Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Microflora Management in the Gastrointestinal Tract of Piglets

  • Metzler, B. (Institute of Animal Nutrition, University of Hohenheim) ;
  • Bauer, E. (Institute of Animal Nutrition, University of Hohenheim) ;
  • Mosenthin, R. (Institute of Animal Nutrition, University of Hohenheim)
  • Published : 2005.09.01
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Abstract

The stressful physiological and environmental conditions around weaning often promote the proliferation of pathogens in the digestive tract of piglets resulting in diarrhoea and reduced daily weight gain. Typical dietary practices to maintain growth performance and health have led to an increased use of antimicrobial growth promoters. Due to the advanced ban of antibiotics in pig production, new concepts have been developed to secure animal health and growth performance, feed efficiency, and product quality as well. Several naturally occurring compounds seem to beneficially affect the composition and activity of the microflora in the gastrointestinal tract (GIT) of pigs. These are, among others, organic acids, probiotics, prebiotics, and enzymes. Organic acids are already widely used, especially in pigs, due to their positive effects on GIT health and growth performance. Probiotics have been shown to be effective against diarrhoea though effects may be dependent on diet composition and environmental conditions. Prebiotics may influence composition and activity of the intestinal microflora. Additionally, pre- and probiotics may exert positive influences on immune response, whereas enzymes may enhance feed digestibility by breaking down anti-nutritional factors. In the following, the focus will be directed to the role of organic acids, probiotics, prebiotics, and feeding enzymes as potential modulators of GIT health.

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References

  1. Adams, C. A. 1999. Antimicrobial nutricines in food safety (Chapter 3). In: Nutricines: Food Components in Health and Nutrition (Ed: C. A. Adams). Nottingham University Press, UK, pp. 35-57.
  2. Bacillus subtilis spores, on the health status and performance of sows and their litters. J. Anim. Physiol. Anim. Nutr. 88:381-392.
  3. Alexopoulos, C., I. E. Georgoulakis, A. Tzivara, C. S. Kyriakis, A. Govaris and S. C. Kyriakis. 2004b. Field evaluation of the effect of a probiotic-containing Bacillus licheniformis and Bacillus subtilis spores on the health status, performance and carcass quality of grower and finisher pigs. J. Vet. Med. A Physiol. Pathol. Clin. Med. 51:306-312.
  4. Bach Knudsen, K. E. 1997. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim. Feed Sci. Technol. 67:319-338. https://doi.org/10.1016/S0377-8401(97)00009-6
  5. Blank, R., R. Mosenthin, W. C. Sauer and S. Huang. 1999. Effect of fumaric acid and dietary buffering capacity on ileal and fecal amino acid digestibility in early-weaned pigs. J. Anim. Sci. 77:2974-2984.
  6. Blank, R., R. Mosenthin, W. C. Sauer, J. Zentek, S. Huang and S. Roth. 2001. Effect of fumaric acid supplementation and dietary buffering capacity on the concentration of microbial metabolites in ileal digesta of young pigs. Can. J. Anim. Sci. 81:345-353.
  7. Benno, Y., K. Endo, N. Shiragami, K. Salama and T. Mitsuoka. 1987. Effects of raffinose intake on the human faecal microflora. Bifido. Microflora 6:59-63.
  8. Branner, G. R., B. M. Bohmer, W. Erhardt, J. Henke and D. A. Roth-Maier. 2004. Investigation on the precaecal and faecal digestibility of lactulose and inulin and their influence on nutrient digestibility and microbial characteristics. Arch. Anim. Nutr. 58:353-366.
  9. Brufau de Barbera, J. 2000. The European Union ban of antibiotic performance enhancers (additives) in animal feeding and its consequences: potential alternatives. In: Selected Topics in Animal Nutrition, Biochemistry and Physiology (Ed. W. Sauer and J. He) Department of Agricultural, Food and Nutritional Science, Faculty of Agriculture, Forestry, and Home Economics, University of Alberta, Alberta, Canada, pp. 93-106.
  10. Canibe, N., S. H. Steien, M. Overland and B. B. Jensen. 2001. Effect of K-diformate in starter diets on acidity, microbiota, and the amount of organic acids in the digestive tract of piglets, and gastric alterations. J. Anim. Sci. 79: 2123-2133.
  11. Cromwell, G. L. 2001. Antimicrobial and Promicrobial Agents (Chapter 18). In: Swine Nutrition. (Ed. A. J. Lewis and L. L. Southern). Second edition, CRC Press, Boca Raton-London-New York-Washington DC, pp. 401-426.
  12. DANMAP. 2002. Available: www.dfvf.dk/Files/Filer/Zoonosecentret/Publikationer/Danmap/Danmap_2002.pdf
  13. Davie, J. R. 2003. Inhibition of histone deacetylase activity by butyrate. J. Nutr. 133:2485S-2493S.
  14. Davis, M. E., C. V. Maxwell, D. C. Brown, B. Z. de Rodas, Z. B. Johnson, E. B. Degley, D. H. Hellwig and R. A. Dvorak. 2002. Effect of dietary mannan oligosaccharides and (or) pharmacological additions of copper sulphate on growth performance and immunocompetence of weanling and growing/finishing pigs. J. Anim. Sci. 80:2887-2894.
  15. Diebold, G., R. Mosenthin, H.-P. Piepho and W. C. Sauer. 2004. Effect of supplementation of xylanase to a wheat based diet for weanling pigs on nutrient digestibility and concentrations of microbial metabolites in ileal digesta and feces. J. Anim. Sci. 82:2647-2656.
  16. Diekenhorst, A. 2002. Alternativen zu konventionellen Leistungsförderern. Großtierpraxis 3:32-37.
  17. Durst, L., M. Feldner, B. Gedek and B. Eckel. 1998. Bacteria as probiotics in sow feeding and piglet rearing. Feed Mag. 9:356-364.
  18. European Commission, Health & Consumer Protection Directorate - General Adopted on 3 July 2001, revised on 24th January 2003. Opinion of the Scientific Committee on Animal Nutrition on the criteria for assessing the safety of microorganisms resistant to antibiotics of human clinical and veterinary importance.
  19. Ewing, W. N. and D. J. A. Cole. 1994. The living gut. Context, Northern Ireland.
  20. FB des Fachbereichs Agrarwirtschaft Soest, Universitat Gesamthochschule Paderborn, 1998. Kritische Betrachtung des Einsatzes von Leistungsforderern in der Tierernahrung. Nr. 8. Paderborn, Germany.
  21. Fishbein, L., M. Kaplan and M. Gough. 1987. Fructooligosaccharides: a review. Vet. Human Toxicol. 30:104-107.
  22. Franco, L. D., M. Fondevila, M. B. Lobera and C. Castrillo. 2005. Effect of combinations of organic acids in weaned pig diets on microbial species of digestive tract contents and their response on digestibility. J. Anim. Physiol. Anim. Nutr. 89:88-93.
  23. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bact. 66:365-378.
  24. Gabert, V. M. and W. C. Sauer. 1994. The effects of supplementing diets for weanling pigs with organic acids. A review. J. Anim. Feed. Sci. 3:73-87.
  25. Gibson, G. R. and B. M. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
  26. Haberer, B. 1997. Einfluss von Nicht-Starke-Polysacchariden im Verdauungstrakt von Schweinen. Lohmann Info. 4:19-25.
  27. Hartemink, R. and F. M. Rombouts. 1997. Gas formation from oligosaccharides by the intestinal microflora. In: Proceedings of the International Symposium 'Non-Digestible Oligosaccharides: Healthy Food for the Colon? (Ed. R. Hartemink). The Graduate School VLAG, Wageningen Institute of Animal Science, Wageningen, pp. 57-66.
  28. Hayes, D. J. and H. H. Jensen. 2003. Lessons from the Danish ban on feed-grade antibiotics. Briefing Paper 03-BP 41. Available: www.card.iastate.edu.
  29. Henry, R. J. and H. S. Saini. 1989. Characterization of cereal sugars and oligosaccharides. Cereal Chem. 66:362-365.
  30. Hidaka, H., T. Eida, T. Takizawa, T. Tokunaga and Y. Tashiro. 1986. Effects of fructooligosaccharides on intestinal flora and human health. Bifido. Microflora 5:37-50.
  31. Hillman, K. 2001. Bacteriological aspects of the use of antibiotics and their alternatives in the feed of non-ruminant animals. In: Recent Advantages in Animal Nutrition-2001 (Ed. P. G. Garnsworthy and J. Wiseman). Nottingham Universitiy Press, Nottingham, UK, pp. 107-134.
  32. Houdijk, J. G. M., R. Hartemink, K. J. M. Van Laere, B. A. Williams, M. W. Bosch, M. W. A. Verstegen and S. Tamminga. 1997. Fructooligosaccharides and transgalacto-oligosaccharides in weaner pigs diet. In: Proceedings of the International Symposium 'Non-digestible Oligosaccharides: Healthy Food for the Colon?' (Ed. R. Hartemink). The Graduate School VLAG, Wageningen Institute of Animal Science, Wageningen, pp. 69-78.
  33. Houdijk, J. G. M. 1998. Effect of non-digestible oligosaccharides in young pig diets. PhD Thesis, Agricultural University of Wageningen, The Netherlands.
  34. Huang, C., S. Qiao, D. Lifa, X. Piao and J. Ren. 2004. Effects of lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian-Aust. J. Anim. Sci. 17:401-409.
  35. Hubener, K., W. Vahjen and O. Simon. 2002. Bacterial responses to different dietary cereal types and xylanase supplementation in the intestine of broiler chicken. Arch. Anim. Nutr. 56:167-187.
  36. Hurley, R., J. de Louvois and A. Mulhall. 1989. Yeast as human and animal pathogens. In: The yeast. Vol. 12th ed. Biology of yeast. Academic Press Limited, London, UK.
  37. Kelly, D. 1998. Probiotics in young and newborn animals. J. Anim. Feed Sci. 7:15-23.
  38. Kirchgessner, M. and F. X. Roth. 1988. Ergotrope Effekte durch organische Sauren in der Ferkelaufzucht und Schweinemast. Ubers. Tierernahr. 10:93-108.
  39. Knarreborg, A., N. Miquel, T. Granli and B. B. Jensen. 2002. Establishment and application of an in vitro methodology to study the effects of organic acids on coliform and lactic acid bacteria in the proximal part of the gastrointestinal tract of piglets. Anim. Feed Sci. Technol. 99:131-140.
  40. Konstantinov, S. R., W. Y. Zhu, B. A. Williams, S. Tamminga, W. M. De Vos and A. D. L. Akkermans. 2003. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiol. Ecol. 43:225-235.
  41. Konstantinov, S. R., A. Awati, H. Smidt, B. A. Williams, A. D. L. Akkermans and W. M. De Vos. 2004. Specific response of a novel and abundant Lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Appl. Environ. Microbiol. 70:3821-3830.
  42. Kumprecht, I. and P. Zobac. 1998. Study of the effect of a combined preparation containing Enterococcus faecium M-74 and mannanoligosaccharides in diets for weanling piglets. Czech. J. Anim. Sci. 43:477-481.
  43. Lee, Y.-K., K. Nomoto, S. Salminen and S. L. Gorbach. 1999. Handbook of probiotics (Ed. John Wiley and Sons). INC, New York-Chichester-Weinheim-Brisbane-Singapore-Toronto, pp. 4-6.
  44. 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. Appl. Environ. Microbiol. 68:673-690.
  45. Leser,T. D., R. H. Lindecrona, T. K. Jensen, B. B. Jensen and K. Moller. 2000. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl. Environ. Microbiol. 66:3290-3296.
  46. Li, D. F., J. Y. Jiang and Y. X. Ma. 2003. Early weaning diets and feed additives (Chapter 9). In: The Neonatal Pig-Gastrointestinal Physiology and Nutrition (Eds. R.-J. Xu and P. Cranwell). Nottingham University Press, Nottingham, UK, pp. 247-274.
  47. Mathew, A. G., C. M. Robbins, S. E. Chattin and J. D. Quigley. 1997. Influence of galactosyl lactose on energy and protein digestibility, enteric microflora and performance of weanling pigs. J. Anim. Sci. 75:1009-1016.
  48. Mathew, A. 2002. Seeking alternatives to growth promoting antibiotics. In: Manitoba Swine Seminar 2002 Volume 16 -Sharing Ideas and Information for Efficient Pork Production. Available: www.gov.mb.ca/agriculture/livestock/pork/swine/pdf/bab15s 10.pdf
  49. Moore, W. E. C., L. V. H. Moore, E. P. Cato, T. D. Wilkins and E. T. Kornegay. 1987. Effect of high-fiber and high-oil diets on the fecal flora of swine. Appl. Environ. Microbiol. 53:1638-1644.
  50. Mosenthin, R. 2003. Strategies for optimizing gut health in piglets. In: Proceedings of the 12th conference on nutrition of domestic animals 'Zadravec-Erjavec Days', pp. 150-157.
  51. Mosenthin, R. and G. Diebold. 2000. Organische Saurezusatze und Futterenzyme in der Schweinefutterung. Veterinarija ir Zootechnika. T. 10 (priedas). Kaunas 2000, pp. 112-119.
  52. Mroz, Z. 2003. Organic acids of various origin and physicochemical forms as potential alternatives to antibiotic growth promoters for pigs. In: Proceedings of the 9th International Symposium on Digestive Physiology in Pigs, Banff, Alberta, Canada, Volume 1, pp. 267-293.
  53. Mul, A. J. and F. G. Perry. 1994. The role of fructooligosaccharides in animal nutrition. In: Recent Advances in Animal Nutrition 1994 (Ed. P. C. Garnsworthy and D. J. A. Cole). Nottingham University Press, Nottingham, pp. 57-79.
  54. Nemcova, R., A. Bomba, S. GancarEikova, R. Herich and P. Guba. 1999. Study of the effect of Lactobacillus paracasei and fructooligosaccharides on the faecal microflora in weanling piglets. Berl. Munch. Tierarztl. Wschr. 112:225-228.
  55. Nousiainen, J. and J. Setala. 1993. Lactic acid bacteria as animal probiotics. In: Lactic Acid Bacteria (Ed. S. Salminen and A. von Wright). Marcel Dekker, New York, USA, pp. 315-356.
  56. Orban, J. I., J. A. Patterson, O. Adeola, A. L. Sutton and G. N. Richards. 1996. Growth performance and intestinal microbial populations of growing pigs fed diets containing sucrose thermal oligosaccharide caramel. J. Anim. Sci. 74:170-175.
  57. Partanen, K. H. 2001. Organic acids-their efficacy and modes of action in pigs. In: Gut Environment of Pigs (Ed. A. Piva, K. E. Bach Knudsen and J. E. Lindberg). University Press, Nottingham, UK, pp. 201-218.
  58. Patterson, J. A. and K. M. Burkholder. 2003. Prebiotic feed additives: rationale and use in pigs. In: Proceedings of the 9th International Symposium on Digestive Physiology in Pigs, Banff, Alberta, Canada, Volume 1, pp. 319-331.
  59. Piva, A. 1998. Non-convential feed additives. J. Anim. Feed Sci. 7:143-154.
  60. Rastall, R. A. and G. R. Gibson. 2002. Prebiotic oligosaccharides: evaluation of biological activities and potential future developments. In: Probiotics and Prebiotics: Where Are We Going? (Ed. G. W. Tannock), Caister Academic Press, Wymondham, UK, pp. 107-148.
  61. Roberfroid, M. B. 1998. Prebiotics and synbiotics: concepts and nutritional properties. Br. J. Nutr. 80 (Suppl. 2):S197-S202.
  62. Robinson, I. M., M. J. Allison and J. A. Bucklin. 1981. Characterization of the cecal bacteria of normal pigs. Appl. Environ. Microbiol. 41:950-955.
  63. Roth, F. X., M. Kirchgessner and U. Eidelsburger. 1993. Zur nutritiven Wirksamkeit von Milchsäure in der Ferkelaufzucht. Agribiol. Res. 46:229-239.
  64. Schierack, P., M. Nordhoff, M. Pollmann, P. Schwerk, D. Taras, A. Lubke-Becker, L. H. Wieler and K. Tedin. 2004. Effects of an Enterococcus faecium probiotic in pigs: Influence on enteropathogenic bacteria. Anim. Res. 53:338 (Abstract).
  65. Sghir, A., J. M. Chow and R. I. Mackie. 1998. Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate. J. Appl. Microbiol. 85:769-777.
  66. Simon, O. 2000. Non starch polysaccharide (NSP) hydrolyzing enzymes as feed additives: mode of action in the gastrointestinal tract. Lohmann Info. 23: 7-13.
  67. Simon, O. K. Hubener, K. Hirsch, L. Beckmann and W. Vahjen. 2002. Effect of xylanases on the intestinal flora. Lohmann Info. 27:1-5.
  68. Simon, O., W. Vahjen and L. Scharek. 2003. Micro-organisms as feed additives-probiotics. In: Proceedings of the 9th International Symposium on Digestive Physiology in Pigs, Banff, Alberta, Canada, Vol. 1, pp. 295-318.
  69. Smiricky-Tjardes, M. R., C. M. Grieshop, E. A. Flickinger, L. L. Bauer and G. C. Fahey Jr. 2003. Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility, ileal and fecal bacterial concentrations, and ileal fermentative characteristics of growing pigs. J. Anim. Sci. 81:2535-2545.
  70. Taras, D., M. Macha, M. Nordhoff, M. Pollmann, L. Scharek, P. Schierack, P. Schwerk, K. Tedin, W. Vahjen, M. F. G. Schmidt, L. H. Wieler and O. Simon. 2005. Response of intestinal microbiota and immune system to a probiotic Bacillus cereus var. toyoi preparation as well as its consequences for piglet performance. Proc. Soc. Nutr. Physiol. 14:70 (Abstract).
  71. Vahjen, W., K. Gläser, K. Schäfer and O. Simon. 1998. Influence of xylanase-supplemented feed on the development of selected bacterial groups in the intestinal tract of broiler chicks. J. Agric. Sci. 130:489-500.
  72. Wang, X. and G. R. Gibson. 1993. Effects of the fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J. Appl. Bacteriol. 73:373-380.
  73. White, L. A., M. C. Newman, G. L. Cromwell and M. D. Lindemann. 2002. Brewers dried yeast as a source of mannan oligosaccharides for weanling pigs. J. Anim. Sci. 80:2619-2628.
  74. Wierup, M. 1998. Animal health effects of the new feed act of 1986. In: Ministry of Agriculture-Seminar on the Swedish Model of Animal Production, Stockholm 3-4 Sept., 6-7.
  75. Xu, Z. R., X. T. Zou, C. H. Hu, M. S. Xia, X. A. Zhan and M. Q. Wang. 2002. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of growing pigs. Asian-Aust. J. Anim. Sci. 15(12):1784-1789.
  76. Zhang, L., D. Li, S. Qiao, J. Wang, L. Bai, Z. Wang and I. K. Han. 2001. The effect of soybean galactooligosacchrides on nutrient and energy digestibility and digesta transit time in weanling piglets. Asian-Aust. J. Anim. Sci. 14:1598-1604.

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