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Influence of fermentable carbohydrates on the intestinal bacteria and enteropathogens in broilers

Published online by Cambridge University Press:  02 March 2009

H. REHMAN ,
W. VAHJEN ,
A. KOHL-PARISINI ,
A. IJAZ  and
J. ZENTEK
H. REHMAN*
Affiliation:
Department of Physiology and Biochemistry, Faculty of Biosciences, University of Veterinary and Animal Sciences, Lahore, Pakistan
W. VAHJEN
Affiliation:
Institute of Nutrition, Faculty of Veterinary Medicine, Free University of Berlin, Brümmerstr. 34, D-14159 Berlin, Germany
A. KOHL-PARISINI
Affiliation:
Federal Institute for Risk Assessment, Diedersdorfer Weg 1, D-12277 Berlin, Germany
A. IJAZ
Affiliation:
Department of Physiology and Biochemistry, Faculty of Biosciences, University of Veterinary and Animal Sciences, Lahore, Pakistan
J. ZENTEK
Affiliation:
Institute of Nutrition, Faculty of Veterinary Medicine, Free University of Berlin, Brümmerstr. 34, D-14159 Berlin, Germany
*
Corresponding author: habibrehman@uvas.edu.pk
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Abstract

The gastrointestinal tract is a complex milieu as a result of interaction between dietary ingredients and the intestinal bacteria. Following the European ban on the use of in-feed antibiotics, research has focused mainly on the potentially beneficial activities of the intestinal microbiota. Fermentable carbohydrates, or ‘prebiotics’, such as non-digestible oligosaccharides, are considered to have beneficial effects on the composition and activity of the indigenous microbiota, which can enhance the resistance of the host against colonisation of pathogenic bacteria in the GIT. Only a limited number of prebiotics has been tested in broilers that include fructo-oligosaccharides, inulin, mannan-oligosaccharides, alpha gluco-oligosaccharides, isomalto-oligosaccharides, different kestoses and lactose along with its derivatives. This review provides an overview pertaining to the potential impact of prebiotics on the intestinal bacterial population in broilers and summarizes the data regarding the role of prebiotics in preventing the colonisation of enteropathogens especially Salmonella spp., Campylobacter spp. and Clostridium spp. Moreover, the influence of prebiotics on the intestinal bacterial fermentation profile, particularly short chain fatty acids, ammonia and lactate, is also discussed. Prebiotics have been found to affect the intestinal bacterial population particularly elevating the caecal count of Lactobacillus spp. and Bifidobacterium spp. The effect of prebiotics on the intestinal bacteria is also evident in terms of change in the total concentration or relative proportion of short chain fatty acids. The ability of prebiotics in controlling the colonisation of different enterpathogens especially Salmonella spp., Clostridium perfringens or Campylobacter spp. showed inconsistent results depending upon the available literature.

Keywords

prebioticsinulinfructo-oligosaccharidemannan-oligosaccharideisomalto-oligosaccharidekestosesbroilersshort chain fatty acidsgastrointestinal tractbacterialactose

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Type
Review Article
Information
World's Poultry Science Journal , Volume 65 , Issue 1 , March 2009 , pp. 75 - 90
Copyright
Copyright © World's Poultry Science Association 2009

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References

ANDERSON, P., STANLEY, V.G., GRACE, B., TAYLOR, O., HUME, M.M. and SEFTON A.E., (2005) Use of Bio-Mos as a pre-harvest treatment in the control of Campylobacter in broiler chicks. Nutritional Biotechnology in the Feed and Food Industries. Proceedings of the 21st. Annual Symposium (Suppl.1), Lexington, Kentucky, USA, pp. 63.Google Scholar
ATKINSON, R.L., KRATZER, F.H. and STEWART, G.F. (1957) Lactose in animal and human feeding: A review. Journal of Dairy Science 40: 114-132.CrossRefGoogle Scholar
BAILEY, J.S., BLANKENSHIP, L.C. and COX, N.A. (1991) Effect of fructo-oligosaccharide on Salmonella colonisation of the chicken intestine. Poultry Science 70: 2433-2438.CrossRefGoogle Scholar
BAURHOO, B., PHILLIP, L. and RUIZ-FERIA, C.A. (2007) Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens. Poultry Science 86: 1070-1078.CrossRefGoogle ScholarPubMed
BIGGS, P. and PARSONS, C. (2005) The effect of oligosaccharides on growth performance, nutrient utilization and cecal microbes in young chicks. Proceedings of the 94th. Annual Meeting of PSA, Auburn, Alabama, USA, pp. 109.Google Scholar
CAO, B.H., ZHANG, X.P., GUO, Y.M., YUAN, J.M. and WIE, N. (2003) Effects of TP and FOS supplementation on performance and caecal microflora counts and metabolites in broilers fed semi-purified diets. Journal of China Agricultural University 8: 85-90.Google Scholar
CAO, B.H., KARASAWA, Y. and GUO, Y.M. (2005) Effects of green tea polyphenols and fructo-oligosaccharides in semi-purified diets on broilers' performance and caecal microflora and their metabolites. Asian Australasian Journal of Animal Science 18: 85-89.CrossRefGoogle Scholar
CHAMBERS, J.R., SPENCER, J.L. and MODLER, H.W. (1997) The influence of complex carbohydrates on Salmonella typhimurium colonisation, pH, and density of broiler ceca. Poultry Science 76: 445-451.CrossRefGoogle ScholarPubMed
CHOI, K.H., NAMKRNG, H. and PAIK, I.K. (1994) Effects of dietary fructo-oligosaccharide on the suppression of intestinal colonisation of Salmonella typhimurium in broiler chickens. Korean Journal of Animal Science 36: 271-284.Google Scholar
CHUNG, C.H. and DAY, D.F. (2002) Gluco-oligosaccharides from Leuconostoc mesenteroides B-742 (ATCC 13146): A potential prebiotic. Journal of Industrial Microbiology and Biotechnology 29: 196-199.CrossRefGoogle Scholar
CHUNG, C.H. and DAY, D.F. (2004) Efficacy of Leuconostoc mesenteroides (ATCC 13146) isomalto-oligosaccharides as a poultry prebiotic. Poultry Science 83: 1302-1306.CrossRefGoogle Scholar
CORRIER, D.E., HINTON, A., ZIPRIN, R.L. and DELOACH, J.R. (1990a) Effect of dietary lactose on Salmonella colonisation of market-age broiler chickens. Avian Diseases 34: 668-676.CrossRefGoogle ScholarPubMed
CORRIER, D.E., HINTON, A., ZIPRIN, R.L., BEIER, R.C. and DELOACH, J.R. (1990b) Effect of dietary lactose on cecal pH, bacteriostatic volatile fatty acids, and Salmonella typhimurium colonisation of broiler chicks. Avian Diseases 34: 617-625.CrossRefGoogle ScholarPubMed
DELOACH, J.R., OYOFU, B.A., CORRIER, D.E., KUBENA, L.F., ZIPRIN, R.L. and NORMAN, J.O. (1990) Reduction of Salmonella typhimurium concentration in broiler chickens by milk or whey. Avian Diseases 34: 389-392.CrossRefGoogle ScholarPubMed
DENEV, S.A., NIKIFOROV, I.P. and DINEV, I. (2005) Effects of mannan oligosaccharides on composition of cecal microflora and performance of broiler chickens. Nutritional Biotechnology in the Feed and Food Industries. Proceedings of the 21st. Annual Symposium (Suppl.1), Lexington, Kentucky, USA, pp. 65.Google Scholar
FERNANDEZ, F., HINTON, M.H. and VAN GILS, B. (2000) Evaluation of the effect of mannan-oligosaccharides on the competitive exclusion of Salmonella enteritidis colonisation in broiler chicks. Avian Pathology 29: 575-581.CrossRefGoogle ScholarPubMed
FERNANDEZ, F., HINTON, M. and VAN GILS, B. (2002) Dietary mannan-oligosaccharides and their effect on chicken caecal microflora in relation to Salmonella Enteritidis colonisation. Avian Pathology 31: 49-58.CrossRefGoogle Scholar
FUJITA, K., HARA, K., SAKAI, S., HASHIMOTO, H. and KITAHATA, S. (1990) Transfructosylation catalyzed by ß-fructofuranosidase I from Arthrobacter sp. K-1. Agricultural and Biological Chemistry 54: 2655-2661.CrossRefGoogle Scholar
FUJITA, K., HARA, K., SAKAI, S., MIYAE, T., YAMASITA, M., TSUNETOMI, Y. and MITSUOKA, T. (1991) Effect of lactosucrose on intestinal flora and its digestibility. Journal of Japanese Society Starch Science 38: 249-255.CrossRefGoogle Scholar
FUKATA, T., SASAI, K., MIYAMOTO, T. and BABA, E. (1999) Inhibitory effects of competitive exclusion and fructo-oligosaccharide, singly and in combination, on Salmonella colonisation of chicks. Journal of Food Protection 62: 229-233.CrossRefGoogle Scholar
GIBSON, G.R. and WANG, X. (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. Journal of Applied Bacteriology 77: 412-20.CrossRefGoogle ScholarPubMed
GIBSON, G.R. and ROBERFROID, M.B. (1995) Dietary manipulation of the human colonic microbiota, introducing the concept of prebiotics. Journal of Nutrition 125: 1401-1412.CrossRefGoogle ScholarPubMed
GIBSON, G.R., WILLEMS, A., READING, S. and COLLINS, M.D. (1996) Fermentation of non-digestible oligosaccharides by human colonic bacteria. Journal of Applied Microbiology 84: 125-132.Google Scholar
GIBSON, G.R., PROBERT, H.M., VAN LOO, J., RASTALL, R.A. and ROBERFROID, M.B. (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews 17: 259-275.CrossRefGoogle ScholarPubMed
HARA, J., LI, S.T., SASAKI, M., MARUYAMA, T., TERADA, A., OGATA, Y., FUJITA, K., ISHIGAMI, H., HARA, K., FUJIMORI, I. and MITSUOKA, T. (1994) Effective dose of lactosucrose on fecal flora and fecal metabolites of humans. Bifidobacteria Microflora 13: 51-63.CrossRefGoogle Scholar
HAYASHI, S., HONITANI, T. and IMADA, K. (1994) The enzymatic reaction for the production of panose and isomaltose by glucosyltransferase from Aureobasidium . Letters in Applied Microbiology 19: 247-252.CrossRefGoogle Scholar
HERTEL, S., HEINZ, F. and VOGEL, M. (2000) Hydrolysis of low molecular-weight oligosaccharides and oligosaccharide alditols by pig intestinal sucrase/isomaltase and glucosidase/maltase. Carbohydrate Research 326: 264-276.CrossRefGoogle ScholarPubMed
HIDAKA, H., EIDA, T., TAKIZAWA, T., TOKUNAGA, T. and TASHIRO, Y. (1986) Effects of fructo-oligosaccharides on intestinal flora and human health. Bifidobacterium Microflora 5: 37-50.CrossRefGoogle Scholar
HINTON, A., CORRIER, D.E., NORMAN, J.O., BEIER, R.C. and DELOACH J.R., (1990) Biological control of Salmonella typhimurium in young chickens. Avian Diseases 34: 626-633.CrossRefGoogle ScholarPubMed
HINTON, A., CORRIER, D.E., ZIPRIN, R.L., SPATES, G.E. and DELOACH, J.R. (1991) Comparison of the efficacy of cultures of cecal anaerobes as innocula with or without dietary lactose. Poultry Science 70: 67-73.CrossRefGoogle ScholarPubMed
HOFACRE, C. L., BEACORN, T., COLLETT, S. and MATHIS G., (2003) Using competitive exclusion, mannan-oligosaccharide and other intestinal products to control necrotic enteritis. Journal of Applied Poultry Research 12: 60-64.CrossRefGoogle Scholar
HUNZIKER, W., SPIESS, M., SEMENZA, G. and LODISH, H.F. (1986) The sucrase-isomaltase complex: Primary structure, membrane- orientation, and evolution of a stalked, intrinsic brush border protein. Cell 46: 227-234.CrossRefGoogle ScholarPubMed
KLEESSEN, B., ELSAYED, N.A.A.E., LOEHREN, U., SCHROEDL, W. and KRUEGER M., (2003) Jerusalem artichokes stimulate growth of broilers chickens and protect them against endotoxins and potential cecal pathogens. Journal of Food Protection 66: 2171-2175.CrossRefGoogle ScholarPubMed
KULLEN, M.J., KHIL, J., BUSTA, F.F., GALLAHER, D.D. and BRADY L.J., (1998) Carbohydrate source and bifidobacteria influence the growth of Clostridium perfringens in vivo and in vitro. Nutrition Research 18: 1889-1897.CrossRefGoogle Scholar
LASAGNO, M., BEOLETTO, V., SESMA, F., RAYA, R., FONT DEVALDEZ, G. and ERASO, A. (2002) Selection of bacteriocin producer strains of lactic acid bacteria from a dairy environment. Microbiologia 25: 37-44.Google ScholarPubMed
LUMPKINS, B.S., BATAL, A.B. and LEE, M. (2008) The effect of gender on the bacterial community in the gastrointestinal tract of broilers. Poultry Science 87: 964-967.CrossRefGoogle ScholarPubMed
MANLEY-HARRIS, M. and RICHARDS, G.N. (1991) Formation of trisaccharides (kestoses) by pyrolysis of sucrose. Journal of Carbohydrate Research 219: 101-114.CrossRefGoogle ScholarPubMed
MANLEY-HARRIS, M. and RICHARDS, G.N. (1994) Thermolysis of sucrose for food products: a sucrose caramel designed to maximise fructose oligosaccharides for beneficial moderation of intestinal bacteria. Zuckerindustrie 119: 924-928.Google Scholar
MCREYNOLDS, J.L., BYRD, J.A., GENOVESE, K.J., POOLE, T.L., DUKE, S.E., FARNELL, M.B. and NISBET, D.J. (2007) Dietary lactose and its effect on the disease condition of necrotic enteritis. Poultry Science 86: 1656-61.CrossRefGoogle ScholarPubMed
MORISHITA, Y., FULLER, R. and COATES, M.E. (1982) Influence of dietary lactose on the gut flora of chicks. British Poultry Science 23: 349-359.CrossRefGoogle ScholarPubMed
NISBET, D.J., CORRIER, D.E., SCANLAN, C.M., HOLLISTER, A.G., BEIER, C. and DELOACH J.R., (1993) Effect of a defined continuous-flow derived bacterial culture and dietary lactose on Salmonella typhimurium colonization in broiler chickens. Avian Diseases 37: 1017-1025.CrossRefGoogle ScholarPubMed
NISBET, D.J., CORRIER, D.E., SCANLAN, C.M., HOLLISTER, A.G., BEIER, R.C. and DELOACH J.R., (1994) Effect of dietary lactose and cell concentration on the ability of a continuous-flow-derived bacterial culture to control salmonella cecal colonization in broiler chickens. Poultry Science 73: 56-62.CrossRefGoogle ScholarPubMed
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 6: 482-490.CrossRefGoogle Scholar
OYARZBAL, O.A. and CONNER, D.E. (1995) In vitro fructo-oligosaccharide utilisation and inhibition of Salmonella spp. by selected bacteria. Poultry Science 74: 1418-1425.CrossRefGoogle Scholar
OYARZBAL, O.A. and CONNER, D.E. (1996) Application of direct-fed microbial bacteria and fructo-oligosaccharides for Salmonella control in broilers during feed withdrawal. Poultry Science 75: 186-190.CrossRefGoogle Scholar
OYOFO, B.A., DELOACH, J.R., CORRIER, D.E., NORMAN, J.O., ZIPRIN, R.L. and MOLLENHAUER, H.H. (1989a) Prevention of Salmonella typhimurium colonisation of broilers with D-mannose. Poultry Science 68: 1357-1360.CrossRefGoogle ScholarPubMed
OYOFO, B.A., DROLESKEY, R.E., NORMAN, J.O., MOLLENHAUER, H.H., ZIPRIN, R.L., CORRIER, D.E. and DELOACH, J.R. (1989b) Inhibition by mannose of in vitro colonisation of chickens small intestine by Salmonella typhimurium. Poultry Science 68: 1351-1356.CrossRefGoogle ScholarPubMed
PATTERSON, J.A., ORBAN, J.I., SUTTON A.L., and RICHARDS, G.N. (1997) Selective enrichment of Bifidobacteria in the intestinal tract of broilers by thermally produced kestoses and effect on broiler performance. Poultry Science 76: 497-500.CrossRefGoogle ScholarPubMed
QIN, Z.R., FUKUTA, T., BABA, E. and ARAKAWA, A. (1995) Effect of lactose and Lactobacillus acidophilis on the colonisation of Salmonella enteritidis in chicks concurrently infected with Emeria tenella. Avian Diseases 39: 548-553.CrossRefGoogle Scholar
RADA, V., DUSKOVA, D., MAROUNEK, M., KOPECNY, P.J., SIMUNEK, J., AVGUSTIN, G. and JAVORSKY, P. (2001) Enrichment of bifidobacteria in the hen caeca by dietary inulin. Folia Microbiologica 46: 73-75.CrossRefGoogle ScholarPubMed
REHMAN, H., VAHJEN, W., AWAD, W.A. and ZENTEK, J. (2007) Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broilers. Archives of Animal Nutrition 61: 319-335.CrossRefGoogle Scholar
REHMAN, H., BÖHM, J. and ZENTEK, J. (2008a) Effects of differentially fermentable carbohydrates on the microbial fermentation profile of the gastrointestinal tract of broilers. Journal of Animal Physiology and Animal Nutrition 92: 471-480.CrossRefGoogle ScholarPubMed
REHMAN, H., HELLWEG, P., TARAS, D. and ZENTEK, J. (2008b) Effects of dietary inulin on the intestinal short chain fatty acids and microbial ecology in broiler chickens as revealed by denaturing gradient gel electrophoresis. Poultry Science 87: 783-789.CrossRefGoogle ScholarPubMed
REID, C.A. and HILLMAN, K. (1999) The effect of retrogradation and amylose/amylase ratio of starch on carbohydrate fermentation and microbial population in porcine colon. Animal Science 68: 503-510.CrossRefGoogle Scholar
ROBERFROID, M.B., VANLOO, J.A.E. and GIBSON, G.R. (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. Journal of Nutrition 128: 11-19.CrossRefGoogle ScholarPubMed
RYCROFT, C.E., JONES, M.R., GIBSON, G.R. and RASTALL, R.A. (2001) A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. Journal of Applied Microbiology 91: 878-887.CrossRefGoogle ScholarPubMed
SHAO, L., ZHOU, L., LI, G. and LIN, F. (2000) Effects of dietary mannan-oligosaccharide and Enterococcus faecium on cell-mediated immunity, intestinal microflora and pH in chickens. Chinese Journal of Veterinary Science 20: 58-61.Google Scholar
SIDDONS, R.C. and COATES, M.E. (1972) The influence of the intestinal microflora on disaccharidase activities in the chick. British Journal of Nutrition 27: 101-112.CrossRefGoogle ScholarPubMed
SPRING, P., WENK, C., DAWSON K.A., and NEWMAN, K.E. (2000) The effect of dietary mannoligosaccharide on caecal parameters and the concentration of enteric bacteria in the caeca of salmonella-challenged broiler chicks. Poultry Science 79: 205-211.CrossRefGoogle Scholar
TAKEDA, T., FUKATA, T., MIYAMOTO, T., SASAI, K., BABA, E. and ARAKAWA, A. (1995) The effects of dietary lactose and rye on caecal colonisation of Clostridium perfringens in chicks. Avian Diseases 39: 375-381.CrossRefGoogle ScholarPubMed
TERADA, A., HARA, H., SAKAMOTO, J., SATO, N., TAKAGI, S., MITSUOKA, T., MINO, R., HARA, K., FUJIMORI, I. and YAMADA, T. (1994) Effects of dietary supplementation with lactosucrose (4G-beta-D-galactosylsucrose) on cecal flora, cecal metabolites, and performance in broiler chickens. Poultry Science 73: 1663-1672.CrossRefGoogle ScholarPubMed
THITARAM S.N., , CHUNG, C.H., DAY, D.F., HINTON, A., BAILEY, J.S. and SIRAGUSA, G.R. (2005) Isomalto-oligosaccharide increases cecal bifidobacterium population in young broiler chickens. Poultry Science 84: 998-1003.CrossRefGoogle Scholar
VAN DER WIELEN, P.W.J.J., VAN KNAPEN, F. and BIESTERVELD, S. (2002) Effect of administration of Lactobacillus crispatus, Clostridium lactatifermentans and dietary lactose on the development of the normal microflora and volatile fatty acids in the caeca of broiler chicks. British Poultry Science 43: 545-550.CrossRefGoogle ScholarPubMed
VETERE, A., GAMINI, A., CAMPA, C. and PAOLETTI S., (2000) Region specific transglycolytic synthesis and structural characterisation of 6-o-alpha-glucopyranosyl-glucopyranose (isomaltose). Biochemical and Biophysical Research Communications 274: 99-104.CrossRefGoogle Scholar
VISPO, C. and KARASOV, W.H. (1997) The interaction of avian gut microbes and their host: An exclusive symbiosis, in: Mackie, R.J,. White, B.A. & Issacson, R.E. (Eds). Gastrointestinal Microbiology1. Gastrointestinal Microbes and Host Interactions, pp. 116-155 (Chapman and Hall, New York).Google Scholar
WALDROUP, A.L., YAMAGUCHI, W., SKINNER, J.T. and WALDROUP, P.W. (1992) Effects of dietary lactose on incidence and levels of salmonellae on carcasses of broiler chickens grown to market age. Poultry Science 71: 288-295.CrossRefGoogle ScholarPubMed
WANG, X. and GIBSON, G.R. (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75: 373-380.CrossRefGoogle ScholarPubMed
WANG, L. and SHAN, A. (2002) Effects of fructo-oligosaccharides, compared with direct-fed microbial bacteria, and zinc bactricin on cecal microbial population and performance of broilers. Journal of Northeast Agricultural University English Edition 9: 42-48.Google Scholar
XIA, Z.S., XIE, J.H., QUAN, Y.H. and ZHOU, J.L. (2001) The effect of dietary with isomalto-oligosaccharides on the performance of yellow broiler chicks. Cereal Feed Industry 8: 32-33.Google Scholar
XU, Z.R., HU, C.H., XIA, M.S., ZHAN, X.A. and WANG, M.Q. (2003) Effects of dietary fructo-oligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82: 1083-1036.CrossRefGoogle Scholar
YANG, Y., IJI, P.A., KOCHER, A., MIKKELSEN, L. L. and CHOCT, M. (2007) Effects of mannanoligosaccharide on growth performance, the development of gut microflora, and gut function of broiler chickens raised on new litter. Journal of Applied Poultry Research 16: 280-288.CrossRefGoogle Scholar
YUSRIZAL, Y. and CHEN, T.C. (2003) Effect of adding chicory fructans in feed on faecal and intestinal microflora and excretory volatile ammonia. International Journal of Poultry Science 2: 188-194.Google Scholar
ZENTEK, J. and KAMPHUES, J. (2002) Investigations of antibiotic and dietary influences on egg taint. Wiener Tierarztliche Monatsschrift 89: 100-106.Google Scholar
ZENTEK, J., MARQUART, B. and PIETRZAK, T. (2002) Intestinal effects of mannanoligosaccharides, transgalactooligosaccharides, lactose and lactulose in dogs. Journal of Nutrition 132: 1682S-1684S.CrossRefGoogle ScholarPubMed
ZENTEK, J., MARQUART, B., PIETRZAK, T., BALLEVRE, O. and ROCHAT, F. (2003) Dietary effects on bifidobacteria and Clostridium perfringens in the canine intestinal tract. Journal of Animal Physiology and Animal Nutrition 87: 397-407.CrossRefGoogle ScholarPubMed
ZHAN, X.A., HU, C.H. and XU, Z.R. (2003) Effects of fructo-oligosaccharide on growth performance and intestinal microflora and morphology of broiler chicks. Chinese Journal of Veterinary Science 23: 196-198.Google Scholar
ZHANG, C. (2000) Research on the application effects and the mechanism of isomalto-oligosaccharides in diet for broilers and piglets. Treatise. China Agricultural University, Beijing.Google Scholar
ZHANG, W.F., LI, D.F., LU, W.Q. and YI, G.F. (2003) Effects of isomalto-oligosaccharides on broiler performance and intestinal microflora. Poultry Science 82: 657-663.CrossRefGoogle ScholarPubMed