999) The isoflavone genistein inhibits internalization of enteric bacteria by cultured Caco-2 and HT-29 enterocytes. J Nutr 129:634–640
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. doi:10.1016/j.bcp.2006.01.012
Cruz N, Alvarez X, Berg RD, Deitch EA (1994) Bacterial translocation across enterocytes: results of a study of bacterial-enterocyte interactions utilizing Caco-2 cells. Shock 1:67–72. doi:10.1097/00024382-199401000-00012
Girardeau JP, Lalioui L, Said AM, De Champs C, Le Bouguénec C (2003) Extended virulence genotype of pathogenic Escherichia coli isolates carrying the afa-8 operon: evidence of similarities between isolates from humans and animals with extraintestinal infections. J Clin Microbiol 41:218–226. doi:10.1128/JCM.41.1.218-226.2003
Pang X, Hua X, Yang Q, Ding D, Che C, Cui L, Jia W, Bucheli P, Zhao L (2007) Inter-species transplantation of gut microbiota from human to pigs. ISME J 1:156–162. doi:10.1038/ismej.2007.23
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. doi:10.1016/j.micinf.2008.01.001
Imaoka A, Setoyama H, Takagi A, Matsumoto S, Umesaki Y (2004) Improvement of human faecal flora-associated mouse model for evaluation of the functional foods. J Appl Microbiol 96:656–663. doi:10.1111/j.1365-2672.2004.02189.x
Raibaud P, Ducluzeau R, Dubos F, Hudault S, Bewa H, Muller MC (1980) Implantation of bacteria from the digestive tract of man and various animals into gnotobiotic mice. Am J Clin Nutr 33:2440–2447
Cruz N, Alvarez X, Specian RD, Berg RD, Deitch EA (1994) Role of mucin, mannose, and beta-1 integrin receptors in Escherichia coli translocation across Caco-2 cell monolayers. Shock 2:121–126. doi:10.1097/00024382-199408000-00007
Jankowska A, Laubitz D, Antushevich H, Zabielski R, Grzesiuk E (2008) Competition of Lactobacillus paracasei with Salmonella enterica for adhesion to Caco-2 cells. J Biomed Biotechnol 2008:357964. doi:10.1155/2008/357964
Townsend S, Hurrell E, Forsythe S (2008) Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. BMC Microbiol 8:64–72. doi:10.1186/1471-2180-8-64
Bartolí R, Mañé J, Cabré E, Lorenzo-Zúñiga V, Planas R, Viñado B, Ausina V, Gassull MA (2007) Effect of the administration of fermentable and non-fermentable dietary fibre on intestinal bacterial translocation in ascitic cirrhotic rats. Clin Nutr 26:383–387. doi:10.1016/j.clnu.2007.01.008
Mogilner JG, Srugo I, Lurie M, Shaoul R, Coran AG, Shiloni E, Sukhotnik I (2007) Effect of probiotics on intestinal regrowth and bacterial translocation after massive small bowel resection in a rat. J Pediatr Surg 42:1365–1371. doi:10.1016/j.jpedsurg.2007.03.035
Murphy CG, Chen G, Winter DC, Bouchier-Hayes DJ (2007) Glutamine preconditioning protects against tourniquet-induced local and distant organ injury in a rodent ischemia-reperfusion model. Acta Orthop 78:559–566. doi:10.1080/17453670710014220
Quirino IEP, Correia MITD, Cardoso VN (2007) The impact of arginine on bacterial translocation in an intestinal obstruction model in rats. Clin Nutr 26:335–340. doi:10.1016/j.clnu.2006.12.007
Palma P, Mihaljevic N, Hasenberg T, Keese M, Koeppel TA (2007) Intestinal barrier dysfunction in developing liver cirrhosis: an in vivo analysis of bacterial translocation. Hepatol Res 37:6–12
Porras M, Martín MT, Yang PC, Jury J, Perdue MH, Vergara P (2006) Correlation between cyclical epithelial barrier dysfunction and bacterial translocation in the relapses of intestinal inflammation. Inflamm Bowel Dis 12:843–852. doi:10.1097/01.mib.0000231571.88806.62
van Minnen LP, Blom M, Timmerman HM, Visser MR, Gooszen HG, Akkermans LMA (2007) The use of animal models to study bacterial translocation during acute pancreatitis. J Gastrointest Surg 11:682–689. doi:10.1007/s11605-007-0088-0
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Katouli, M., Ramos, N.L., Nettelbladt, C.G. et al. Host species-specific translocation of Escherichia coli . Eur J Clin Microbiol Infect Dis 28, 1095–1103 (2009). https://doi.org/10.1007/s10096-009-0754-0
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DOI: https://doi.org/10.1007/s10096-009-0754-0