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Feed additives to control Salmonella in poultry

  • F. Van Immerseel (a1), K. Cauwerts (a1), L.A. Devriese (a1), F. Haesebrouck (a1) and R. Ducatelle (a1)...


Poultry meat and eggs are important sources of human pathogens. Salmonella is a major cause of human foodborne infections following consumption of poultry products. The original ambition of the EU to eradicate zoonotic agents from the animal production chain has been tempered to reducing the infection pressure of specified zoonotic agents at all levels of the production chain. This can be done by a combination of pre-harvest, harvest and post-harvest measures. Feed additives constitute an important group of pre-harvest measures which can help in controlling Salmonella on the farm. Feed additives used for the control of Salmonella can be of different types, including antibiotics, prebiotics, probiotics and synbiotics. Public concerns regarding possible antibiotic resistance transfer lead to the ban of antibiotics as growth promoters in monogastric diets within the EU. Experimental and practical use of pre-, pro- and synbiotics, as well as volatile fatty acids as feed additives are discussed in this review. The effects of these additives on resistance to infection, on the extent of excretion and on the persistence of infection are reviewed. Attention is paid also to possible undesirable effects of some of these products. Taking into consideration the underestimated high level of contamination of poultry, the feed additives reviewed in this article can certainly play a valuable part in control strategies during the pre-harvest phase aiming at reducing the infection pressure and thus limiting the risk of contamination of poultry products.


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Allen, V.M., Fernandez, F. and Hinton, M.H. (1997) Evaluation of the influence of supplementing the diet with mannose or palm kernel meal on Salmonella colonization in poultry. British Poultry Science 38: 485488.
Audisio, M., Oliver, G. and Apella, M.C. (1999) Antagonistic effect of Enterococcus faecium J96 against human and poultry pathogenic Salmonella spp. Journal of Food Protection 62: 751755.
Audisio, M, Oliver, G., Apella, M.C. (2000) Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella Pullorum. Journal of Food Protection 63: 13331337.
Bager, F., Madsen, M., Christensen, J. and Aarestrup, F.M. (1997) Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Preventive Veterinary Medicine 31: 95–112.
Bailey, J.S., Blankenship, L.C. and Cox, N.A. (1991) Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poultry Science 70: 24332438.
Bedford, M. (2000) Removal of antibiotic growth promoters from poultry diets: implications and strategies to minimise subsequent problems. World's Poultry Science Journal 56: 347354.
Bengmark, S. (1998) Immunonutrition: role of biosurfactants, fiber and probiotic bacteria. Nutrition 14: 585594.
Bengmark, S. (2001) Pre-, pro- and synbiotics. Current Opinion in Clinical Nutrition and Metabolic care 4: 571579.
Bolder, N.M., Wagenaar, J.A., Putirulan, F.F., Veldman, K.T. and Sommer, M. (1999) The effect of Flavophospholipol (Flavomycin) and Salinomycin sodium (Sacox) on the excretion of Clostridium perfringens, Salmonella Enteritidis and Campylobacter jejuni in broilers after experimental infection. Poultry Science 78: 16811689.
Buzetti, F., Eisenberg, F., Grant, H.N., Keller-Schierlein, W., Voser, W. and Zähner, H. (1968) Avilamycin. Experientia 24: 320323.
Campbell, G.L., Classen, H.L. and Balance, G.M. (1986) Gamma irradiation treatment of cereal grains for chicken diets. Journal of Nutrition 116: 560569
Cherrington, C.A., Hinton, M. and Chopra, I. (1990) Effect of short-chain organic acids on macromolecular synthesis in Escherichia coli. Journal of Applied Bacteriology 68: 6974.
Cherrington, C.A., Hinton, M., Pearson, G. and Chopra, I. (1991) Short-chain organic acids at pH 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. Journal of Applied Bacteriology 70: 161165.
Collins, M.D. and Gibson, R. (1999) Probiotics, prebiotics and synbiotics: approaches for modulating the microbial ecology of the gut. American Journal of Clinical Nutrition 69: 1052S1057S.
Corrier, D.E., Hargis, B.M., Hinton, A.J. 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 Diseases 37: 4752.
Corry, J.E. and Hinton, M.H. (1997) Zoonoses in the meat industry: a review. Acta Veterinaria Hungaria 45: 457479.
Corry, J.E. and Atabay, H.I. (2001) Poultry as a source of Campylobacter and related organisms. Society for Applied Microbiology Symposium Series 30: 96S114S.
Cummings, J.H. (1981) Short-chain fatty acids in the human colon. Gut 22: 763779.
Desmidt, M., Ducatelle, R. and Haesebrouck, F. (1998) Immunohistochemical observations in the ceca of chickens infected with Salmonella Enteritidis phage type four. Poultry Science 77: 7374.
Droumev, D. (1983) Review of the antimicrobial growth promoting agents available. Veterinary Research Communications 7: 8599.
Ducatelle, R., De Bruycker, V., De Smet, I., De Buck, J., Van Immerseel, F. and Haesebrouck, F. (2000) An experimental model for the Salmonella Enteritidis carrier state in replacement pullets. XXI World's Poultry CongressMontréal, Canada2000.
Durant, J.A., Lowry, V.K., Nisbet, D.J., Stanker, L.H., Corrier, D.E. and Ricke, S.C. (1999) Short-chain fatty acids affect cell-association and invasion of Hep-2 cells by Salmonella typhimurium. Journal of Environmental Science and Health, part B. 34: 10831099.
Durant, J.A., Corrier, D.E. and Ricke, S.C. (2000) Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella Typhimurium. Journal of Food Protection 63: 573578.
Durst, L. (1996) Der Einsatz von Fructo- und Galakto-Oligosacchariden in der Broilermast. Archiv fur Geflügelkunde 60: 160164.
Dutta, G.N. and Devriese, L.A. (1984) Observations on the in vitro sensitivity of Gram-positive intestinal bacteria of farm animals to growth promoting antibacterials. Journal of Applied Bacteriology 56: 117123.
Edens, F.W., Parkhurst, C.R., Casas, I.A. and Dobrogorz, W.J. (1997) Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri. Poultry Science 76: 179196.
El-Gedaily, A., Paesold, G., Chen, C.Y., Guiney, D.G.andKrause, M. (1997) Plasmid virulence gene expression induced by short-chain fatty acids in Salmonella Dublin: identification of rpoS-dependent and rpoS-independent mechanisms. Journal of Bacteriology 179: 14091412.
Farkas, J. (1998) Irradiation as a method for decontaminating food: a review. International Journal of Food Microbiology 44: 189204.
Fernandez, F., Hinton, M. and Van GILS, B. (2000) Evaluation of the effect of mannan-oligosaccharides on the competitive exclusion of Salmonella Enteritidis colonization in broiler chicks. Avian Pathology 29: 575581.
Finucane, M., Spring, P. and Newman, K. (1999)Incidence of mannose sensitive adhesins in enteric bacteria. Abstracts 88th Annual Meeting Poultry Science Association: 139.
Ford, A.M., Fagerberg, D.J., Quarles, C.L., George, B.A. and McKinley, G.A. (1981) Influence of salinomycin on incidence, shedding, and antimicrobial resistance of Salmonella Typhimurium in experimentally infected broiler chicks. Poultry Science 60: 24412453.
Fuchs, P.C., Barry, A.L. and Brown, S.D. (1999) In vitro activities of SCH27899 alone and in combination with 17 other antimicrobial agents. Antimicrobial Agents and Chemotherapy 43: 29962997.
Fukata, T., Sasai, K., Miyamoto, T. and Baba, E. (1999) Inhibitory effects of competitive exclusion and fructooligosaccharide, singly and in combination, on Salmonella colonization of chicks. Journal of Food Protection 62: 229233.
Fuller, R. (1989) Probiotics in man and animals. Journal of Applied Bacteriology 66: 365378.
Fuller, R. (1999) Probiotics for farm animals. Probiotics. A Critical Review. (ed. Tannock, G.W.), Horizon Scientific Press, Norfolk, England, 1522.
Fusunyan, R.D., Quinn, JJ., Fujimoto, M., Macdermott, R.P., Sanderson, I.R. (1999) Butyrate switches the pattern of chemokine secretion by intestinal epthelial cells through histone acetylation. Molecular Medicine 5: 631640.
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.
Gomez, T.M., Motarjemi, Y., Miyagawa, S., Käferstein, F.K. and Stöhr, K. (1997) Foodborne Salmonellosis. World Health Quarterly 50: 8189.
Gumila, C., Ancelin, M.-L., Delort, A.-M., Jeminet, G. and Vial, H.J. (1997) Characterization of the potent in vitro and in vivo antimalarial activities of ionophore compounds. Antimicrobial Agents and Chemotherapy, 41: 523529.
Gusils, C., Perez Chaia, A., Gonzalez, S. and Oliver, G. (1999) Lactobacilli isolated from chicken intestines: potential use as probiotics. Journal of Food Protection, 62: 252256.
Hinton, M. (1988) Salmonella colonization in young chickens given feed supplemented with the growth promoting antibiotic avilamycin. Journal of Veterinary Pharmacology and Therapy 11: 269275.
Hinton, M. and Linton, A.H. (1988) Control of Salmonella infections in broiler chickens by the acid treatment of their feed. Veterinary Record 123: 416.
Hofacre, C.L., Froyman, R., Gautrais, B., George, B., Goodwin, M.A. and Brown, J. (1998) Use of Aviguard and other intestinal bioproducts in experimental Clostridium perfringens - associated necrotic enteritis in broiler chickens. Avian Diseases 42: 579584.
Houf, K., Devriese, L.A., De Zutter, L., Van Hoof, J. and Vandamme, P. (2001) Development of a new protocol for the isolation and quantification of Arcobacter species from poultry products. International Journal of Food Microbiology 71: 189196.
Huber, G. and Nesemann, G. (1968) Moenomycin, an inhibitor of cell wall synthesis. Biochemical and Biophysical Research Communications 30: 713.
Hume, M.E., Corrier, D.E., Ivie, G.W. and Deloach, J.R. (1993) Metabolism of (14C) propionic acid in broiler chicks. Poultry Science 72: 786793.
Humpert, F., Lalande, F., L'hospitalier, R., Salvat, G.and Bennejean, G. (1991) Effect of four antibiotics additives on the Salmonella contamination of chicks protected by an adult caecal flora. Avian Pathology 20: 577584.
Iji, P.A. and Tivey, D.R. (1998) Natural and synthetic oligosaccharides in broiler chicken diets. World's Poultry Science Journal 54: 129143.
Ishihara, N., Chu, D.C., Akachi, S. and Jujena, L.R. (2000) Preventive effect of partially hydrolyzed guar gum on infection of Salmonella Enteritidis in young and laying hens. Poultry Science 79: 689697.
Izat, A.L., Tidwell, N.M., Thomas, R.A., Reiber, M.A., Adams, M.H., Colberg, M. and Waldroup, P.M. (1990) Effects of formic acid or calcium formate in feed on performance and microbiological characteristics of broilers. Poultry Science 69: 18761882.
Jin, L.Z., Ho, Y.W., Abdullah, N., Ali, M.A. and Jalaludin, S. (1996a) Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chickens. Letters in Applied Microbiology 23: 6771.
Jin, L.Z., Ho, Y.W., Abdullah, N., Ali, M.A. and Jalaludin, S. (1996b) Effect of adherent Lactobacillus spp. on in vitro adherence of Salmonellae to the intestinal epithelial cells of chicken. Journal of Applied Bacteriology 81: 201206.
Kruse, H., Johansen, B.K., Rorvik, L.M. and Schaller, G. (1999) The use of avoparcin as a growth promoter and the occurrence of vancomycin-resistant Enterococcus species in Norwegian poultry and swine production. Microbial Drug Resistance 5: 135139.
Kwon, Y.M. and Ricke, S.C. (1998). Induction of acid resistance of Salmonella Typhimurium by exposure to short-chain fatty acids. Applied and Environmental Microbiology 64: 34583463.
Le Blay, G., Michel, C., Blottière, H.M. and Cherbut, C. (1999) Prolonged intake of fructooligosacharides induces a short-term elevation of lactic-acid-producing bacteria and a persistent increase in cecal butyrate in rats. Journal of Nutrition 129: 22312235.
Libby, S.J., Lesnick, M., Hasegawa, P., Weidenhammer, E. and Guiney, D.G. (2000) The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cellular Microbiology 2: 4958.
Lindsay, D.S. and Blagburn, B.L. (1995) Antiprotozoan drugs. In: Adams, H.R. Veterinary Pharmacology and Therapeutics. Iowa State University Press, Ames, 969983.
Line, J.E., Bailey, S., Cox, N.A., Stern, N.J. and Tompkins, T. (1998) Effect of yeast-supplemented feed on Salmonella and Campylobacter populations in broilers. Poultry Science 77: 405410.
Manning, J.G., Hargis, B.M., Hinton, A. Jr., Corrier, D.E., Deloach, J.R. and Creger, C.R. (1999) Effect of selected antibiotics and anticoccidials on Salmonella enteritidis cecal colonization and organ invasion in Leghorn chicks. Avian Diseases 38: 256261.
Martin, G. and Meyer, H. (1994) The effect of coccidostats on the growth capacity and the survival of Salmonella live vaccines. Berliner und Munchener Tierarztliche Wochenschrift 107: 382384.
Mead, G.C. (2000). Prospects for competitive exclusion treatment to control Salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111123.
Metchnikoff, E. (1907) The prolongation of life, Heinemann, London, England.
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. Probiotics 2: Applications and practical aspects (ed. Fuller, R.), Chapman & Hall, London, 187207.
Nurmi, E. and Rantala, M. (1973). New aspects of Salmonella infection in broiler production. Nature 241: 210211.
Oyofo, B.A., Deloach, J.R., Corrier, D.E., Norman, J.O., Ziprin, R.L. and Mollenhauer, H.H. (1989) Prevention of Salmonella Typhimurium colonization of broilers with D-mannose. Poultry Science 68: 13571360.
Pascual, M., Hugas, M., Badiola, J.I., Monfort, J.M. and Garriga, M. (1999) Lactobacillus salivarius CTC2197 prevents Salmonella Enteritidis colonization in chickens. Applied and Environmental Microbiology 65: 49814986.
Poppe, C. (2000) Salmonella infections in the domestic fowl. In: Wray, C, Wray, A. Salmonella in domestic animals, CAB International, p. 107124.
Roberfroid, M.B. and Delzenne, N.M. (1998) Dietary fructans. Annual Review of Nutrition 18: 117143.
Rouse, J., Rolow, A. and Nelson, C.E. (1988) Effect of chemical treatment of poultry feed on survival of Salmonella. Poultry Science 67: 12251228.
Russell, T.J. (1998) The effect of natural source of non-digestible oligosaccharides on the fecal microflora of the dog and effects on digestion. Friskies R&D Center, Missouri, USA.
Schoeni, J.L. and Wong, A.C. (1994) Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Applied and Environmental Microbiology 60: 11911197.
Schrezenmeir, J. and De Vrese, M. (2001). Probiotics, prebiotics and synbiotics - approaching a definition. American Journal of Clinical Nutrition 73: 361S364S.
Screenivas, P.T. (1998) Salmonella control strategies for the feed industry. Feed Mix 6: 811.
Siavoshian, S., Blottiere, H.M., Le Foll, E., Kaeffer, B., Cherbut, C. and Galmiche, J.P. (1997) Comparison of the effect of different short-chain fatty acids on the growth and differentiation of human colon carcinoma cell lines in vitro. Cell Biology International 21: 281287.
Spring, P., Wenk, C., Dawson, K.A. and Newman, K.E. (2000) The effects of dietary mannanoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella-challenged broiler chicks. Poultry Science 79: 205211.
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: 636642.
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: 16631672.
Thompson, J.L. and Hinton, M. (1997) Antibacterial activity of formic acid and propionic acid in the diet of hens on Salmonellas in the crop. British Poultry Science 38: 5965.
Todd, E.C.D. (1997) Epidemiology of foodborne diseases: a worldwide review. World Health Quarterly 50: 2950.
Van Der Wielen, P.W., Biesterveld, S., Notermans, S., Hofstra, H., Urlings, B.A. and Van Knapen, F. (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Applied and Environmental Microbiology 66: 25362540.
Van Immersee, F., De Smet, I., De Buck, J., Meulemans, G., Haesebrouck, F. and Ducatelle, R. (2002) Development of a chicken caecal epithelial cell model to study in vitro Salmonella-epithelium interactions. International Symposium Salmonella and SalmonellosisPloufraganFrance.
Waldroup, A., Kaniawati, S. and Mauromoustakos, A. (1995) Performance characteristics and microbiological aspects of broilers fed diets supplemented with organic acids. Journal of Food Protection 58: 482489
Waldroup, A.L. (1996) Contamination of raw poultry with pathogens. World's Poultry Science Journal 52: 725.
Watanabe, K., Watanabe, J., Kuramitsu, S. and Maruyama, H.B. (1981) Comparison of the activity of ionophores with other antibacterial agents against anaerobes. Antimicrobial Agents and Chemotherapy 19: 519525.
Wesley, I.V. and Baetz, A.L. (1999) Natural and experimental infections of Arcobacter in poultry. Poultry Science 78: 536545.
Wolf, H. (1973) Avilamycin, an inhibitor of the 30S ribosomal subunit function. FEBS Letters 36: 181186.
Wray, C. and Davies, R.H. (2000) Competitive exclusion – an alternative to antibiotics. Veterinary Journal 59: 107108.


Feed additives to control Salmonella in poultry

  • F. Van Immerseel (a1), K. Cauwerts (a1), L.A. Devriese (a1), F. Haesebrouck (a1) and R. Ducatelle (a1)...


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