Planktonic and biofilm communities from 7-day-old chicken cecal microflora cultures: characterization and resistance to salmonella colonization

Journal of Food Protection

Volumn 72, Issue 9, 2009, Pages 1812-1820

  Sheffield, C L ^a   Crippen, T L ^a   Andrews, K ^a   Bongaerts, R J ^b   Nisbet, D J ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); KLEBSIELLA PNEUMONIAE; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

ANIMAL; ANIMAL DISEASE; ANIMAL SALMONELLOSIS; ARTICLE; BACTERIAL COUNT; BIOFILM; BIRD DISEASE; CECUM; CHICKEN; DISEASE PREDISPOSITION; FOOD CONTAMINATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; NEWBORN; PHYSIOLOGY; PRODUCT SAFETY; RIBOTYPING; SALMONELLA TYPHIMURIUM;

ANIMALS; ANIMALS, NEWBORN; BIOFILMS; CECUM; CHICKENS; COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; DISEASE SUSCEPTIBILITY; FOOD CONTAMINATION; HUMANS; POULTRY DISEASES; RIBOTYPING; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM;

EID: 70349421027     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-72.9.1812     Document Type: Article

References (57)

1. 1. Amit-Romach, E., D. Sklan, and Z. Uni. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult. Sci. 83:1093-1098, (Pubitemid 39197146)
2. Andrews, W. H., and T. S. Hammack. 2006. salmonella. In G. J. Jackson, R. I. Merker, and R. Bandler (ed.), Bacteriological analytical manual. U.S. Food and Drug Administration, Washington, DC.
3. Barnes, E. M., C. S. Impey, and D. M. Cooper. 1980. Manipulation of the crop and intestinal flora of the newly hatched chick. Am. J. Clin. Nutr. 33:2426-2433.
4. Barnes, E. M., G. C. Mead, and D. A. Bamum. 1972. The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. Br. Poult. Sci. 13:311-326.
5. Barrow, P. A. 1992. Probiotics for chickens, p. 227-252. In R. Fuller (ed.), Probiotics: the scientific basis. Chapman & Hall, London.
6. Battin, T. J., W. T. Sloan, S. Kjelleberg, H. Daims, I. M. Head, T. P. Curtis, and L. Eberl. 2007. Microbial landscapes: new paths to biofilm research. Nat. Rev. Microbiol. 5:76-81.
7. Bower, C. K., and M. A. Daeschel. 1999. Resistance responses of microorganisms in food environments. Int. J. Food Microbiol. 50:33-44.
8. Bradshaw, D. J., P. D. Marsh, K. M. Schilling, and D. Cummins. 1996. A modified chemostat system to study the ecology of oral biofilms. J. Appl. Bacteriol. 80:124-130.
9. Bryers, J. D. 2008. Medical biofilms. Biotechnol. Bioeng. 100:1-18.
10. Carman, R. J., M. A. Simon, H. Fernandez, M. A. Miller, and M. J. Bartholomew. 2004. Ciprofloxacin at low levels disrupts colonization resistance of human fecal microflora growing in chemostats. Regul. Toxicol. Pharmacol. 40:319-326.
11. Condon, S., and T. M. Cogan. 2000. Stimulation of propionic acid bacteria by lactic acid bacteria in cheese manufacture, Dairy Products Research Centre, Carlow, Ireland.
12. Corrier, D. E., A. Hinton, Jr., R. L. Ziprin, R. C. Beier, and J. R. DeLoach. 1990. Effect of dietary lactose on cecal pH, bacteriostatic volatile fatty acids and salmonella typhimurium colonization of broiler chicks. Avian Dis. 34:617-625.
13. Corner, D. E., D. J. Nisbet, C. M. Scanlan, A. G. Hollister, and J. R. DeLoach. 1995. Control of salmonella typhimurium colonization in broiler chicks with a continuous-flow characterized mixed culture of cecal bacteria. Poult. Sci. 74:916-924,
14. Crippen, T. L., C. L. Sheffield, K. Andrews, S. E. Dowd, R. J. Bongaerts, and D. J. Nisbet. 2008. Planktonic and biofilm community characterization and salmonella resistance of 14-day-old chicken cecal microflora-derived continuous-flow cultures. J. Food Prot. 71: 1981-1987.
15. 15. Davey,.M. E., and G. A. O'Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microb. Mol. Biol. Rev. 64:847-867. (Pubitemid 32475933)
16. Fanatico, A. 2002. Sustainable poultry: production overview-Part I. Production management. National Center for Appropriate Technology, Butte, MT.
17. Freter, R., G. D. Abrams, and A. Aranki. 1973. Patterns of interaction in gnotobiotic mice among bacteria of a synthetic "normal" intestinal flora, p. 429-433. In J. B. Heneghan (ed.), Germfree research: biological effect of gnotobiotic environments. Academic Press, New York.
18. 18. Freter, R., H. Brickner, M. Botney, D. Cleven, and A. Aranki. 1983. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect. Immun. 39:676-685. (Pubitemid 13188346)
19. 19. Freter, R., E. Stauffer, D. Cleven, L. V. Holdeman, and W. E. C. Moore. 1983. Continuous-flow cultures as in vitro models of the ecology of large intestinal flora. Infect. Immun. 39:666-675. (Pubitemid 13188345)
20. 20. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108. (Pubitemid 39490064)
21. Harvey, R. B., R. E. Droleskey, M. E. Hume, R. C. Anderson, K. J. Genovese, K. Andrews, and D. J. Nisbet. 2002. In vitro inhibition of salmonella enterica serovars Choleraesuis and Typhimurium, Escherichia coli F-18, and Escherichia coli 0157:H7 by a porcine continuous-flow competitive exclusion culture. Curr. Microbiol. 45: 226-229.
22. 22. Hautefort, I., M. J. Proenca, and J. C. D. Hinton. 2003. Single copy green fluorescent protein gene fusion allows accurate measurement of salmonella gene expression in vitro and during infection of mammalian cells. Appl. Environ. Microbiol. 69:7480-7491. (Pubitemid 38585404)
23. Hollister, A. G., D. E. Corner, D. J. Nisbet, and J. R. DeLoach. 1999. Effects of chicken-derived cecal microorganisms maintained in continuous culture on cecal colonization by salmonella typhimurium in turkey poults. Poult. Sci. 78:546-549.
24. 24. Hudault, S., H. Bewa, C. Bridonneau, and P. Raibaud. 1985. Efficiency of various bacterial suspensions derived from cecal flora of conventional chickens in reducing the population level of salmonella typhimurium in gnotobiotic mice and chicken intestines. Can. J. Microbiol. 31:832-838. (Pubitemid 16198480)
25. Hume, M. E., D. J. Nisbet, S. A. Buckley, R. L. Ziprin, R. C. Anderson, and L. H. Stanker. 2001. Inhibition of in vitro salmonella typhimurium colonization in porcine cecal bacteria continuous-flow competitive exclusion cultures. J. Food Prot. 64:17-22.
26. Hume, M. E., D. J. Nisbet, C. M. Scanlan, D. E. Corrier, and J. R. DeLoach. 1995. Fermentation of radiolabeled substrates by batch cultures of caecal microflora maintained in a continuous-flow culture. J. Appl. Bacteriol. 76:677-683.
27. Hunt, S. M., E. M. Werner, B. Huang, M. A. Hamilton, and P. S. Stewart. 2004. Hypothesis for the role of nutrient starvation in biofilm detachment. Appl. Environ. Microbiol. 70:7418-7425.
28. 28. Joseph, B., S. T. Otta, and I. Karunasagar. 2001. Biofilm formation by salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64:367-372. (Pubitemid 32186402)
29. Ledeboer, N. A., and B. D. Jones. 2005. Exopolysaccharide sugars contribute to biofilm formation by salmonella enterica serovar typhimurium on HEp-2 cells and chicken intestinal epithelium. J. Bacteriol. 187:3214-3226.
30. Lewis, K. 2001. Riddle of biofilm resistance. Antimkrob. Agents Chemother. 45:999-1007.
31. Mead, G. C. 1997. Bacteria in the gastrointestinal tract of bird, p. 216-240. In R. J. Mackie, B. A. White, and R. E. Isaacson (ed.), Gastrointestinal microbiology. Chapman & Hall, New York.
32. Mead, G. C., and B. W. Adams. 1975. Some observations on the caecal microflora of the chick during the first two weeks of life. Br. Poult. Sci. 16:169-176.
33. 33. Morales, C. A., S. Porwollik, J. G. Frye, H. Kinde, M. McClelland, and J. Guard-Bouldin. 2005. Correlation of phenotype with the genotype of egg-contaminating salmonella enterica serovar enteritidis. Appl. Environ. Microbiol. 71:4388-4399. (Pubitemid 41129492)
34. Nisbet, D. 2002. Defined competitive exclusion cultures in the prevention of enteropathogen colonization in poultry and swine. Antonie Leeuwenhoek 81:481-4867.
35. Nisbet, D. J., R. C. Anderson, D. E. Corrier, R. B. Harvey, and L. H. Stanker. 2000. Modeling the survivability of salmonella typhimurium in the chicken cecae using an anaerobic continuous-culture of chicken cecal bacteria. Microb. Ecol. Health Dis. 12:42-44
36. 36. Nisbet, D. J., D. E. Corrier, S. C. Ricke, M. E. Hume, J. A. Byrd, and J. R. DeLoach. 1996. Maintenance of the biological efficacy in chicks of a cecal competitive exclusion culture against salmonella by continuous-flow fermentation. J. Food Prot. 59:1279-1283. (Pubitemid 27047765)
37. Nurmi, E., and M. Rantala. 1973. New aspects of salmonella infection in broiler production. Nature 241:210-211.
38. Poole, T. L., M. E. Hume, K. J. Genovese, T. J. Anderson, C. L. Sheffield, K. M. Bischoff, and D. J. Nisbet. 2001. Persistence of a vancomycin-resistant Enterococcus faecium in an anaerobic continuous-flow culture of porcine microflora in the presence of subtherapeutic concentrations of vancomycin. Microb. Drug Resist. 7:343-348.
39. 39. Revolledo, L., C. S. Astolfi-Ferreira, and J. J. Piantino-Ferreira. 2003. Comparison of experimental competitive-exclusion cultures for controlling salmonella colonization in broiler chicks. Braz. J. Microbiol. 34:354-358. (Pubitemid 40747489)
40. 40. Revolledo, L., A. J. P. Ferreira, and G. C. Mead. 2006. Prospects in salmonella control: competitive exclusion, probiotic and enhancement of avian intestinal immunity. J. Appl. Poult. Res. 15: 341-351. (Pubitemid 43974247)
41. Roberts, T. 1989. Human illness costs of food-borne bacteria. Am. Agrie. Econ. Assoc. 192:494-497.
42. Salanitro, J. P., I. G. Fairchilds, and Y. D. Zgomicki. 1974. Isolation, culture characteristics, and identification of anaerobic bacteria from the chicken cecum. Appl. Microbiol. 27:678-687.
43. Savage, D. C. 1977. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31:107-133.
44. 44. Schneitz, C. 2005. Competitive exclusion in poultry-30 years of research. Food Control 16:657-667. (Pubitemid 40331414)
45. Schneitz, C., M. Häkkinen, L. Nuotio, E. Nurmi, and G. Mead. 1990. Droplet application for protecting chicks against salmonella colonization by competitive exclusion. Vet. Rec. 126:510.
46. Sheffield, C. L., T. L. Crippen, K. Andrews, R. J. Bongaerts, and D. J. Nisbet. 2009. Characterization of planktonic and biofilm communities of day-of-hatch chicks cecal microflora and their resistance to salmonella colonization. J. Food Prot. 72:959-965.
47. Singh, P. K., M. R. Parsek, E. P. Greenberg, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552-555.
48. Snoeyenbos, G. H., O. M. Weinack, and C. F. Smyser. 1978. Protecting chicks and poults from salmonellae by oral administration of "normal" gut microflora. Avian Dis. 22:273-287.
49. Spoering, A. L., and K. Lewis. 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183:6746-6751.
50. Stavrick, S. 1987. Microbial colonization of chicken intestine using defined cultures. Food Technol. 41:93-98.
51. Suci, P. A., and B. J. Tyler. 2003. A method for discrimination of subpopulations of Candida albicans biofilm cells that exhibit relative levels of phenotypic resistance to Chlorhexidine. J. Microbiol. Methods 53:313-325.
52. 52. Trachoo, N., J. F. Frank, and N. J. Stem. 2002. Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J. Food Prot. 65:1110-1116. (Pubitemid 34776095)
53. van der Wielen, P. W. J. J., S. Biesterveld, L. J. A. Lipman, and F. van Knapen. 2001. Inhibition of a glucose-limited sequencing fedbatch culture of salmonella entérica serovar Enteritidis by volatile fatty acids representative of the ceca of broiler chickens. Appl. Environ. Microbiol. 67:1979-1982.
54. van der Wielen, P. W. J. J., S. Biesterveld, S. Notermans, H. Hofstra, B. A. P. Urlings, and F. van Knapen. 2000. Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl. Environ. Microbiol. 66:2536-2540.
55. Wagner, R. D., D. D. Paine, and C. E. Cemiglia. 2003. Phenotypic and genotypic characterization of competitive exclusion products for use in poultry. J. Appl. Microbiol. 94:1098-1107.
56. 56. Wuertz, S., S. Okabe, and M. Hausner. 2004. Microbial communities and their interactions in biofilm systems: an overview. Water Sci. Technol. 49:327-336. (Pubitemid 39117212)
57. 57. Zhao, T., M. P. Doyle, and P. Zhao. 2004. Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Appl. Environ. Microbiol. 70:3996-4003. (Pubitemid 38969740)