Chapter 4 : Animals and Humans as Sources of Fecal Indicator Bacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Animals and Humans as Sources of Fecal Indicator Bacteria, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816865/9781555816087_Chap04-1.gif /docserver/preview/fulltext/10.1128/9781555816865/9781555816087_Chap04-2.gif


This chapter talks about the distribution of the major indicator bacteria, , spp., and a variety of anaerobes (including , spp., and members of the ) in humans, in domesticated animals and birds, and in undomesticated animal hosts. Enterococci are gram-positive bacteria ubiquitously found in the gastrointestinal (GI) tracts of animals, birds, and humans, as well as in soil and water. Enterococci are widely distributed among undomesticated mammals and birds, reptiles, and insects. Culture-independent analyses of total fecal bacterial microflora have been conducted with swine and equine samples using 16S rRNA gene libraries prepared from fecal DNA extracts and universal PCR primers for eubacterial 16S rRNA genes. A study by Fogarty and Voytek confirmed the presence of in the feces of deer ( sp.) inhabiting Virginia and West Virginia. In this study, feces were collected from 21 individual deer and extracted DNA was amplified with primers capable of amplifying 16S rRNA DNA from members of the group. Fecal indicator bacteria shed by humans and domestic animals are subject to profound alteration of their abundance and characteristics by anthropogenic effects of antibiotic use and waste treatment.

Citation: Yost C, Diarra M, Topp E. 2011. Animals and Humans as Sources of Fecal Indicator Bacteria, p 67-91. In Sadowsky M, Whitman R (ed), The Fecal Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816865.ch4

Key Concept Ranking

Microbial Ecology
Bacterial Proteins
Reverse Transcriptase PCR
Meat and Meat Products
Gram-Positive Cocci
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Aarestrup, F. M. 2006. Antimicrobial Resistance in Bacteria of Animal Origin. ASM Press, Washington, DC.
2. Aarestrup, F. M.,, P. Butaye,, and W. Whitte. 2002. Nonhuman reservoirs of enterocci, p. 5599. In M.S. Gilmore, D.B. Clewell, P.M. Courvalin, G.M. Dunny, B.E. Murray, and L. B. Rice (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. ASM Press, Washington, DC.
3. Adlerberth, I.,, and A. E. Wold. 2009. Establishment of the gut microbiota in western infants. Acta Paediat. 98:229238.
4. Aguirre, A. A.,, A. Angerbjorn,, M. Tannerfeldt,, and T. Morner. 2000. Health evaluation of arctic fox (Alopex lagopus) cubs in Sweden. J. Zoo Wildl. Med. 31:3640.
5. Ahmed, W.,, J. Stewart,, D. Powell,, and T. Gardner. 2008. Evaluation of the host-specificity and prevalence of Enterococci surface protein (esp) marker in sewage and its application for sourcing human fecal pollution. J. Environ. Qual. 37: 15831588.
6. Alam, M. J.,, and L. Zurek. 2004. Association of Escherichia coli O157:H7 with houseflies on a cattle farm. Appl. Environ. Microbiol. 70:75787580.
7. Anderson, J. F.,, T.D. Parrish, M. Akhtar,, L. Zurek,, and H. Hirt. 2008. Antibiotic resistance of Enterococci in American bison (Bison bison) from a nature preserve compared to that of Enterococci in pastured cattle. Appl. Environ. Microbiol. 74:17261730.
8. Aschfalk, A.,, N. Kemper,, and C. Holler. 2003. Bacteria of pathogenic importance in faeces from cadavers of free-ranging or corralled semi-domesticated reindeer in Northern Norway. Vet. Res. Commun. 27:93100.
9. Bach Knudsen, K. E. 2001. Development of antibiotic resistance and options to replace antimicrobials in animal diets. Proc. Nutr. Soc. 60:291299.
10. Bager, F.,, M. Madsen,, J. Christensen,, and F. M. Aarestrup. 1997. Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Prevent. Vet. Med. 31:95112.
11. Bartosch, S.,, A. Fite,, G.T. MacFarlane, and M. E. T. McMurdo. 2004. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl. Environ. Microbiol. 70:35753581.
12. Baurhoo, B.,, A. Letellier,, X. Zhao,, and C. A. Ruiz-Feria. 2007. Cecal populations of lactobacilli and bifidobacteria and Escherichia coli populations after in vivo Escherichia coli challenge in birds fed diets with purified lignin or mannanoligosaccharides. Poult. Sci. 86:25092516.
13. Bernhard, A. E.,, and K. G. Field. 2000. A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA. Appl. Environ. Microbiol. 66:45714574.
14. Beutin, L. 1999. Escherichia coli as a pathogen in dogs and cats. Vet. Res. 30:285298.
15. Boerlin, P.,, and R. J. Reid-Smith. 2008. Antimicrobial resistance: its emergence and transmission. Anim. Health Res. Rev. 9:115126.
16. Bonjoch, X.,, E. Ballese,, and A. R. Blanch. 2004. Multiplex PCR with 16S rRNA gene-targeted primers of Bifidobacterium spp. to identify sources of fecal pollution. Appl. Environ. Microbiol. 70: 31713175.
17. Bonnet, C.,, F, Diarrassouba,, R. Brousseau,, L. Masson,, and M. S. Diarra. 2009. Pathotype and antibiotic resistance gene distribution of Escherichia coli isolates from broiler chickens raised on antimicrobial supplemented diets. Appl. Environ. Microbiol. 75:69556962.
18. Buck, J. D.,, R.S. Wells, H.L. Rhinehart, and L. J. Hansen. 2006. Aerobic microorganisms associated with free-ranging bottlenose dolphins in coastal Gulf of Mexico and Atlantic Ocean waters. J. Wildl. Dis. 42:536544.
19. Butaye, P.,, L.A. Devriese, and F. Haesebrouck. 2003. Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin. Microbiol. Rev. 16:175188.
20. Buttiaux, R.,, and D. A. A. Mossel. 1961. The significance of various organisms of faecal origins and drinking water. J. Appl. Microbiol. 24:353364.
21. Byappanahalli, M. N.,, K. Przybyla-Kelly,, D.A. Shively, and R. L. Whitman. 2008. Environmental occurence of the enterococcal surface protein (esp) gene is an unreliable indicator of human fecal contamination. Environ. Sci.Technol. 42:80148020.
22. Call, D. R.,, M.A. Davis, and A. A. Sawant. 2008. Antimicrobial resistance in beef and dairy cattle production. Anim. Health Res. Rev. 9:159167.
23. Callaway, T. R.,, M.A. Carr, T.S. Edrington, R.C. Anderson, and D. J. Nisbet. 2009. Diet, Escherichia coli O157:H7, and cattle: a review after 10 years. Curr. Issues Mol. Biol. 11:6780.
24. Callaway, T. R.,, T.S. Edrington, R.C. Anderson, R.B. Harvey, K.J. Genovese, C.N. Kennedy, D.W. Venn, and D. J. Nisbet. 2008. Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim. Health Res. Rev. 9:217225.
25. Carman, R. J.,, S. Sayeed,, J.H. Li, C.W. Genheimer, M.F. Hiltonsmith, T.D. Wilkins, and B. A. McClane. 2008. Clostridium perfringens toxin genotypes in the feces of healthy North Americans. Anaerobe 14:102108.
26. Cauwerts, K.,, A. Decostere,, E. M. De Graef,, F. Haesebrouck,, and F. Pasmans. 2007. High prevalence of tetracycline resistance in enterococcus isolates from broilers carrying the erm(b) gene. Avaian Pathol. 36:395399.
27. Chase-Topping, M.,, D. Gally,, C. Low,, L. Matthews,, and M. Woolhouse. 2008. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat. Rev. Micro. 6:904912.
28. CIPARS. 2005. Canadian Integrated Program for Antimicrobial Resistance Surveillance: Annual Report. Health Canada, Ottawa, Ontario.
29. Cocito, C.,, M. Di Giambattista,, E. Nyssen,, and P. Vannuffel. 1997. Inhibition of protein synthesis by streptogramins and related antibiotics. J. Antimicrob. Chemother. 39: 713.
30. Conly, J. 2002. Antimicrobial resistance in Canada. Can. Med. Ass. J. 167:885891.
31. Coque, T. M. 2008. Evolutionary biology of pathogenic enterococci, p. 501521. In F. Baquero,, C. Nombela,, G.H. Cassell, and J. A. Guitiérrez (ed.), Evolutionary Biology of Bacterial and Fungal Pathogens. ASM Press, Washington, DC.
32. Cotruvo, J.,, A. Dufour,, G. Rees,, J. Bartram,, R. Carr,, D. Cliver,, G. Craun,, R. Fayer,, and V. P. J. Gannon (ed.). 2004. Waterborne Zoonoses: Identification, Causes and Control. IWA, London, UK.
33. Cotta, M. A.,, T.R. Whitehead, and R. L. Zeltwanger. 2003. Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits. Environ. Microbiol. 5:737745.
34. Cox, P.,, M. Griffith,, M. Angles,, D. Deere,, and C. Ferguson. 2005. Concentrations of pathogens and indicators in animal feces in the Sydney watershed. Appl. Environ. Microbiol. 71:59295934.
35. Damborg, P.,, S.S. Nielsen, and L. Guardabassi. 2009a. Escherichia coli shedding patterns in humans and dogs: Insights into within-household transmission of phylotypes associated with urinary tract infections. Epidemiol. Infect. 137:14571464.
36. Damborg, P.,, J. Top,, A. P.A. Hendrickx, S. Dawson,, R. J.L. Willems, and L. Guardabassi. 2009b. Dogs are a reservoir of ampicillin-resistant Enterococcus faecium lineages associated with human infections. Appl. Environ. Microbiol. 75: 23602365.
37. Delsol, A. A.,, L. Randall,, S. Cooles,, M.J. Woodward, J. Sunderland,, and J. M. Roe. 2005. Effect of the growth promoter avilamycin on emergence and persistence of antimicrobial resistance in enteric bacteria in the pig. J. Appl. Microbiol. 98:564571.
38. Deshpande, L. M.,, T.R. Fritsche, G.J. Moet, D.J. Biedenbach, and R. N. Jones. 2007. Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the sentry antimicrobial surveillance program. Diagn. Microbiol. Infect. Dis. 58:163170.
39. Diarra, M. S.,, F.G. Silversides, F. Diarrassouba,, J. Pritchard,, L. Masson,, R. Brousseau,, C. Bonnet,, P. Delaquis,, S. Bach,, B.J. Skura, and E. Topp. 2007. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Appl. Environ. Microbiol. 73:65666576.
40. Diarrassouba, F.,, M.S. Diarra, S. Bach,, P. Delaquis,, J. Pritchard,, E. Topp,, and B. J. Skura. 2007. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J. Food Prot. 70:13161327.
41. Dick, L. K.,, A.E. Bernhard, T.J. Brodeur, J. W.S. Domingo, J.M. Simpson, S.P. Walters, and K. G. Field. 2005. Host distributions of uncultivated fecal Bacteroidales bacteria reveal genetic markers for fecal source identification. Appl. Environ. Microbiol. 71:31843191.
42. Donnenberg, M. S. 2000. Pathogenic strategies of enteric bacteria. Nature 68:70287038.
43. Doyle, M. P.,, F. Busta,, B.R. Cords, P.M. Davidson, J. Hawke,, H.S. Hurd, R.E. Isaacson, K. Matthews,, J. Maurer,, J. Meng,, T.J. Montville, T.R. Shryock, J.N. Sofos, A.K. Vidaver, and L. Vogel. 2006. Antimicrobial resistance: implications for the food system: an expert report, funded by the IFT foundation. Comp. Rev. Food Sci. Food Saf. 5:71137.
44. Duriez, P.,, and E. Topp. 2007. Temporal dynamics and impact of manure storage on antibiotic resistance patterns and population structure of Escherichia coli isolates from a commercial swine farm. Appl. Environ. Microbiol. 73:54865493.
45. Duriez, P.,, Y. Zhang,, Z. Lu,, A. Scott,, and E. Topp. 2008. Loss of virulence genes in Escherichia coli populations during manure storage on a commercial swine farm. Appl. Environ. Microbiol. 74:39353942.
46. Edwards, J. E.,, S.A. Huws, E.J. Kim, M. R. F. Lee,, A. H. Kingston-Smith,, and N. D. Scollan. 2008. Advances in microbial ecosystem concepts and their consequences for ruminant agriculture. Animal 2:653660.
47. Facklam, R. R.,, M. G.S. Carvalho, and L. M. Teixeira. 2002. History, taxonomy, biochemical characteristics, and antibiotic susceptibility testing of Enterococci, p. 154. In M.S. Gilmore, D.B. Clewell, P.M. Courvalin, G.M. Dunny, B.E. Murray, and L. B. Rice (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. ASM Press, Washington, DC.
48. Fava, F.,, H. Mäkivuokko,, H. Siljander-Rasi,, H. Putaala,, K. Tiihonen,, J. Stowell,, K. Tuohy,, G. Gibson,, and N. Rautonen. 2007. Effect of polydextrose on intestinal microbes and immune functions in pigs. Br. J. Nutr. 98: 123133.
49. Field, K. G.,, and M. Samadpour. 2007. Fecal source tracking, the indicator paradigm, and managing water quality. Water Res. 41:35173538.
50. Fiksdal, L.,, J.S. Maki, S.J. Lacroix, and J. T. Staley. 1985. Survival and detection of Bacteroides spp., prospective indicator bacteria. Appl. Environ. Microbiol. 49:148150.
51. Finegold, S. M.,, H.R. Attebery, and V. L. Sutter. 1974. Effect of diet on human fecal flora -comparison of Japanese and American diets. Am. J. Clin. Nutr. 27:14561469.
52. Flammer, K.,, and L. A. Drewes. 1988. Species-related differences in the incidence of gram-negative bacteria isolated from the cloaca of clinically normal psittacine birds. Avian Dis. 32: 7983.
53. Fogarty, L. R.,, and M. A. Voytek. 2005. Comparison of Bacteroides-Prevotella 16S rRNA genetic markers for fecal samples from different animal species. Appl. Environ. Microbiol. 71:59996007.
54. Frey, J. C.,, J.M. Rothman, A.N. Pell, J.B. Nizeyi, M.R. Cranfield, and E. R. Angert. 2006. Fecal bacterial diversity in a wild gorilla. Appl. Environ. Microbiol. 72:37883792.
55. Fujita, S.,, and T. Kageyama. 2007. Polymerase chain reaction detection of Clostridium perfringens in feces from captive and wild chimpanzees, Pan troglodytes. J. Med. Primatol. 36:2532.
56. Garcia-Migura, L.,, E. Pleydell,, S. Barnes,, R.H. Davies, and E. Liebana. 2005. Characterization of vancomycin-resistant Enterococcus faecium isolates from broiler poultry and pig farms in england and wales. J. Clin. Microbiol. 43:32833289.
57. Gavini, F.,, V. Delcenserie,, K. Kopeinig,, S. Pollinger,, H. Beerens,, C. Bonaparte,, and M. Upmann. 2006. Bifidobacterium species isolated from animal feces and from beef and pork meat. J. Food Prot. 69:871877.
58. Gopee, N. V.,, A.A. Adesiyun, and K. Caesar. 2000. A longitudinal study of Escherichia coli strains isolated from captive mammals, birds, and reptiles in Trinidad. J. Zoo Wildl. Med. 31:353360.
59. Gordon, D. M.,, and A. Cowling. 2003. The distribution and genetic structure of Escherichia coli in australian vertebrates: host and geographic effects. Microbiology 149:35753586.
60. Graham, J. P.,, L.B. Price, S.L. Evans, T.K. Graczyk, and E. K. Silbergeld. 2009. Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci.Total Environ. 407: 27012710.
61. Gray, M. J.,, S. Rajeev,, D.L. Miller, A.C. Schmutzer, E.C. Burton, E.D. Rogers, and G. J. Hickling. 2007. Preliminary evidence that american bullfrogs (Rana catesbeiana) are suitable hosts for Escherichia coli O157:H7. Appl. Environ. Microbiol. 73:40664068.
62. Guzmán, M. C., M., de los Angeles Bistoni, L.M., Tamagnini, and R. D. González. 2004. Recovery of Escherichia coli in fresh water fish, Jenynsia multidentata and Bryconamericus iheringi. Water Res. 38:23682374.
63. Gyles, C. L. 2008. Antimicrobial resistance in selected bacteria from poultry. Anim. Health Res. Rev. 9:149158.
64. Gyles, C. L. 1994. Escherichia coli in Domestic Animals and Humans. CAB International, Wallingford, UK.
65. Hancock, L. E.,, and M. S. Gilmore. 2006. Pathogenicity of enterococci, p. 299311. In V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, and J. I. Rood (ed.), Gram-Positive Pathogens, 2nd ed. ASM Press, Washington, DC.
66. Hansen, D. L.,, J.J. Clark, S. Ishii,, M.J. Sadowsky, and R. E. Hicks. 2008. Sources and sinks of Escherichia coli in benthic and pelagic fish. J. Great Lakes Res. 34:228234.
67. Harwood, V. J.,, J. Butler,, D. Parrish,, and V. Wagner. 1999. Isolation of fecal coliform bacteria from the diamondback terrapin (Malaclemys terrapin centrata). Appl. Environ. Microbiol. 65:865867.
68. Hayashi, H.,, M. Sakamoto,, and Y. Benno. 2002. Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol. Immunol. 46:535548.
69. Hayes, J. R.,, L.L. English, P.J. Carter, T. Proescholdt,, K.Y. Lee, D.D. Wagner, and D. G. White. 2003. Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl. Environ. Microbiol. 69: 71537160.
70. Hong, P.-Y.,, J.-H. Wu,, and W.-T. Liu. 2008. Relative abundance of Bacteroides spp. in stools and wastewaters as determined by hierarchical oligonucleotide primer extension. Appl. Environ. Microbiol. 74:28822893.
71. Hongoh, Y.,, H. Yuzawa,, M. Ohkuma,, and T. Kudo. 2003. Evaluation of primers and PCR conditions for the analysis of 16S rRNA genes from a natural environment. FEMS Microbiol. Lett. 221: 299304.
72. Itoh, K.,, T. Mitsuoka,, K. Maejima,, C. Hiraga,, and K. Nakano. 1984. Comparison of fecal flora of cats based on different housing conditions with special reference to Bifidobacterium. Lab. Animal 18: 280284.
73. Jackson, C. R.,, P. J. Fedorka-Cray,, J.B. Barrett, L.M. Hiott, and T. A. Woodley. 2007. Prevalence of streptogramin resistance in enterococci from animals: Identification of Vatd from animal sources in the USA. Int. J. Antimicrob. Agents 30:6066.
74. Janda, J. M.,, and S. L. Abbott (ed.). 2006. Escherichia coli, p. 2358. In The Enterobacteria, 2nd ed. ASM Press, Washington, DC.
75. Jeter, S. N.,, C.M. McDermott, P.A. Bower, J.L. Kinzelman, M.J. Bootsma, G.W. Goetz, and S. L. McLellan. 2009. Bacteroidales diversity in ring-billed gulls (Larus delawarensis) residing at Lake Michigan beaches. Appl. Environ. Microbiol. 75:15251533.
76. Jiang, X. P.,, H. Yang,, B. Dettman,, and M. P. Doyle. 2006. Analysis of fecal microbial flora for antibiotic resistance in ceftiofur-treated calves. Foodborne Pathog. Dis. 3:355365.
77. Johnson, A. P.,, and D. M. Livermore. 1999. Quinupristin/dalfopristin, a new addition to the antimicrobial arsenal. Lancet 354:20122013.
78. Kanakaraj, R.,, D.L. Harris, J.G. Songer, and B. Bosworth. 1998. Multiplex PCR assay for detection of Clostridium perfringens in feces and intestinal contents of pigs and in swine feed. Vet. Microbiol. 63:2938.
79. Kikuchi, E.,, Y. Miyamoto,, S. Narushima,, and K. Itoh. 2002. Design of species-specific primers to identify 13 species of Clostridium harbored in human intestinal tracts. Microbiol. Immunol. 46: 353358.
80. Kildare, B. J.,, C.M. Leutenegger, B.S. McSwain, D.G. Bambic, V.B. Rajal, and S. Wuertz. 2007. 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: A bayesian approach. Water Res. 41:37013715.
81. Klibi, N.,, K. Ben Slama,, Y. Saenz,, A. Masmoudi,, S. Zanetti,, L.A. Sechi, A. Boudabous,, and C. Torres. 2007. Detection of virulence factors in high-level gentamicin-resistant Enterococcus faecalis and Enterococcus faecium isolates from a Tunisian hospital. Can. J. Microbiol. 53:372379.
82. Kozak, G. K.,, P. Boerlin,, N. Janecko,, R. J. Reid-Smith,, and C. Jardine. 2009. Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl. Environ. Microbiol. 75:559566.
83. La Ragione, R. M.,, A. Best,, M.J. Woodward, and A. D. Wales. 2009. Escherichia coli O157:H7 colonization in small domestic ruminants. FEMS Microbiol. Rev. 33:394410.
84. Lamendella, R.,, J. W. Santo Domingo,, C. Kelty,, and D. B. Oerther. 2008. Bifidobacteria in feces and environmental waters. Appl. Environ. Microbiol. 74:575584.
85. Lamendella, R.,, J. W. Santo Domingo,, D.B. Oerther, J.R. Vogel, and D. M. Stoeckel. 2007. Assessment of fecal pollution sources in a small northern-plains watershed using PCR and phylogenetic analyses of Bacteroidetes 16S rRNA gene. FEMS Microbiol. Ecol. 59:651660.
86. Langendijk, P. S.,, F. Schut,, G.J. Jansen, G.C. Raangs, G.R. Kamphuis, M. H.F. Wilkinson, and G. W. Welling. 1995. Quantitative fluorescence in-situ hybridization of Bifidobacterium spp with genus-specific 16S ribosomal-RNA-targeted probes and its application in fecal samples. Appl. Environ. Microbiol. 61:30693075.
87. Lauková, A.,, M. Simonová,, V., Strompfová, I., Styriak, A.C., Ouwehand, and M. Várady. 2008. Potential of enterococci isolated from horses. Anaerobe 14:234236.
88. Layton, A.,, L. McKay,, D. Williams,, V. Garrett,, R. Gentry,, and G. Sayler. 2006. Development of Bacteroides 16S rRNA gene taqman-based realtime PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl. Environ. Microbiol. 72:42144224.
89. Leclercq, R.,, and P. M. Courvalin. 2005. Enterococcus, p. 299313. In S.B. Levy, D. G., White,, M.N. Alekshun, and P. F. McDermott (ed.), Frontiers in Antimicrobial Resistance: A Tribute to Stuart B. Levy. ASM Press, Washington, DC.
90. Lefebvre, B.,, F. Malouin,, G. Roy,, K. Giguere,, and M. S. Diarra. 2006. Growth performance and shedding of some pathogenic bacteria in feed-lot cattle treated with different growth-promoting agents. J. Food Prot. 69:12561264.
91. Leser, T. D.,, J.Z. Amenuvor, T.K. Jensen, R.H. Lindecrona, M. Boye,, and K. Moller. 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl. Environ. Microbiol. 68:673690.
92. Lisle, J. T.,, J.J. Smith, D.D. Edwards, and G. A. McFeters. 2004. Occurrence of microbial indicators and Clostridium perfringens in wastewater, water column samples, sediments, drinking water, and weddell seal feces collected at McMurdo Station, Antarctica. Appl. Environ. Microbiol. 70: 72697276.
93. Lu, J.,, J. W. Santo Domingo,, S. Hill,, and T. A. Edge. 2009. Microbial diversity and host-specific sequences of Canada goose feces. Appl. Environ. Microbiol. 75:59195926.
94. Lu, J. R.,, and J. Santo Domingo. 2008. Turkey fecal microbial community structure and functional gene diversity revealed by 16S rRNA gene and metagenomic sequences. J. Microbiol. 46:469477.
95. Lu, J. R.,, J. Santo Domingo,, and O. C. Shanks. 2007. Identification of chicken-specific fecal microbial sequences using a metagenomic approach. Water Res. 41:35613574.
96. Lu, J. R.,, J. W. Santo Domingo,, R. Lamendella,, T. Edge,, and S. Hill. 2008. Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl. Environ. Microbiol. 74: 39693976.
97. Lu, J. R.,, U. Idris,, B. Harmon,, C. Hofacre,, J.J. Maurer, and M. D. Lee. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl. Environ. Microbiol. 69:68166824.
98. Lu, Z.,, D. Lapen,, A. Scott,, A. Dang,, and E. Topp. 2005. Identifying host sources of fecal pollution: diversity of Escherichia coli in confined dairy and swine production systems. Appl. Environ. Microbiol. 71:59925998.
99. Macovei, L.,, and L. Zurek. 2006. Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings. Appl. Environ. Microbiol. 72:40284035.
100. Maria, R.,, J. Ramer,, T. Reichard,, P.J. Tolson, and M. M. Christopher. 2007. Biochemical reference intervals and intestinal microflora of free-ranging Ricord’s Iguanas (Cyclura ricordii). J. Zoo Wild. Med. 38:414419.
101. Marks, S. L.,, E.J. Kather, P.H. Kass, and A. C. Melli. 2002. Genotypic and phenotypic characterization of Clostridium perfringens and Clostridium difficile in diarrheic and healthy dogs. J. Vet. Intern. Med. 16:533540.
102. Martinez, J.,, P. Dabert,, S. Barrington,, and C. Burton. 2009. Livestock waste treatment systems for environmental quality, food safety, and sustain-ability. Bioresour. Technol. 100:55275536.
103. Matsuda, K.,, H. Tsuji,, T. Asahara,, K. Matsumoto,, T. Takada,, and K. Nomoto. 2009. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl. Environ. Microbiol. 75:19611969.
104. Matsuki, T.,, K. Watanabe,, J. Fujimoto,, Y. Kado,, T. Takada,, K. Matsumoto,, and R. Tanaka. 2004. Quantitative PCR with 16S rRNA-gene-targeted species-specific primers for analysis of human intestinal bifidobacteria. Appl. Environ. Microbiol. 70: 167173.
105. McDermott, P. F.,, P. Cullen,, S.K. Hubert, S. D. McDermott,, M. Bartholomew,, S. Simjee,, and D. D. Wagner. 2005. Changes in antimicrobial susceptibility of native Enterococcus faecium in chickens fed virginiamycin. Appl. Environ. Microbiol. 71:49864991.
106. Mentula, S.,, J. Harmoinen,, M. Heikkila,, E. Westermarck,, M. Rautio,, P. Huovinen,, and E. Kononen. 2005. Comparison between cultured small-intestinal and fecal microbiotas in beagle dogs. Appl. Environ. Microbiol. 71:41694175.
107. Miller, J. J.,, B.P. Handerek, B.W. Beasley, E. C.S. Olson, L.J. Yanke, F.J. Larney, T.A. McAllister, B.M. Olson, L.B. Selinger, D.S. Chanasyk, and P. Hasselback. 2004. Quantity and quality of runoff from a beef cattle feedlot in Southern Alberta. J. Environ. Qual. 33:10881097.
108. Montgomery, J.,, D. Gillespie,, P. Sastrawan,, T. Fredeking,, and G. Stewart. 2002. Aerobic salivary bacteria in wild and captive komodo dragons. J. Wildl. Dis. 38:545551.
109. Moriarty, E. M.,, L.W. Sinton, M.L. Mackenzie, N. Karki,, and D. R. Wood. 2008. A survey of enteric bacteria and protozoans in fresh bovine faeces on New Zealand dairy farms. J. Appl. Microbiol. 105:20152025.
110. Mueller, S.,, K. Saunier,, C. Hanisch,, E. Norin,, L. Alm,, T. Midtvedt,, A. Cresci,, S. Silvi,, C. Orpianesi,, M.C. Verdenelli, T. Clavel,, C. Koebnick,, H. J.F. Zunft, J. Dore,, and M. Blaut. 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl. Environ. Microbiol. 72:10271033.
111. Nagachinta, S.,, and J. Chen. 2008. Transfer of class 1 integron-mediated antibiotic resistance genes from shiga toxin-producing Escherichia coli to a susceptible E. coli K-12 strain in storm water and bovine feces. Appl. Environ. Microbiol. 74:50635067.
112. Nandi, S.,, J.J. Maurer, C. Hofacre,, and A. O. Summers. 2004. Gram-positive bacteria are a major reservoir of class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:71187122.
113. National Research Council, and Committee on Indicators for Waterborne Pathogens (ed.). 2004. Indicators for Waterborne Pathogens. National Academies Press, Washington, DC.
114. Nebra, Y.,, X. Bonjoch,, and A. R. Blanch. 2003. Use of Bifidobacterium dentium as an indicator of the origin of fecal water pollution. Appl. Environ. Microbiol. 69:26512656.
115. Nisbet, D. J.,, T.R. Callaway, T.S. Edrington, R.C. Anderson, and T. L. Poole. 2008. Effects of ionophores on enterococcus faecalis and E. faecium growth in pure and mixed ruminal culture. Foodborne Pathog. Dis. 5:193198.
116. Novais, C.,, T.M. Coque, J.C. Sousa, and L. V. Peixe. 2006. Antimicrobial resistance among faecal enterococci from healthy individuals in Portugal. Clin. Microbiol. Infect. 12:11311134.
117. Nulsen, M. F.,, M.B. Mor, and D. E. B. Lawton. 2008. Antibiotic resistance among indicator bacteria isolated from healthy pigs in New Zealand. N. Z. Vet. J. 56:2935.
118. O’Hara, A. M.,, and F. Shanahan. 2006. The gut flora as a forgotten organ. EMBO Rep. 7:688693.
119. Ogier, J. C.,, and P. Serror. 2008. Safety assessment of dairy microorganisms: the Enterococcus genus. Int. J. Food Microbiol. 126:291301.
120. Okabe, S.,, and Y. Shimazu. 2007. Persistence of host-specific Bacteroides-Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity. Appl. Microbiol. Biotechnol. 76:935944.
121. Overland, M.,, N.P. Kjos, M. Borg,, E. Skjerve,, and H. Sorum. 2008. Organic acids in diets for entire male pigs: effect on skatole level, microbiota in digesta, and growth performance. Livest. Sci. 115:169178.
122. Petersson-Wolfe, C. S.,, S. Adams,, S.L. Wolf, and J. S. Hogan. 2008. Genomic typing of enterococci isolated from bovine mammary glands and environmental sources. J. Dairy Sci. 91:615619.
123. Picard, C.,, J. Fioramonti,, A. Francois,, T. Robinson,, F. Neant,, and C. Matuchansky. 2005. Review article: Bifidobacteria as probiotic agents - physiological effects and clinical benefits. Aliment Pharmacol.Ther. 22:495512.
124. Pierson, M. D.,, D.L. Zink, and L. M. Smoot. 2007. Indicator microorganisms and microbiological criteria, p. 6985. In L. R. Beuchat, and M. P. Doyle (ed.), Food Microbiology: Fundamentals and Frontiers, 3rd ed. ASM Press, Washington, DC.
125. Poeta, P.,, D. Costa,, G. Igrejas,, J. Rodrigues,, and C. Torres. 2007. Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Sus scrofa). Vet. Microbiol. 125:368374.
126. Potter, A.,, V. Gerdts,, and S.D. Littel-van den Hurk. 2008. Veterinary vaccines: alternatives to antibiotics? Anim. Health Res. Rev. 9:187199.
127. Prescott, J. F. 2008. Antimicrobial use in food and companion animals. Anim. Health Res. Rev. 9: 127133.
128. Rada, V.,, and J. Petr. 2002. Enumeration of bifidobacteria in animal intestinal samples. Vet. Med. 47:14.
129. Ram, J. L.,, B. Thompson,, C. Turner,, J.M. Nechuatal, H. Sheehan,, and J. Bobrin. 2007. Identification of pets and raccoons as sources of bacterial contamination of urban storm sewers using a sequence-based bacterial source tracking method. Water Res. 41:36053614.
130. Resnick, I. G.,, and M. A. Levin. 1981. Assessment of Bifidobacteria as indicators of human fecal pollution. Appl. Environ. Microbiol. 42:433438.
131. Rhodes, M. W.,, and J. Kator. 1999. Sorbitol-fermenting Bifidobacteria as indicators of diffuse human faecal pollution in estuarine watersheds. J. Appl. Microbiol. 87:528535.
132. Ricca, D. M.,, and J. J. Cooney. 1998. Coliphages and indicator bacteria in birds around Boston harbor. J. Ind. Microbiol. Biotechnol. 21:2830.
133. Rood, J. I.,, and S. T. Cole. 1991. Molecular genetics and pathogenesis of Clostridium perfringens. Microbiol. Rev. 55:621648.
134. Russell, J. B.,, and J. L. Rychlik. 2001. Factors that alter rumen microbial ecology. Science 292: 11191122.
135. Salyers, A. A.,, A. Gupta,, and Y. Wang. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 12:412416.
136. Sang, Y.,, and F. Blecha. 2008. Antimicrobial pep-tides and bacteriocins: alternatives to traditional antibiotics. Anim. Health Res. Rev. 9:227235.
137. Santoro, M.,, G. Hernandez,, M. Caballero,, and F. Garcia. 2006. Aerobic bacterial flora of nesting green turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. J. Zoo Wildl. Med. 37:549552.
138. Savichtcheva, O.,, and S. Okabe. 2006. Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res. 40: 24632476.
139. Sayah, R. S.,, J.B. Kaneene, Y. Johnson,, and R. Miller. 2005. Patterns of antimicrobial resistance observed in escherichia coli isolates obtained from domestic-and wild-animal fecal samples, human septage, and surface water. Appl. Environ. Microbiol. 71:13941404.
140. Scott, T. M.,, T.M. Jenkins, J. Lukasik,, and J. B. Rose. 2005. Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ. Sci. Technol. 39:283287.
141. Sghir, A.,, G. Gramet,, A. Suau,, V. Rochet,, P. Pochart,, and J. Dore. 2000. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl. Environ. Microbiol. 66:22632266.
142. Shah, H. N. 1991. The Genus Bacteroides and Related Taxa. Springer-Verlag, New York, NY.
143. Sharma, R.,, K. Munns,, T. Alexander,, T. Entz,, P. Mirzaagha,, L.J. Yanke, M. Mulvey,, E. Topp,, and T. McAllister. 2008. Diversity and distribution of commensal fecal Escherichia coli bacteria in beef cattle administered selected subtherapeutic antimicrobials in a feedlot setting. Appl. Environ. Microbiol. 74:61786186.
144. Silbergeld, E. K.,, J. Graham,, and L. B. Price. 2008. Industrial food animal production, antimicrobial resistance, and human health. Ann. Rev. Pub. Health 29:151169.
145. Simjee, S.,, L.B. Jensen, S.M. Donabedian, and M. J. Zervos. 2006. Enterococcus, p. 315328. In F. M. Aarestrup (ed.), Antimicrobial Resistance in Bacteria of Animal Origin. ASM Press, Washington DC.
146. Sinton, L. W.,, R.R. Braithwaite, C.H. Hall, and M. L. Mackenzie. 2007. Survival of indicator and pathogenic bacteria in bovine feces on pasture. Appl. Environ. Microbiol. 73:79177925.
147. Sjölund, M.,, J. Bonnedahl,, J. Hernandez,, S. Bengtsson,, G. Cederbrant,, J. Pinhassi,, G. Kahlmeter,, and B. Olsen. 2008. Dissemination of multidrug-resistant bacteria into the Arctic. Emerg. Infect. Dis. 14:7072.
148. Skurnik, D.,, R. Ruimy,, A. Andremont,, C. Amorin,, P. Rouquet,, B. Picard,, and E. Denamur. 2006. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 57:12151219.
149. Suchodolski, J. S.,, J. Camacho,, and J. M. Steiner. 2008. Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microb. Ecol. 66:567578.
150. Tannock, G. W.,, and G. Cook. 2002. Enterococci as members of the intestinal microflora of humans, p. 101132. In M.S. Gilmore, D.B. Clewell, P.M. Courvalin, G.M. Dunny, B.E. Murray and L. B. Rice (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. ASM Press, Washington, DC.
151. Tillotson, K.,, J. L. Traub-Dargatz,, C.E. Dickinson, R.P. Ellis, P.S. Morley, D.R. Hyatt, R.J. Magnuson, W.T. Riddle, D. Bolte,, and M. D. Salman. 2002. Population-based study of fecal shedding of Clostridium perfringens in broodmares and foals. J. Am. Vet. Med. Assoc. 220:342348.
152. Top, J.,, R. Willems,, and M. Bonten. 2008. Emergence of cc17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunol. Med. Microbiol. 52:297308.
153. Topp, E.,, A. Scott,, D.R. Lapen, E. Lyautey,, and P. Duriez. 2009. Livestock waste treatment systems for reducing environmental exposure to hazardous enteric pathogens: some considerations. Bioresour. Technol. 100:53955398.
154. Tschirdewahn, B.,, S. Notermans,, K. Wernars,, and F. Untermann. 1991. The presence of enterotoxigenic Clostridium perfringens strains in feces of various animals. Int. J. Food Microbiol. 14:175178.
155. Vilanova, X.,, A. Manero,, M. Cerda-Cuellar,, and A. R. Blanch. 2004. The composition and persistence of faecal coliforms and enterococcal populations in sewage treatment plants. J. Appl. Microbiol. 96:279288.
156. Walk, S. T.,, J.M. Mladonicky, J.A. Middleton, A.J. Heidt, J.R. Cunningham, P. Bartlett,, K. Sato,, and T. S. Whittam. 2007. Influence of antibiotic selection on genetic composition of Escherichia coli populations from conventional and organic dairy farms. Appl. Environ. Microbiol. 73:59825989.
157. Wassenaar, T. M.,, and P. Silley. 2008. Antimicrobial resistance in zoonotic bacteria: lessons learned from host-specific pathogens. Anim. Health Res. Rev. 9:177186.
158. Waturangi, D. E.,, A. Suwanto,, S. Schwarz,, and W. Erdelen. 2003. Identification of class 1 integrons-associated gene cassettes in Escherichia coli isolated from Varanus spp. in Indonesia. J. Antimi-crob. Chemother. 51:175177.
159. Weaver, K. 2006. Enterococcal genetics, p. 312331. In V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, and J. I. Rood (ed.), Gram-Positive Pathogens, 2nd ed. ASM Press, Washington, DC.
160. Weese, S. J. 2008. Antimicrobial resistance in companion animals. Anim. Health Res. Rev. 9: 169176.
161. Wheeler, A. L.,, P.G. Hartel, D.G. Godfrey, J.L. Hill, and W. I. Segars. 2002. Potential of Enterococcus faecalis as a human fecal indicator for microbial source tracking. J. Environ. Qual. 31:12861293.
162. Wood, A. J.,, and T. J. Trust. 1972. Some qualitative and quantitative aspects of the intestinal microflora of the glaucous-winged gull (Larus glauce-scens). Can. J. Microbiol. 18:15771583.
163. Yang, I. C.,, J.Y. Wang, and D. Y. C. Sihh. 2006. The level of fecal carriage and the toxic potential of Clostridium perfringens in the feces of a Taiwan subpopulation. J. Food Drug Anal. 14:8992.
164. Yates, M. V. 2007. Classical indicators in the 21st century - far and beyond the coliform. Wat. Environ. Res. 79:279286.
165. Yoon, J. W.,, and C. J. Hovde. 2008. All blood, no stool: enterohemorrhagic Escherichia coli O157:H7 infection. J. Vet. Sci. 9:219231.
166. Zaleski, K. J.,, K.L. Josephson, C.P. Gerba, and I. L. Pepper. 2005. Potential regrowth and recolonization of Salmonellae and indicators in bio-solids and biosolid-amended soil. Appl. Environ. Microbiol. 71:37013708.
167. Zhu, X. Y.,, T.Y. Zhong, Y. Pandya,, and R. D. Joerger. 2002. 16S rRNA-based analysis of mi-crobiota from the cecum of broiler chickens. Appl. Environ. Microbiol. 68:124137.


Generic image for table
Table 1

Indicator bacteria

Citation: Yost C, Diarra M, Topp E. 2011. Animals and Humans as Sources of Fecal Indicator Bacteria, p 67-91. In Sadowsky M, Whitman R (ed), The Fecal Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555816865.ch4

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error