Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T21:29:00.795Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of the commensal gut microbial community in broiler chickens

Published online by Cambridge University Press:  18 September 2007

Y. Lan ,
M.W.A. Verstegen ,
S. Tamminga  and
B.A. Williams
Y. Lan
Affiliation:
Animal Nutrition Group, Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
M.W.A. Verstegen*
Affiliation:
Animal Nutrition Group, Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
S. Tamminga
Affiliation:
Animal Nutrition Group, Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
B.A. Williams
Affiliation:
Animal Nutrition Group, Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
*
*Corresponding author: Martin.Verstegen@wur.nl
Get access

Abstract

To understand the relationship between the gastrointestinal inhabiting microbial community and broiler health, a literature review is presented. The available information on the development of gut microbial community, the relationship between commensal microflora and digestive function, the role of gut microorganisms on competitive exclusion of chickens against pathogens, and modulation of the gut microbial community by addition of prebiotics to the diet is summarized. Gut dominant microbial communities become more complex as broilers grow older. The establishment of the dominant bacterial community is affected by dietary and host-related factors. Dietary prebiotics can modulate bacterial community shift towards non-harmful bacteria, which is beneficial for the health of broiler chickens. Gut commensal microorganisms play an important role in the prevention of colonization by pathogens in the gastrointestinal tract of chickens, a process known as competitive exclusion. In conclusion, the dilemma caused by the forthcoming ban of antibiotics feed additives and need to maintain the intestinal health of broiler chickens, has produced an enormous interest in finding alternatives. Modulating the intestinal microbial community in a healthy direction, by dietary ingredients such as prebiotics, could be a good solution.

Keywords

gut microbial communitycompetitive exclusiongut mucosal cell proliferationprebioticbroiler chickens
Type
Reviews
Information
World's Poultry Science Journal , Volume 61 , Issue 1 , March 2005 , pp. 95 - 104
Copyright
Copyright © Cambridge University Press 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amit-Romach, E., Sklan, D. and Unil, Z. (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poultry Science 83: 1093–1098.CrossRefGoogle ScholarPubMed
Ane Knarreborg, M.A., Simon, , Engberg, R.M., Jensen, B.B. and Tannock, G.W. (2002) Effects of Dietary Fat Source and Subtherapeutic Levels of Antibiotic on the Bacterial Community in the Ileum of Broiler Chickens at Various Ages. Applied and Environmental Microbiology 68: 5918–5924.CrossRefGoogle ScholarPubMed
Apajalahti, J.H., Kettunen, A., Bedford, M.R. and Holben, W.E. (2001) Percent G+C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Applied and Environmental Microbiology 67: 5656–5667.CrossRefGoogle ScholarPubMed
Barnes, E.M., Impey, C.S. and Cooper, D.M. (1980) Manipulation of the crop and intestinal flora of the newly hatched chick. American Journal of Clinical Nutrition 33(11 Suppl): 2426–2433.CrossRefGoogle ScholarPubMed
Befus, A.D., Johnston, N., Leslin, G.A. and Bienenstock, J. (1980) Gut-associated lymphoid tissue in the chicken. I. Morphology, ontogeny, and some functional characteristics of Peyer's patches. The Journal of Immunology 125: 2626–2632.CrossRefGoogle ScholarPubMed
Berg, R.D. and Savage, D.C. (1975) Immune responses of specific germ-free and gnotobiotic mice to antigens of indigenous and nonindigenous microorganisms. Infection Immunology 11: 320–329.CrossRefGoogle ScholarPubMed
Braun, E.J. and Campbell, C.E. (1989) Uric acid decomposition in the lower gastrointestinal tract. The Journal of Experimental Zoology Supplement 3: 70–74.CrossRefGoogle ScholarPubMed
Carter, C.P. and Pollard, M. (1971) Host responses to “normal” microbial flora in germ-free mice. Journal of the Reticuloendothelial Society 9: 580–587.Google ScholarPubMed
Chu, S. and Montrose, M.H. (1995) Extracellular pH regulation in microdomains of colonic crypts: effects of short-chain fatty acids. Proceedings of the National Academy of Sciences USA: 3303–3307.CrossRefGoogle Scholar
Collins, M.D. and Gibson, G.R. (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. American Journal of Clinical Nutrition 69: 1052S–1057SCrossRefGoogle ScholarPubMed
Coloe, P.J., Bagust, T.J. and Ireland, L. (1984) Development of the normal gastrointestinal microflora of specific pathogen-free chickens. The Journal of Hygiene (Lond) 92(1): 79–87.CrossRefGoogle ScholarPubMed
Corrier, D.E., Hargis, B.M., Hinton, A. Jr. and Deloach, J.R. (1993) Protective effect of used poultry litter and lactose in the feed ration on Salmonella enteritidis colonization of leghorn chicks and hens. Avian Disease 37: 47–52.CrossRefGoogle ScholarPubMed
Drew, M.D., Van Kessel, A.G. and Maenz, D.D. (2003) Absorption of methionine and 2-hydroxy-4-methylthiobutoanic acid in conventional and germ-free chickens. Poultry Science 82: 1149–53.CrossRefGoogle ScholarPubMed
Engberg, R.M., Hedemann, M.S., Leser, T.D. and Jensen, B.B. (2000) Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poultry Science 79: 1311–1319.CrossRefGoogle ScholarPubMed
Ferreira, A. J., Ferreira, C.S., Knobl, T., Moreno, A.M., Bacarro, M.R., Chen, M., Robach, M. and Mead, G.C. (2003) Comparison of three commercial competitive-exclusion products for controlling Salmonella colonization of broilers in Brazil. Journal of Food Protection 66: 490–492.CrossRefGoogle ScholarPubMed
Fukunaga, T.M., Sasaki, Y., Araki, T., Okamoto, T., Yasuoka, T., Tsujikawa, , FUjiyama, Y. and Bamba, T. (2003) Effects of the soluble fibre pectin on intestinal cell proliferation, fecal short chain Fatty Acid production and microbial population. Digestion 67: 42–49.CrossRefGoogle ScholarPubMed
Furuse, M. and Yokota, H. (1984a) Effect of the gut microflora on the size and weight of organs of chicks fed diets of different protein content. British Poultry Science 25: 429–439.CrossRefGoogle ScholarPubMed
Furuse, M. and Yokota, H. (1984b) Protein and energy utilization in germ-free and conventional chicks given diets containing different levels of dietary protein. British Journal of Nutrition 51: 255–264.CrossRefGoogle ScholarPubMed
Gibson, G.R. (1998) Dietary modulation of the human gut microflora using prebiotics. British Journal of Nutrition 80: S209–S212.CrossRefGoogle ScholarPubMed
Gibson, G.R. and Roberfroid, M.B. (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125: 1401–1412.CrossRefGoogle ScholarPubMed
Glunder, G. (2002) Influence of diet on the occurrence of some bacteria in the intestinal flora of wild and pet birds. Deutsche tierarztliche Wochenschrift 109: 266–270.Google ScholarPubMed
Gong, J., Forster, R.J., Yu, H., Chambers, J.R., Sabour, P.M., Wheatcroft, R. and Chen, S. (2002) Diversity and phylogenetic analysis of bacteria in the mucosa of chicken caeca and comparison with bacteria in the caecal lumen. FEMS Microbiology Letters 208: 1–7.CrossRefGoogle Scholar
Goodlad, R.A., Ratcliffe, B., Fordham, J.P. and Wright, N.A. (1989) Does dietary fibre stimulate intestinal epithelial cell proliferation in germ free rats? Gut 30: 820–825.CrossRefGoogle ScholarPubMed
Goren, E., De Jong, W.A., Doornenbal, P., Koopman, J.P. and Kennis, H.M. (1984) Protection of chicks against Salmonella infantis infection induced by strict anaerobically cultured intestinal microflora. The Veterinary Quarterly 6: 22–26.CrossRefGoogle ScholarPubMed
Haller, D., Bode, C. and Hammes, W.P. (1999). Cytokine secretion by stimulated monocytes depends on the growth phase and heat treatment of bacteria: a comparative study between lactic acid bacteria and invasive pathogens. Microbiology Immunology 43: 925–935.CrossRefGoogle ScholarPubMed
Hegde, S.N., Rolls, B.A. and Coates, M.E. (1982) The effects of the gut microflora and dietary fibre on energy utilization by the chick. British Journal of Nutrition 48: 73–80.CrossRefGoogle ScholarPubMed
Hume, M.E., Byrd, J.A., Stanker, L.H. and Ziprin, R.L. (1998) Reduction of caecal Listeria monocytogenes in Leghorn chicks following treatment with a competitive exclusion culture (PREEMPT). Letter Applied Microbiology 26: 432–426.CrossRefGoogle ScholarPubMed
Hume, M.E., Kubena, L.F., Edrington, T.S., Donskey, C.J., Moore, R.W., Ricke, S.C. and Nisbet, D.J. (2003) Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poultry Science 82: 1100–1107.CrossRefGoogle ScholarPubMed
Jiangrang, L., Idris, U., Harmon, B., Hofacre, C., Maurer, J.J. and Lee, M.D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied Environmental Microbiology 69: 6816–6824.Google Scholar
Knarreborg, A., Simon, M.A., Engberg, R.M., Jensen, B.B. and Tannock, G.W. (2002) Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Applied and Environmental Microbiology 68: 5918–5924.CrossRefGoogle ScholarPubMed
Komai, M. and Kimura, S. (1980) Gastrointestinal responses to graded levels of cellulose feeding in conventional and germ-free mice. Journal of Nutrition Science Vitaminology (Tokyo) 26: 389–399.CrossRefGoogle ScholarPubMed
Kubena, L.F., Byrd, J.A., Young, C.R. and Corrier, D.E. (2001) Effects of tannic acid on caecal volatile fatty acids and susceptibility to Salmonella typhimurium colonization in broiler chicks. Poultry Science 80: 1293–1298.CrossRefGoogle ScholarPubMed
Lan, P.T., Hayashi, H., Sakamoto, M. and Benno, Y. (2002) Phylogenetic analysis of caecal microbiota in chicken by the use of 16S rDNA clone libraries. Microbiology Immunology 46: 371–382.CrossRefGoogle ScholarPubMed
Lan, Y., Xun, S., Tamminga, S., Williams, B.A., Verstegen, M.W.A. and Erdi, G. (2004) Realtime based detection of lactic acid bacteria in caecal contents of e. Tenella infected broilers fed soybean oligosaccharides and soluble soybean polysaccharides. Poultry Science 83: 1696–1702.CrossRefGoogle Scholar
Langhout, D.J., Schutte, J.B., De Jong, J., Sloetjes, H., Verstegen, M.W.A. And Tamminga, S. (2000) Effect of viscosity on digestion of nutrients in conventional and germ-free chicks. British Journal of Nutrition 83: 533–540.CrossRefGoogle ScholarPubMed
Le Blay, G., Blottiere, H.M., Ferrier, L., Le Foll, E.C., Bonnet, J. P., Galmiche, and Cherbut, C. (2000) Short-chain fatty acids induce cytoskeletal and extracellular protein modifications associated with modulation of proliferation on primary culture of rat intestinal smooth muscle cells. Digestive Disease Science 45: 1623–1630.CrossRefGoogle ScholarPubMed
Lupton, J.R., Coder, D.M. and Jacobs, L.R. (1985) Influence of luminal pH on rat large bowel epithelial cell cycle. American Journal of Physiology 249: G382–G388.Google ScholarPubMed
Mattocks, J.G. (1971) Goose feeding and cellulose digestion. Wild life 22: 107–113.Google Scholar
Mcbain, A.J. and Macfarlane, G.T. (2001) Modulation of genotoxic enzyme activities by non-digestible oligosaccharide metabolism in in-vitro human gut bacterial ecosystems. Journal of Medical Microbiology 50: 833–842.CrossRefGoogle ScholarPubMed
Mead, G.C. (1989) Microbes of the avian caecum: types present and substrates utilized. Journal of Experimental Zoology Suppl;3: 48–54.CrossRefGoogle ScholarPubMed
Mead, G.C. (2000) Prospects for ‘competitive exclusion’treatment to control salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111–123.CrossRefGoogle ScholarPubMed
Mead, G.C. and Adams, B.W. (1975) Some observations on the caecal microflora of the chick during the first two weeks of life. British Poultry Science 16: 169–176.CrossRefGoogle ScholarPubMed
Muramatsu, T., Kodama, H., Morishita, T., Furuse, M. and Okumura, J. (1991) Effect of intestinal microflora on digestible energy and fibre digestion in chickens fed a high-fibre diet. American Journal of Veterinary Research 52: 1178–1181.CrossRefGoogle Scholar
Muramatsu, T., Nakajima, S. and Okumura, J. (1994) Modification of energy metabolism by the presence of the gut microflora in the chicken. British Journal of Nutrition 71: 709–717.CrossRefGoogle ScholarPubMed
Muramatsu, T., Takasu, O. and Okumura, J. (1993) Research note: fructose feeding increases lower gut weights in germ-free and conventional chicks. Poultry Science 72: 1597–1600.CrossRefGoogle ScholarPubMed
Muramatsu, T., Takasu, O., Furuse, M. and Okumura, J. (1988) Effect of diet type on enhanced intestinal protein synthesis by the gut microflora in the chick. Journal of Nutrition 118: 1068–1074.CrossRefGoogle ScholarPubMed
Ohya, T. and Sato, S. (1983) Effects of dietary antibiotics on intestinal microflora in broiler chickens. National Institute of Animal Health quarterly (Tokyo) 23: 49–60.Google ScholarPubMed
Palmer, M.F. and Rolls, B.A. (1983) The activities of some metabolic enzymes in the intestines of germfree and conventional chicks. British Journal of Nutrition 50: 783–790.CrossRefGoogle ScholarPubMed
Parsons, C.M., Potter, L.M. and Brown, R.D. Jr. (1983) Effects of dietary carbohydrate and of intestinal microflora on excretion of endogenous amino acids by poultry. Poultry Science 62: 483–489.CrossRefGoogle ScholarPubMed
Philips, S.M. and Fuller, R. (1983) The activities of amylase and a trypsin-like protease in the gut contents of germ-free and conventional chickens. British Poultry Science 24: 115–121.CrossRefGoogle Scholar
Powrie, F. (1995) T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity 3: 171–174.CrossRefGoogle ScholarPubMed
Reilly, K.J., Frankel, W.L., Bain, A.M. and Rombeau, J.L. (1995) Colonic short chain fatty acids mediate jejunal growth by increasing gastrin. Gut 37: 81–86.CrossRefGoogle ScholarPubMed
Salvat, G., Lalande, F., Humbert, F. and Lahellec, C. (1992) Use of a competitive exclusion product (Broilact) to prevent Salmonella colonization of newly hatched chicks. International Journal of Food Microbiology 15: 307–311.CrossRefGoogle ScholarPubMed
Schiffrin, E.J. and Blum, S. (2002) Interactions between the microbiota and the intestinal mucosa. European Journal of Clinical Nutrition 56(Suppl 3): S60–S64.CrossRefGoogle ScholarPubMed
Schoeni, J.L. and Wong, A.C. (1994) Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Applied Environmental Microbiology 60: 1191–1197.CrossRefGoogle ScholarPubMed
Shea, K.M. (2003) Antibiotic resistance: what is the impact of agricultural uses of antibiotics on children's health? Pediatrics 112: 253–258.CrossRefGoogle ScholarPubMed
Silva, E.N., Snoeyenbos, G.H., Weinack, O.M. and Smyser, C.F. (1981) The influence of native gut microflora on the colonization and infection of Salmonella gallinarum in chickens. Avian Disease 25: 68–73.CrossRefGoogle ScholarPubMed
Sissons, J.W. (1989) potential of probiotic organisms to prevent diarrhoea and promote digestion in farm animals: a review. Journal Science Food Agriculture 49: 1–13.CrossRefGoogle Scholar
Smith, H.W. (1965) The development of the flora of the alimentary tract in young animals. Journal of Pathology and Bacteriology 90: 495–513.CrossRefGoogle ScholarPubMed
Snoeyenbos, G.H., Soerjadi, A.S. and Weinack, O.M. (1982) Gastrointestinal colonization by salmonellae and pathogenic Escherichia coli in monoxenic and holoxenic chicks and poults. Avian Disease 26: 566–575.CrossRefGoogle ScholarPubMed
Soerjadi, A.S., Rufner, R., Snoeyenbos, G.H. and Weinack, O.M. (1982) Adherence of salmonellae and native gut microflora to the gastrointestinal mucosa of chicks. Avian Disease 26: 576–584.CrossRefGoogle Scholar
Soerjadi-Liem, A.S., Snoeyenbos, G.H. and Weinack, O.M. (1984) Establishment and competitive exclusion of Yersinia enterocolitica in the gut of monoxenic and holoxenic chicks. Avian Disease 28: 256–260.CrossRefGoogle ScholarPubMed
Stavric, S., Gleeson, T.M. and Blanchfield, B. (1991) Effect of avian intestinal microflora possessing adhering and hydrophobic properties on competitive exclusion of Salmonella typhimurium from chicks. Journal of Applied Bacteriology 70: 414–421.CrossRefGoogle ScholarPubMed
Stern, N.J. (1994) Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poultry Science 73: 402–407.CrossRefGoogle ScholarPubMed
Takahashi, T., Oka, T., Iwana, H., Kuwata, T. and Yamamoto, Y. (1993) Immune response of mice to orally administered lactic acid bacteria. Bioscience, Biotechnology, and Biochemistry 57: 1557–1560.CrossRefGoogle Scholar
Tannock, G.W. (2001) Molecular assessment of intestinal microflora. American Journal of Clinical Nutrition 73(suppl): 410S–414SCrossRefGoogle ScholarPubMed
Tappenden, K.A. and Mcburney, M.I. (1998) Systemic short-chain fatty acids rapidly alter gastrointestinal structure, function, and expression of early response genes. Digestive Diseases and Sciences 43: 1526–1536.CrossRefGoogle ScholarPubMed
Tlaskalova-Hogenova, H. and Stepankova, R. (1980) Development of antibody formation in germ-free and conventionally reared rabbits: the role of intestinal lymphoid tissue in antibody formation to E. coli antigens. Folia Biology (Praha) 26: 81–93.Google ScholarPubMed
Tlaskalova-Hogenova, H., Mandel, L., Trebichavsky, I., Kovaru, F., Barot, R. and Sterzl, J. (1994) Development of immune responses in early pig ontogeny. Veterinary Immunology and Immunopathology 43: 135–142.CrossRefGoogle ScholarPubMed
Tlaskalova-Hogenova, H., Sterzl, J. and Stepankova, R. (1983) Development of immulogical capacity under germfree and conventional conditions. Annual N Y Academic Science 409: 96–113.CrossRefGoogle Scholar
Tottori, J., Yamaguchi, R., Murakawa, Y., Sato, M., Uchida, K. and Tateyama, S. (1997) The use of feed restriction for mortality control of chickens in broiler farms. Avian Disease 41: 433–4377.CrossRefGoogle ScholarPubMed
Van Der Waaij, D. and Nord, C.E. (2000) Development and persistence of multi-resistance to antibiotics in bacteria; an analysis and a new approach to this urgent problem. International Journal of Antimicrobial Agents 16: 191–197.CrossRefGoogle Scholar
Van Der Wielen, P.W., Keuzenkamp, D.A., Lipman, L.J., Van Knapen, F. and Biesterveld, S. (2002) Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microbial ecology 44: 286–293.CrossRefGoogle ScholarPubMed
Watkins, B.A. and Miller, B.F. (1983) Competitive gut exclusion of avian pathogens by Lactobacillus acidophilus in gnotobiotic chicks. Poultry Science 62: 1772–1979.CrossRefGoogle ScholarPubMed
Weinack, O.M., Snoeyenbos, G.H. and Smyser, C.F. (1979) A supplemental test system to measure competitive exclusion of Salmonellae by native microflora in the chicken gut. Avian Disease 23: 1019–1030.CrossRefGoogle ScholarPubMed
Xiang, Y.Z., Tanya, Z., Yoga, P. and Joerger, R.D. (2002) 16S rRNA-Based Analysis of Microbiota from the Caecum of Broiler Chickens. Applied and Environmental Microbiology 68: 124–137.Google Scholar
Xu, Z.R., Hu, C.H., Xia, M.S., Zhan, X.A. and Wang, M.Q. (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82: 1030–1036.CrossRefGoogle ScholarPubMed
Yazawa, K., Imai, K. and Tamura, Z. (1978) Oligosaccharides and polysaccharides specifically utilizable by bifidobacteria. Chemical Pharmacological Bulletin (Tokyo) 26: 3306–3311.CrossRefGoogle ScholarPubMed
Zhu, X.Y. and Joerger, R.D. (2003) Composition of microbiota in content and mucus from caecae of broiler chickens as measured by fluorescent in situ hybridization with group-specific, 16S rRNA-targeted oligonucleotide probes. Poultry Science 82: 1242–1249.CrossRefGoogle Scholar
Zhu, X.Y., Zhong, T., Pandya, Y. and Joerger, R.D. (2002) 16S rRNA-based analysis of microbiota from the caecum of broiler chickens. Applied and Environmental Microbiology 68: 124–137.CrossRefGoogle ScholarPubMed