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Strategies to control Salmonella in the broiler production chain

  • F. VAN IMMERSEEL (a1), L. DE ZUTTER (a2), K. HOUF (a2), F. PASMANS (a1), F. HAESEBROUCK (a1) and R. DUCATELLE (a1)...


Broiler meat is one of the sources of Salmonella contamination of humans. Concerns about food safety have prompted the poultry industry and governments to introduce control plans to combat Salmonella. This has been strengthened by legislation, as is the case in the EU, where targets have been set forcing member states to decrease Salmonella prevalence in poultry flocks. Strategies to prevent transmission of Salmonella to humans should focus on the whole production chain of broiler meat and on the subsequent storage and handling of meat, thus from farm to fork. In the primary production phase, both hygienic measures and general farm management strategies are important. These management strategies should include in-feed Salmonella control and product administration. A wide range of feed additives is currently available for that purpose. Hygienic measures and logistic slaughter are tools to reduce the Salmonella contamination in the slaughterhouse. At retail and in the consumer's kitchen, care needs to be taken of product storage and handling to avoid contamination and bacterial growth. The numbers of contaminated Salmonella broiler flocks will most likely decrease in the future due to the established action plans, but complete eradication of Salmonella is unrealistic. The main issue is, however, to keep the flock prevalence, the within-flock prevalence and the numbers of bacteria in infected animals at such a low level, that contamination of meat, and thus transmission to humans, becomes a highly unlikely event. This clearly underlines the need for coordinated action of governments and poultry-related industries (including feed industry and slaughterhouses), at all stages of the production chain.


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AGUNOS, A., IBUKI, M., YOKOMIZO, F. and MINE, Y. (2007) Effect of dietary beta1-4 mannobiose in the prevention of Salmonella enteritidis infection in broilers. British Poultry Science 48: 331-341.
AL-CHALABY, Z.A.M., HINTON, M. and LINTON, A.H. (1985) Failure of drinking water sanitisation to reduce the incidence of natural Salmonella in broiler chickens. The Veterinary Record 116: 364-365.
ALTEKRUSE, S., BAUER, N., CHANLONGBUTRA, A., DESAGUN, R., NAUGLE, A., SCHLOSSER, W., UMHOLTZ, R. and WHITE, P. (2005) Salmonella Enteritidis in broiler chickens, United States, 2000-2005. Emerging Infections Diseases 12: 1848-1852.
ANDREATTI FILHO, R.L., HIGGINS, J.P., WOLFENDEN, A.D., HIGGINS, S.E., TELLEZ, G. and HARGIS, B.M. (2007) Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo. Poultry Science 86: 1904-1909.
ATTERBURY, R.J., VAN BERGEN, M.A., ORTIZ, F., LOVELL, M.A., HARRIS, J.A., DE BOER, A., WAGENAAR, J.A., ALLEN, V.M. and BARROW, P.A. (2007) Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Applied and Environmental Microbiology 73: 4543-4549.
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.
AVILA, L.A., NASCIMENTO, V.P., SALLE, C.T. and MORAES, H.L. (2006) Effects of probiotics and maternal vaccination on Salmonella enteritidis infection in broiler chicks. Avian Diseases 50: 608-612.
BAILEY, J., BLANKENSHIP, L.C. and COX, N.A. (1991) Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poultry Science 70: 2433-2438.
BARNHART, E.T., CALDWELL, D.J., CROUCH, M.C., BYRD, J.A., CORRIER, D.E. and HARGIS, B.M. (1999) Effect of lactose administration in drinking water prior to and during feed withdrawal on Salmonella recovery from broiler crops and ceca. Poultry Science 78: 211-214.
BARROW, P.A., TUCKER, J.F. and SIMPSON, J.M. (1987) Inhibition of colonization of the chicken alimentary tract with Salmonella typhimurium gram-negative facultative anaerobic bacteria. Epidemiology and Infection 98: 311-322.
BENGMARK, S. (1998) Immunonutrition: role of biosurfactants, fiber and probiotic bacteria. Nutrition 14: 585-594.
BERCHIERI, A. JR. and BARROW, P.A. (1990) Further studies on the inhibition of colonization of the chicken alimentary tract with Salmonella typhimurium by pre-colonization with an avirulent mutant. Epidemiology and Infection 104: 427-441.
BERTHELOT, F., BEAUMONT, C., MOMPART, C., MOMPART, F., GIRARD-SANTOSUOSSO, O., PARDON, P. and DUCHET-SUCHAUX, M. (1998) Estimated heritability of the resistance to cecal carrier state of Salmonella enteritidis in chickens. Poultry Science 77: 797-801.
BERTHELOT-HERAULT, F., MOMPART, F., ZYGMUNT, M.S., DUBRAY, G. and DUCHET-SUCHAUX, M. (2003) Antibody responses in the serum and gut of chicken lines differing in cecal carriage of Salmonella enteritidis. Veterinary Immunology and Immunopathology 96: 43-52.
BJERRUM, L. (2005) The intestinal microbiota of broiler chickens. PhD Thesis, Arhus, Denmark.
BLANKENSHIP L.C., , BAILEY, J.S., COX, N.A., STERN, N.J., BREWER, R. and WILLIAMS, O. (1993) Two step mucosal competitive exclusion flora treatment to diminish Salmonellae in commercial broiler chickens. Poultry Science 72: 1667-1672.
BOHEZ, L., DEWULF, J., DUCATELLE, R., PASMANS, F., HAESEBROUCK, F. and VAN IMMERSEEL, F. (2008) The effect of oral administration of a homologous hilA mutant strain on the long-term colonization and transmission of Salmonella enteritidis in broiler chickens. Vaccine 26: 372-378.
BOHEZ, L., DUCATELLE, R., PASMANS, F., BOTTELDOORN, N., HAESEBROUCK, F. and VAN IMMERSEEL, F. (2006) Salmonella enterica serovar enteritidis colonization of the chicken caecum requires the HilA regulatory protein. Veterinary Microbiology 116: 202-210.
BRADEN, C.R. (2006) Salmonella enterica serotype enteritidis and eggs: a national epidemic in the United States. Clinical Infectious Diseases 43: 512-517.
BUCHER, O., HOLLEY, R.A., AHMED, R., TABOR, H., NADON, C., NG, L.K. and D'AOUST, J.Y. (2007) Occurrence and characterization of Salmonella from chicken nuggets, strips, and pelleted broiler feed. Journal of Food Protection 70: 2251-2258.
BUMSTEAD, N. and BARROW, P.A. (1988) Genetics of resistance to Salmonella typhimurium in newly hatched chicks. British Poultry Science 29: 521-529.
BYWATER, R.J. (2004) Veterinary use of antimicrobials and emergence of resistance in zoonotic and sentinel bacteria in the EU. Journal of Veterinary Medicine B 51: 361-363.
CARDINALE, E., TALL, F., GUEYE, E.F., CISSE, M. and SALVAT, G. (2004) . Risk factors for Salmonella enterica subsp. Enterica infection in Senegalese broiler-chicken flocks. Preventive Veterinary Medicine 63: 151-161.
CHAMBERS, J.R., SPENCER, J.L. and MODLER, H.W. (1997) The influence of complex carbohydrates on Salmonella typhimurium colonization, pH, and density of broiler ceca. Poultry Science 76: 445-451.
CORRIER, D.E., HARGIS, B.M., HINTON, A.J. and DELOACH, J.R. (1993) Protective effects of used poultry litter and lactose in the feed ration on Salmonella enteritidis colonization of leghorn chicks and hens. Avian Diseases 37: 47-52.
COX, N.A., BAILEY, J.S., THOMSON, J.E. and JUVEN, B.J. (1983) Salmonella and other Enterobacteriaceae found in commercial poultry feed. Poultry Science 62: 2169-2175.
CRAVEN S.E., , COX, N.A., BAILEY, J.S. and BLANKENSHIP, L.C. (1992) Binding of Salmonella strains to immobilized intestinal mucosal preparations from broiler chickens. Avian Diseases 36: 296-303.
CRAVEN, S.E. and WILLIAMS, D.D. (1997) Inhibition of Salmonella typhimurium attachment to chicken cecal mucus by intestinal isolates of Enterobacteriaceae and lactobacilli. Avian Diseases 41: 548-558.
CRAVEN, S.E. and WILLIAMS, D.D. (1998) In vitro attachment of Salmonella typhimurium to chicken cecal mucus: effect of cations and pretreatment with Lactobacillus spp. isolated from the intestinal tracts of chickens. Journal of Food Protection 61: 265-271.
DAVIES, R., BRESLIN, M., CORRY, J.E.E, HUDSIN, W. and ALLEN, V.M. (2001) Observations on the distribution and control of Salmonella species in two integrated broiler companies. Veterinary Record 149: 227-232.
DAVIES, R.H. and BRESLIN, M. (2003a) Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Veterinary Record 152: 283-287.
DAVIES, R.H. and BRESLIN, M. (2003b) Persistence of Salmonella enteritidis phage type 4 in the environment and arthropod vectors on an empty free-range chicken farm. Environmental Microbiology 5: 79-84.
DAVIES, R.H. and WRAY, C. (1995) Mice as carriers of Salmonella enteritidis on persistently infected poultry units. Veterinary Record 137: 337-341.
DAVIES, R.H. and WRAY, C. (1996) Studies on contamination of three broiler breeder houses with Salmonella enteritidis before and after cleansing and disinfection. Avian Diseases 40: 626-633.
DEMBÉLÉ, T., OBDRZALEK, V. and VOTAVA, M. (1998) Inhibition of bacterial pathogens by lactobacilli. Zentralblat fur Bakteriologie 288: 395-401.
DESMIDT, M., DUCATELLE, R. and HAESEBROUCK, F. (1998) Serological and bacteriological observations on experimental infection with Salmonella Hadar in chickens. Veterinary Microbiology 60: 259-269.
DE ZUTTER, L. (2000) Crates inoculate broilers with Salmonella and Campylobacter. World Poultry 16(4): 19.
DIBB-FULLER, M.P., ALLEN-VERCOE, E., THORNS, C.J. and WOODWARD, M.J. (1999) Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella Enteritidis. Microbiology 145: 1023-1031.
DUCHET-SUCHAUX, M., MOMPART, F., BERTHELOT, F., BEAUMONT, C., LÉCHOPIER, P. and PARDON, P. (1997) Differences in frequency, level, and duration of cecal carriage between four outbred chicken lines infected orally with Salmonella Enteritidis. Avian Diseases 41: 559-567.
DUNCAN, S.H., HOLTROP, G., LOBLEY, G.E., CALDER, A.G., STEWART, C.S. and FLINT, H.J. (2004) Contribution of acetate to butyrate formation by human faecal bacteria. British Journal of Nutrition 91: 915-923.
EDENS, F.W., PARKHURST, C.R., CASAS, I.A. and DOBROGOSZ, W.J. (1997) Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri. Poultry Science 76: 179-196.
EECKHAUT, V., VAN IMMERSEEL, F., DEWULF, J., PASMANS, F., HAESEBROUCK, F., DUCATELLE, R., COURTIN, C.M., DELCOUR, J.A. and BROEKAERT, W. (2008) Arabinoxylooligosaccharides from wheat bran inhibit Salmonella colonization in broiler chickens. Poultry Science 87: 2329-2334.
EECKHAUT, V., VAN IMMERSEEL, F., LOUIS, P., PASMANS, F., FIEVEZ, V., HAESEBROUCK, F., DUCATELLE, R. and VANDAMME, P. (2008) Butyricicoccus pullicaecorum gen. nov., sp. Nov., an anaerobic, butyrate producing bacterium isolated from the caecal content of a broiler chicken. International Journal of Systematic and Evolutionary Microbiology 58: 2799-2802.
EFSA, and EUROPEAN FOOD SAFETY AUTHORITY, (2007a) The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic agents, Antimicrobial Resistance and Foodborne Outbreaks in the European Union in 2006.
EFSA, and EUROPEAN FOOD SAFETY AUTHORITY, (2007b) Report of the Task Force on Zoonoses Data Collection on the Analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus, in the EU, 2005-2006. Part A: Salmonella prevalence estimates. The EFSA Journal 98: 1-85.
FAO/WHO, (2003) Risk assessments of Salmonella in eggs and broiler chickens. Microbiological risk assessment series; no. 2. Geneva, Switzerland: World Health Organization.
FEBERWEE, A., DE VRIES, T.S., HARTMAN, E.G., DE WIT, J.J., ELBERS, A.R.W. and DE JONG, W.A. (2001) Vaccination against Salmonella enteritidis in Dutch commercial layer flocks with a vaccine based on a live Salmonella Gallinarum 9R strain : evaluation of efficacy, safety, and performance of serologic Salmonella tests. Avian Diseases 45: 83-91.
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.
FRIEDMAN, A., BAR-SHIRA, E. and SKLAN, D. (2003) Ontogeny of gut associated immune competence in the chick. World's Poultry Science Journal 59: 209-220.
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.
GANTOIS, I., DUCATELLE, , R, , PASMANS, F., HAESEBROUCK, F., HAUTEFORT, I., THOMPSON, A., HINTON, J. and VAN IMMERSEEL, F. (2006a) Butyrate specifically decreases Salmonella Pathogenicity Island I gene expression. Applied and Environmental Microbiology 72: 946-949.
GANTOIS, I., DUCATELLE, R., TIMBERMONT, L., BOYEN, F., BOHEZ, L., HAESEBROUCK, F., PASMANS, F. and VAN IMMERSEEL, F. (2006b) Oral immunisation with the live vaccine strains of TAD Salmonella vacE and TAD Salmonella vacT reduces internal egg contamination with Salmonella enteritidis. Vaccine 24: 6250-6255.
GARBER, L., SMELTZER, M., FEDORKA-CRAY, P., LADELY, S. and FERRIS, K. (2003) Salmonella enterica serotype enteritidis in table egg layer house environments and in mice in US layer houses and associated risk factors. Avian Diseases 47: 134-142.
GAST, R.K. and BEARD, C.W. (1989) Age-related changes in the persistence and Pathogenicity of Salmonella typhimurium in chicks. Poultry Science 68: 1454-1460.
GEISSLER, H. and KÖSTERS, J. (1972) Hygienic significance of lesser mealworm (Alphitobius diasperinus Panz.) in broiler production. Deutsche Tierarztliche Wochenschrift 79: 179-181.
GHAFIR, Y., CHINA, B., KORSAK, N., DIERICK, K., COLLARD, J.-M., GODARD, C., DE ZUTTER, L. and DAUBE, G. (2005) Belgian Surveillance Plans to Assess Changes in Salmonella Prevalence in Meat at Different Production Stages. Journal of Food Protection 68: 2269-2277.
GHEBREMICAEL, S.B., HASENSTEIN, J.R. and LAMONT, S.J. (2008) Association of interleukin-10 cluster genes and Salmonella response in the chicken. Poultry Science 87: 22-26.
GIBSON, G. and ROBERFROID, M. (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125: 1401.
GIRARD-SANTOSUOSSO, O., MENANTEAU, P., DUCHET-SUCHAUX, M., BERTHELO, F., MOMPART, F., PROTAIS, J., COLIN, P., GUILLOT, J.F., BEAUMONT, C. and LANTIER, F. (1998) Variability in the resistance of four chicken lines to experimental intravenous infection with Salmonella enteritidis phage type 4. Avian Diseases 42: 462-469.
GOREN E., , DE JONG, W.A., DOORNENBAL, P., KOOPMAN, J.P. and KENNIS, H.M. (1984) Protection of chicks against Salmonella infection induced by spray application of intestinal microflora in the hatchery. Veterinary Quarterly 6: 73-79.
GREER, G.G. (2005) Bacteriophage control of foodborne bacteria. Journal of Food Protection 68: 1102-1111.
GUSILS, C., PÉREZ CHAIA, A., GONZALEZ, S. and OLIVER, G. (1999) Lactobacilli isolated from chicken intestines: potential use as probiotics. Journal of Food Protection 62: 252-256.
HACKING, W.C., MITCHELL, W.R. and CARLSON, H.C. (1978) Salmonella investigation in an Ontario feed mill. Canadian Journal of Comparative Medicine 42: 400-406.
HALD, B., OLSEN, A. and MADSEN, M. (1998) Typhaea stercorea (Coleoptera: Mycetophagidae), a carrier of Salmonella enterica serovar infantis in a Danish broiler house. Journal of Economical Entomology 91: 660-664.
HAREIN, P.K., DE LAS CASAS, E., POMEROY, S. and YORK, M.D. (1970) Salmonella spp. and serotypes of Escherichia coli isolated from the lesser mealworm collected in poultry brooder houses. Journal of Economical Entomology 63: 80-82.
HASENSTEIN, J.R. and LAMONT, S.J. (2007) Chicken gallinacin gene cluster associated with Salmonella response in advanced intercross line. Avian Diseases 51: 561-567.
HENZLER, D.J. and OPITZ, H.M. (1992) The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian Diseases 36: 625-631.
HERMOSO, J.A., GARCIA, J.L. and GARCIA, P. (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Current Opinion in Microbiology 10: 461-472.
HEYNDRICKX, M., VANDEKERCHOVE, D., HERMAN, L., ROLLIER, I., GRIJSPEERDT, K. and DE ZUTTER, L. (2002) Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiological Infections 129: 253-265.
HIGGINS, J.P., ANDREATTI FILHO, R.L., HIGGINS, S.E., WOLFENDEN, A.D., TELLEZ, G. and HARGIS, B.M. (2008) Evaluation of Salmonella-lytic properties of bacteriophages isolated from commercial broiler houses. Avian Diseases 52: 139-142.
HINTON, A.J.R., CORRIER, D.E., ZIPRIN, R.L., SPATES, G.E. and DELOACH, J.R. (1991) Comparison of the efficacy of cultures of cecal anaerobes as inocula to reduce Salmonella typhimurium colonization in chicks with or without dietary lactose. Poultry Science 70: 67-73.
HINTON, M. and LINTON, A.H. (1988) Control of Salmonella infections in broiler chickens by the acid treatment of their feed. The Veterinary Record 123: 416-421.
HIGGINS, R., MALO, R., RENÉ-ROBERGE, E. and GAUTHIER, R. (1982) Studies on the dissemination of Salmonella in nine broiler-chicken flocks. Avian Diseases 26: 26-33.
HOLMA, R., JUVONEN, P., ASMAWI, M.Z., VAPAATALO, H. and KORPELA, R. (2002) Galacto-oligosaccharides stimulate the growth of bifidobacteria but fail to attenuate inflammation in experimental colitis in rats. Scandinavian Journal of Gastroenterology 37: 1042-1047.
HOLT, P.S., GEDEN, C.J., MOORE, R.W. and GAST, R.K. (2007) Isolation of Salmonella enteritica serovar enteritidis from houseflies (Musca domestica) found in rooms containing Salmonella serovar enteritidis-challenged hens. Applied and Environmental Microbiology 73: 6030-6035.
HUMBLOT, C., BRUNEAU, A., SUTREN, M., LHOSTE, E.F., DORE, J., ANDRIEUX, C. and RABOT, S. (2005) Brussels sprouts, inulin and fermented milk alter the faecal microbiota of human microbiota-associated rats as shown by PCR-temporal temperature gradient gel electrophoresis using universal, Lactobacillus and Bifidobacterium 16S rRNA gene primers. British Journal of Nutrition 93: 677-684.
HUME, M.E., KUBENA, L.F., BEIER, R.C., HINTON, A. JR., CORRIER, D.E. and DELOACH, J.R. (1992) Fermentation of [14C] lactose in broiler chicks by cecal anaerobes. Poultry Science 71: 1464-1470.
HUMPHREY, T.J. and LANNING, D.G. (1988) The vertical transmission of Salmonella and formic acid treatment of chicken feed. Epidemiology and Infection 100: 43-49.
HUNTER, P.R. (1992) Epizootics of Salmonella infection in poultry may be the result of modern selective breeding practices. European Journal of Epidemiology 8: 851-859.
IBA, A.M. and BERCHIERI, A. (1995) Studies on the use of a formic acid-propionic acid mixture (Bio-Add™) to control experimental Salmonella infection in broiler chickens. Avian Pathology 24: 303-311.
IBA, A.M., BERCHIERI, A. JR. and BARROW, P.A. (1995) Interference between Salmonella serotypes in intestinal colonization of chickens: correlation with in vitro behaviour. FEMS Microbiology Letters 131: 153-159.
INTERNATIONAL CHICKEN GENOME SEQUENCING CONSORTIUM, (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-716.
ISHIHARA, N., CHU, D., AKACHI, S. and JUJENA, L. (2000) Preventive effect of partially hydrolyzed guar gum on infection of Salmonella enteritidis in young and laying hens. Poultry Science 79: 689-697.
ISOLAURI, E., SALMINEN, S. and OUWENHAND, A.C. (2004) Probiotics. Best Practice and Research Clinical Gastroenterology 18: 299-313.
JIN, L.Z., HO Y.W., , ABDULLAH, N., ALI, M.A. and JALALUDIN, S. (1996) Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chickens. Letters in Applied Microbiology 23: 67-71.
JONES, F.T. and RICHARDSON, K.E. (2004) Salmonella in commercially manufactured feeds. Poultry Science 83: 384-391.
KHAN, M. and KATAMAY, M. (1969) Antagonistic effects of fatty acids against Salmonella in meat and bone meal. Applied Microbiology 17: 402-404.
KIEN, C.L., BLAUWIEKEL, R., BUNN, J.Y., JETTON, T.L., FRANKEL, W.L. and HOLST, J.J. (2007) Cecal infusion of butyrate increases intestinal cell proliferation in piglets. Journal of Nutrition 137: 916-922.
KIM, A., LEE, Y.J., KANG, M.S., KWAG, M.S. and CHO, J.K. (2007) Dissemination and tracking of Salmonella spp. in integrated broiler operation. Journal of Veterinary Science 8: 155-161.
KIMURA, A.C., REDDY, V., MARCUS, R., CIESLAK, P.R., MOHLE-BOETANI, J.C., KASSENBORG, H.D., SEGLER, S.D., HARDNETT, F.P., BARRETT, T. and SWERDLOW, D.L. (2004) Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case-control study in FoodNet sites. Clinical Infectious Diseases 38: S244-52.
KINDE, H., CASTELLAN, D.M., KERR, D., CAMPBELL, J., BREITMEYER, R. and ARDANS, A. (2005) Longitudinal monitoring of two commercial layer flocks and their environments for Salmonella enterica serovar enteritidis and other Salmonellae. Avian Diseases 49: 189-194.
KIZERWETTER-SWIDA, M. and BINEK, M. (2005) Selection of potentially probiotic Lactobacillus strains towards their inhibitory activity against poultry enteropathogenic bacteria. Polish Journal of Microbiology 54: 287-294.
KLEESSEN, B., HARTMANN, L. and BLAUT, M. (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. British Journal of Nutrition 86: 291-300.
KOENEN, M.E., KRAMER, J., VAN DER HULST, R., HERES, L., JEURISSEN, S.H. and BOERSMA, W.J. (2004) Immunomodulation by probiotic lactobacilli in layer- and meat-type chickens. British Poultry Science 45: 355-366.
KOTUNIA, A., WOLINSKI, J., LAUBITZ, D., JURKOWSKA, M., ROMÉ, V., GUILLOTEAU, P. and ZABEILSKI, R. (2004) Effect of sodium butyrate on the small intestine development in neonatal piglets fed by artificial sow. Journal of Physiology and Pharmacology 55(S2): 59-68.
LAMONT, S.J. (2004) New advances in controlling poultry disease. British Poultry Science 45: S11-S12.
LAWHON, S.D., MAURER, R., SUYEMOTO, M. and ALTIER, C. (2002) Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Molecular Microbiology 46: 1451-1464.
LEESON, S. and MARCOTTE, M. (1993a) Irradiation of poultry feed I. Microbial status and bird response. World's Poultry Science Journal 49: 19-33.
LEESON, S. and MARCOTTE, M. (1993b) Irradiation of poultry feed II. Effect on nutrient composition. World's Poultry Science Journal 49: 120-131.
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.
MANNING, T.S. and GIBSON, G.R. (2004) Prebiotics. Best Practice and Research Clinical Gastroenterology 18: 287-298.
MARTIN, G., METHNER, U., RYCHLIK, I. and BARROW, P.A. (2002) Specificity of inhibition between Salmonella strains. Deutsche Tierarztliche Wochenschrift 109: 154-157.
MCALLISTER, J.C., STEELMAN, C.D. and SKEELES, J.K. (1994) Reservoir competence of the lesser mealworm (Coleoptera: Tenebronidae) for Salmonella typhimurium (Eubacteriales: Enterobacteriaceae). Journal of Medical Entomology 31: 369-372.
MACKENZIE, M.A. and BAINS, B.S. (1976) Dissemination of Salmonella serotypes from raw feed ingredients to chicken carcasses. Poultry Science 55: 957-960.
MEAD G.C., (2000) Prospects for competitive exclusion treatment to control Salmonellas and other foodborne pathogens in poultry. Veterinary Journal 159: 111-123.
MEAD, P.S., SLUTSKER, L., DIETZ, V., MCCAIG, L.F., BRESEE, J.S., SHAPIRO, C., GRIFFIN, P.M. and TAUXE, R.V. (1999) Food-related illness and death in the United States. Emerging Infectious Diseases 5: 607-625.
METHNER, U. and STEINBACH, G. (1997) Efficacy of maternal Salmonella antibodies against oral infection of chicks with Salmonella enteritidis. Berliner und Münchner Tierärztliche Wochenschrift 110: 373-377.
METHNER, U., STEINBACH, G. and MEYER, H. (1994) Investigations on the efficacy of Salmonella immunization of broiler breeder birds to Salmonella colonization of these birds and their progeny following experimental oral infection. Berliner und Münchner Tierärztliche Wochenschrift 107: 192-198.
MIAN, L.S., MAAG, H. and TACAL, J.V. (2002) Isolation of Salmonella from muscoid flies at commercial animal establishments in San Bernardino County, California. Journal of Vector Ecology 27: 82-85.
MIYAMOTO, T., HORIE, T., FUJIWARA, T., FUKATA, T., SASAI, K. and BABA, E. (2000) Lactobacillus flora in the cloaca and vagina of hens and its inhibitory activity against Salmonella enteritidis in vitro. Poultry Science 79: 7-11.
MORGAN-JONES, S. (1987) Practical aspects of disinfection and infection control, in: LINTON, A.H. (Ed) Disinfection in veterinary practice, pp. 144-147 (England, UK: Blackwell Scientific Publication).
MORO, C.V., FRAVALO, P., AMELOT, M., CHAUVE, C., ZENNER, L. and SALVAT, G. (2007) Colonization and organ invasion in chicks experimentally infected with Dermanyssus gallinae contaminated by Salmonella enteritidis. Avian Pathology 36: 307-311.
NISBET, D.J., CORRIER, D.E. and DELOACH, J.R. (1993) Effect of mixed cecal microflora maintained in continuous culture and of dietary lactose on Salmonella Typhimurium colonization of broiler chicks. Poultry Science 37: 528-535.
NISBET, D.J., CORRIER, D.E., SCANLAN, C.M., HOLLISTER, A.G., BEIER, R.C. and DELOACH, J.R. (1994) Effect if 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.
NUOTIO, L., SCHNIETZ, C., HALONEN, U. and NURMI, E. (1992) Use of competitive exclusion to protect newly-hatched chicks against intestinal colonisation and invasion by Salmonella enteritidis PT4. British Poultry Science 33: 775-779.
NURMI, E. and RANTALA, M. (1973) New aspects of Salmonella infection in broiler production. Nature 241: 210-211.
OCANA, V.S., PESCE DE RUIZ HOLGADO, A.A. and NADER-MACIAS, M.E. (1999) Characterisation of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain. Applied and Environmental Microbiology 65: 5631-5635.
OLSEN, A.R. and HAMMACK, T.S. (2000) Isolation of Salmonella spp. from the housefly, Musca domestica L., and the dump fly, Hydrotaea aenescenc (Wiedermann) (Diptera: Muscidae), at caged-layer houses. Journal of Food Protection 63: 958-960.
OLSEN, J.E., BROWN, D.J., MADSEN, M. and BISGAARD, M. (2003) Cross-contamination with Salmonella on a broiler slaughterhouse line demonstrated by use of epidemiological markers. Journal of. Applied Microbiology 94: 826-835.
OYARZABAL, O.A. and CONNER, D.E. (1996) Application of direct-fed microbial bacteria and fructooligosaccharides for Salmonella control in broilers during feed withdrawal. Poultry Science 75: 186-190.
OYOFO, B.A., DELOACH, J.R., CORRIER, D.E., NORMAN, J.O., ZIPRIN, R.L. and MOLLENHAUER, H.H. (1989) Effect of carbohydrates on Salmonella typhimurium colonization in broiler chickens. Avian Diseases 33: 531-534.
PALMU, L. and CAMELIN, I. (1997) The use of competitive exclusion in broilers to reduce the level of Salmonella contamination on the farm and at the processing plant. Poultry Science 76: 1501-1505.
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.
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.
POPPE, C., BARNUM, D.A. and MITCHELL, W.R. (1986) Effect of chlorination of drinking water on experimental Salmonella infection in poultry. Avian Diseases 30: 362-369.
PROUX, K., JOUY, E., HOUDAYER, C., PROTAIS, J., DIBB-FULLER, M., BOSCHER, E., GILLARD, A., GRACIEUX, P., GILBERT, F., BEAUMONT, C. and DUCHET-SUCHAUX, M. (2002) Reliable ELISAs showing differences between resistant and susceptible lines in hens orally inoculated with Salmonella enteritidis. Veterinary Research 33: 23-33.
PRYDE, S.E., DUNCAN, S.H., HOLD, G.L., STEWART, C.S. and FLINT, H.J. (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiology Letters 217: 133-139.
RADA, V. and PETR, J. (2000) A new selective medium for the isolation of glucose non-fermenting Bifidobacteria from hen caeca. Journal of Microbiological Methods 43: 127-132.
RADA, V., DUSKOVA, D., MAROUNEK, M. and PETR, J. (2001) Enrichment of Bifidobacteria in the hen caeca by dietary inulin. Folia Microbiologica 46: 76-75.
RASSCHAERT, G., HOUF, K. and DE ZUTTER, L. (2007) Impact of the slaughter line contamination on the presence of Salmonella on broiler carcasses. Journal of Applied Microbiology 103: 333-341.
RASSCHAERT, G., HOUF, K., GODARD, C., WILDEMAUWE, C., PASTUSZCZ-FRAK, M. and DE ZUTTER, L. (2008) Contamination of carcasses with Salmonella during poultry slaughter. Journal of Food Protection 71: 146-152.
REITER, M.G., FIORESE, M.L., MORETTO, G., LOPEZ, M.C. and JORDANO, R. (2007) Prevalence of Salmonella in a poultry slaughterhouse. Journal of Food Protection 70: 1723-1725.
RIGBY, C.E., PETTIT, J.R., EBTLEY, A.H., SALOMONS, M.O. and LIOR, H. (1980) The relationships of Salmonellae from infected broiler flocks, transport crates or processing plants to contamination of eviscerated carcasses. Canadian Journal of Comparative Medicine 46: 272-278.
ROSE, N., BEAUDEAU, F., DROUIN, P., TOUX, J.Y., ROSE, V. and COLIN, P. (2000) Risk factors for Salmonella persistence after cleansing and disinfection in French broiler houses. Preventive Veterinary Medicine 44: 9-20.
ROSE, N., MARIANI, J.P., DROUIN, P., TOUX, J.Y., ROSE, V. and COLIN, P. (2003) A decision-support system for Salmonella in broiler-chicken flocks. Preventive Veterinary Medicine 59: 27-42.
ROSSI, M., CORRADINI, C., AMARETTI, A., NICOLINI, M., POMPEI, A., ZANONI, S. and MATTEUZZI, D. (2005) Fermentation of fructooligosaccharides and inulin by Bifidobacteria: a comparative study of pure and fecal cultures. Applied and Environmental Microbiology 71: 6150-6158.
RUSSELL, J.B. and DIEZ-GONZALEZ, F. (1998) The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 39: 205-234.
SALMINEN, S., BOULEY, C., BOUTROIN-RUAULT, M.C., CUMMINGS, J.H., FRANCK, A., GIBSON, G.R., ISOLAURI, E., MOREAU, M.C., ROBERFROID, M. and ROWLAND, I. (1998) Functional food science and gastrointestinal physiology and function. British Journal of Nutrition 80: S147-177.
SCHLEIFER, J.H., JUVEN, B.J., BEARD, C.W. and COX, N.A. (1984) The susceptibility of chicks to Salmonella montevideo in artificially contaminated poultry feed. Avian Diseases 28: 497-503.
SCHLUNDT, J., TOYOFUKU, H., JANSEN, J. and HERBST, S.A. (2004) Emerging food-borne diseases. Revue Sciencifique et Technologique OIE 23: 513-533.
SCHNEITZ C., , NUOTIO, L., MEAD, G. and NURMI, E. (1992) Competitive exclusion in the young bird: challenge models, administration and reciprocal protection. International Journal of Food Microbiology 15: 241-244.
SEO K.H., , HOLT, P.S., GAST, R.K. and HOFACRE, C.L. (2000) Combined effect of antibiotic and competitive exclusion treatment on Salmonella enteritidis fecal shedding in polted laying hens. Journal of Food Protection 63: 545-548.
SKOV, M.N., SPENCER, A.G., HALD, B., PETERSEN, L., NAUERBY, B., CARSTENSEN, B. and MADSEN, M. (2004) The role of litter beetles as potential reservoir for Salmonella enterica and thermophilic Campylobacter spp. between broiler flocks. Avian Diseases 48: 9-18.
SMITH, H.W. and TUCKER, J.F. (1975) The effect of antibiotic therapy on the faecal excretion of Salmonella typhimurium by experimentally infected chickens. Journal of Hygiene (London) 75: 275-292.
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.
SPRONG, R.C., HULSTEIN, M.F.E. and VAN DER MEER, R. (2001) Bactericidal activities of milk lipids. Antimicrobial Agents and Chemotherapy 45: 1298-1301.
THITARAM, S.N., CHUNG, C.H., DAY, D.F., HINTON, A. JR., BAILEY, J.S. and SIRAGUSA, G.R. (2005) Isomaltooligosaccharide increases cecal Bifidobacterium population in young broiler chickens. Poultry Science 84: 998-1003.
THOMPSON, J.L. and HINTON, M. (1997) Antibacterial activity of formic and propionic acids in the diet of hens on Salmonellas in the crop. British Poultry Science 38: 59-65.
TUOHY, K.M., ROUZAUD, G.C., BRÜCK, W.M. and GIBSON, G.R. (2005) Modulation of the human gut microflora towards improved health using prebiotics – assessment of efficacy. Current Pharmaceutical Design 11: 75-90.
TZORTZIS, G., GOULAS, A.K., GEE, J.M. and GIBSON, G.R. (2005) A novel galactooligosaccharide mixture increases the Bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. Journal of Nutrition 135: 1726-1731.
VAN COILLIE, E., GORIS, J., CLEENWERCK, I., GRIJSPEERDT, K., BOTTELDOORN, N., VAN IMMERSEEL, F., DE BUCK, J., VANCANNEYT, M., SWINGS, J., HERMAN, L. and HEYNDRICKX, M. (2007) Identification of Lactobacilli isolated from the cloaca of laying hens and characterization for potential use as probiotics to control Salmonella enteritidis. Journal of Applied Microbiology 102: 1095-1106.
VAN DUIJKEREN, E., WANNET, W.J., HOUWERS, D.J. and VAN PELT, W. (2003) Antimicrobial susceptibilities of Salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. Journal of Clinical Microbiology 41: 3574-2578.
VAN IMMERSEEL, F., CAUWERTS, K., DE VRIESE, L., HAESEBROUCK, F. and DUCATELLE, R. (2002) Feed additives to control Salmonella in poultry, World's Poultry Science Journal 58: 501-513.
VAN IMMERSEEL, F., DE BUCK, J., MEULEMANS, G., PASMANS, F., VELGE, P., BOTTREAU, E., HAESEBROUCK, F. and DUCATELLE, R. (2003) Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids, International Journal of Food Microbiology 85: 237 - 248.
VAN IMMERSEEL, F., DE BUCK, J., BOYEN, F., BOHEZ, L., PASMANS, F., VOLF, J., SEVCIK, M., RYCHLIK, I., HAESEBROUCK, F. and DUCATELLE, R. (2004a) Medium-chain fatty acids decrease colonization and invasion shortly after infection with Salmonella enteritidis in chickens through hilA suppression. Applied and Environmental Microbiology 70: 3582-3587.
VAN IMMERSEEL, F., FIEVEZ, V., DE BUCK, J., PASMANS, F., MARTEL, A., HAESEBROUCK, F. and DUCATELLE, R. (2004b) Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella enteritidis in young chickens. Poultry Science 83: 69-74.
VAN IMMERSEEL, F., METHNER, U., RYCHLIK, I., NAGY, B., VELGE, P., MARTIN, G., FOSTER, N., DUCATELLE, R. and BARROW, P.A. (2005) Vaccination and early protection against non-host-specific Salmonella serotypes in poultry: exploitation of innate immunity and microbial activity. Epidemiology and Infection 133: 959-978.
VAN IMMERSEEL, F., RUSSELL, J.B., FLYTHE, M.D., GANTOIS, I., TIMBERMONT, L., PASMANS, F., HAESEBROUCK, F. and DUCATELLE, R. (2006) The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathology 35: 182-188.
VELDMAN, A., VAHL, H.A., BORGGREVE, G.J. and FULLER, D.C. (1995) A survey of the incidence of Salmonella species and Enterobacteriaceae in poultry feeds and feed components. Veterinary Record 136: 169-172.
WACHTERSHAUSER, A. and STEIN, J. (2000) Rationale for the luminal provision of butyrate in intestinal diseases. European Journal of Nutrition 39: 164-171.
WALDROUP, A.L., SKINNER, J.T., HIERHOLZER, R.E. and WALDROUP, P.W. (1993) An evaluation of fructooligosaccharide in diets for broiler chickens and effects on Salmonellae contamination of carcasses. Poultry Science 72: 643-650.
WALES, A., BRESLIN, M., CARTER, B., SAYERS, R. and DAVIES, R. (2007) A longitudinal study of environmental Salmonella contamination in cages and free-range layer flocks. Avian Pathology 36: 187-197.
WILLIAMS, J.E. (1981) . Salmonella in poultry feeds – A worldwide review. World's Poultry Science Journal 37: 6-25.
WONG, G.K., LIU, B., WANG, J., ZHANG, Y., YANG, X., ZHANG, Z., MENG, Q., ZHOU, J., LI, D. and ET AL., (2004) A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432: 717-722.
WOODWARD, M.J., GETTINBY, G., BRESLIN, M.F., CORKISH, J.D. and HOUGHTON, S. (2002) The efficacy of Salenvac, a Salmonella enterica subsp. Enterica serotype enteritidis iron-restricted bacterin vaccine, in laying chickens. Avian Pathology 31: 383-392.


Strategies to control Salmonella in the broiler production chain

  • F. VAN IMMERSEEL (a1), L. DE ZUTTER (a2), K. HOUF (a2), F. PASMANS (a1), F. HAESEBROUCK (a1) and R. DUCATELLE (a1)...


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