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Effects of esculin and esculetin on the survival of Escherichia coli O157 in human faecal slurries, continuous-flow simulations of the rumen and colon and in calves

Published online by Cambridge University Press:  09 March 2007

Sylvia H. Duncan*
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
E. Carol McWilliam Leitch
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Karen N. Stanley
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Anthony J. Richardson
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Richard A. Laven
Affiliation:
Scottish Agricultural College, St Mary's Industrial Estate, Dumfries DG1 1DX, UK
Harry J. Flint
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Colin S. Stewart
Affiliation:
Gut Microbiology and Immunology Division, Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Dr S. H. Duncan, fax +44 1224 716687, email shd@rri.sari.ac.uk
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Abstract

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The human pathogen Escherichia coli O157:H7 is thought to be spread by direct or indirect contact with infected animal or human faeces. The present study investigated the effects of the plant coumarin esculin and its aglycone esculetin on the survival of a strain of E. coli O157 under gut conditions. The addition of these compounds to human faecal slurries and in vitro continuous-flow fermenter models simulating conditions in the human colon and rumen caused marked decreases in the survival of an introduced strain of E. coli O157. When four calves were experimentally infected with E. coli O157 and fed esculin, the pathogen was detected in five of twenty-eight (18 %) of faecal samples examined post-inoculation, compared with thirteen of thirty-five (37 %) of faecal samples examined from five control calves not fed esculin. Coumarin compounds that occur naturally in dietary plants or when supplemented in the diet probably inhibit the survival of E. coli O157 in the gut.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2004

References

Barbosa, TM & Levy, SB (2000) The impact of antibiotic use on antibiotic resistance development and persistence Drug Resist Uptake 3, 303311.CrossRefGoogle ScholarPubMed
Bryant, MP (1972) Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr 25, 13241328.CrossRefGoogle ScholarPubMed
Chapman, PA & Siddons, CA (1996) A comparison of immunomagnetic separation and direct culture for the isolation of verocytotoxin-producing Escherichia coli O157 from cases of bloody diarrhoea, non-bloody diarrhoea and asymptomatic contacts. J Med Microbiol 44, 267271.CrossRefGoogle ScholarPubMed
Chesson, A, Stewart, CS & Wallace, RJ (1982) Influence of plant phenolic acids on growth and cellulolytic activity of rumen bacteria. Appl Environ Microbiol 44, 597603.CrossRefGoogle ScholarPubMed
Dean-Nystrom, EA, Bosworth, BT, Moon, HW & O'Brien, AD (1998) Escherichia coli O157:H7 requires intimin for enteropathogenicity in calves. Infect Immun 66, 45604563.CrossRefGoogle ScholarPubMed
Diez-Gonzalez, F, Callaway, TR, Kizoulis, MG & Russell, JB (1998) Grain feeding and the dissemination of acid-resistant Escherichia coli from cattle. Science 281, 16661668.CrossRefGoogle ScholarPubMed
Duncan, SH (2001) Effects of rumen and gut microorganisms and their metabolites on the growth and survival of Escherichia coli O157. PhD thesis, University of Aberdeen, Aberdeen, Scotland, UK.Google Scholar
Duncan, SH, Flint, HJ & Stewart, CS, (1998) Inhibitory activity of gut bacteria against Escherichia coli O157 mediated by dietary plant metabolites. FEMS Microbiol Lett 164, 283288.CrossRefGoogle ScholarPubMed
Flint, HJ, Duncan, SH & Stewart, CS, (1987) Transmissible antibiotic resistance in strains of Escherichia coli isolated from the ovine rumen. Lett Appl Microbiol 5, 4749.CrossRefGoogle Scholar
Franks, AH, Harmsen, HJM, Raangs, GC, Jansen, GJ, Schut, F & Welling, GW (1998) Variations in bacterial populations in human faeces measured by fluorescent in situ hybridization with group-specific 16S rRNA targeted oligonucleotide probes. Appl Environ Microbiol 64, 33363345.CrossRefGoogle ScholarPubMed
Griffin, PM & Tauxe, RV (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and associated hemolytic uremic syndrome. Epidemiol Rev 13, 6098.CrossRefGoogle ScholarPubMed
Hammer, KA, Carlson, CF & Riley, TV (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86, 985990.CrossRefGoogle ScholarPubMed
Hungate, RE (1966) The Rumen and its Microbes New York: Academic Press.Google Scholar
James, CE, Stanley, KN, Allison, HE, Flint, HJ, Stewart, CS, Sharp, RJ, Saunders, JR & McCarthy, AJ (2001) Lytic and lysogenic infection of diverse Escherichia coli and Shigella strains with a verocytotoxigenic bacteriophage. Appl Environ Microbiol 67, 43354337.CrossRefGoogle ScholarPubMed
Kudva, IT, Blanch, K & Hovde, CJ (1998) Analysis of Escherichia coli O157:H7 survival in ovine or bovine manure and manure slurry. Appl Environ Microbiol 64, 13631370.CrossRefGoogle ScholarPubMed
Kudva, IT, Hatfield, PG & Hovde, CJ (1995) Effect of diet on the shedding of Escherichia coli O157 in a sheep model. Appl Environ Microbiol 61, 31663174.CrossRefGoogle Scholar
Laven, RA, Ashmore, A & Stewart, CS (2003) Escherichia coli in the rumen and colon of slaughter cattle, with particular reference to E coli O157. Vet J 165, 7883.CrossRefGoogle ScholarPubMed
McDougall, EI (1948) Studies on ruminant saliva. 1. The composition and output of sheep's saliva. Biochem J 43, 99109.CrossRefGoogle ScholarPubMed
Macfarlane, GT, Hay, S & Gibson, GR (1989) Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system J Appl Bacteriol 66, 407417.CrossRefGoogle Scholar
McKain, N, Wallace, RJ & Watt, ND (1992) Selective isolation of bacteria with dipeptidyl aminopeptidase type I activity from the sheep rumen FEMS Microbiol Lett 95, 169174.CrossRefGoogle Scholar
Miyazaki, K, Martin, JC, Marinsek-Logar, R & Flint, HJ (1997) Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P ruminicola subsp. brevis ) B14. Anaerobe 3, 373381.CrossRefGoogle ScholarPubMed
Moniello, G, Richardson, AJ, Duncan, SH & Stewart, CS (1996) Effects of coumarin and sparteine on attachment to cellulose and cellulolysis by Neocallimastix frontalis RE1 Appl Environ Microbiol 62, 46664668.CrossRefGoogle ScholarPubMed
Murray, RDH, Mendez, J & Brown, SA (1982) The Natural Coumarins: Occurrence, Chemistry and Biochemistry Chichester, UK: Wiley.Google Scholar
Nagy, JG & Tengerdy, RP (1968) Antibacterial action of essential oils of Artemisia as an ecological factor Appl Microbiol 16, 441444.CrossRefGoogle ScholarPubMed
Neill, MA (1998) Treatment of disease due to shigh toxin-producing Escherichia coli O157:H7 and Other Shiga Toxin-producing E coli Strains, pp. 357363, Kaper, JB and O'Brien, AD, editors]. Washington DC: ASM.Google Scholar
Ohnishi, M, Tanaka, C, Kuharas, S et al. , (1999) Chromosome of the enterohemorrhagic Escherichia coli O157:H7; comparative analysis with K-12 MG1655 revealed the acquisition of large amounts of foreign DNAs DNA Res 6, 361368.CrossRefGoogle ScholarPubMed
Parry, SM & Salmon, RL (1998) Sporadic STEC O157 infection: secondary household transmission in Wales. Emerg Infect Dis 4, 657661.CrossRefGoogle ScholarPubMed
Pryde, SE, Duncan, SHHold, GL, Stewart, CS & Flint, HJ (2002) The microbiology of butyrate formation in the human colon FEMS Microbiol Lett 217, 133139.CrossRefGoogle ScholarPubMed
Ramsak, A, Peterka, M, Tajima, K, Martin, JC, Wood, J, Johnston, MEA, Aminov, RI, Flint, HJ & Avgustin, G (2000) Unravelling the genetic diversity of ruminal bacteria belonging to the CBF phylum FEMS Microbiol Ecol 33, 6979.CrossRefGoogle Scholar
Rasmussen, MA, Cray, WC Jr, Casey, TA & Whipp, SC (1993) Rumen contents as a reservoir of enterohemorrhagic Escherichia coli FEMS Microbiol Lett 114, 7984.CrossRefGoogle ScholarPubMed
Rasmussen, MA, Wickman, TA, Cray, WC Jr & Casey, TA (1999) Escherichia coli O157 and the rumen environment Escherichia coli O157 in Farm Animals, pp.3949 [Stewart, CS and Flint, HJ, editors]. Wallingford. CABI Publishing.Google Scholar
Richardson, AJ, Calder, AG, Stewart, CS & Smith, A (1989) Simultaneous determination of volatile and non-volatile acid fermentation products of anaerobes by capillary gas chromatography Lett Appl Microbiol 9, 58.CrossRefGoogle Scholar
Russell, JB & Rychlik, JL (2001) Factors that alter rumen microbial ecology. Science 292, 11191122.CrossRefGoogle ScholarPubMed
Sambrook, J, Fritsch, EF & Maniatis, T (1982) Molecular Cloning - a Laboratory Manual 2nd ed. Cold Spring Harbor, NYCold Spring Harbor Laboratory.Google Scholar
Scott, KP, Mercer, DK, Glover, LA & Flint, HJ (1998) The green fluorescent protein as a visible marker for lactic acid bacteria in complex ecosystems FEMS Microbiol Ecol 26, 219230.CrossRefGoogle Scholar
Shoemaker, NB, Vlamakis, HHayes, K & Salyers, AA (2001) Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon Appl Environ Microbiol 64, 13901399.Google Scholar
Suau, A, Bonnet, RSutren, M, Godon, J-J, Gibson, GRCollins, MD & Dore, J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut Appl Environ Microbiol 65, 47994807.CrossRefGoogle ScholarPubMed
Tajima, K, Aminov, RI, Nagamine, T, Ogata, K, Nakamura, M, Matsui, H & Benno, Y (1999) Rumen bacterial diversity as determined by sequence analysis of 16S rDNA libraries. FEMS Microbiol Ecol 29, 159169.CrossRefGoogle Scholar
Teather, RM & Sauer, FD (1988) A naturally-compartmented rumen simulation system for the continuous culture of rumen bacteria and protozoa. J Dairy Sci 71, 666673.CrossRefGoogle Scholar
Toda, M, Okubo, S, Hiyoshi, R & Shimamura, T (1989) The bactericidal activity of tea and coffee. Lett Appl Microbiol 8, 123125.CrossRefGoogle Scholar
Van Soest, PJ (1994) The Nutritional Ecology of the Ruminant 2nd ed. Ithaca, NY: Cornell University PressCrossRefGoogle Scholar
Wallace, RJ, Arthaud, L & Newbold, CJ (1994) Influence of Yucca shidigera extract on rumen ammonia concentrations and ruminal microorganisms. Appl Environ Microbiol 60, 17621767.CrossRefGoogle ScholarPubMed
Wallace, RJ, Falconer, ML & Bhargava, PK (1989) Toxicity of volatile fatty acids at rumen pH prevents enrichment of Escherichia coli by sorbitol in rumen contents. Curr Microbiol 19, 277281.CrossRefGoogle Scholar
Wilson, KH (1997) Biota of the human gastrointestinal tract. In Gastrointestinal Microbiology, 3958 [Mackie, RI, Whyte, BA and Isaacson, RE, editors]. New York: ITP.CrossRefGoogle Scholar
Wolin, MJ (1969) Volatile fatty acids and inhibition of Escherichia coli growth by rumen fluid. Appl Environ Microbiol 17, 8387.CrossRefGoogle ScholarPubMed
Wolin, MJ (1981) Fermentation in the rumen and the human large intestine. Science 213, 14631468.CrossRefGoogle ScholarPubMed
Wong, CS, Jelacic, S, Habeeb, RL, Watkins, SL & Tarr, PI (2000) The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. New Eng J Med 342, 19301936.CrossRefGoogle ScholarPubMed
Zhao, T, Doyle, MP, Harmon, BG, Brown, CA, Mueller, POE & Parks, AH (1998) Reduction of carriage of enterohaemorrhagic Escherichia coli O157:H7 in cattle by inoculation with probiotic bacteria. J Clin Microbiol 36, 641647.CrossRefGoogle ScholarPubMed