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Control strategies for Campylobacter infection in poultry production

Published online by Cambridge University Press:  25 February 2013

K. GHAREEB ,
W.A. AWAD ,
M. MOHNL ,
G. SCHATZMAYR  and
J. BÖHM
K. GHAREEB
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, and
W.A. AWAD*
Affiliation:
Clinic for Avian, Reptile and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Veterinärplatz 1, A-1210 Vienna, Austria
M. MOHNL
Affiliation:
BIOMIN Holding GmBH, Industriestrasse 21, 3130 Herzogenburg, Austria
G. SCHATZMAYR
Affiliation:
BIOMIN Research Center, Technopark 1, 3430 Tulln, Austria
J. BÖHM
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, and
*
Corresponding author: wageha.awad@vetmeduni.ac.at
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Abstract

Campylobacteriosis is the most frequent zoonotic disease in humans worldwide. Poultry meat contaminated by Campylobacter jejuni (C. jejuni) is an important source of this enteric zoonosis. Broiler chickens are the common natural host for this pathogen and infected birds carry a very high Campylobacter load in their gastrointestinal tract. Therefore, intervention at the farm level by reducing pathogen colonisation should be taken into consideration in any control policy. In addition, hygienic measures at the farm and control measures during carcass processing can reduce Campylobacter numbers on the retail product. It is important to differentiate between prevention and colonisation-reducing measures, which intervene at a different stage of the infection process. Several approaches have been conducted to reduce the number of Campylobacter in poultry, such as vaccination, passive immunisation, bacteriophages, bacteriocins, organic acids or their derivatives and medium chain of fatty acids, all with varying degrees of success. Nonetheless, to date there is no reliable and practical intervention measure available to reduce colonisation of the broiler gut with Campylobacter. A possible way to reduce Campylobacter contamination in poultry is to develop new strategies at the primary production level. As a consequence, it has become necessary to develop alternatives such as beneficial microorganisms (probiotics). The use of probiotics can help to improve the natural defence of animals against pathogenic bacteria and is an effective approach for livestock to reduce bacterial contamination. This review summarises current on-farm control options to reduce the prevalence and colonisation of Campylobacter in poultry. The interaction between poultry welfare and Campylobacter colonisation is also discussed.

Keywords

Campylobacteriosiszoonotic diseasesbacteriophagespassive immunityprobiotics
Type
Reviews
Information
World's Poultry Science Journal , Volume 69 , Issue 1 , March 2013 , pp. 57 - 76
Copyright
Copyright © World's Poultry Science Association 2013

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References

ACUFF, G.R., VANDERZANT, C., HANNA, M.O., EHLERS, J.G., GOLAN F.A., and GARDNER, F.A. (1986) Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey products. Journal of Food Protection 49: 712-717.CrossRefGoogle ScholarPubMed
ACUFF, G.R., VANDERZANT, C., GARDNER, F.A. and GOLAN, F.A. (1982) Examination of turkey eggs, poults and brooder house facilities for Campylobacter jejuni. Journal of Food Protection 45: 1279-1281.CrossRefGoogle ScholarPubMed
ALLEN, V.M., WEAVER, H., RIDLEY, A.M., HARRIS, J.A., SHARMA, M., EMERY, J., SPARKS, N., LEWIS, M. and EDGE, S. (2008) Sources and spread of thermophilic Campylobacter spp. during partial depopulation of broiler chicken flocks. Journal of Food Protection 71: 264-270.CrossRefGoogle ScholarPubMed
ALLEN, V. and NEWELL, D.G. (2005) Food standards agency report: evidence for the effectiveness of biosecurity to exclude Campylobacter from poultry flocks. Http://www.food.gov.uk/multimedia/pdfs/biocampy.pdf, (04/07/06).Google Scholar
ATTERBURY, R.J., DILLON, E., SWIFT, C., CONNERTON, P.L., FROST, J.A., DODD, C.E.R., REES, C.E.D. and CONNERTON, I.F. (2005) Correlation of Campylobacter bacteriophage with reduced presence of host in broiler chicken cæca. Applied Environmental Microbiology 71: 4885-4887.CrossRefGoogle Scholar
BAURHOO, B., FERKET, P.R. and ZHAO, X. (2009) Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, caecal and litter microbial populations, and carcass parameters of broilers. Poultry Science 88: 2262-2272.CrossRefGoogle ScholarPubMed
BEERY, J.T., HUGDAHL, M.B. and DOYLE, M.P. (1988) Colonisation of gastrointestinal tracts of chicks by Campylobacter jejuni. Applied Environmental Microbiology 54: 2365-2370.CrossRefGoogle ScholarPubMed
BERRANG, M.E., SMITH, D.P., WINDHAM, W.R. and FELDNER, P.W. (2004) Effect of intestinal content contamination on broiler carcass Campylobacter counts. Journal of Food Protection 67: 235-238.CrossRefGoogle ScholarPubMed
BOYSEN, L. and ROSENQUIST, H. (2009) Reduction of thermotolerant Campylobacter species on broiler carcasses following physical decontamination at slaughter. Journal of Food Protection 72: 497-502.CrossRefGoogle ScholarPubMed
BUCKLEY, A.M., WANG, J.H., HUDSON, D.L., GRANT, A.J., JONES, M.A., MASKELL, D.J. and STEVENS, M.P. (2010) Evaluation of live-attenuated Salmonella vaccines expressing Campylobacter antigens for control of C. jejuni in poultry. Vaccine 28: 1094-1105.CrossRefGoogle ScholarPubMed
BULL S.A., , ALLEN, V.M., DOMINGUE, G., JØRGENSEN, F., FROST, J.A., URE, R., WHYTE, R., TINKER, D., CORRY, J.E.L., GILLARD-KING, J. and HUMPHREY, T.J. (2006) Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Applied Environmental Microbiology 72: 645-652.CrossRefGoogle ScholarPubMed
BULL, S.A., THOMAS, A., HUMPHREY, T., ELLIS-IVERSEN, J., COOK, A.J., LOVELL, R. and JORGENSEN, F. (2008) Flock health indicators and Campylobacter spp. In commercial housed broilers reared in Great Britain. Applied Environmental Microbiology 74: 5408-5413.CrossRefGoogle ScholarPubMed
BYRD, J.A., HARGIS, B.M., CALDWELL, D.J., BAILEY, R.H., HERRON, K.L., MCREYNOLDS, J.L., BREWER, R.L., ANDERSON, R.C., BISCHOFF, K.M., CALLAWAY, T.R. and KUBENA, L.F. (2001) Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poultry Science 80: 278-283.CrossRefGoogle ScholarPubMed
CALDERON-GOMEZ, L.I., HARTLEY, L.E., MCCORMACK, A., RINGOIR, D.D. and KOROLIK, V. (2009) Potential use of characterised hyper-colonising strain(s) of Campylobacter jejuni to reduce circulation of environmental strains in commercial poultry. Veterinary Microbiology 134: 353-361.CrossRefGoogle ScholarPubMed
CALLICOTT, K.A., FRIÐRIKSDÓTTIR, V., REIERSEN, J., LOWMAN, R., BISAILLON, J.R., GUNNARSSON, E., BERNDTSON, E., HIETT, K.L., NEEDLEMAN, D.S. and STERN, N.J. (2006) Lack of evidence for vertical transmission of Campylobacter spp. in chickens. Applied Environmental Microbiology 72: 5794-5798.CrossRefGoogle ScholarPubMed
CARVALHO, C.M., GANNON, B.W., HALFHIDE, D.E., SANTOS, S.B., HAYES, C.M., ROE, J.M. and AZEREDO, J. (2010) The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiology 10: 232.CrossRefGoogle ScholarPubMed
CHANG, M.H. and CHEN, T.C. (2000) Reduction of Campylobacter jejuni in a simulated chicken digestive tract by lactobacilli cultures. Journal of Food Protection 63: 1594-1597.CrossRefGoogle Scholar
CHAVEERACH, A. KEUZENKAMP, P.D., , LIPMAN, L.J.A. and VAN KNAPEN, F. (2002) In vitro study on the effect of organic acids on Campylobacter jejuni/coli population in mixtures of water and feed. Poultry Science 81: 621-628.CrossRefGoogle Scholar
CHAVEERACH, P., LIPMAN, L.J. and VAN KNAPEN, F. (2004a) Antagonistic activities of several bacteria on in vitro growth of 10 strains of Campylobacter jejuni/coli. International Journal of Food Microbiology 90: 43-50.CrossRefGoogle ScholarPubMed
CHAVEERACH, P., KEUZENKAMP, D.A., LIPMAN, L.J.A. and VAN KNAPEN, F. (2004b) Effect of organic acids in drinking water for young broilers on Campylobacter infection, volatile fatty acid production, gut microflora and histological cell changes. Poultry Science 83: 330-334CrossRefGoogle ScholarPubMed
CHEN, C.C. and WALKER, W.A. (2005) Probiotics and prebiotics: role in clinical disease states. Advanced Pediatrics 52: 77-113.CrossRefGoogle ScholarPubMed
CHEN, H.C. and STERN, N.J. (2001) Competitive exclusion of heterologous Campylobacter spp. in chicks. Applied and Environmental Microbiology 67: 848-851.CrossRefGoogle ScholarPubMed
CHUMA, T., MAKINO, K., OKAMOTO, K. and YUGI, H. (1997) Analysis of distribution of Campylobacter jejuni and Campylobacter coli in broilers by using restriction fragment length polymorphism of flagellin gene. Journal of Veterinary Medical Science 59: 1011-1015.CrossRefGoogle ScholarPubMed
CLARK, A.G. and BUESCHKENS, D.H. (1988) Horizontal spread of human and poultry-derived strains of Campylobacter jejuni among broiler chickens held in incubators and shipping boxes. Journal of Food Protection 51: 438-441.CrossRefGoogle Scholar
CLEVELAND, J., MONTVILLE, T.J., NES, I.F. and CHIKINDAS, M.L. (2001) Bacteriocins safe, natural antimicrobials for food preservation. International Journal of Food Microbiology 71: 1-20.CrossRefGoogle ScholarPubMed
CORRY, J.E. and ATABAY, H.I. (2001) Poultry as a source of Campylobacter and related organisms. Symposium Series (Society for Applied Microbiology) 30: 96S-114S.CrossRefGoogle Scholar
DE ZOETE, M.R., VAN PUTTEN, J.P.M. and WAGENAAR, J.A. (2007) Vaccination of chickens against Campylobacter. Vaccine 25: 5548-5557.CrossRefGoogle ScholarPubMed
EC (COUNCIL DIRECTIVE), NO 1999/74/EC of 19 July 1999 laying down minimum standards for the protection of laying hens. (OJ No. L 203, 03. 08. 1999 and p. 53).Google Scholar
EFSA, (2010a) Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008. Part A: Campylobacter and Salmonella prevalence estimates, EFSA J. 8, 1503 (p. 99) doi:10.2903/j.efsa.2010.1503.CrossRefGoogle Scholar
EFSA, (2010b) Panel on Biological Hazards (BIOHAZ), scientific opinion on quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. EFSA J. 8, 1437 (p. 89) doi:10.2903/ j.efsa.2010.1437.CrossRefGoogle Scholar
EFSA, (2009) The Community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2007. Information on specific zoonoses. Campylobacter. EFSA J. 223:109-133.Google Scholar
EFSA, (2008) Assessing health benefits of controlling Campylobacter in the food chain. EFSA Scientific colloquium summary report. p. 179. EFSA, Parma, Italy.Google Scholar
EKDAHL, K., NORMANN, B. and ANDERSSON, Y. (2005) Could flies explain the elusive epidemiology of campylobacteriosis ? BMC Infectious Diseases 5: 11.CrossRefGoogle ScholarPubMed
ELLIS-IVERSEN, J., JORGENSEN, F., BULL, S., POWELL, L., COOK, A.J., HUGAS, M., TSIGARIDA, E., ROBINSON, T. and CALISTRI, P. (2009) The EFSA Scientific Panel on Biological Hazards first mandate: May 2003-May 2006. Insight into foodborne zoonoses. Trends Food Science Technology 20:188-193.Google Scholar
EL-SHIBINY, A., SCOTT, A., TIMMS, A., METAWEA, Y., CONNERTON, P. and CONNERTON, I. (2009) Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. Journal of Food Protection 72: 733-740.CrossRefGoogle ScholarPubMed
EVANS, S.J. and SAYERS, A.R. (2000) A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Preventive Veterinary Medicine 46: 209-223.CrossRefGoogle ScholarPubMed
FERNANDEZ, F., SHARMA, R., HINTON, M. and BEDFORD, M.R. (2000) Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cellular and Molecular Life Sciences 57: 1793-1801.CrossRefGoogle ScholarPubMed
FIGUEROA, G., HIDALGO, H., TRONCOSCO, M., ROSENDE, S. and SOTO, V. (1983) Campylobacter jejuni in broilers, hens, and eggs in developing countries, in: PEARSON, A.D., SKIRROW, M.B., ROWS, B., DAVIES, J.R. & JONES, D.M. (Eds) Campylobacter II, pp. 161-162 (London Public Health Laboratory Service, London).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 colonisation 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
GHAREEB, K., AWAD, W.A., MOHNL, M., PORTA, R., BIARNÉS, M. and SCHATZMAYR, G. (2012) Evaluating the efficacy of an avian-specific probiotic to reduce the colonisation of Campylobacter jejuni in broiler chickens. Poultry Science 91:.1825-1832.CrossRefGoogle ScholarPubMed
GIBBENS, J.C., GIBBENS, J.C., PASCOE, S.J.S., EVANS, S.J., DAVIES, R.H. and SAYERS, A.R. (2001) A trial of biosecurity as a means to control campylobacter infection of broiler chickens. Preventive Veterinary Medicine 48: 85-99.CrossRefGoogle ScholarPubMed
GOODE, D., ALLEN, V.M. and BARROW, P.A. (2003) Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophage. Applied Environmental Microbiology 69: 5032-5036.CrossRefGoogle Scholar
HAGENS, S. and LOESSNER, M.J. (2010) Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Current Pharmaceutical Biotechnology 11: 58-68.CrossRefGoogle ScholarPubMed
HALD, B., SKOVGARD, H., PEDERSEN, K. and BUNKENBORG, H. (2008) Influxed insects as vectors for Campylobacter jejuni and Campylobacter coli in Danish broiler houses. Poultry Science 87: 1428-1434.CrossRefGoogle ScholarPubMed
HALD, B., SOMMER, H.M. and SKOVGARD, H. (2007) Use of fly screens to reduce Campylobacter spp. introduction in broiler houses. Emerging Infectious Disease 13: 1951-1953.CrossRefGoogle ScholarPubMed
HERES, L., ENGEL, B., URLINGS, H.A., WAGENAAR, J.A. and VAN KNAPEN, F. (2004) Effect of acidified feed on susceptibility of broiler chickens to intestinal infection by Campylobacter and Salmonella. Veterinary Microbiology 99: 259-267.CrossRefGoogle ScholarPubMed
HERES, L., ENGEL, B., VAN KNAPEN, F., WAGENAAR, J.A. and URLINGS, B.A.P. (2003) Effect of fermented feed on the susceptibility for Campylobacter jejuni colonisation in broiler chickens with and without concurrent inoculation of Salmonella enteritidis. International Journal of Food Microbiology 87: 75-86.CrossRefGoogle ScholarPubMed
HERMAN, L., HEYNDRICKX, M., GRIJSPEERDT, K., VANDEKERCHOVE, D., ROLLIER, I. and DE ZUTTER, L. (2003) Routes for Campylobacter contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 131: 1169-1180.CrossRefGoogle ScholarPubMed
HERMANS, D., MARTEL, A., VAN DEUN, K., VERLINDEN, M., VAN IMMERSEEL, F., GARMYN, A., MESSENS, W., HEYNDRICKX, M., HAESEBROUCK, F. and PASMANS, F. (2010) Intestinal mucus protects Campylobacter jejuni in the caeca of colonised broiler chickens against the bactericidal effects of medium-chain fatty acids. Poultry Science 89: 1144-1155.CrossRefGoogle Scholar
HERMANS, D., VAN DEUN, K., MESSENS, W., MARTEL, A., VAN IMMERSEEL, F., HAESEBROUCK, F. RASSCHAERT, G., , HEYNDRICKX, M. and PASMANS, F. (2011) Campylobacter control in poultry by current intervention measures ineffective: Urgent need for intensified fundamental research. Veterinary Microbiology 152: 219-228.CrossRefGoogle ScholarPubMed
HILMARSSON, H., THORMAR, H., THRAINSSON, J.H. and GUNNARSSON, E. (2006) Effect of glycerol monocaprate (monocaprin) on broiler chickens: An attempt at reducing intestinal Campylobacter infection. Poultry Science 85: 588-592.CrossRefGoogle ScholarPubMed
HUGAS, M., TSIGARIDA, E., ROBINSON, T. and CALISTRI, P. (2009) The EFSA Scientific Panel on Biological Hazards first mandate: May 2003-May 2006. Insight into foodborne zoonoses. Trends Food Science Technology 20: 188-193.CrossRefGoogle Scholar
HUMPHREY, T., O'BRIEN, S. and MADSEN, M. (2007) Campylobacters as zoonotic pathogens: a food production perspective. International Journal of Food Microbiology 117: 237-257.CrossRefGoogle ScholarPubMed
HUTCHINSON, M.L., WALTERS, L.D., AVERY, S.M., MUNRO, F. and MOORE, A. (2005) Analyses of livestock production, waste storage, and pathogen levels and prevalence's in farm manures. Applied Environmental Microbiology 71: 1231-1236.CrossRefGoogle Scholar
JACOBS-REITSMA, W.F., VAN DE GIESSEN, A.W., BOLDER, N.M. and MULDER, R.W. (1995) Epidemiology of Campylobacter spp. at two Dutch broiler farms. Epidemiology and Infection 114: 413-421.CrossRefGoogle ScholarPubMed
JACOBS-REITSMA, W. (2000) Campylobacter in the food supply, in: NACHAMKIN, I. & BLASER, M.J. (Eds) Campylobacter. 2nd ed., pp. 467-481 (American Society for Microbiology Press, Washington, DC).Google Scholar
JIN, L.Z., HO, Y.W., ABDULLAH, N. and JALALUDIN, S. (1996) Influence of dried Bacillus subtilis and lactobacilli cultures on intestinal microflora and performance in broilers. Asian-Australasian Journal of Animal Science 9: 397-404.CrossRefGoogle Scholar
KAPPERUD, G., SKJERVE, E., VIK, L., HAUGE, K., LYSAKER, A., AALMEN, I., OSTROFF, S.M. and POTTER, M. (1993) Epidemiological investigation of risk factors for Campylobacter colonisation in Norwegian broiler flocks. Epidemiology and Infection 111: 245-255.CrossRefGoogle ScholarPubMed
KASRAZADEH, M. and GENIGEORGIS, C. (1987) Origin and prevalence of Campylobacter jejuni in ducks and duck meat at the farm and processing plant level. Journal of Food Protection 50: 321-326.CrossRefGoogle ScholarPubMed
KEENER, K.M., BASHOR, M.P., CURTIS, P.A., SHELDON, B.W. and KATHARIOU, S. (2004) Comprehensive review of Campylobacter and poultry processing. Comprehensive Reviews in Food Science and Food Safety 3: 105-116.CrossRefGoogle ScholarPubMed
KHOURY, C.A. and MEINERSMANN, R.J. (1995) A genetic hybrid of the Campylobacter jejuni flaA gene with LT-B of Escherichia coli and assessment of the efficacy of the hybrid protein as an oral chicken vaccine. Avian Diseases 39: 812-820.CrossRefGoogle ScholarPubMed
KIM, J.W. and RAJAGOPAL, S.N. (2001) Antibacterial activities of Lactobacillus crispatus ATCC 33820 and L. gasseri ATCC 33323. The Journal of Microbiology 39: 146-148.Google Scholar
LAYTON, S.L., MORGAN, M.J., COLE, K., KWON, Y.M., DONOGHUE, D.J., HARGIS, B.M. and PUMFORD, N.R. (2010) Evaluation of Salmonella-vectored Campylobacter peptide epitopes for reduction of Campylobacter jejuni in broiler chickens. Clinical Vaccine and Immunology 18: 449-454.CrossRefGoogle ScholarPubMed
LIN, J. (2009) Novel approaches for Campylobacter control in poultry. Foodborne Pathogens and Disease 6: 755-765.CrossRefGoogle ScholarPubMed
LINE, J.E., SVETOCH, E.A., ERUSLANOV, B.V., PERELYGIN, V.V., MITSEVICH, E.V., MITSEVICH, I.P., LEVCHUK, V.P., SVETOCH, O.E., SEAL, B.S., SIRAGUSA, G.R. and STERN, N.J. (2008) Isolation and purification of enterocin E-760 with broad antimicrobial activity against gram-positive and gram-negative bacteria. Antimicrobial Agents and Chemotherapy 52: 1094-1100.CrossRefGoogle ScholarPubMed
MESSENS, W., HARTNETT, E., GELLYNCK, X., VIAENE, J., HALET, D., HERMAN, L. and GRIJSPEERDT, K. (2007) Quantitative risk assessment of human campylobacteriosis through the consumption of chicken meat in Belgium. Pages 167-168 in Proceedings of the XVIII European Symposium on the Quality of Poultry Meat, Praha, Czech Republic.Google Scholar
MESSENS, W., HERMAN, L., DE ZUTTER, L. and HEYNDRICKX, M. (2009) Multiple typing for the epidemiological study of contamination of broilers with thermotolerant Campylobacter. Veterinary Microbiology 138: 120-131.CrossRefGoogle ScholarPubMed
MOORE, J.E. (2001) Bacterial dormancy in Campylobacter: abstract theory or cause for concern? International Journal of Food Science & Technology 36: 593-600.CrossRefGoogle Scholar
MORISHITA, T.Y., AYE, P.P., HARR, B.S., COBB, C.W. and CLIFFORD, J.R. (1997) Evaluation of an avian specific probiotic to reduce the colonisation and shedding of Campylobacter jejuni in broilers. Avian Diseases 41: 850-855.CrossRefGoogle ScholarPubMed
NAHASHON, S.N., NAKAUE, H.S. and MIROSH, L.W. (1996) Nutrient retention and production parameters of Single Comb White Leghorn layers fed diets with varying crude protein levels and supplemented with direct-fed microbials. Animal Feed Science and Technology 61: 17-26.CrossRefGoogle Scholar
NÄTHER, G., ALTER, T., MARTIN, A. and ELLERBROEK, L. (2009) Analysis of risk factors for Campylobacter species infection in broiler flocks. Poultry Science 88: 1299-1305.CrossRefGoogle ScholarPubMed
NEIL, S.D., CAMPBELL, J.N. and GREENE, J.H. (1984) Campylobacter species in broiler chickens. Avian Pathology 13: 777-785.CrossRefGoogle Scholar
NEWELL, D.G. and FEARNLEY, C. (2003) Sources of Campylobacter colonisation in broiler chickens. Applied Environmental Microbiology 69: 4343-4351.CrossRefGoogle ScholarPubMed
NICHOLS, G.L. (2005) Fly transmission of Campylobacter. Emerging Infectious Disease 11: 361-364.CrossRefGoogle ScholarPubMed
NICHOLSON, F.A., GROVES, S.J. and CHAMBERS, B.J. (2005) Pathogen survival during livestock manure storage and following land application. Bioresource Technology 96: 135-143.CrossRefGoogle ScholarPubMed
NURMI, E. and RANTALA, M. (1973) New aspects of Salmonella infection in broiler production. Nature 241: 210-211.CrossRefGoogle ScholarPubMed
OPORTO, B., ESTEBAN, J.I., ADURIZ, G., JUSTE, R.A. and HURTADO, A. (2007) Prevalence and strain diversity of thermophilic campylobacters in cattle, sheep and swine farms. Journal of Applied Microbiology 103: 977-984.CrossRefGoogle ScholarPubMed
PATTERSON, J.A. and BURKHOLDER, K.M. (2003) Application of prebiotics and probiotics in poultry production. Poultry Science 82: 627-631.CrossRefGoogle ScholarPubMed
PRESCOTT, J.F. and GELMER, O.S. (1984) Intestinal carriage of Campylobacter jejuni and Salmonella by chicken flocks at slaughter. Canadian Journal of comparative Medicine 48: 329-331.Google ScholarPubMed
RAMABU, S.S., BOXALL, N.S., MADIE, P. and FENWICK, S.G. (2004) Some potential sources for transmission of Campylobacter jejuni to broiler chickens. Letters in Applied Microbiology 39: 252-256.CrossRefGoogle ScholarPubMed
REICH, F., ATANASSOVA, V., HAUNHORST, E. and KLEIN, G. (2008) The effects of Campylobacter numbers in caeca on the contamination of broiler carcasses with Campylobacter. International Journal of Food Microbiology 127: 116-120.CrossRefGoogle ScholarPubMed
RICE, B.E., ROLLINS, D.M., MALLINSON, E.T., CARR, L. and JOSEPH, S.W. (1997) Campylobacter jejuni in broiler chickens: Colonisation and humoral immunity following oral vaccination and experimental infection. Vaccine 15: 1922-1932.CrossRefGoogle ScholarPubMed
RIVOAL, K., RAGIMBEAU, C., SALVAT, G., COLIN, P. and ERMEL, G. (2005) Genomic diversity of Campylobacter coli and Campylobacter jejuni isolates recovered from free-range broilers farms and comparison with isolates of various origins. Applied Environmental Microbiology 71: 6216-6227.CrossRefGoogle ScholarPubMed
ROBERFROID, M.B., VANLOO, J.A.E. and GIBSON, G.R. (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. Journal of Nutrition 128: 11-19.CrossRefGoogle ScholarPubMed
ROSENQUIST, H., BOYSEN, L., GALLIANO, C., NORDENTOFT, S., ETHELBERG, S. and BORCK, B. (2009) Danish strategies to control Campylobacter in broilers and broiler meat: facts and effects. Epidemiology and Infection 137: 1742-1750.CrossRefGoogle ScholarPubMed
ROSENQUIST, H., SOMMER, H.M., NIELSEN, N.L. and CHRISTENSEN, B.B. (2006) The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter. International Journal of Food Microbiology 108: 226-232.CrossRefGoogle ScholarPubMed
ROSENQUIST, H., NIELSEN, N.L., SOMMER, H.M., NORRUNG, B. and CHRISTENSEN, B.B. (2003) Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology 83: 87-103.CrossRefGoogle ScholarPubMed
ROWE, M.T. and MADDEN, R.H. (2000) Campylobacter, in: ROBINSON, R.K., BATT, C.A. & PATEL, P.D. (Eds) Encyclopedia of Food Microbiology, pp. 335-352 (Academic Press, Washington, DC).Google Scholar
RUIZ-PALACIOS, G.M., ESCAMILLA, E. and TORRES, N. (1981) Experimental Campylobacter diarrhea in chickens. Infection and Immunity 34: 250-255.CrossRefGoogle ScholarPubMed
SAHIN, O., LUO, N.D., HUANG, S.X. and ZHANG, Q.J. (2003) Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonisation in young chickens. Applied Environmental Microbiology 69: 5372-5379.CrossRefGoogle ScholarPubMed
SALEHA, A.A. (2002) Isolation and characterization of Campylobacter jejuni from broiler chickens in Malaysia. International journal of Poultry Science 1:94-97.Google Scholar
SANTINI, C., BAFFONI, L., GAGGIA, F., GRANATA, M., GASBARRI, R., GIOIA, D.D. and BIAVATI, B. (2010) Characterization of probiotic strains: An application as feed additives in poultry against Campylobacter jejuni. International Journal of Food Microbiology 141: 98-108.CrossRefGoogle ScholarPubMed
SCHILLINGER, U. and LUCKE, F.-K. (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Applied Environmental Microbiology 8: 1901-1906.CrossRefGoogle Scholar
SCHOENI, J.L. and WONG, A.C. (1994) Inhibition of Campylobacter jejuni colonisation in chicks by defined competitive exclusion bacteria. Applied Environmental Microbiology 60: 1191-1197.CrossRefGoogle ScholarPubMed
SHANE, S.M. (2000) Campylobacter infection of commercial poultry. Revue Scientifique et Technique-Office International des Epizooties 19: 376-395.CrossRefGoogle ScholarPubMed
SHANKER, S., LEE, A. and SORRELL, T.C. (1986) Campylobacter jejuni in broilers: the role of vertical transmission. Journal of Hygiene 96: 153-159.CrossRefGoogle ScholarPubMed
SHANKER, S., LEE, A. and SORRELL, T.C. (1990) Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiology and Infection 104: 101-110.CrossRefGoogle ScholarPubMed
SKANSENG, B., KALDHUSDAL, M., MOEN, B., GJEVRE, A.-G., JOHANNESSEN, G.S., SEKELJA, M., TROSVIK, P. and RUDI, K. (2010) Prevention of intestinal Campylobacter jejuni colonisation in broilers by combinations of in-feed organic acids. Journal of Applied Microbiology 109: 1265-1273.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
SOERJADI-LIEM, A.S., SNOEYENBOS, G.H. and WEINACK, O.M. (1984) Comparative studies on competitive exclusion of three isolates of Campylobacter fetus subsp. jejuni in chickens by native gut microflora. Avian Diseases 28: 139-146.CrossRefGoogle ScholarPubMed
SOLIS DE LOS SANTOS, F.S., HUME, M., VENKITANARAYANAN, K., DONOGHUE, A.M., HANNING, I., SLAVIK, M.F., AGUIAR, V.F., METCALF, J.H., REYES-HERRERA, I., BLORE, P.J. and DONOGHUE, D.J. (2010) Caprylic acid reduces enteric Campylobacter colonisation in market-aged broiler chickens but does not appear to alter caecal microbial populations. Journal of Food Protection 73: 251-257.CrossRefGoogle Scholar
SOLIS DE LOS SANTOS, F., DONOGHUE, A.M., VENKITANARAYANAN, K., METCALF, J.H., REYES-HERRERA, I., DIRAIN, M.L., AGUIAR, V.F., BLORE, P.J. and DONOGHUE, D.J. (2009) The natural feed additive caprylic acid decreases Campylobacter jejuni colonisation in market-aged broiler chickens. Poultry Science 88: 61-64.CrossRefGoogle ScholarPubMed
SOLIS DE LOS SANTOS, F.S., DONOGHUE, A.M., VENKITANARAYANAN, K., DIRAIN, M.L., REYES-HERRERA, I., BLORE, P.J. and DONOGHUE, D.J. (2008) Caprylic acid supplemented in feed reduces enteric Campylobacter jejuni colonisation in ten-day-old broiler chickens. Poultry Science 87: 800-804.CrossRefGoogle ScholarPubMed
STANLEY, K. and JONES, K. (2003) Cattle and sheep farms as reservoirs of Campylobacter. Journal of Applied Microbiology 94: 104-113.CrossRefGoogle ScholarPubMed
STERN, N.J., BANNOV, V.A., SVETOCH, E.A., MITSEVICH, E.V., MITSEVICH, I.P., VOLOZHANTSEV, N.V., GUSEV, V.V. and PERELYGIN, V.V. (2004) Distribution and characterization of Campylobacter spp. from Russian poultry. Journal of Food Protection 67: 239-245.CrossRefGoogle ScholarPubMed
STERN, N.J., MEINERSMANN, R.J., COX, N.A., BAILEY, J.S. and BLANKENSHIP, L.C. (1990b) Influence of host lineage on caecal colonisation by Campylobacter jejuni in chickens. Avian Diseases 34: 602-606.CrossRefGoogle ScholarPubMed
STERN, N.J., MEINERSMANN, R.J. and DICKERSON, H.W. (1990a) Influence of antibody treatment of Campylobacter jejuni on the dose required to colonise chicks. Avian Diseases 34: 595-601.CrossRefGoogle ScholarPubMed
STERN, N.J., ROBACH, M.C., COX, N.A. and MUSGROVE, M.T. (2002) Effect of drinking water chlorination on Campylobacter spp. colonisation of broilers. Avian Diseases 46: 401-404.CrossRefGoogle ScholarPubMed
SUZUKI, H. and YAMAMOTO, S. (2009) Campylobacter contamination in retail poultry meats and by-products in Japan: a literature survey. Food Control 20: 531-537.CrossRefGoogle Scholar
SVETOCH, E.A. and STERN, N.J. (2010) Bacteriocins to control Campylobacter spp. in poultry —a review. Poultry Science 89: 1763-1768.CrossRefGoogle ScholarPubMed
SWAGGERTY, C.L., PEVZNER, I.Y., HE, H., GENOVESE, K.J., NISBET, D.J., KAISER, P. and KOGUT, M.H. (2009) Selection of broilers with improved innate immune responsiveness to reduce on-farm infection by foodborne pathogens. Foodborne Pathogens and Diseases 6: 777-783.CrossRefGoogle ScholarPubMed
THORMAR, H., HILMARSSON, H. and BERGSSON, G. (2006) Stable concentrated emulsions of the 1- monoglyceride of capric acid (monocaprin) with microbicidal activities against the food-borne bacteria Campylobacter jejuni, Salmonella spp., and Escherichia coli. Applied and Environmental Microbiology 75: 522-526.CrossRefGoogle Scholar
TSUBOKURA, K., BERNDTSON, E., BOGSTEDT, A., KAIJSER, B., KIM, M., OZEKI, M. and HAMMARSTROM, L. (1997) Oral administration of antibodies as prophylaxis and therapy in Campylobacter jejuni-infected chickens. Clinical Experimental Immunology 108: 451-455.CrossRefGoogle ScholarPubMed
VANDAMME, P. (2000) Taxonomy of the family Campylobacteraceae, in: NACHAMKIN, I. & BLASER, M.J. (Eds) Campylobacter. 2nd Edition, pp. 3-10 (ASM Press, Washington, DC).Google Scholar
VAN DE GIESSEN, A.W., BLOEMBERG, B.P., RITMEESTER, W.S. and TILBURG, J.J. (1996) Epidemiological study on risk factors and risk reducing measures for Campylobacter infections in Dutch broiler flocks. Epidemiology and Infection 117: 245-250.CrossRefGoogle ScholarPubMed
VAN DE GIESSEN, A.W., TILBURG, J.J., RITMEESTER, W.S. and VAN DER PLAS, J. (1998) Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiology and Infection 121: 57-66.CrossRefGoogle ScholarPubMed
VAN DER WIELEN, P.W. (2002) Role of volatile fatty acids in competitive exclusion of Salmonella enteritidis. Thesis: Faculty of Veterinary Medicine, Utrecht, The Netherlands.Google Scholar
VAN DER ZEE, H., WIT B., and VOLLEMA, A.R. (2005) Survey pathogenen en bacteriële resistentie in kipproducten uit biologische teelt, Jaar 2004. Voedsel en Waren Autoriteit/Keuringsdienst van Waren Oost, p. 10.Google Scholar
VAN DEUN, K., HAESEBROUCK, F., VAN IMMERSEEL, F., DUCATELLE, R. and PASMANS, F. (2008) Short-chain fatty acids and l-lactate as feed additives to control Campylobacter jejuni infections in broilers. Avian Pathology 37: 379-383.CrossRefGoogle ScholarPubMed
VAN GERWE, T., BOUMA, A., KLINKENBERG, D., WAGENAAR, J.A., JACOBS-REITSMA, W.F. and STEGEMAN, A. (2010) Medium chain fatty acid feed supplementation reduces the probability of Campylobacter jejuni colonisation in broilers. Veterinary Microbiology 143: 314-318.CrossRefGoogle ScholarPubMed
VAN GERWE, T., MIFLIN, J.K., TEMPLETONBOUMA, J.MA., WAGENAAR, J.A., JACOBS-REITSMA, W.F., STEGEMAN, A. and KLINKENBERG, D. (2009) Quantifying transmission of Campylobacter jejuni in commercial broiler flocks. Applied Environmental Microbiology 75: 625-628.CrossRefGoogle ScholarPubMed
VAN GERWE, T.J.W.M., BOUMA, A., JACOBS-REITSMA, W.F., VAN DEN BROEK, J., KLINKENBERG, D., STEGEMAN, J.A. and HEESTERBEEK, J.A.P. (2005) Quantifying transmission of Campylobacter spp. among broilers. Applied Environmental Microbiology 71: 5765-5770.CrossRefGoogle ScholarPubMed
WAGENAAR, J.A., VAN BERGEN, M.A.P., MUELLER, M.A., WASSENAAR, T.M. and CARLTON, R.A. (2005) Phage therapy reduces Campylobacter jejuni colonisation in broilers. Veterinary Microbiology 109: 275-283.CrossRefGoogle ScholarPubMed
WELKOS, S.L. (1984) Experimental gastroenteritis in newly-hatched chicks injected with Campylobacter jejuni. Journal of Medical Microbiology 18: 233-248.CrossRefGoogle Scholar
WESTRELL, T., CIAMPA, N., BOELAERT, F., HELWIGH, B., KORSGAARD, H., CHRÍEL, M., AMMON, A. and MÄKELÄ, P. (2009) Zoonotic infections in Europe in 2007: a summary of the EFSA. Eurosurveillance 14: 1-3.CrossRefGoogle ScholarPubMed
WIDDERS, P.R., THOMAS, L.M., LONG, K.A., TOKHI, M.A., PANACCIO, M. and APOS, E. (1998) The specificity of antibody in chickens immunised to reduce intestinal colonisation with Campylobacter jejuni. Veterinary Microbiology 64: 39-50.CrossRefGoogle ScholarPubMed
WILKIE, D.C. (2006) Non-antibiotic approaches to control pathogens in the gastrointestinal tract of the broiler chicken. Thesis: University of Saskatchewan, Saskatoon (Canada).Google Scholar
WILLIS, W.L. and REID, L. (2008) Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni presence. Poultry Science 87: 606-611.CrossRefGoogle ScholarPubMed
WINGSTRAND, A., NEIMANN, J., ENGBERG, J. NIELSEN, E.M., GERNER-SMIDT, P., , WEGENER, H.C. and MOLBAK, K. (2006) Fresh chicken as main risk factor for campylobacteriosis, Denmark. Emerging Infectious Diseases 12: 280-284.CrossRefGoogle ScholarPubMed
WYSZYNSKA, A., RACZKO, A., LIS, M. and JAGUSZTYN-KRYNICKA, E.K. (2004) Oral immunisation of chickens with avirulent Salmonella vaccine strain carrying C. jejuni 72D92 cjaA gene elicits specific humoral immune response associated with protection against challenge with wild-type Campylobacter. Vaccine 22: 1379-1389.CrossRefGoogle ScholarPubMed
XU, Z.R., HU, C.H., XIA, M.S., ZHAN, X.A. and WANG, M.Q. (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82: 1083-1036.CrossRefGoogle ScholarPubMed
YOUNG, K.T., DAVIS, L.M. and DIRITA, V.J. (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nature Reviews Microbiology 5: 665-679.CrossRefGoogle ScholarPubMed