Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-07T09:55:06.474Z Has data issue: false hasContentIssue false
  • English
  • Français

Microflora of the digestive tract: critical factors and consequences for poultry

Published online by Cambridge University Press:  01 September 2006

I. GABRIEL ,
M. LESSIRE ,
S. MALLET  and
J.F. GUILLOT
I. GABRIEL*
Affiliation:
Station de Recherches Avicoles, INRA, 37 380Nouzilly, France
M. LESSIRE
Affiliation:
Station de Recherches Avicoles, INRA, 37 380Nouzilly, France
S. MALLET
Affiliation:
Station de Recherches Avicoles, INRA, 37 380Nouzilly, France
J.F. GUILLOT
Affiliation:
Université de Tours, IUT, 37 082Tours, Cedex 2, France
*
*Corresponding author: [email protected]
Get access

Abstract

The microflora of the digestive tract of poultry is still incompletely known. Microbial populations of varying size and complexity occur throughout the digestive tract and the highest and most complex floras are found in the crop and the caeca. The upper part of the digestive tract is predominantly settled by facultative anaerobes, whereas the caeca are mainly the site of obligate anaerobes. The types, numbers and metabolic activities of the organisms are affected by numerous factors such as individual, animal age, environment, and diet. Bacteria produce various metabolites that can be useful or detrimental to the host. Interactions between bacteria and the gastrointestinal epithelium lead to various structural and functional modifications of the digestive tract. Bacteria can impair lipid digestion and may modify carbohydrate and protein digestion. They cause an increase in energy and amino acid requirements. They have a negative effect on vitamin nutrition. Beneficial bacteria can protect birds against pathogens through a competitive exclusion process. Moreover, the flora is involved in the development of the intestinal immune system. Overall, bacteria have a negative effect on bird growth. They may also have an effect on meat and egg quality. Improved knowledge of the microflora of the digestive tract and its consequences may contribute to its control and beneficial use for birds as well as breeders, consumers and the environment.

Keywords

poultrymicrofloramodification of bacterial communitydigestive tractdigestionmetabolismhealthintestinal immune systemgrowthproduct quality
Type
Review Article
Information
World's Poultry Science Journal , Volume 62 , Issue 3 , September 2006 , pp. 499 - 511
Copyright
Copyright © World's Poultry Science Association 2006

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.)

Footnotes

From a paper originally presented at the 5th Journée de la Recherche Avicole, Tours, France, March 26-27, 2003

References

APAJALAHTI, J., KETTUNEN, A. and GRAHAM, H. (2004) Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poultry Science Journal 60: 223–232.CrossRefGoogle Scholar
BARNES, E.M. (1979) The intestinal microflora of poultry and game birds during life and after storage. Journal of Applied Bacteriology 46: 407–419.CrossRefGoogle ScholarPubMed
BJERRUM, L., ENGBERG, R.M., JENSEN, B.B., LESER, T., FINSTER, K. and PEDERSEN, K. (2004) Investigation of the intestinal microflora of broilers. Proc. AFAC Workshop, Alternatives to feed antibiotics and anticoccidials in the pig and poultry meat production, Aarhus (Denmark) 19–20. September: 4 pages.Google Scholar
BOYD, F.M. and EDWARDS, H.M. (1967) Fat absorption by germ-free chicks. Poultry Science 46: 1481–1483.CrossRefGoogle ScholarPubMed
BRAUN, E.J. (2003). Regulation of renal and lower gastrointestinal function: role in fluid and electrolyte balance. Comparative Biochemistry and Physiology. A. Molecular and Integrative Physiology 136: 499–505.CrossRefGoogle ScholarPubMed
BRAUN, E.J. and CAMPBELL, C.E. (1989) Uric acid decomposition in the lower gastrointestinal tract. Journal of Experimental Zoology 3: 70–74.CrossRefGoogle ScholarPubMed
CHERBUT, C. (2003) Motor effects of short-chain fatty acids and lactate in the gastrointestinal tract. Proceeding of the Nutrition Society 62: 95–99.CrossRefGoogle ScholarPubMed
COATES, M.E. (1980) The gut microflora and growth. In: Growth in animals, (Lawrence, T.L.J. ed), pp. 175–188, London: Butterworths.CrossRefGoogle Scholar
DUCLUZEAU, R. and RAIBAUD, P. (1979) Ecologie microbienne du tube digestif, INRA actualités scientifiques et agronomiques, (Ducluzeau, R. and Raibaud, P. eds), 95 pages, Paris: Masson Ltd.Google Scholar
ENGBERG, R.M., HEDEMANN, M.S. and JENSEN, B.B. (2002) The influence of grinding and pelleting of feed on the microbial composition and activity in the digestive tract of broiler chickens. British Poultry Science 43: 569–579.CrossRefGoogle ScholarPubMed
ENGBERG, R.M., HEDEMANN, M.S., STEENFELDT, S. and JENSEN, B.B. (2004) Influence of whole wheat and xylanase on broiler performance and microbial composition and activity in the digestive tract. Poultry Science 83: 925–938.CrossRefGoogle ScholarPubMed
FARNER, D.S. (1942) The hydrogen ion concentration in avian digestive tracts. Poultry Science 21: 445–450.CrossRefGoogle Scholar
FULLER, R. (1984) Microbial activity in the alimentary tract of birds. Proceedings of the Nutrition Society 43: 55–61.CrossRefGoogle ScholarPubMed
FURUSE, M. and OKUMURA, J. (1994) Nutritional and physiological characteristics in germ-free chickens. Comparative Biochemistry and Physiology 109A: 547–556.Google Scholar
FURUSE, M. and YOKOTA, H. (1984) 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
GABRIEL, I., MALLET, S., LECONTE, M., FORT, G. and NACIRI, M. (2003) Effects of whole wheat feeding on the development of coccidial infection in broiler chickens. Poultry Science 82: 1668–1676.CrossRefGoogle ScholarPubMed
GILLILAND, S.E. and SPECK, M.L. (1977) Antagonistic action of Lactobacillus acidophilus toward intestinal and foodborne pathogens in associative cultures. Journal of Food Protection 40: 820–823.CrossRefGoogle ScholarPubMed
GONG, J., FORSTER, R.J., YU, H., CHAMBERS, J.R., WHEATCROFT, R., SABOUR, P.M. and CHEN, S. (2002) Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum. FEMS Microbiology Ecology 41: 171–179.CrossRefGoogle ScholarPubMed
HADDADIN, M.S.Y., ABDULRAHIM, S.M., HASHLAMOUN, E.A.R. and ROBINSON, R.K. (1996) The effect of Lactobacillus acidophilus on the production and chemical composition of hen's eggs. Poultry Science 75: 491–494.CrossRefGoogle ScholarPubMed
HENRY, P.R., AMMERMAN, C.B., CAMPBELL, D.R. and MILES, R.D. (1987) Effect of antibiotics on tissue trace mineral concentration and intestinal tract weight of broiler chicks. Poultry Science 66: 1014–1018.CrossRefGoogle ScholarPubMed
HERICH, R. and LEVKUT, M. (2002) Lactic acid bacteria, probiotics and immune system. Veterinarni Medicina 47: 169–180.CrossRefGoogle Scholar
JOZEFIAK, D., RUTKOWSKI, A. and MARTIN, S.A. (2004) Carbohydrate fermentation in the avian ceca: a review. Animal Feed Science and Technology 113: 1–15.CrossRefGoogle Scholar
KIMURA, N., MIMURA, F., NISHIDA, S., KOBAYASHI, A. and MITSUOKA, T. (1976) Studies on the relationship between intestinal flora and cecal coccidiosis in chicken. Poultry Science 55: 1375–1383.CrossRefGoogle ScholarPubMed
KLASING, K.C., JOHNSTONE, B.J. and BENSON, B.N. (1991) Implications of an immune response on growth and nutrient requirements of chicks. In: Recent advances in animal nutrition, (Haresign, W.Cole, D.J.A. eds), pp. 135–146, Oxford: Butterworth-Heinemann Ltd.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
KUSSAIBATI, R., GUILLAUME, J. and LECLERCQ, B. (1982a) The effect of gut microflora on the digestibility of starch and proteins in young chicks. Annales de Zootechnie 31: 483–488.CrossRefGoogle Scholar
KUSSAIBATI, R., GUILLAUME, J., LECLERCQ, B. and LAFONT, J.P. (1982b) Effect of the intestinal microflora and added bile salts on the metabolisable energy and digestibility of saturated fats in the chicken. Archiv für Geflügelkunde 46: 42–46.Google Scholar
LAN, P.T., HAYASHI, H., SAKAMOTO, M. and BENNO, Y. (2002) Phylogenetic analysis of cecal microbiota in chicken by the use of 16S rDNA clone libraries. Microbiology and Immunology 46: 371–382.CrossRefGoogle ScholarPubMed
LEPKOVSKY, S., WAGNER, M., FURUTA, F., OZINE, K. and KOIKE, T. (1964) The proteases, amylase and lipase of the pancreas and intestinal contents of germfree and conventional chicken. Poultry Science 43: 722–726.CrossRefGoogle Scholar
LU, J., IDRIS, U., HARMON, B., HOFACRE, C., MAURER, J. and LEE, M.D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology 69: 6816–6824.CrossRefGoogle ScholarPubMed
MAASSEN, C.B.M., HOLTEN, J.C.A.M.V., BALK, F., BAK-GLASHOUWER, M.J.H.D., LEER, R., LAMAN, J.D., BOERSMA, W.J.A. and CLAASSEN, E. (1998) Orally administered Lactobacillus strains differentially affect the direction and efficacy of the immune response. Veterinary Quarterly 20: S81–S83.CrossRefGoogle ScholarPubMed
MAISONNIER, S., GOMEZ, J., BREE, A., BERRI, C., BAEZA, E. and CARRÉ, B. (2003) Effects of microflora status, dietary bile salts and guar gum on lipid digestibility, intestinal bile salts and histomorphology, in broiler chickens. Poultry Science 82: 805–814.CrossRefGoogle ScholarPubMed
MATHLOUTHI, N., MALLET, S., SAULNIER, L., QUEMENER, B. and LARBIER, M. (2002) Effects of xylanase and b-glucanase addition on performance, nutrient digestibility, and physico-chemical conditions in the small intestine contents and caecal microflora of broiler chickens fed a wheat and barley-based diet. Animal Research 51: 395–406.CrossRefGoogle Scholar
MEAD, G.C. (1989) Microbes of the avian cecum. Types present and substrates utilized. Journal of Experimental Zoology 3 sup: 48–54.CrossRefGoogle Scholar
MOHAN, B., KADIRVEL, R., BHASKARAN, M. and NATARAJAN, A. (1995) Effect of probiotic supplementation on serum/yolk cholesterol and on egg shell thickness in layers. British Poultry Science 36: 799–803.CrossRefGoogle ScholarPubMed
MORETO, M. and PLANAS, J.M. (1989) Sugar and amino acid transport properties of the chicken caeca. Journal of Experimental Zoology 3 sup: 111–116.CrossRefGoogle Scholar
MULDER, R.W.A.W., HAVENAAR, R. and HUIS IN'T VELDT, J.H.J. (1997) Intervention strategies: the use of probiotics and competitive exclusion microfloras against contamination with pathogens in pigs and poultry. In: Probiotics 2: Applications and practical aspects, (Fuller, R.ed.), pp. 187–207, London: Chapman & Hall.CrossRefGoogle Scholar
MURAMATSU, T., TAKASU, O., FURUSE, M., TASAKI, I. and OKUMURA, J. (1987) Influence of the gut microflora on protein synthesis in tissues and in the whole body of chicks. Biochemical Journal 246: 475–479.CrossRefGoogle ScholarPubMed
NAHASHON, S.N., NAKAUE, H.S. and MIROSH, L.W. (1994a) Production variables and nutrient retention in Single Comb White Leghorn laying pullets fed diets supplemented with direct-fed microbials. Poultry Science 73: 1699–1711.CrossRefGoogle ScholarPubMed
NAHASHON, S.N., NAKAUE, H.S., SNYDER, S.P. and MIROSH, L.W. (1994b) Performance of Single Comb White Leghorn layers fed corn-soybean meal and barley-corn-soybean meal diets supplemented with a direct-fed microbial. Poultry Science 73: 1712–1723.CrossRefGoogle ScholarPubMed
NEISH, A.S., GEWIRTZ, A.T., ZENG, H., YOUNG, A.N., HOBERT, M.E., KARMALI, V., RAO, A.S. and MADARA, J.L. (2000) Prokaryotic regulation of epithelial responses by inhibition of I kappa B-alpha ubiquitination. Science 289: 1560–1563.CrossRefGoogle Scholar
ORBAN, J.I., PATTERSON, J.A., SUTTON, A.L. and RICHARDS, G.N. (1997) Effect of sucrose thermal oligosaccharide caramel, dietary vitamin-mineral level, and brooding temperature on growth and intestinal bacterial populations of broiler chickens. Poultry Science 76: 482–490.CrossRefGoogle ScholarPubMed
PANDA, A.K., REDDY, M.R., RAMARAO, S.V. and PRAHARAJ, N.K. (2000) Effect of dietary supplementation of probiotic on performance and immune response of layers in the decline phase of production. Indian Journal of Poultry Science 35: 102–104.Google Scholar
PÉREZ DE ROZAS, A.M., ROCA, M., CARABANO, R., DE BLAS, C., FRANCESCH, M., BRUFAU, J., MARIN-ORUE, S.M., GASA, J., CAMPOY, S., BARBE, J. and BADIOLA, I. (2004) A comparative study of intestinal microbial diversity from birds, pigs and rabbits by restriction fragment length polymorphism analysis. Reproduction Nutrition Development 44: 4.Google Scholar
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
PIARD, J.C. and DESMAZEAUD, M. (1991) Inhibiting factors produced by lactic acid bacteria. 1. Oxygen metabolites and catabolism end-products. Lait 71: 525–541.CrossRefGoogle Scholar
ROLFE, R.D. (1991) Population dynamics of the intestinal tract. In: Colonization control of human bacterial enteropathogens in poultry, (Blankenship, L. C. ed), pp. 59–75, San Diego: Academic Press Inc.CrossRefGoogle Scholar
SAKATA, T. and SETOYAM, H. (1995) Local stimulatory effect of short chain fatty acids on the mucus release from the hindgut mucosa of rats (Rattus norvegicus). Comparative Biochemistry and Physiology. A. Physiology 111: 429–432.CrossRefGoogle ScholarPubMed
SALMINEN, S., BOULEY, C., BOUTRON-RUAULT, M.C., CUMMINGS, J.H., FRANCK, A., GIBSON, G.R., ISOLAURI, E., MOREAU, M.C., ROBERFROID, M. and ROWLAND, I. (1998) Functional food science and gastrointestinal physiology and function. British Journal of Nutrition 80: S147–171.CrossRefGoogle ScholarPubMed
SALTER, D.N. and FULFORD, R.J. (1974) The influence of the gut microflora on the digestion of dietary and endogenous proteins: studies of the amino acid composition of the excreta of germ-free and conventional chicks. British Journal of Nutrition 32: 625–637.CrossRefGoogle ScholarPubMed
SMITH, H.W. (1965) Observations on the flora of the alimentary tract of animals and factors affecting its composition. Journal of Pathology and Bacteriology 89: 95–122.CrossRefGoogle ScholarPubMed
SMITH, J.C. and SOARES, J.H. (1984) Minerals. In: The germ-free animal in biomedical research, (Coates, M.E.Gustafsson, B. eds), pp. 275–284. London: Laboratory Animals handbooks.Google Scholar
STAVRIC, S. and D'AOUST, J.Y. (1993) Undefined and defined bacterial preparations for the competitive exclusion of Salmonella in poultry – a review. Journal of Food Protection 56: 173–180.CrossRefGoogle ScholarPubMed
SUZUKI, K., KODAM, Y. and MITSUOKA, T. (1989) Stress and intestinal flora. Bifidobacteria and microflora 8: 23–38.CrossRefGoogle Scholar
TAKEUCHI, T., KITAGAWA, H., IMAGAWA, T. and UEHARA, M. (1998) Proliferation and cellular kinetics of villous epithelial cells and M cells in the chicken caecum. Journal of Anatomy 193: 233–239.CrossRefGoogle Scholar
TELLEZ, G., DEAN, C.E., CORRIER, D.E., DELOACH, J.R., JAEGER, L. and HARGIS, B.M. (1993) Effect of dietary lactose on cecal morphology, pH, organic acids, and Salmonella enteritidis organ invasion in Leghorn chicks. Poultry Science 72: 636–642.CrossRefGoogle ScholarPubMed
THOMKE, S. and ELWINGER, K. (1998) Growth promotants in feeding pigs and poultry. I. Growth and feed efficiency responses to antibiotic growth promotants. Annales de Zootechnie 47: 85–91.CrossRefGoogle Scholar
TORTUERO, F. and FERNANDEZ, E. (1995) Effects of inclusion of microbial cultures in barley-based diets fed to laying hens. Animal Feed Science and Technology 53: 255–265.CrossRefGoogle Scholar
WAMBEKE, F.V. and PEETERS, J. (1995) The effect of Paciflor(R) on the performances, carcass composition and caecal bacterial numbers of broilers. Archiv für Geflügelkunde 59: 125–129.Google Scholar
WIELEN, P.W.J.J.V.D., BIESTERVELD, S., NOTERMANS, S., HOFSTRA, H., URLINGS, B.A.P. and KNAPEN, F.V. (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Applied and Environmental Microbiology 66: 2536–2540.CrossRefGoogle ScholarPubMed
XIA, M.S., HU, C.H. and XU, Z.R. (2004) Effects of copper-bearing montmorillonite on growth performance, digestive enzyme activities, and intestinal microflora and morphology of male broilers. Poultry Science 83: 1868–1875.CrossRefGoogle ScholarPubMed
YOKOTA, H. and COATES, M.E. (1982) The uptake of nutrients from the small intestine of gnotobiotic and conventional chicks. British Journal of Nutrition 47: 349–356.CrossRefGoogle ScholarPubMed
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