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Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease

Published online by Cambridge University Press:  22 December 2008

T. R. Callaway ,
T. S. Edrington ,
R. C. Anderson ,
R. B. Harvey ,
K. J. Genovese ,
C. N. Kennedy ,
D. W. Venn  and
D. J. Nisbet
T. R. Callaway*
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
T. S. Edrington
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
R. C. Anderson
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
R. B. Harvey
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
K. J. Genovese
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
C. N. Kennedy
Affiliation:
Kennedy and Associates Research, Colorado Springs, CO, USA
D. W. Venn
Affiliation:
Department of Biology, Georgia State University, Atlanta, GA, USA
D. J. Nisbet
Affiliation:
Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, Agricultural Research Service, USDA, College Station, TX 77845, USA
*
*Corresponding author: E-mail: todd.callaway@ars.usda.gov
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Abstract

The microbial population of the intestinal tract is a complex natural resource that can be utilized in an effort to reduce the impact of pathogenic bacteria that affect animal production and efficiency, as well as the safety of food products. Strategies have been devised to reduce the populations of food-borne pathogenic bacteria in animals at the on-farm stage. Many of these techniques rely on harnessing the natural competitive nature of bacteria to eliminate pathogens that negatively impact animal production or food safety. Thus feed products that are classified as probiotics, prebiotics and competitive exclusion cultures have been utilized as pathogen reduction strategies in food animals with varying degrees of success. The efficacy of these products is often due to specific microbial ecological factors that alter the competitive pressures experienced by the microbial population of the gut. A few products have been shown to be effective under field conditions and many have shown indications of effectiveness under experimental conditions and as a result probiotic products are widely used in all animal species and nearly all production systems. This review explores the ecology behind the efficacy of these products against pathogens found in food animals, including those that enter the food chain and impact human consumers.

Keywords

probioticsfood safetymicrobial ecology
Type
Review Article
Information
Animal Health Research Reviews , Volume 9 , Issue 2: Symposium on Antimicrobial Resistance in Bacteria from Animals , December 2008 , pp. 217 - 225
Copyright
Copyright © Cambridge University Press 2008

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References

Al-Qumber, M and Tagg, JR (2006). Commensal bacilli inhibitory to mastitis pathogens isolated from the udder microbiota of healthy cows. Journal of Applied Microbiology 101: 1152–1160.CrossRefGoogle ScholarPubMed
Alexander, TJL, Thornton, K, Boon, G, Lysons, RJ and Gush, AF (1980). Medicated early weaning to obtain pigs free from pathogens endemic to the herd of origin. Veterinary Record 106: 114–119.Google Scholar
Anderson, RC, Stanker, LH, Young, CR, Buckley, SA, Genovese, KJ, Harvey, RB, Deloach, JR, Keith, NK and Nisbet, DJ (1999). Effect of competitive exclusion treatment on colonization of early-weaned pigs by Salmonella serovar cholerasuis. Journal of Swine Health and Production 7: 155–160.Google Scholar
Barnes, EM, Impey, CS and Stevens, BJH (1979). Factors affecting the incidence and anti-Salmonella activity of the anerobic cecal flora of the chick. Journal of Hygiene 82: 263–283.Google Scholar
Barroga, AJ, Salas, RCD, Martin, EA, Besa, WG and Santos, CADC (2007). Efficacy of probiotics, enzymes and dried porcine solubles in swine. Philippine Agricultural Scientist 90: 71–74.Google Scholar
Bertschinger, HU (1999). Postweaning Escherichia coli diarrhea and edema disease. In: Straw, BE, D'Allaire, S, Mengeling, WL and Taylor, DJ (eds) Diseases of Swine, 8th edn. Ames, IA: Iowa State University Press, pp. 441–454.Google Scholar
Bhandari, SK, Xu, B, Nyachoti, CM, Giesting, DW and Krause, DO (2008). Evaluation of alternatives to antibiotics using an Escherichia coli K88+ model of piglet diarrhea: effects on gut microbial ecology. Journal of Animal Science 86: 836–847.Google Scholar
Bielke, LR, Elwood, AL, Donoghue, DJ, Donoghue, AM, Newberry, LA, Neighbor, NK and Hargis, BM (2003). Approach for selection of individual enteric bacteria for competitive exclusion in turkey poults. Poultry Science 82: 1378–1382.CrossRefGoogle ScholarPubMed
Bomba, A, Nemcova, R, Gancarcikova, S, Herich, R and Kastel, R (1999). Potentiation of the effectiveness of Lactobacillus casei in the prevention of E. coli induced diarrhea in conventional and gnotobiotic pigs. In: Paul, PS and Francis, DH (eds) Mechanisms in the Pathogenesis of Enteric Diseases 2. New York: Kluwer Academic/Plenum Publishers, pp. 185–190.CrossRefGoogle Scholar
Bomba, A, Nemcová, R, Mudronová, D and Guba, P (2002). The possibilities of potentiating the efficacy of probiotics. Trends in Food Science Technology 13: 121–126.CrossRefGoogle Scholar
Branner, GR and Roth-Maier, DA (2006). Influence of pre-, pro-, and synbiotics on the intestinal availability of different B-vitamins. Archives of Animal Nutrition 60: 191–204.Google Scholar
Brashears, MM, Galyean, ML, Loneragan, GH, Mann, JE and Killinger-Mann, K (2003a). Prevalence of Escherichia coli O157:H7 and performance by beef feedlot cattle given Lactobacillus direct-fed microbials. Journal of Food Protection 66: 748–754.CrossRefGoogle ScholarPubMed
Brashears, MM, Jaroni, D and Trimbl, J (2003b). Isolation, selection, and characterization of lactic acid bacteria for a competitive exclusion product to reduce shedding of Escherichia coli O157:H7 in cattle. Journal of Food Protection 66: 355–363.Google Scholar
Collado, MC, Grzeskowiak, C and Salminen, S (2007). Probiotic strains and their combination inhibit in vitro adhesion of pathogens to pig intestinal mucosa. Current Microbiology 55: 260–265.CrossRefGoogle ScholarPubMed
Collins, DM and Gibson, GR (1999). Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. American Journal of Clinical Nutrition 69: 1052S–1057S.CrossRefGoogle ScholarPubMed
Cox, NA, Bailey, JS, Mauldin, JM and Blankenship, LC (1990). Research note: Presence and impact of Salmonella contamination in commercial broiler hatcheries. Poultry Science 69: 1606–1608.Google Scholar
Crittenden, RG (1999). Prebiotics. In: Tannock, GW (ed.) Probiotics: A Critical Review. Wymondham, UK: Horizon Scientific Press, pp. 141–156.Google Scholar
Dawson, KA, Newman, KE and Boling, JA (1990). Effects of microbial supplements containing yeast and lactobacilli on roughage-fed ruminal microbial activities. Journal of Animal Science 68: 3392–3398.CrossRefGoogle ScholarPubMed
DiBaise, JK, Zhang, H, Crowell, MD, Krajmalnik-Brown, R, Decker, GA and Rittmann, BE (2008). Gut microbiota and its possible relationship with obesity. Mayo Clinic Proceedings 83: 460–469.CrossRefGoogle ScholarPubMed
Drasar, BS and Barrow, PA (1985). Intestinal microbiology. In: Drasar, BS and Barrow, PA (eds). Washington, DC: ASM Press, pp. 19–40.Google Scholar
Duncker, SC, Lorentz, A, Schroeder, B, Breves, G and Bischoff, SC (2006). Effect of orally administered probiotic E. coli strain Nissle 1917 on intestinal mucosal immune cells of healthy young pigs. Veterinary Immunology and Immunopathology 111: 239–250.Google Scholar
Fedorka-Cray, PJ and Harris, DL (1995). Elimination of Salmonella Species in Swine by Isolated Weaning – The First Critical Control Point. Kansas City, MO: Food Safety Consortium, pp. 146–149.Google Scholar
Fedorka-Cray, PJ, Harris, DL and Whipp, SC (1997). Using isolated weaning to rear Salmonella free pigs. Veterinary Medicine 44: 376–382.Google Scholar
Fedorka-Cray, PJ, Bailey, JS, Stern, NJ, Cox, NA, Ladely, SR and Musgrove, M (1999). Mucosal competitive exclusion to reduce Salmonella in swine. Journal of Food Protection 62: 1376–1380.CrossRefGoogle ScholarPubMed
Finegold, SM (2008). Therapy and epidemiology of autism-clostridial spores as key elements. Medical Hypotheses 70: 508–511.CrossRefGoogle ScholarPubMed
Fuller, R (1989). Probiotics in man and animals. Journal of Applied Bacteriology 66: 365–378.Google Scholar
Genovese, KJ, Anderson, RC, Harvey, RB, Callaway, TR, Poole, TL, Edrington, TS, Fedorka-Cray, PJ and Nisbet, DJ (2003). Competitive exclusion of Salmonella from the gut of neonatal and weaned pigs. Journal of Food Protection 66: 1353–1359.CrossRefGoogle ScholarPubMed
Gomes, AMP and Malcata, FX (1999). Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends in Food Science Technology 10: 139–157.CrossRefGoogle Scholar
Gomez-Alarcon, RA, Huber, JT, Higginbotham, GE, Wiersma, F, Ammon, D and Taylor, B (1991). Influence of feeding Aspergillus oryzae fermentation extract on the milk yields, eating patterns, and body temperatures of lactating cows. Journal of Dairy Science 72: 1733–1740.Google Scholar
Harvey, RB, Ebert, RC, Schmitt, CS, Andrews, K, Genovese, KJ, Anderson, RC, Scott, HM, Callaway, TR and Nisbet, DJ (2003). Use of a porcine-derived, defined culture of commensal bacteria as an alternative to antibiotics used to control E. coli disease in weaned pigs. 9th International Symposium on Digestive Physiology in Pigs, Banff, AB, Canada, pp. 72–74.Google Scholar
Harvey, RB, Anderson, RC, Genovese, KJ, Calloway, TR and Nisbet, DJ (2005). Use of competitive exclusion to control enterotoxigenic strains of Escherichia coli in weaned pigs. Journal of Animal Science 83 (E. suppl.): E44–E47.CrossRefGoogle Scholar
Hollowell, CA and Wolin, MJ (1965). Basis for the exclusion of Escherichia coli from the rumen ecosystem. Applied Microbiology 13: 918–924.CrossRefGoogle ScholarPubMed
Houdijk, JGM, Bosch, MW, Verstegen, MWA and Berenpas, HJ (1998). Effects of dietary oligosaccharides on the growth and faecal characteristics of young growing pigs. Animal Feed Science and Technology 71: 35–48.CrossRefGoogle Scholar
Hungate, RE (1966). The Rumen and its Microbes. New York: Academic Press, pp. 61–69.Google Scholar
Jack, RW, Tagg, JR and Ray, B (1995). Bacteriocins of gram-positive bacteria. Microbiological Reviews 59: 171–200.Google Scholar
Jayne-Williams, DJ and Fuller, R (1971). The influence of the intestinal microflora on nutrition. In: Bell, DJ and Freeman, BM (eds) Physiology and Biochemistry of the Domestic Food. London, UK: Academic Press, pp. 74–92.Google Scholar
Keen, J and Elder, R (2000). Commercial probiotics are not effective for short-term control of enterohemorrhagic Escherichia coli O157 infection in beef cattle. 4th International Symposium and Workshop on Shiga Toxin (Verocytotoxin)-producing Escherichia coli Infections, Kyoto, Japan, 92 (Abstr.).Google Scholar
Koenen, ME, Kramer, J, Van Der Hulst, R, Heres, L, Jeurissen, SHM and Boersma, WJA (2004). Immunomodulation by probiotic lactobacilli in layer- and meat-type chickens. British Poultry Science 45: 355–366.Google Scholar
Kontula, P (1999). In vitro and in vivo characterization of potential prebiotic lactic acid bacteria and prebiotic carbohydrates. Finnish Journal of Dairy Science 54: 1–2.Google Scholar
Kyriakis, SC, Tsiloyiannis, VK, Vlemmas, J, Sarris, K, Tsinas, AC, Alexopoulos, C and Jansegers, L (2001). The effect of probiotic LSP 122 on the control of post-weaning diarrhea syndrome of piglets. Research in Veterinary Science 67: 223–238.Google Scholar
Leenen, CHM and Dieleman, LA (2007). Inulin and oligofructose in chronic inflammatory bowel disease. Journal of Nutrition 137: 2572S–2575S.CrossRefGoogle ScholarPubMed
Lehloenya, KV, Stein, DR, Allen, DT, Selk, GE, Jones, DA, Aleman, MM, Rehberger, TG, Mertz, KJ and Spicer, LJ (2008). Effects of feeding yeast and propionibacteria to dairy cows on milk yield and components, and reproduction. Journal of Animal Physiology and Animal Nutrition 92: 190–202.Google Scholar
LeJeune, JT, Kauffman, MD, Amstutz, MD and Ward, LA (2006). Limited effects of a commercial direct-fed microbial on weaning pig performance and gastrointestinal microbiology. Journal of Swine Health and Production 14: 247–252.Google Scholar
Lema, M, Williams, L and Rao, DR (2001). Reduction of fecal shedding of enterohemorrhagic Escherichia coli O157:H7 in lambs by feeding microbial feed supplement. Small Ruminant Research 39: 31–39.CrossRefGoogle ScholarPubMed
Ley, RE, Turnbaugh, PJ, Klein, S and Gordon, JI (2006). Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022–1023.Google Scholar
Lloyd, AB, Cumming, RB and Kent, RD (1974). Competitive exclusion as exemplified by Salmonella typhimurium. Australasian Poultry Science Convention, World Poultry Science Association, Australia Branch, p. 155.Google Scholar
Lu, J, Idris, U, Hofacre, C, Maurer, JJ, Lee, MD and Harmon, B (2003). Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology 69: 6816–6824.CrossRefGoogle ScholarPubMed
Meyer, D (2008). Prebiotic dietary fibres and the immune system. Agro-Food Industry Hi-Tech 19: 12–15.Google Scholar
Midilli, M, Alp, M, Kocabagli, N, Muglali, OH, Turan, N, Yilmaz, H and Cakir, S (2008). Effects of dietary probiotic and prebiotic supplementation on growth performance and serum IgG concentration of broilers. South African Journal of Animal Science 38: 21–27.CrossRefGoogle Scholar
Mosenthin, R and Bauer, E (2000). The potential use of prebiotics in pig nutrition. Asian-Australian Journal of Animal Science 13: 315–325.Google Scholar
Moxley, RA, Smith, D, Klopfenstein, TJ, Erickson, G, Folmer, J, Macken, C, Hinkley, S, Potter, A and Finlay, B (2003). Vaccination and feeding a competitive exclusion product as intervention strategies to reduce the prevalence of Escherichia coli O157:H7 in feedlot cattle. Proceedings 5th International Symposium on Shiga Toxin-Producing Escherichia coli Infections, Edinburgh, UK, 23 (Abstr.).Google Scholar
Nava, GM, Bielke, LR, Callaway, TR and Castaneda, MP (2005). Probiotic alternatives to reduce gastrointestinal infections: the poultry experience. Animal Health Research Reviews 6: 105–118.Google Scholar
Nemcova, R, Bomba, A, Gancarcikova, S, Reiffova, K, Guba, P, Koscova, J, Jonecova, Z, Scirankova, L and Bugarsky, A (2007). Effects of the administration of lactobacilli, maltodextrins and fructooligosaccharides upon the adhesion of E. coli O8:K88 to the intestinal mucosa and organic acid levels in the gut contents of piglets. Veterinary Research Communication 31: 791–800.CrossRefGoogle Scholar
Nisbet, DJ, Corrier, DE and DeLoach, JR (1993a). Effect of mixed cecal microflora maintained in continuous culture and of dietary lactose on Salmonella typhimurium colonization in broiler chicks. Avian Diseases 37: 528–535.Google Scholar
Nisbet, DJ, Corrier, DE, Scanlan, CM, Hollister, AG, Beier, RC and DeLoach, JR (1993b). 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, DJ, Corrier, DE, Ricke, S, Hume, ME, Byrd, JA and DeLoach, JR (1996). Maintenance of the biological efficacy in chicks of a cecal competitive-exclusion culture against Salmonella by continuous-flow fermentation. Journal of Food Protection 59: 1279–1283.CrossRefGoogle ScholarPubMed
Nurmi, E and Rantala, M (1973). New aspects of Salmonella infection in broiler production. Nature 24: 210–211.CrossRefGoogle Scholar
Nurmi, E, Nuotio, L and Schncitz, C (1992). The competitive exclusion concept: development and future. International Journal of Food Microbiology 15: 237–240.CrossRefGoogle Scholar
Ohya, T, Marubashi, T and Ito, H (2000). Significance of fecal volatile fatty acids in shedding of Escherichia coli O157 from calves: experimental infection and preliminary use of a probiotic product. The Journal of Veterinary Medical Science 62: 1151–1155.CrossRefGoogle ScholarPubMed
Otero, MC, Morelli, L and Nader-Macias, ME (2006). Probiotic properties of vaginal lactic acid bacteria to prevent metritis in cattle. Letters in Applied Microbiology 43: 91–97.CrossRefGoogle ScholarPubMed
Prohaszka, L and Baron, F (1983). Antibacterial effect of volatile fatty acids on Enterobacteriae in the large intestine. Acta Veterinaria Hungarica 30: 9–16.Google Scholar
Ransom, JR, Belk, KE, Sofos, JN, Scanga, JA, Rossman, ML, Smith, GC and Tatum, JD (2003). Investigation of On-farm Management Practices as Pre-harvest Beef Microbiological Interventions. Centennial, CO: National Cattlemen's Beef Association Research Fact Sheet.Google Scholar
Respondek, F, Goachet, AG and Julliand, V (2008). Effects of dietary short-chain fructooligosaccharides on the intestinal microflora of horses subjected to a sudden change in diet. Journal of Animal Science 86: 316–323.Google Scholar
Schierack, P, Wieler, LH, Taras, D, Herwig, V, Tachu, B, Hlinak, A, Schmidt, MFG and Scharek, L (2007). Bacillus cereus var. toyoi enhanced systemic immune response in piglets. Veterinary Immunology and Immunopathology 118: 1–11.Google Scholar
Schrezenmeir, J and de Vrese, M (2001). Probiotics, prebiotics, and synbiotics-approaching a definition. American Journal of Clinical Nutrition 73 (Suppl.): 354s–361s.Google Scholar
Schroeder, B, Duncker, S, Barth, S, Bauerfeind, R, Gruber, AD, Deppenmeier, S and Breves, G (2006). Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Digestive Diseases and Sciences 51: 724–731.Google Scholar
Seifert, S and Watz, B (2007). Inulin and oligofructose: review of experimental data on immune modulation. Journal of Nutrition 137: 2563S–2567S.Google Scholar
Shoaf, K, Mulvey, GL, Armstrong, GD and Hutkins, RW (2006). Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infection and Immunity 74: 6920–6928.Google Scholar
Songer, JG, Jones, R, Anderson, MA, Barbara, AJ, Post, KW and Trinh, HT (2007). Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Veterinary Microbiology 124: 358–361.Google Scholar
Stahl, CH, Callaway, TR, Lincoln, LM, Lonergan, SM and Genovese, KJ (2004). Inhibitory activities of colicins against Escherichia coli strains responsible for postweaning diarrhea and edema disease in swine. Antimicrobial Agents and Chemotherapy 48: 3119–3121.CrossRefGoogle ScholarPubMed
Stavric, S (1992). Defined cultures and prospects. International Journal of Food Microbiology 55: 245–263.CrossRefGoogle Scholar
Stavric, S and D'Aoust, J-Y (1993). Undefined and defined bacterial preparations for competitive exclusion of Salmonella in poultry. Journal of Food Protection 56: 173–180.CrossRefGoogle ScholarPubMed
Stavric, S and Kornegay, ET (1995). Microbial probiotics for pigs and poultry. In: Wallace, RJ and Chesson, A (eds) Biotechnology in Animal Feeds and Animal Feeding. New York: VCH, pp. 205–230.CrossRefGoogle Scholar
Steer, T, Carpenter, H, Tuohy, K and Gibson, GR (2000). Perspectives on the role of the human gut microbiota and its modulation by pro and prebiotics. Nutrition Research Reviews 13: 229–254.Google Scholar
Stephens, TP, Loneragan, GH, Karunasena, E and Brashears, MM (2007). Reduction of Escherichia coli O157 and Salmonella in feces and on hides of feedlot cattle using various doses of a direct-fed microbial. Journal of Food Protection 70: 2386–2391.CrossRefGoogle ScholarPubMed
Tabe, ES, Oloya, J, Doetkott, DK, Bauer, ML, Gibbs, PS and Khaitsa, ML (2008). Comparative effect of direct-fed microbials on fecal shedding of Escherichia coli O157:H7 and Salmonella in naturally infected feedlot cattle. Journal of Food Protection 71: 539–544.Google Scholar
Takahashi, S, Egawa, Y, Simojo, N, Tsukahara, T and Ushida, K (2007). Oral administration of Lactobacillus plantarum strain Lq80 to weaning piglets stimulates the growth of indigenous lactobacilli to modify the lactobacillal population. Journal of General and Applied Microbiology 53: 325–332.Google Scholar
Tkalcic, S, Zhao, T, Harmon, BG, Doyle, MP, Brown, CA and Zhao, P (2003). Fecal shedding of enterohemorrhagic Escherichia coli in weaned calves following treatment with probiotic Escherichia coli. Journal of Food Protection 66: 1184–1189.CrossRefGoogle ScholarPubMed
Torres-Rodriguez, A, Higgins, SE, Vicente, JLS, Wolfenden, AD, Gaona-Ramirez, G, Barton, JT, Tellez, G, Donoghue, AM and Hargis, BM (2007). Effect of lactose as a prebiotic on turkey body weight under commercial conditions. Journal of Applied Poultry Research 16: 635–641.Google Scholar
Underdahl, R, Torres-Medina, A and Doster, AR (1982). Effect of Streptococcus faecium C-68 in control of Escherichia coli induced diarrhea in gnotobiotic pigs. American Journal of Veterinary Research 43: 2227–2232.Google Scholar
Ushe, TC and Nagy, B (1985). Inhibition of small intestinal colonization of enterotoxigenic Escherichia coli by Streptococcus faecium M74 in pigs. Zentralblatt fur Bakteriologie und Hygiene. I. Abteilung Originale B. 181: 374–382.Google Scholar
Vahjen, W, Taras, D and Simon, O (2007). Effect of the probiotic Enterococcus faecium NCIMB10415 on cell numbers of total Enterococcus spp., E. faecium and E. faecalis in the intestine of piglets. Current Issues in Intestinal Microbiology 8: 1–8.Google Scholar
Walsh, MC, Gardiner, GE, Hart, OM, Lawlor, PG, Daly, M, Lynch, B, Richert, BT, Radcliffe, S, Giblin, L, Hill, C, Fitzgerald, GF, Stanton, C and Ross, P (2008). Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiology Ecology 64: 317–327.CrossRefGoogle ScholarPubMed
Weinack, OM, Snoeyenbos, GH, Smyser, CF and Soerjadi, AS (1982). Reciprocal competitive exclusion of Salmonella and Escherichia coli by native intestinal microflora of the chicken and turkey. Avian Diseases 26: 585–595.CrossRefGoogle ScholarPubMed
Wiemann, M (2003). How do probiotic feed additives work? International Poultry Production 11: 7–9.Google Scholar
Willard, MD, Simpson, RB, Cohen, ND and Clancy, JS (2000). Effects of dietary fructooligosaccharide on selected bacterial populations in feces of dogs. American Journal of Veterinary Research 61: 820–825.Google Scholar
Winkler, J, Butler, R and Symonds, E (2007). Fructo-oligosaccharide reduces inflammation in a dextran sodium sulphate mouse model of colitis. Digestive Diseases Sciences 52: 52–58.CrossRefGoogle Scholar
Wolin, MJ (1969). Volatile fatty acids and the inhibition of Escherichia coli growth by rumen fluid. Applied Microbiology 17: 83–87.CrossRefGoogle ScholarPubMed
Younts-Dahl, SM, Galyean, ML, Loneragan, GH, Elam, NA and Brashears, MM (2004). Dietary supplementation with lactobacillus- and propionibacterium-based direct-fed microbials and prevalence of Escherichia coli O157 in beef feedlot cattle and on hides at harvest. Journal of Food Protection 67: 889–893.CrossRefGoogle ScholarPubMed
Zeyner, A and Boldt, E (2006). Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets. Journal of Animal Physiology and Animal Nutrition 90: 25–31.Google Scholar
Zhang, W, Azevedo, MSP, Gonzalez, AM, Saif, LJ, Van Nguyen, T, Wen, K, Yousef, AE and Yuan, L (2008). Influence of probiotic lactobacilli colonization on neonatal B cell responses in a gnotobiotic pig model of human rotavirus infection and disease. Veterinary Immunology Immunopathology 122: 175–181.Google Scholar
Zhao, T, Doyle, MP, Harmon, BG, Brown, CA, Mueller, POE and Parks, AH (1998). Reduction of carriage of enterohemorrhagic Escherichia coli O157:H7 in cattle by inoculation with probiotic bacteria. Journal of Clinical Microbiology 36: 641–647.CrossRefGoogle ScholarPubMed
Zhao, T, Tkalcic, S, Doyle, MP, Harmon, BG, Brown, CA and Zhao, P (2003). Pathogenicity of enterohemorrhagic Escherichia coli in neonatal calves and evaluation of fecal shedding by treatment with probiotic Escherichia coli. Journal of Food Protection 66: 924–930.CrossRefGoogle ScholarPubMed