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Feed additives to control Salmonella in poultry

Published online by Cambridge University Press:  18 September 2007

F. Van Immerseel ,
K. Cauwerts ,
L.A. Devriese ,
F. Haesebrouck  and
R. Ducatelle
F. Van Immerseel*
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
K. Cauwerts
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
L.A. Devriese
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
F. Haesebrouck
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
R. Ducatelle
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
*
*Corresponding author: e-mail: [email protected]
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Abstract

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.

Keywords

Salmonellafeed additivesprebioticsprobioticsfatty acidspoultry
Type
Reviews
Information
World's Poultry Science Journal , Volume 58 , Issue 4 , December 2002 , pp. 501 - 513
Copyright
Copyright © Cambridge University Press 2002

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References

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: 485–488.CrossRefGoogle ScholarPubMed
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: 751–755.Google Scholar
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: 1333–1337.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Bailey, J.S., Blankenship, L.C. and Cox, N.A. (1991) Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poultry Science 70: 2433–2438.CrossRefGoogle ScholarPubMed
Bedford, M. (2000) Removal of antibiotic growth promoters from poultry diets: implications and strategies to minimise subsequent problems. World's Poultry Science Journal 56: 347–354.Google Scholar
Bengmark, S. (1998) Immunonutrition: role of biosurfactants, fiber and probiotic bacteria. Nutrition 14: 585–594.CrossRefGoogle ScholarPubMed
Bengmark, S. (2001) Pre-, pro- and synbiotics. Current Opinion in Clinical Nutrition and Metabolic care 4: 571–579.CrossRefGoogle ScholarPubMed
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: 1681–1689.CrossRefGoogle ScholarPubMed
Buzetti, F., Eisenberg, F., Grant, H.N., Keller-Schierlein, W., Voser, W. and Zähner, H. (1968) Avilamycin. Experientia 24: 320–323.CrossRefGoogle Scholar
Campbell, G.L., Classen, H.L. and Balance, G.M. (1986) Gamma irradiation treatment of cereal grains for chicken diets. Journal of Nutrition 116: 560–569CrossRefGoogle Scholar
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: 69–74.CrossRefGoogle ScholarPubMed
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: 161–165.CrossRefGoogle ScholarPubMed
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: 1052S–1057S.CrossRefGoogle ScholarPubMed
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: 47–52.CrossRefGoogle ScholarPubMed
Corry, J.E. and Hinton, M.H. (1997) Zoonoses in the meat industry: a review. Acta Veterinaria Hungaria 45: 457–479.Google ScholarPubMed
Corry, J.E. and Atabay, H.I. (2001) Poultry as a source of Campylobacter and related organisms. Society for Applied Microbiology Symposium Series 30: 96S–114S.CrossRefGoogle Scholar
Cummings, J.H. (1981) Short-chain fatty acids in the human colon. Gut 22: 763–779.Google Scholar
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: 73–74.Google Scholar
Droumev, D. (1983) Review of the antimicrobial growth promoting agents available. Veterinary Research Communications 7: 85–99.Google Scholar
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.Google Scholar
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: 1083–1099.CrossRefGoogle ScholarPubMed
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: 573–578.Google Scholar
Durst, L. (1996) Der Einsatz von Fructo- und Galakto-Oligosacchariden in der Broilermast. Archiv fur Geflügelkunde 60: 160–164.Google Scholar
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: 117–123.CrossRefGoogle Scholar
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: 179–196.Google Scholar
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: 1409–1412.Google Scholar
Farkas, J. (1998) Irradiation as a method for decontaminating food: a review. International Journal of Food Microbiology 44: 189–204.Google Scholar
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: 575–581.CrossRefGoogle ScholarPubMed
Finucane, M., Spring, P. and Newman, K. (1999)Incidence of mannose sensitive adhesins in enteric bacteria. Abstracts 88th Annual Meeting Poultry Science Association: 139.Google Scholar
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: 2441–2453.Google Scholar
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: 2996–2997.Google Scholar
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: 229–233.CrossRefGoogle ScholarPubMed
Fuller, R. (1989) Probiotics in man and animals. Journal of Applied Bacteriology 66: 365–378.Google Scholar
Fuller, R. (1999) Probiotics for farm animals. Probiotics. A Critical Review. (ed. Tannock, G.W.), Horizon Scientific Press, Norfolk, England, 15–22.Google Scholar
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: 631–640.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Gomez, T.M., Motarjemi, Y., Miyagawa, S., Käferstein, F.K. and Stöhr, K. (1997) Foodborne Salmonellosis. World Health Quarterly 50: 81–89.Google ScholarPubMed
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: 523–529.Google Scholar
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: 252–256.CrossRefGoogle ScholarPubMed
Hinton, M. (1988) Salmonella colonization in young chickens given feed supplemented with the growth promoting antibiotic avilamycin. Journal of Veterinary Pharmacology and Therapy 11: 269–275.Google Scholar
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.Google Scholar
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: 579–584.CrossRefGoogle ScholarPubMed
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: 189–196.Google Scholar
Huber, G. and Nesemann, G. (1968) Moenomycin, an inhibitor of cell wall synthesis. Biochemical and Biophysical Research Communications 30: 7–13.CrossRefGoogle ScholarPubMed
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: 786–793.CrossRefGoogle ScholarPubMed
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: 577–584.Google Scholar
Iji, P.A. and Tivey, D.R. (1998) Natural and synthetic oligosaccharides in broiler chicken diets. World's Poultry Science Journal 54: 129–143.Google Scholar
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: 689–697.CrossRefGoogle Scholar
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: 1876–1882.CrossRefGoogle ScholarPubMed
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: 67–71.Google Scholar
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: 201–206.CrossRefGoogle Scholar
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: 135–139.Google Scholar
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: 3458–3463.CrossRefGoogle ScholarPubMed
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: 2231–2235.Google Scholar
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: 49–58.Google Scholar
Lindsay, D.S. and Blagburn, B.L. (1995) Antiprotozoan drugs. In: Adams, H.R. Veterinary Pharmacology and Therapeutics. Iowa State University Press, Ames, 969–983.Google Scholar
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: 405–410.Google Scholar
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: 256–261.Google Scholar
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: 382–384.Google Scholar
Mead, G.C. (2000). Prospects for competitive exclusion treatment to control Salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111–123.Google Scholar
Metchnikoff, E. (1907) The prolongation of life, Heinemann, London, England.Google 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. Probiotics 2: Applications and practical aspects (ed. Fuller, R.), Chapman & Hall, London, 187–207.Google Scholar
Nurmi, E. and Rantala, M. (1973). New aspects of Salmonella infection in broiler production. Nature 241: 210–211.Google Scholar
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: 1357–1360.CrossRefGoogle ScholarPubMed
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: 4981–4986.CrossRefGoogle ScholarPubMed
Poppe, C. (2000) Salmonella infections in the domestic fowl. In: Wray, C, Wray, A. Salmonella in domestic animals, CAB International, p. 107–124.Google Scholar
Roberfroid, M.B. and Delzenne, N.M. (1998) Dietary fructans. Annual Review of Nutrition 18: 117–143.Google Scholar
Rouse, J., Rolow, A. and Nelson, C.E. (1988) Effect of chemical treatment of poultry feed on survival of Salmonella. Poultry Science 67: 1225–1228.CrossRefGoogle ScholarPubMed
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.Google Scholar
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: 1191–1197.Google Scholar
Schrezenmeir, J. and De Vrese, M. (2001). Probiotics, prebiotics and synbiotics - approaching a definition. American Journal of Clinical Nutrition 73: 361S–364S.Google Scholar
Screenivas, P.T. (1998) Salmonella control strategies for the feed industry. Feed Mix 6: 8–11.Google Scholar
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: 281–287.Google Scholar
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: 205–211.Google 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.Google Scholar
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.Google Scholar
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: 59–65.Google Scholar
Todd, E.C.D. (1997) Epidemiology of foodborne diseases: a worldwide review. World Health Quarterly 50: 29–50.Google Scholar
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: 2536–2540.CrossRefGoogle ScholarPubMed
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.Google Scholar
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: 482–489Google Scholar
Waldroup, A.L. (1996) Contamination of raw poultry with pathogens. World's Poultry Science Journal 52: 7–25.CrossRefGoogle Scholar
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: 519–525.CrossRefGoogle ScholarPubMed
Wesley, I.V. and Baetz, A.L. (1999) Natural and experimental infections of Arcobacter in poultry. Poultry Science 78: 536–545.Google Scholar
Wolf, H. (1973) Avilamycin, an inhibitor of the 30S ribosomal subunit function. FEBS Letters 36: 181–186.Google Scholar
Wray, C. and Davies, R.H. (2000) Competitive exclusion – an alternative to antibiotics. Veterinary Journal 59: 107–108.Google Scholar