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Identification of virulence attributes of gastrointestinal Escherichia coli isolates of veterinary significance

Published online by Cambridge University Press:  28 February 2007

Chitrita DebRoy  and
Carol W. Maddox
Chitrita DebRoy*
Affiliation:
Gastroenteric Disease Center, Department of Veterinary Science, The Pennsylvania State University, University Park, PA 16802Urbana, IL 61802, USA
Carol W. Maddox
Affiliation:
Veterinary Diagnostic Laboratory, University of Illinois- Urbana/Champaign, Urbana, IL 61802, USA
*
*Gastroenteric Disease Center, Wiley Laboratory, Orchard Road, Pennsylvania State University, University Park, PA 16802, USA E-mail: rcd3@psu.edu
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Abstract

The pathogenic strains of Escherichia coli recovered from the intestinal tract of animals fall into categories called enterotoxigenic, enteropathogenic, enterohemorrhagic and necrotoxigenic. The other two categories, enteroinvasive and enteroaggregative, have not been reported in animals. The pathogenicity of these strains is determined by the presence of certain genes that encode adhesins and toxins, are generally organized in large blocks in chromosomes, large plasmids or phages, and are often transmitted horizontally between strains. In this review, we summarize current knowledge of the virulence attributes that determine the pathogenic potential of E. coli strains and the methods available to assess the virulence of the strains. We also discuss the clinical symptoms, the gross and histological lesions, and the molecular diagnostic methods our laboratories have implemented for detecting pathogenic strains of E. coli that are isolated from the gastrointestinal tract of animals.

Type
Research Article
Information
Animal Health Research Reviews , Volume 2 , Issue 2 , December 2001 , pp. 129 - 140
Copyright
Copyright © CAB International 2001

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References

Alexander, TJL (1994). Neonatal diarrhea in pigs. In: Gyles, CL (ed.), Escherichia coli in Domestic Animals and Humans. Wallingford: CAB International, pp. 151–170.Google Scholar
An, H, Fairbrother, J, Desautels, C and Mabrouk, T (2000). Presence of the Lee (locus of enterocyte effacement) in pig attaching effacing Escherichia coli and characterization of the eae, espA, espB and espD genes of PEPEC (pig EPEC) strain 1390. Microbial Pathogenesis 28: 291–300.CrossRefGoogle Scholar
Anderson, DG and Moseley, SL (1988). Escherichia coli F41 adhesin: genetic organization, nucleotide sequence and homology with the K88 determinant. Journal of Bacteriology 170: 4890–4896.CrossRefGoogle ScholarPubMed
Bertschinger, HU and Gyles, CL (1994). Oedema disease in pigs. In: Gyles, CL (ed.), Escherichia coli in Domestic Animals and Humans. Wallingford: CAB International, pp. 193–291.Google Scholar
Bilge, SS, Clausen, CR, Lau, W and Moseley, SL (1989). Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. Journal of Bacteriology 171: 4281–4289.CrossRefGoogle ScholarPubMed
Blanco, M, Blanco, JE, Blanco, J, Alonso, MP, Balsalobre, C, Mourino, M, Madrid, C and Juarez, A (1996). Polymerase chain reaction for detection of Escherichia coli strains producing cytotoxic necrotizing factor type 1 and type 2 (CNF-1 and CNF-2). Journal of Microbiological Methods 26: 95–101.CrossRefGoogle Scholar
Bosworth, BT, Dean-Nystrom, EA, Casey, TA and Neisbergs, HL (1998). Differentiation of F18ab+ and F18ac+ Escherichia coli by single-strand conformational polymorphism analysis of the major fimbrial subunit gene (fedA). Clinical and Diagnostic Laboratory Immunology 5: 299–302.CrossRefGoogle ScholarPubMed
Braaten, BA and Myers, LL (1977). Biochemical characteristics of enterotoxigenic and nonenterotoxigenic Escherichia coli isolated from calves with diarrhoea. American Journal of Veterinary Research 38: 1989–1991.Google Scholar
Butler, DG and Clarke, RC (1994). Diarrhoea and dysentery in calves. In: Gyles, CL (ed.), Escherichia coli in Domestic Animals and Humans. Wallingford: CAB International, pp. 91–116.Google Scholar
Campos, LC, Vieira, MA, Trabulsi, LR, da Silva, LA, Montiero-Neto, V and Gomes, TA (1999). Diffusely adhering Escherichia coli (DAEC) strains of fecal origin rarely express F1845 adhesin. Microbiology and Immunology 43: 167–170.CrossRefGoogle ScholarPubMed
China, B, Pirson, V, Mainil, J (1998). Prevalence and molecular typing of attaching and effacing Escherichia coli among calf populations in Belgium. Veterinary Microbiology 63: 249–259.CrossRefGoogle ScholarPubMed
Cox, E and Houvernaghel, A (1993). Comparison of the in vitro adhesion of K88, K99, F41 and 987P positive Escherichia coli to intestinal villi of 4–5 week old pigs. Veterinary Microbiology 34: 7–18.CrossRefGoogle Scholar
Dallas, WS, Gill, DM and Falkow, S (1979). Cistron encoding Escherichia coli heat labile toxin. Journal of Bacteriology 139: 850–858.CrossRefGoogle ScholarPubMed
DebRoy, C and Dangler, CA (1996). Generation of nucleic acid probe molecules. In: Dangler, CA (ed.), Nucleic Acid Analysis. Principles and Bioapplications. New York: Wiley-Liss, pp. 31–46.Google Scholar
DeGraaf, FK, Krenn, BE and Klaasen, P (1984). Organization and expression of genes involved in the biosynthesis of K99 fimbriae. Infection and Immunity 43: 508–514.CrossRefGoogle Scholar
De Rycke, J, Milon, A and Oswald, E (1999). Necrotoxic Escherichia coli (NTEC): two emerging categories of human and animal pathogens. Veterinary Research 30: 221–233.Google ScholarPubMed
DeVinney, R, Gauthier, A, Abe, A and Finlay, BB (1999). Enteropathogenic Escherichia coli: a pathogen that inserts its own receptor into host cells. Cell and Molecular Life Science 55: 961–976.Google ScholarPubMed
Endo, Y, Tsurugi, K, Yutsudo, T, Takeda, Y, Ogasawara, T and Igarashi, K. (1988). Site of action of a verotoxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes: RNA: N-glycosidase activity of the toxins. European Journal of Biochemistry 171: 45–50.CrossRefGoogle ScholarPubMed
Fagan, PK, Hornitzky, MA, Bettelheim, KA and Djordjevic, SP (1999). Detection of Shiga-like toxin (stx1 and stx2 ), intimin (eaeA) and enterohemorrhagic Escherichia coli (EHEC) hemolysin (EHEC hlyA) genes in animal feces by multiplex PCR. Applied and Environmental Microbiology 65: 868–872.CrossRefGoogle ScholarPubMed
Falzano, L, Fiorentini, C, Donelli, G, Michel, E, Kocks, C, Cossart, P, Cabanie, L, Oswald, E and Boquet, P (1993). Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor. Molecular Microbiology 9: 1247–1254.CrossRefGoogle ScholarPubMed
Faubert, C and Drolet, R (1992). Hemorrhagic gastroenteritis caused by Escherichia coli in piglets: clinical, pathological and microbiological findings. Canadian Veterinary Journal 33: 251–256.Google ScholarPubMed
Fischer, J, Maddox, C, Moxley, R, Kinden, D and Miller, M (1994). Pathogenicity of a bovine attaching and effacing Escherichia coli isolate lacking Shiga-like toxins. American Journal of Veterinary Research 55: 991–999.CrossRefGoogle ScholarPubMed
Francis, DH, Erikson, AK and Grange, PA (1999). K88 adhesins of enterotoxigenic Escherichia coli and their porcine enterocyte receptors. Advances in Experimental Medicine and Biology 473: 147–154.CrossRefGoogle ScholarPubMed
Franck, SM, Bosworth, BT and Moon, HW (1998). Multiplex PCR for enterotoxigenic, attaching and effacing and Shigatoxin-producing Escherichia coli from calves. Journal of Clinical Microbiology 36: 1795–1797.CrossRefGoogle Scholar
Gannon, VPJ, Rashed, M, King, RK and Thomas, EJG (1993). Detection and characterization of the eae gene of Shiga-like toxin producing Escherichia coli using polymerase chain reaction. Journal of Clinical Microbiology 31: 1268–1274.CrossRefGoogle ScholarPubMed
Goffaux, F, China, B, Jannssen, L, Pirson, V, Mainil, J (1999). The locus for enterocyte effacement (LEE) of enteropathogenic Escherichia coli (EPEC) from dogs and cats. Advances in Experimental Medical Biology 473: 129–136.CrossRefGoogle ScholarPubMed
Goffaux, F, China, B, Janssen, L and Mainil, J (2000) Genotypic characterization of enteropathogenic Escherichia coli (EPEC) isolated in Belgium from dogs and cats. Research in Microbiology 150: 865–871.CrossRefGoogle Scholar
Griffin, PM (1999). Escherichia coli O157:H7 and other enterohemorrhagic Escherichia coli. In: Blaser, MJ, Smith, PD, Ravdin, JI, Greenberg, HB and Guerrant, RL (eds), Infections of the Gastrointestinal Tract. New York: Raven Press, pp. 736–761.Google Scholar
Hampton, DJ (1994). Postweaning Escherichia coli diarrhoea in pigs. In: Gyles, CL (ed.), Escherichia coli in Domestic Animals and Humans. Wallingford: CAB International, pp. 171–191.Google Scholar
Hodgson, JC (1994). Disease due to E. coli in sheep. In: Gyles, CL (ed.), Escherichia coli in Domestic Animals and Humans. Wallingford: CAB International, pp. 135–150.Google Scholar
Humbert, J, Jouve, M, Le Bouguenec, C and Gounon, P (2000). Electron microscopic improvement in the study of diarrheagenic Escherichia coli . Microscopy Research and Technique 49: 383–393.3.0.CO;2-R>CrossRefGoogle Scholar
Inman, L, Cantey, J and Formal, S (1986). Colonization, virulence and mucosal interaction of an enteropathogenic Escherichia coli (strain RDEC-1) expressing Shigella somatic antigen in the rabbit intestine. Journal of Infectious Diseases 154: 742–751.CrossRefGoogle ScholarPubMed
Isaacson, RE, Fusco, PC, Brinton, CC and Moon, HW (1978 a). In vitro adhesion of Escherichia coli to porcine small intestinal epithelial cells: pili as adhesive factors. Infection and Immunity 21: 392–397.CrossRefGoogle ScholarPubMed
Isaacson, RE, Moon, HW and Schneider, RA (1978 b). Distribution and virulence of Escherichia coli in the small intestines of calves with and without diarrhea. American Journal of Veterinary Research 39: 1750–1755.Google ScholarPubMed
Jerse, AE and Kaper, JB (1991). The eae gene of enteropathogenic Escherichia coli encodes a 94- kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infection and Immunity 59: 4302–4309.CrossRefGoogle ScholarPubMed
Kaper, JB (1994). Molecular pathogenesis of enteropathogenic Escherichia coli. In: Miller, VL, Kaper, JB, Portnoy, DA and Isberg, RR (eds), Molecular Genetics of Bacterial Pathogenesis. Washington, DC: ASM Press, pp. 173–195.Google Scholar
Kaper, JB and O'Brien, AD (eds), 1998. Escherichia coli O157: H7 and other Shiga toxin-producing E. coli strains. Washington, DC: ASM Press.Google Scholar
Kenney, B, DeViney, R, Stein, M, Reinscheid, DJ, Frey, EA and FinPay, BB (1997). Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511–520.CrossRefGoogle Scholar
Korth, MJ, Schneider, RA and Moseley, SL (1991). An F41-K88-related genetic determinant of bovine septicemic Escherichia coli mediates expression of CS31A fimbriae and adherence to epithelial cells. Infection and Immunity 59: 2333–2340.CrossRefGoogle ScholarPubMed
Krogh, HV (1983). Occurrence of enterotoxigenic Escherichia coli in calves with acute neonatal diarrhoea. Nordisk Veterinaermedicin 35: 346–352.Google ScholarPubMed
Lalioui, L, Jouve, M, Gounon, P, Le Bouguenec, C (1999). Molecular cloning and characterization of the afa-7 and afa-8 gene clusters encoding afimbrial adhesin in Escherichia coli strains associated with diarrhea or septicemia in calves. Infection and Immunity 67: 5048–5059.CrossRefGoogle ScholarPubMed
Lathe, R, Hirth, P, DeWilde, M, Harford, N and Lecocq, JP (1980). Cell-free synthesis of enterotoxin of E. coli from a cloned gene. Nature 284: 473–474.CrossRefGoogle ScholarPubMed
Lee, CH, Moseley, SL, Moon, HW, Whipp, SC, Gyles, CL and So, M (1983). Characterization of the gene encoding heat-stable toxin II and preliminary molecular epidemiological studies of enterotoxigenic Escherichia coli heat-stable toxin II producers. Infection and Immunity 42: 264–268.CrossRefGoogle ScholarPubMed
Mainil, J (1999). Shiga/verocytotoxins and Shiga/verotoxigenic Escherichia coli in animals. Veterinary Research 30: 235–257.Google ScholarPubMed
Mainil, JG, Daube, G, Jacquemin, E, Pohl, P and Kaeckenbeeck, A (1998). Virulence plasmids of enterotoxigenic Escherichia coli isolates from piglets. Veterinary Microbiology 62: 291–301.CrossRefGoogle ScholarPubMed
Mainil, J, Gerardin, J and Jacquemin, E (2000). Identification of the F17 fimbrial subunit- and adhesin-encoding (f17A and f17G) gene variants in necrotoxigenic Escherichia coli from cattle, pigs and humans. Veterinary Microbiology 73: 327–335.CrossRefGoogle ScholarPubMed
Mooi, FR, DeGraaf, FK and VanEmbden, JDA (1979). Cloning, mapping and expression of the genetic determinant that encodes for the K88ab antigen. Nucleic Acids Research 6: 849–865.CrossRefGoogle ScholarPubMed
Moon, H, Nielsen, N, Kramer, T (1970). Experimental enteritic colibacillosis of the newborn pig: histopathology of the small intestine and changes in plasma electrolytes. American Journal of Veterinary Research 31: 103–112.Google Scholar
Morrissey, PM and Gougon, G (1986). Expression of a cloned 987P adhesion-antigen fimbrial determinant in Escherichia coli K-12 strain HB 101. Gene 43: 79–84.CrossRefGoogle Scholar
Moseley, SL, Echeverria, P, Seriwatana, J, Tirapat, C, Chaicumpa, W, Sakudaipeara, T and Falkow, S (1982). Identification of enterotoxigenic Escherichia coli by colony hybridization using three enterotoxin gene probes. Journal of Infectious Diseases 145: 863–869.CrossRefGoogle ScholarPubMed
Moseley, SL, Hardy, JW, Hug, MI, Echeverria, P and Falkow, S (1983). Isolation of nucleotide sequence determination of a gene encoding a heat-stable enterotoxin of Escherichia coli . Infection and Immunity 39: 1167–1174.CrossRefGoogle ScholarPubMed
Moxley, RA (2000). Edema disease. In: Smith, RA and Helman, RG (eds), Veterinary Clinics of North America: Food Animal Practice. Philadelphia: W. B. Saunders, pp. 175–185.Google Scholar
Moxley, R, Berberov, E, Francis, D, Xing, J, Moayeri, M, Welch, R, Baker, D and Barletta, R (1998). Pathogenicity of an enterotoxigenic Escherichia coli hemolysin (hlyA) mutant in gnotobiotic piglets. Infection and Immunity 66: 5031–5035.CrossRefGoogle ScholarPubMed
Nagy, B and Fekete, PZ (1999). Enterotoxigenic Escherichia coli (ETEC) in farm animals. Veterinary Research 30: 259–284.Google ScholarPubMed
Nagy, B, Whipp, S, Imberechts, H, Berstschneiger, H, Dean-Nystrom, E, Casey, T and Salajka, E (1997). Biological relationship between F18ab and F18ac fimbriae of enterotoxigenic and verotoxigenic Escherichia coli from weaned pigs with oedema disease or diarrhoea. Microbial Pathogenesis 22: 1–11.CrossRefGoogle ScholarPubMed
Nataro, JP and Kaper, JB (1998). Diarrheagenic Escherichia coli . Clinical Microbiology Review 11: 142–201.CrossRefGoogle ScholarPubMed
Newland, JW and Neill, RJ (1988). DNA probes for Shiga-like toxins I and II and toxin converting bacteriophages. Journal of Clinical Microbiology 26: 1292–1297.CrossRefGoogle ScholarPubMed
Ojeniyi, B, Ahrens, P and Meyling, A (1994). Detection of fimbrial and toxin genes in Escherichia coli and their prevalence in piglets with diarrhoea. The application of colony hybridization assay, polymerase chain reaction and phenotypic assays. Journal of Veterinary Medicine B 41: 49–59.CrossRefGoogle ScholarPubMed
Orden, JA, Ruiz-Santa-Quiteria, JA, Cid, D, Garcia, S and de la Fuente, R (1999). Prevalence and characteristics of necrotoxigenic Escherichia coli (NTEC) strains isolated from diarrhoeic dairy calves. Veterinary Microbiology 66: 265–273.CrossRefGoogle ScholarPubMed
Oswald, E, Schmidt, H, Morabito, S, Karch, H, Marches, O and Caprioli, A (2000). Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infection and Immunity 68: 64–71.CrossRefGoogle ScholarPubMed
Paton, AW and Paton, JC (1998). Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1 , stx2 , eaeA, enterohemorrhagic E. coli hlyA, rfb O111 and rfb O157 . Journal of Clinical Microbiology 36: 598–602.CrossRefGoogle Scholar
Salyers, A and Whitt, D (1994). Escherichia coli gastrointestinal infections in bacterial pathogenesis: a molecular approach. In: Bacterial Pathogenesis. Washington DC: ASM Press, pp. 190–204.Google Scholar
Saxena, SK, O'Brien, AD and Ackerman, EJ (1989). Shiga toxin, Shiga-like toxin II variant, and ricin are all single site RNA N-glycosidase of 28S RNA when microinjected into Xenopus oocytes. Journal of Biological Chemistry 264: 596–601.CrossRefGoogle ScholarPubMed
Schultsz, C, Pool, GJ, van Ketel, R, De Wevek, B, Speelman, P and Dankert, J (1994). Detection of enterotoxigenic Escherichia coli in stool samples by using nonradioactively labeled oligonucleotide DNA probes and PCR. Journal of Clinical Microbiology 32: 2393–2397.CrossRefGoogle ScholarPubMed
Small, PLC and Falkow, S (1986). Development of a DNA probe for the virulence plasmid of Shigella spp. and enteroinvasive Escherichia coli. In: Leive, L, Bonventre, PF, Morello, JA, Silver, SD and Wu, WC (eds), Microbiology—1986. Washington, DC: American Society for Microbiology, pp. 121–124.Google Scholar
Sommerfelt, H, Kallard, KH, Raj, P, Moseley, SL, Bhan, MK and Bjorvatn, B (1988). Cloned polynucleotide and synthetic oligonucleotide probes used in colony hybridization are equally efficient in the identification of enterotoxigenic Escherichia coli . Journal of Clinical Microbiology 26: 2275–2278.CrossRefGoogle ScholarPubMed
Turk, J, Maddox, C, Fales, W, Ostlund, E, Miller, M, Johnson, G, Pace, L, Turnquist, S and Kreeger, J. (1998). Examination for heat-labile, heat stable, and Shiga-like toxins and for the eaeA gene in Escherichia coli isolates obtained from dogs dying with diarrhea: 122 cases (1992–1996). Journal of the American Veterinary Medical Association 212: 1735–1736.CrossRefGoogle ScholarPubMed
Tobe, T, Hayashi, T, Han, CG, Schoolnick, GK, Ogtsubo, E and Sasakawa, C (1999). Complete DNA sequence and structural analysis of the enteropathogenic Escherichia coli adherence factor plasmid. Infection and Immunity 67: 5455–5562.CrossRefGoogle ScholarPubMed
Van den Broeck, W, Cox, E, Oudega, B and Goddeeris, BM (2000). The F4 fimbrial antigen of Escherichia coli and its receptors. Veterinary Microbiology 71: 223–244.CrossRefGoogle ScholarPubMed
Weinstein, DL, Jackson, MP, Samuel, JE, Holmes, RK and O'Brien, AD (1988). Cloning and sequencing of a Shigalike toxin type II variant from an Escherichia coli strain responsible for edema disease of swine. Journal of Bacteriology 170: 4223–4230.CrossRefGoogle ScholarPubMed
Witham, PK, Yamashiro, CT, Livak, KJ and Batt, CA (1996). A PCR-based assay for the detection of Escherichia coli Shiga-like toxin gene in ground beef. Applied Environmental Microbiology 62: 1347–1353.CrossRefGoogle ScholarPubMed
Wray, C, McLaren, I and Pearson, GR (1989). Occurrence of attaching and effacing lesions in the small intestine of calves experimentally infected with bovine isolates of verocytotoxic E. coli . Veterinary Record 125: 365–368.CrossRefGoogle ScholarPubMed