Abstract
It is estimated that there are approximately nine million cases of human campylobacteriosis per year in the EU27. The disease burden of campylobacteriosis and its sequelae is 0.35 million disability‐adjusted life years (DALYs) per year and total annual costs are 2.4 billion €. Broiler meat may account for 20% to 30% of these, while 50% to 80% may be attributed to the chicken reservoir as a whole (broilers as well as laying hens). The public health benefits of controlling Campylobacter in primary broiler production are expected to be greater than control later in the chain as the bacteria may also spread from farms to humans by other pathways than broiler meat. Strict implementation of biosecurity in primary production and GMP/HACCP during slaughter may reduce colonization of broilers with Campylobacter, and contamination of carcasses. The effects cannot be quantified because they depend on many interrelated local factors. In addition, the use of fly screens, restriction of slaughter age, or discontinued thinning may further reduce consumer risks but have not yet been tested widely. After slaughter, a 100% risk reduction can be reached by irradiation or cooking of broiler meat on an industrial scale. More than 90% risk reduction can be obtained by freezing carcasses for 2–3 weeks. A 50–90% risk reduction can be achieved by freezing for 2–3 days, hot water or chemical carcass decontamination. Achieving a target of 25% or 5% BFP in all other MS is estimated to result in 50% and 90% reduction of public health risk, respectively. A public health risk reduction > 50% or > 90% could be achieved if all batches would comply with microbiological criteria with a critical limit of 1000 or 500 CFU/gram of neck and breast skin, respectively, while 15% and 45% of all tested batches would not comply with these criteria.
Keywords: Broiler meat, Campylobacter, campylobacteriosis, control, microbiological criteria, QMRA, targets
EFSA Panel on Biological Hazards (BIOHAZ) ; Scientific Opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA Journal 2011;9(4):2105. [141 pp.]. doi: 10.2903/j.efsa.2011.2105.
Panel members: Olivier Andreoletti, Herbert Budka, Sava Buncic, John D Collins, John Griffin, Tine Hald, Arie Havelaar, James Hope, Günter Klein, James McLauchlin, Christine Müller‐Graf, Christophe Nguyen‐The, Birgit Noerrung, Luisa Peixe, Miguel Prieto Maradona, Antonia Ricci, John Sofos, John Threlfall, Ivar Vågsholm and Emmanuel Vanopdenbosch
Correspondence: biohaz@efsa.europa.eu
Acknowledgement: The Panel wishes to thank the members of the Working Group on Campylobacter on broiler meat: control options and performance objectives and/or targets for the preparatory work on this scientific opinion: Paolo Calistri, Pierre Colin, Janet Corry, Arie Havelaar, Merete Hofshagen, Günter Klein, Maarten Nauta, Diane Newell, Hanne Rosenquist, Moez Sanaa, John Sofos, Mieke Uyttendaele and Jaap Wagenaar, and EFSA staff Michaela Hempen, Pietro Stella, Winy Messens and Pablo Romero Barrios for the support provided to this EFSA scientific opinion.
Adoption date: 10 March 2011
Published date: 7 April 2011
Question number: EFSA‐Q‐2009‐00233
On request from: European Commission
References
- Adkin A, Hartnett E, Jordan L, Newell D and Davison H, 2006. Use of a systematic review to assist the development of Campylobacter control strategies in broilers. J Appl Microbiol, 100, 306–15. [DOI] [PubMed] [Google Scholar]
- Allen VM, Bull SA, Corry JEL, Domingue G, Jorgensen F, Frost JA, Whyte R, Gonzalez A, Elviss N and Humphrey TJ, 2007a. Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation. International Journal of Food Microbiology, 113, 54–61. [DOI] [PubMed] [Google Scholar]
- Allen VM, Burton CH, Wilkinson DJ, Whyte RT, Harris JA, Howell M and Tinker DB, 2008a. Evaluation of the performance of different cleaning treatments in reducing microbial contamination of poultry transport crates. Br Poult Sci, 49, 233–40. [DOI] [PubMed] [Google Scholar]
- Allen VM, Ridley A, Harris JA, Morris VK, Weaver H, Emery J, Sharma M, Sparks N and Edge S, 2007b. Sources and spread of Campylobacter spp. during partial depopulation of broiler chicken flocks. Zoonoses and Public Health, 54, 136–36. [DOI] [PubMed] [Google Scholar]
- Allen VM, Tinker DB, Hinton MH and Wathes CM, 2003. Dispersal of micro‐organisms in commercial defeathering systems. British Poultry Science, 44, 53–59. [DOI] [PubMed] [Google Scholar]
- Allen VM, Weaver H, Ridley AM, Harris JA, Sharma M, Emery J, Sparks N, Lewis M and Edge S, 2008b. Sources and spread of thermophilic Campylobacter spp. during partial depopulation of broiler chicken flocks. J Food Prot, 71, 264–70. [DOI] [PubMed] [Google Scholar]
- Allen VM, Whyte RT, Burton CH, Harris JA, Lovell RDL, Atterbury RJ and Tinker DB, 2008c. Effect of ultrasonic treatment during cleaning on the microbiological condition of poultry transport crates. British Poultry Science, 49, 423–28. [DOI] [PubMed] [Google Scholar]
- Anonymous 2009. Georgia's traditional industries program for food processing. Annual report. www.foodpac.gatech.edu/pdfs/FoodPAC_2009_Annual.pdf (accessed 14/02/2011).
- Arnold JW and Silvers S, 2000. Comparison of poultry processing equipment surfaces for susceptibility to bacterial attachment and biofilm formation. Poultry Science, 79, 1215–21. [DOI] [PubMed] [Google Scholar]
- Arsenault J, Letellier A, Quessy S and Boulianne M, 2007. Prevalence and risk factors for Salmonella and Campylobacter spp. carcass contamination in broiler chickens slaughtered in Quebec, Canada. J Food Prot, 70, 1820–8. [DOI] [PubMed] [Google Scholar]
- Avrain L, Allain L, Vernozy‐Rozand C and Kempf I, 2003. Disinfectant susceptibility testing of avian and swine Campylobacter isolates by a filtration method. Vet Microbiol, 96, 35–40. [DOI] [PubMed] [Google Scholar]
- Axelsson‐Olsson D, Waldenstrom J, Broman T, Olsen B and Holmberg M, 2005. Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni . Appl Environ Microbiol, 71, 987–92. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ayling RD, Woodward MJ, Evans S and Newell DG, 1996. Restriction fragment length polymorphism of polymerase chain reaction products applied to the differentiation of poultry Campylobacter for epidemiological investigations. Res Vet Sci, 60, 168–72. [DOI] [PubMed] [Google Scholar]
- Bailey JS, Stern NJ, Fedorka‐Cray P, Craven SE, Cox NA, Cosby DE, Ladely S and Musgrove MT, 2001. Sources and movement of Salmonella through integrated poultry operations: A multistate epidemiological investigation. Journal of Food Protection, 64, 1690–97. [DOI] [PubMed] [Google Scholar]
- Bare J, Sabbe K, Huws S, Vercauteren D, Braeckmans K, van Gremberghe I, Favoreel H and Houf K, 2010. Influence of temperature, oxygen and bacterial strain identity on the association of Campylobacter jejuni with Acanthamoeba castellanii . Fems Microbiology Ecology, 74, 371–81. [DOI] [PubMed] [Google Scholar]
- Bashor MP, Curtis PA, Keener KM, Sheldon BW, Kathariou S and Osborne JA, 2004. Effects of carcass washers on Campylobacter contamination in large broiler processing plants. Poult Sci, 83, 1232–9. [DOI] [PubMed] [Google Scholar]
- Bates C, Hiett KL and Stern NJ, 2004. Relationship of Campylobacter isolated from poultry and from darkling beetles in New Zealand. Avian Diseases, 48, 138–47. [DOI] [PubMed] [Google Scholar]
- Bauermeister LJ, Bowers JW, Townsend JC and McKee SR, 2008a. The microbial and quality properties of poultry carcasses treated with peracetic acid as an antimicrobial treatment. Poult Sci, 87, 2390–8. [DOI] [PubMed] [Google Scholar]
- Bauermeister LJ, Bowers JW, Townsend JC and McKee SR, 2008b. Validating the efficacy of peracetic acid mixture as an antimicrobial in poultry chillers. J Food Prot, 71, 1119–22. [DOI] [PubMed] [Google Scholar]
- Bayliss PA and Hinton MH, 1990. Transportation of broilers with special reference to mortality‐rates. Applied Animal Behaviour Science, 28, 93–118. [Google Scholar]
- Berg JD, Roberts PV and Matin A, 1986. Effect of chlorine dioxide on selected membrane functions of Escherichia coli . Journal of Applied Bacteriology, 60, 213–20. [DOI] [PubMed] [Google Scholar]
- Bergsma NJ, Fischer ARH, Van Asselt ED, Zwietering MH and De Jong AEI, 2007. Consumer food preparation and its implication for survival of Campylobacter jejuni on chicken. British Food Journal, 109, 548–61. [Google Scholar]
- Berndtson E, Danielsson‐Tham ML and Engvall A, 1996. Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. Int J Food Microbiol, 32, 35–47. [DOI] [PubMed] [Google Scholar]
- Berrang ME and Bailey JS, 2009. On‐line brush and spray washers to lower numbers of Campylobacter and Escherichia coli and presence of Salmonella on broiler carcasses during processing. Journal of Applied Poultry Research, 18, 74–78. [Google Scholar]
- Berrang ME, Bailey JS, Altekruse SF, Patel B, Shaw WK, Jr. , Meinersmann RJ and Fedorka‐Cray PJ, 2007. Prevalence and numbers of Campylobacter on broiler carcasses collected at rehang and postchill in 20 US Processing plants. J Food Prot, 70, 1556–60. [DOI] [PubMed] [Google Scholar]
- Berrang ME, Buhr RJ, Cason JA and Dickens JA, 2001. Broiler carcass contamination with Campylobacter from feces during defeathering. J Food Prot, 64, 2063–6. [DOI] [PubMed] [Google Scholar]
- Berrang ME, Dickens JA and Musgrove MT, 2000. Effects of hot water application after defeathering on the levels of Campylobacter, coliform bacteria, and Escherichia coli on broiler carcasses. Poult Sci, 79, 1689–93. [DOI] [PubMed] [Google Scholar]
- Berrang ME and Northcutt JK, 2005. Use of water spray and extended drying time to lower bacterial numbers on soiled flooring from broiler transport coops. Poult Sci, 84, 1797–801. [DOI] [PubMed] [Google Scholar]
- Berrang ME, Northcutt JK and Cason JA, 2004a. Recovery of Campylobacter from broiler feces during extended storage of transport cages. Poult Sci, 83, 1213–7. [DOI] [PubMed] [Google Scholar]
- Berrang ME, Northcutt JK, Fletcher DL and Cox NA, 2003. Role of dump cage fecal contamination in the transfer of Campylobacter to carcasses of previously negative broilers. Journal of Applied Poultry Research, 12, 190–95. [Google Scholar]
- Berrang ME, Smith DP, Windham WR and Feldner PW, 2004b. Effect of intestinal content contamination on broiler carcass Campylobacter counts. J Food Prot, 67, 235–8. [DOI] [PubMed] [Google Scholar]
- Bilgili SF, 2002. Slaughter quality as influenced by feed withdrawal. Worlds Poultry Science Journal, 58, 123–30. [Google Scholar]
- Bilgili SF and Hess JB, 1997. Tensile strength of broiler intestines as influenced by age and feed withdrawal. Journal of Applied Poultry Research, 6, 279–83. [Google Scholar]
- Black RE, Levine MM, Clements ML, Hughes TP and Blaser MJ, 1988. Experimental Campylobacter jejuni infection in humans. J Infect Dis, 157, 472–9. [DOI] [PubMed] [Google Scholar]
- Blaser MJ, Smith PF, Wang WL and Hoff JC, 1986. Inactivation of Campylobacter jejuni by chlorine and monochloramine. Appl Environ Microbiol, 51, 307–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bolder NM, 2007. Microbial challenges of poultry meat production. Worlds Poultry Science Journal, 63, 401–11. [Google Scholar]
- Booth IR, 1985. Regulation of cytoplasmic ph in bacteria. Microbiological Reviews, 49, 359–78. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouwknegt M, van de Giessen AW, Dam‐Deisz WD, Havelaar AH, Nagelkerke NJ and Henken AM, 2004. Risk factors for the presence of Campylobacter spp. in Dutch broiler flocks. Prev Vet Med, 62, 35–49. [DOI] [PubMed] [Google Scholar]
- Boyd Y, Herbert EG, Marston KL, Jones MA and Barrow PA, 2005. Host genes affect intestinal colonisation of newly hatched chickens by Campylobacter jejuni . Immunogenetics, 57, 248–53. [DOI] [PubMed] [Google Scholar]
- 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. [DOI] [PubMed] [Google Scholar]
- Brynestad S, Braute L, Luber P and Bartelt E, 2008. Quantitative microbiological risk assessment of campylobacteriosis cases in the German population due to consumption of chicken prepared in home. International Journal of Risk Assessment and Risk management, 8, 194–213. [Google Scholar]
- Buhr RJ, Berrang ME and Cason JA, 2003. Bacterial recovery from breast skin of genetically feathered and featherless broiler carcasses immediately following scalding and picking. Poult Sci, 82, 1641–7. [DOI] [PubMed] [Google Scholar]
- Bull SA, Allen VM, Domingue G, Jorgensen F, Frost JA, Ure R, Whyte R, Tinker D, Corry JE, Gillard‐King J and Humphrey TJ, 2006. Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol, 72, 645–52. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bull SA, Thomas A, Humphrey T, Ellis‐Iversen J, Cook AJ, Lovell R and Jorgensen F, 2008. Flock health indicators and Campylobacter spp. in commercial housed broilers reared in great britain. Appl Environ Microbiol, 74, 5408–13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Byrd J, Bailey RH, Wills R and Nisbet D, 2007. Recovery of Campylobacter from commercial broiler hatchery trayliners. Poult Sci, 86, 26–9. [DOI] [PubMed] [Google Scholar]
- Byrd JA, Corrier DE, Hume ME, Bailey RH, Stanker LH and Hargis BM, 1998. Effect of feed withdrawal on Campylobacter in the crops of market‐age broiler chickens. Avian Dis, 42, 802–6. [PubMed] [Google Scholar]
- Byrd JA, Hargis BM, Caldwell DJ, Bailey RH, Herron KL, McReynolds JL, Brewer RL, Anderson RC, Bischoff KM, Callaway TR and Kubena LF, 2001. Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poult Sci, 80, 278–83. [DOI] [PubMed] [Google Scholar]
- Callicott KA, Friethriksdottir V, Reiersen J, Lowman R, Bisaillon JR, Gunnarsson E, Berndtson E, Hiett KL, Needleman DS and Stern NJ, 2006. Lack of evidence for vertical transmission of Campylobacter spp. in chickens. Appl Environ Microbiol, 72, 5794–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Callicott KA, Stern NJ, Hiett KL and Campy Ice C, 2005. Isolation of DNA for PCR assays from noncultivable Campylobacter jejuni isolates. Poultry Science, 84, 1530–32. [DOI] [PubMed] [Google Scholar]
- Camarda A, Newell DG, Nasti R and Di Modugnoa G, 2000. Genotyping Campylobacter jejuni strains isolated from the gut and oviduct of laying hens. Avian Dis, 44, 907–12. [PubMed] [Google Scholar]
- Cardinale E, Tall F, Gueye EF, Cisse M and Salvat G, 2004. Risk factors for Campylobacter spp. infection in senegalese broiler‐chicken flocks. Prev Vet Med, 64, 15–25. [DOI] [PubMed] [Google Scholar]
- Cawthraw S, Ayling R, Nuijten P, Wassenaar T and Newell DG, 1994. Isotype, specificity, and kinetics of systemic and mucosal antibodies to Campylobacter jejuni antigens, including flagellin, during experimental oral infections of chickens. Avian Dis, 38, 341–9. [PubMed] [Google Scholar]
- Cawthraw S, Gorringe C and Newell D, 1998. Prior infection, but not a killed vaccine, reduces colonization of chickens by Campylobacter jejuni. Cape Town, South Africa. 364–72. [Google Scholar]
- Cawthraw SA and Newell DG, 2010. Investigation of the presence and protective effects of maternal antibodies against Campylobacter jejuni in chickens. Avian Diseases, 54, 86–93. [DOI] [PubMed] [Google Scholar]
- Chantarapanont W, Berrang ME and Frank JF, 2004. Direct microscopic observation of viability of Campylobacter jejuni on chicken skin treated with selected chemical sanitizing agents. J Food Prot, 67, 1146–52. [DOI] [PubMed] [Google Scholar]
- Chaveerach P, Keuzenkamp DA, Lipman LJA and Van Knapen F, 2004. 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, 330–34. [DOI] [PubMed] [Google Scholar]
- Chaveerach P, Keuzenkamp DA, Urlings HA, Lipman LJ and van Knapen F, 2002. In vitro study on the effect of organic acids on Campylobacter jejuni/coli populations in mixtures of water and feed. Poult Sci, 81, 621–8. [DOI] [PubMed] [Google Scholar]
- Chaveerach P, ter Huurne AA, Lipman LJ and van Knapen F, 2003. Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl Environ Microbiol, 69, 711–4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen HC and Stern NJ, 2001. Competitive exclusion of heterologous Campylobacter spp. in chicks. Applied and Environmental Microbiology, 67, 848–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chun HH, Kim JY, Lee BD, Yu DJ and Song KB, 2010. Effect of uv‐c irradiation on the inactivation of inoculated pathogens and quality of chicken breasts during storage. Food Control, 21, 276–80. [Google Scholar]
- Cogan TA, Thomas AO, Rees LE, Taylor AH, Jepson MA, Williams PH, Ketley J and Humphrey TJ, 2007. Norepinephrine increases the pathogenic potential of Campylobacter jejuni . Gut, 56, 1060–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Colles FM, Jones TA, McCarthy ND, Sheppard SK, Cody AJ, Dingle KE, Dawkins MS and Maiden MC, 2008. Campylobacter infection of broiler chickens in a free‐range environment. Environ Microbiol, 10, 2042–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Connerton PL and Connerton IF, 2006. Campylobacter and their bacteriophage in poultry. Avian gut function in health and disease, 311–21.
- Connerton PL, Loc Carrillo CM, Swift C, Dillon E, Scott A, Rees CE, Dodd CE, Frost J and Connerton IF, 2004. Longitudinal study of Campylobacter jejuni bacteriophages and their hosts from broiler chickens. Appl Environ Microbiol, 70, 3877–83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corrier DE, Byrd JA, Hargis BM, Hume ME, Bailey RH and Stanker LH, 1999. Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal. Poultry Science, 78, 45–49. [DOI] [PubMed] [Google Scholar]
- Corry J, Purnell G, James C and James S (Food Standards Agency) , 2006. Commercial trials to investigate the feasibility under commercial conditions of decontaminating chicken carcasses using hot water immersion at 80oC for 20 s. FSA Project no. MO 1019: Physical methods readily adapted to existing commercial lines for reducing pathogens, particularly Campylobacter, on raw poultry. Bristol. www.ukmeat.org/pdf/ExtensionProject2Report.pdf (accessed 02/03/2011).
- Corry J, Purnell G, James C, Pinho R, Hedges A, Jorgensen F, James SJ and Howell M, 2008. Evaluation of chemicals for the inactivation of naturally occurring thermophilic Campylobacter spp. On poultry carcasses. Food Microbiology, Aberdeen, 1–4 September 2008,
- Corry JE, James C, James SJ and Hinton M, 1995. Salmonella, Campylobacter and Escherichia coli O157:H7 decontamination techniques for the future. Int J Food Microbiol, 28, 187–96. [DOI] [PubMed] [Google Scholar]
- Corry JE, James C, O'Neill D, Yaman H and Hinton M, 2003. Physical methods, readily adapted to existing commercial processing plants, for reducing numbers of Campylobacter, on raw poultry. Int J Med Microbiol, 293, S32. [Google Scholar]
- Corry JE and Mead DJ, 1996. Decontamination of meat. In: Microbial control in the meat industry. Vol. 3. Hinton, MH , Mead, DJ , Rowlings, C (eds.). University of Bristol Press, Bristol. ISBN 0862924448. [Google Scholar]
- Corry JEL, Allen VM, Hudson WR, Breslin MF and Davies RH, 2002. Sources of Salmonella on broiler carcasses during transportation and processing: Modes of contamination and methods of control. Journal of Applied Microbiology, 92, 424–32. [DOI] [PubMed] [Google Scholar]
- Corry JEL and Atabay HI, 2001. Poultry as a source of Campylobacter and related organisms. Journal of Applied Microbiology, 90, 96S–114S. [DOI] [PubMed] [Google Scholar]
- Corry JEL, James SJ, Purnell G, Barbedo‐Pinto CS, Chochois Y, Howell M and James C, 2007. Surface pasteurisation of chicken carcasses using hot water. Journal of Food Engineering, 79, 913–19. [Google Scholar]
- Cosansu S and Ayhan K, 2010. Effects of lactic and acetic acid treatments on Campylobacter jejuni inoculated onto chicken leg and breast meat during storage at 4°C and −18°C. Journal of Food Processing and Preservation, 34, 34 (Suppl. 1) 98–113. [Google Scholar]
- Cox JM and Pavic A, 2010. Advances in enteropathogen control in poultry production. Journal of Applied Microbiology, 108, 745–55. [DOI] [PubMed] [Google Scholar]
- de Boer P, Wagenaar J, Achterberg R, van Putten J and Duim B, 2001. Generation of Campylobacter jejuni diversity in vivo. [DOI] [PubMed]
- de los Santos FS, Donoghue AM, Venkitanarayanan K, Metcalf JH, Reyes‐Herrera I, Dirain ML, Aguiar VF, Blore PJ and Donoghue DJ, 2009. The natural feed additive caprylic acid decreases Campylobacter jejuni colonization in market‐aged broiler chickens. Poult Sci, 88, 61–4. [DOI] [PubMed] [Google Scholar]
- de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Bartelds AI and van Duynhoven YT, 2001. Gastroenteritis in sentinel general practices, the Netherlands. Emerg Infect Dis, 7, 82–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Zoete MR, van Putten JP and Wagenaar JA, 2007. Vaccination of chickens against Campylobacter . Vaccine, 25, 5548–57. [DOI] [PubMed] [Google Scholar]
- Debruyne L, On SLW, De Brandt E and Vandamme P, 2009. Novel Campylobacter lari‐like bacteria from humans and molluscs: Description of Campylobacter peloridis sp nov., Campylobacter lari subsp concheus subsp nov and Campylobacter lari subsp lari subsp nov . International Journal of Systematic and Evolutionary Microbiology, 59, 1126–32. [DOI] [PubMed] [Google Scholar]
- Delezie E, Zoons J, Buyse J and Decuypere E, 2006. Influence of whole wheat inclusion on optimal feed withdrawal duration. British Poultry Science, 47, 572–75. [DOI] [PubMed] [Google Scholar]
- Dincer AH and Baysal T, 2004. Decontamination techniques of pathogen bacteria in meat and poultry. Critical Reviews in Microbiology, 30, 197–204. [DOI] [PubMed] [Google Scholar]
- Edson DC, Empson S and Massey LD, 2009. Pathogen detection in food microbiology laboratories: An analysis of qualitative proficiency test data, 1999–2007. Journal of Food Safety, 29, 521–30. [Google Scholar]
- EFSA , 2005. The community summary report on trends and sources of zoonoses, zoonotic agents and antimicrobial resistance in the European Union in 2004. The EFSA Journal, 310. ISBN 92–9199‐016‐7.
- EFSA , 2006. Evaluation of the efficacy of the lactic acid on poultry carcasses. The EFSA Journal, 346, 1–6. [Google Scholar]
- EFSA , 2007. Opinion of the scientific panel on biological hazards (BIOHAZ) on microbiological criteria and targets based on risk analysis. The EFSA Journal, 462, 1–29. [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 Journal 2010; 8(03):1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- EFSA , 2010b. 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 B: Analysis of factors associated with Campylobacter colonisation of broiler batches and with Campylobacter contamination of broiler carcasses; and investigation of the culture method diagnostic characteristics used to analyse broiler carcass samples. The EFSA Journal, 8(8):1522. [Google Scholar]
- EFSA , 2010c. The community summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in the European Union in 2008. The EFSA Journal, 2010, 8(7):1658. [DOI] [PMC free article] [PubMed] [Google Scholar]
- EFSA , 2010d. Scientific opinion on quantification of the risk posed by broiler meat to human campylobaceriosis in the EU. The EFSA Journal, 8(1):1437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- EFSA , 2011. Scientific opinion on irradiation of food (efficacy and microbiological safety). The EFSA Journal, 9(4), 2103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- EFSA/ECDC , 2011. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2009. The EFSA Journal, 9(3):2090. [Google Scholar]
- Ekdahl K and Andersson Y, 2004. Regional risks and seasonality in travel‐associated campylobacteriosis. BMC Infect Dis, 4, 54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ekdahl K and Giesecke J, 2004. Travellers returning to Sweden as sentinels for comparative disease incidence in other european countries, Campylobacter and giardia infection as examples. Euro Surveill, 9, 6–9. [PubMed] [Google Scholar]
- El‐Shibiny A, Connerton PL and Connerton IF, 2005. Enumeration and diversity of Campylobacter and bacteriophages isolated during the rearing cycles of free‐range and organic chickens. Appl Environ Microbiol, 71, 1259–66. [DOI] [PMC free article] [PubMed] [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, 733–40. [DOI] [PubMed] [Google Scholar]
- Ellerbroek L, Lienau JA, Alter T and Schlichting D, 2007. Effectiveness of different chemical decontamination methods on the Campylobacter load of poultry carcasses. Zoonoses and Public Health, 54, 128–28. [Google Scholar]
- Evans SJ, 1992. Introduction and spread of thermophilic Campylobacter in broiler flocks. Vet Rec, 131, 574–6. [PubMed] [Google Scholar]
- Evans SJ and Sayers AR, 2000. A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Prev Vet Med, 46, 209–23. [DOI] [PubMed] [Google Scholar]
- Fabrizio KA, Sharma RR, Demirci A and Cutter CN, 2002. Comparison of electrolyzed oxidizing water with various antimicrobial interventions to reduce Salmonella species on poultry. Poultry Science, 81, 1598–605. [DOI] [PubMed] [Google Scholar]
- FAO/WHO , 2003. Hazard characterization for pathogens in food and water. Guidelines. Microbiological risk assessment series 3, Rome/Geneva. www.fao.org/docrep/006/y4666e/y4666e00.htm (accessed 18/03/2011).
- FAO/WHO 2008. Benefits and risks of the use of chlorine‐containing disinfectants in food production and food processing: Report of a joint fao/who expert meeting, 27–30 May 2008, Ann Arbor, MI, USA, 1–288. www.fao.org/ag/agn/agns/files/Active%20Chlorine%20Report%20Version%20Final%20December%202009.pdf (accessed 16/12/2010).
- FAO/WHO 2009a. Joint FAO/WHO food standards programme CODEX Committee on food hygiene. Proposed draft guidelines for control of Campylobacter and Salmonella spp. in chicken meat (N08‐2007), Coronado, USA. [Google Scholar]
- FAO/WHO 2009b. Risk assessment of Campylobacter spp. in broiler chicken. Technical report. Microbiological risk assessment series 12. 161 pp. www.fao.org/ag/agn/agns/JEMRA/MRA%2012%20final%20for%20web.pdf (accessed 14/09/2010)
- FAO/WHO 2009c. Technical meeting on Salmonella and Campylobacter in chicken meat. 4–8 May 2009, Rome, Italy. ftp://ftp.fao.org/ag/agn/jemra/MRA1911Nov09.pdf (accessed 10/05/2010). [Google Scholar]
- Farhat A, Edward ME, Costell MH, Hadley JA, Walker PN and Vasilatos‐Younken R, 2002. A low residue nutritive supplement as an alternative to feed withdrawal in broilers: Efficacy for gastrointestinal tract emptying and maintenance of live weight prior to slaughter. Poultry Science, 81, 1406–14. [DOI] [PubMed] [Google Scholar]
- Farkas J, 1998. Irradiation as a method for decontaminating food. A review. Int J Food Microbiol, 44, 189–204. [DOI] [PubMed] [Google Scholar]
- Figueroa G, Troncoso M, Lopez C, Rivas P and Toro M, 2009. Occurrence and enumeration of Campylobacter spp. during the processing of chilean broilers. Bmc Microbiology, 9, [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fluckey WM, Sanchez MX, McKee SR, Smith D, Pendleton E and Brashears MM, 2003. Establishment of a microbiological profile for an air‐chilling poultry operation in the united states. J Food Prot, 66, 272–9. [DOI] [PubMed] [Google Scholar]
- FSIS/USDA 2008a. Compliance guideline for controlling Salmonella and Campylobacter in poultry. Second edition, May 2008. www.fsis.usda.gov/pdf/compliance_guideline_controlling_salmonella_poultry.pdf (accessed 10/05/2010).
- FSIS/USDA 2008b. Improvements for poultry slaughter inspection, Appendix C‐literature review of the poultry slaughter process. www.fsis.usda.gov/OPPDE/NACMPI/Feb2008/Slaughter_Appendix_C.pdf (accessed 10/05/2010)
- Geenen PL, Koene MGJ, Blaak H, Havelaar A and Van De Giessen AW (National Insitute for Public Health and the Environment) , 2011. Risk profile on antimicrobial resistance transmissible from food animals to humans. Bilthoven, the Netherlands. www.rivm.nl/bibliotheek/rapporten/330334001.pdf (accessed 07/03/2011). [Google Scholar]
- Gellynck X, Messens W, Halet D, Grijspeerdt K, Hartnett E and Viaene J, 2008. Economics of reducing Campylobacter at different levels within the belgian poultry meat chain. J Food Prot, 71, 479–85. [DOI] [PubMed] [Google Scholar]
- Georgsson F, Porkelsson AE, Geirsdottir M, Reiersen J and Stern NJ, 2006a. The influence of freezing and duration of storage on Campylobacter and indicator bacteria in broiler carcasses. Food Microbiology, 23, 677–83. [DOI] [PubMed] [Google Scholar]
- Georgsson F, Thornorkelsson AE, Geirsdottir M, Reiersen J and Stern NJ, 2006b. The influence of freezing and duration of storage on Campylobacter and indicator bacteria in broiler carcasses. Food Microbiol, 23, 677–83. [DOI] [PubMed] [Google Scholar]
- Gibbens JC, Pascoe SJ, Evans SJ, Davies RH and Sayers AR, 2001. A trial of biosecurity as a means to control Campylobacter infection of broiler chickens. Prev Vet Med, 48, 85–99. [DOI] [PubMed] [Google Scholar]
- Gomez‐Lopez VM, Rajkovic A, Ragaert P, Smigic N and Devlieghere F, 2009. Chlorine dioxide for minimally processed produce preservation: A review. Trends in Food Science & Technology, 20, 17–26. [Google Scholar]
- Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B and Nielsen H, 2009. Increased short‐ and long‐term risk of inflammatory bowel disease after Salmonella or Campylobacter gastroenteritis. Gastroenterology, 137, 495–501. [DOI] [PubMed] [Google Scholar]
- Gregory E, Barnhart H, Dreesen DW, Stern NJ and Corn JL, 1997. Epidemiological study of Campylobacter spp. in broilers: Source, time of colonization, and prevalence. Avian Dis, 41, 890–8. [PubMed] [Google Scholar]
- Guerin MT, Martin W, Reiersen J, Berke O, McEwen SA, Bisaillon JR and Lowman R, 2007. A farm‐level study of risk factors associated with the colonization of broiler flocks with Campylobacter spp. in Iceland, 2001–2004. Acta Vet Scand, 49, 18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guerin MT, Sir C, Sargeant JM, Waddell L, O'Connor AM, Wills RW, Bailey RH and Byrd JA, 2010. The change in prevalence of Campylobacter on chicken carcasses during processing: A systematic review. Poultry Science, 89, 1070–84. [DOI] [PubMed] [Google Scholar]
- Guerrero I and Taylor AJ, 1994. Meat surface decontamination using lactic‐acid from chemical and microbial sources. Food Science and Technology‐Lebensmittel‐Wissenschaft & Technologie, 27, 201–09. [Google Scholar]
- Haagsma JA, Siersema PD, De Wit NJ and Havelaar AH, 2006. Disease burden of post‐infectious irritable bowel syndrome in the Netherlands. Epidemiology and Infection, First View, 1–7. [DOI] [PubMed]
- Haas D, Posch J, Schmidt S, Wust G, Sixl W, Feierl G, Marth E and Reinthaler FH, 2005. A case study of airborne culturable microorganisms in a poultry slaughterhouse in Styria, Austria. Aerobiologia, 21, 193–201. [Google Scholar]
- Habib I, Sampers I, Uyttendaele M, De Zutter L and Berkvens D, 2008. A bayesian modelling framework to estimate Campylobacter prevalence and culture methods sensitivity: Application to a chicken meat survey in Belgium. J Appl Microbiol, 105, 2002–8. [DOI] [PubMed] [Google Scholar]
- Hald B, Rattenborg E and Madsen M, 2001. Role of batch depletion of broiler houses on the occurrence of Campylobacter spp. In chicken flocks. Lett Appl Microbiol, 32, 253–6. [DOI] [PubMed] [Google Scholar]
- Hald B, Skovgard H, Bang DD, Pedersen K, Dybdahl J, Jespersen JB and Madsen M, 2004. Flies and Campylobacter infection of broiler flocks. Emerg Infect Dis, 10, 1490–2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hald B, Skovgard H, Pedersen K and Bunkenborg H, 2008. Influxed insects as vectors for Campylobacter jejuni and Campylobacter coli in Danish broiler houses. Poult Sci, 87, 1428–34. [DOI] [PubMed] [Google Scholar]
- Hald B, Skovgard H, Pedersen K, Bunkenborg H and Madsen M, 2005. Insect screen against Campylobacter, an intervention study in broiler houses. 13. International Workshop on Campylobacter, Helicobacter and Related Organisms, 4–8 September 2005, Gold Coast, Quensland, Australia. Abstracts of Scientific Presentations, p. 112.
- Hald B, Sommer HM and Skovgard H, 2007. Use of fly screens to reduce Campylobacter spp. introduction in broiler houses. Emerg Infect Dis, 13, 1951–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hald B, Wedderkopp A and Madsen M, 2000. Thermophilic Campylobacter spp. in Danish broiler production: A cross‐sectional survey and a retrospective analysis of risk factors for occurrence in broiler flocks. Avian Pathology, 29, 123–31. [DOI] [PubMed] [Google Scholar]
- Hansson I, Ederoth M, Andersson L, Vagsholm I and Engvall EO, 2005. Transmission of Campylobacter spp. to chickens during transport to slaughter. Journal of Applied Microbiology, 99, 1149–57. [DOI] [PubMed] [Google Scholar]
- Hansson I, Forshell LP, Gustafsson P, Boqvist S, Lindblad J, Engvall EO, Andersson Y and Vagsholm I, 2007a. Summary of the Swedish Campylobacter program in broilers, 2001 through 2005. J Food Prot, 70, 2008–14. [DOI] [PubMed] [Google Scholar]
- Hansson I, Vagsholm I, Svensson L and Olsson Engvall E, 2007b. Correlations between Campylobacter spp. prevalence in the environment and broiler flocks. J Appl Microbiol, 103, 640–9. [DOI] [PubMed] [Google Scholar]
- Hartnett E, Kelly L, Newell D, Wooldridge M and Gettinby G, 2001. A quantitative risk assessment for the occurrence of Campylobacter in chickens at the point of slaughter. Epidemiol Infect, 127, 195–206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Havelaar AH, de Wit MA, van Koningsveld R and van Kempen E, 2000. Health burden in the Netherlands due to infection with thermophilic Campylobacter spp. Epidemiol Infect, 125, 505–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Havelaar AH, Mangen MJ, de Koeijer AA, Bogaardt MJ, Evers EG, Jacobs‐Reitsma WF, van Pelt W, Wagenaar JA, de Wit GA, van der Zee H and Nauta MJ, 2007. Effectiveness and efficiency of controlling Campylobacter on broiler chicken meat. Risk Anal, 27, 831–44. [DOI] [PubMed] [Google Scholar]
- Havelaar AH, Van Duynhoven YT, Nauta MJ, Bouwknegt M, Heuvelink AE, De Wit GA, Nieuwenhuizen MG and van de Kar NC, 2004. Disease burden in the Netherlands due to infections with shiga toxin‐producing Escherichia coli O157. Epidemiol Infect, 132, 467–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Helms M, Vastrup P, Gerner‐Smidt P and Molbak K, 2003. Short and long term mortality associated with foodborne bacterial gastrointestinal infections: Registry based study. BMJ, 326 (7356), 357. [PMC free article] [PubMed] [Google Scholar]
- 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. Epidemiol Infect, 131, 1169–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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 ceca of colonized broiler chickens against the bactericidal effects of medium‐chain fatty acids. Poultry Science, 89, 1144–55. [DOI] [PubMed] [Google Scholar]
- Hermosilla AM, 2004. Transfer of contamination of Campylobacter spp. from positive broiler flocks to negative flocks during processing. MSc Thesis, University of Bristol, Bristol. [Google Scholar]
- Hiett KL, Stern NJ, Fedorka‐Cray P, Cox NA, Musgrove MT and Ladely S, 2002. Molecular subtype analyses of Campylobacter spp. From Arkansas and California poultry operations. Appl Environ Microbiol, 68, 6220–36. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilmarsson H, Thormar H, Thrainsson JH, Gunnarsson E and Dadadottir S, 2006. Effect of glycerol monocaprate (monocaprin) on broiler chickens: An attempt at reducing intestinal Campylobacter infection. Poult Sci, 85, 588–92. [DOI] [PubMed] [Google Scholar]
- Hinton A, Buhr RJ and Ingram KD, 2000a. Physical, chemical, and microbiological changes in the crop of broiler chickens subjected to incremental feed withdrawal. Poultry Science, 79, 212–18. [DOI] [PubMed] [Google Scholar]
- Hinton A, Buhr RJ and Ingram KD, 2000b. Reduction of Salmonella in the crop of broiler chickens subjected to feed withdrawal. Poultry Science, 79, 1566–70. [DOI] [PubMed] [Google Scholar]
- Hinton A, Jr. , Buhr RJ and Ingram KD, 2002. Carbohydrate‐based cocktails that decrease the population of Salmonella and Campylobacter in the crop of broiler chickens subjected to feed withdrawal. Poult Sci, 81, 780–4. [DOI] [PubMed] [Google Scholar]
- Hirshfield IN, Terzulli S and O'Byrne C, 2003. Weak organic acids: A panoply of effects on bacteria. Science Progress, 86, 245–69. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hofshagen M, Jonsson M and Opheim M (National Veterinary Institute) , 2010. The surveillance and control programme for Campylobacter spp. in broiler flocks in Norway. Annual report 2009. Surveillance and control programmes for terrestrial and aquatic animals in Norway. Oslo, Norway. [Google Scholar]
- Hofshagen M and Kruse H, 2005. Reduction in flock prevalence of Campylobacter spp. in broilers in Norway after implementation of an action plan. Journal of Food Protection, 68, 2220–23. [DOI] [PubMed] [Google Scholar]
- Hofshagen M, Opheim M, Johannessen GS, Lyngstad T, Jonsson M and Hauge K, 2008. Plan of action against Campylobacter in poultry for slaughter. Norsk Veterinartidsskrift, 120, 154–56. [Google Scholar]
- Hong J, Jung WK, Kim JM, Kim SH, Koo HC, Ser J and Park YH, 2007. Quantification and differentiation of Campylobacter jejuni and Campylobacter coli in raw chicken meats using a real‐time PRC method. J Food Prot, 70, 2015–22. [DOI] [PubMed] [Google Scholar]
- Hong Y, Ku K, Kim M, Won M, Chung K and Song KB, 2008. Survival of Escherichia coli O157:H7 and Salmonella Typhimurium inoculated on chicken by aqueous chlorine dioxide treatment. J Microbiol Biotechnol, 18, 742–5. [PubMed] [Google Scholar]
- Hue O, Le Bouquin S, Laisney MJ, Allain V, Lalande F, Petetin I, Rouxel S, Quesne S, Gloaguen PY, Picherot M, Santolini J, Salvat G, Bougeard S and Chemaly M, 2010. Prevalence of and risk factors for Campylobacter spp. contamination of broiler chicken carcasses at the slaughterhouse. Food Microbiology, 27, 992–99. [DOI] [PubMed] [Google Scholar]
- Hugas M and Tsigarida E, 2008. Pros and cons of carcass decontamination: The role of the European Food Safety Authority. Meat Science, 78, 43–52. [DOI] [PubMed] [Google Scholar]
- Humphrey T, 2006. Are happy chickens safer chickens? Poultry welfare and disease susceptibility. Br Poult Sci, 47, 379–91. [DOI] [PubMed] [Google Scholar]
- Humphrey TJ, Henley A and Lanning DG, 1993. The colonization of broiler chickens with Campylobacter jejuni: Some epidemiological investigations. Epidemiol Infect, 110, 601–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huneau‐Salaun A, Denis M, Balaine L and Salvat G, 2007. Risk factors for Campylobacter spp. colonization in french free‐range broiler‐chicken flocks at the end of the indoor rearing period. Prev Vet Med, 80, 34–48. [DOI] [PubMed] [Google Scholar]
- Hutchison ML, Walters LD, Avery SM, Munro F and Moore A, 2005. Analyses of livestock production, waste storage, and pathogen levels and prevalences in farm manures. Applied and Environmental Microbiology, 71, 1231–36. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hwang CA and Beuchat LR, 1995. Efficacy of a lactic acid/sodium benzoate wash solution in reducing bacterial contamination of raw chicken. Int J Food Microbiol, 27, 91–8. [DOI] [PubMed] [Google Scholar]
- ICMSF , 1996. Characteristics of microbial pathogens. Vol. 5. Roberts, TA , Baird‐Parker, AC , Tompkin, RB (eds.). Blackie Academic & Professional, London. [Google Scholar]
- Isohanni PMI and Lyhs U, 2009. Use of ultraviolet irradiation to reduce Campylobacter jejuni on broiler meat. Poultry Science, 88, 661–68. [DOI] [PubMed] [Google Scholar]
- Izat AL, Gardner FA, Denton JH and Golan FA, 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poult Sci, 67, 1568–72. [DOI] [PubMed] [Google Scholar]
- Jacobs‐Reitsma WF, 1995. Campylobacter bacteria in breeder flocks. Avian Dis, 39, 355–9. [PubMed] [Google Scholar]
- Jacobs‐Reitsma WF, Bolder NM and Mulder RWAW (Office for Official Publications of the European Communities, Luxembourg) , 1996. The influence of pre‐slaughter stresses on incidence and extent of human pathogens in poultry. Prevention of Contamination of Poultry Meat, Eggs and Egg Products. Cost Action 97. 3–6. [Google Scholar]
- Jacobs‐Reitsma WF, van de Giessen AW, Bolder NM and Mulder RW, 1995. Epidemiology of Campylobacter spp. at two dutch broiler farms. Epidemiol Infect, 114, 413–21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacxsens L, Kussaga J, Luning PA, Van der Spiegel M, Devlieghere F and Uyttendaele M, 2009. A microbial assessment scheme to measure microbial performance of food safety management systems. International Journal of Food Microbiology, 134, 113–25. [DOI] [PubMed] [Google Scholar]
- James C, James SJ, Hannay N, Purnell G, Barbedo‐Pinto C, Yaman H, Araujo M, Gonzalez ML, Calvo J, Howell M and Corry JEL, 2007. Decontamination of poultry carcasses using steam or hot water in combination with rapid cooling, chilling or freezing of carcass surfaces. International Journal of Food Microbiology, 114, 195–203. [DOI] [PubMed] [Google Scholar]
- Jasson V, Uyttendaele M, Rajkovic A and Debevere J, 2007. Establishment of procedures provoking sub‐lethal injury of Listeria monocytogenes, Campylobacter jejuni and Escherichia coli O157 to serve method performance testing. Int J Food Microbiol, 118, 241–9. [DOI] [PubMed] [Google Scholar]
- Johannessen GS, Johnsen G, Okland M, Cudjoe KS and Hofshagen M, 2007. Enumeration of thermotolerant Campylobacter spp. from poultry carcasses at the end of the slaughter‐line. Lett Appl Microbiol, 44, 92–7. [DOI] [PubMed] [Google Scholar]
- Johnsen G, Kruse H and Hofshagen M, 2006. Genetic diversity and description of transmission routes for Campylobacter on broiler farms by amplified‐fragment length polymorphism. Journal of Applied Microbiology, 101, 1130–39. [DOI] [PubMed] [Google Scholar]
- Johnsen G, Kruse H and Hofshagen M, 2007. Genotyping of thermotolerant Campylobacter from poultry slaughterhouse by amplified fragment length polymorphism. J Appl Microbiol, 103, 271–9. [DOI] [PubMed] [Google Scholar]
- Jore S, Viljugrein H, Brun E, Heier BT, Borck B, Ethelberg S, Hakkinen M, Kuusi M, Reiersen J, Hansson I, Engvall EO, Lofdahl M, Wagenaar JA, van Pelt W and Hofshagen M, 2010. Trends in Campylobacter incidence in broilers and humans in six European countries, 1997–2007. Preventive Veterinary Medicine, 93, 33–41. [DOI] [PubMed] [Google Scholar]
- Kaiser P, Howell MMJ, Fife M, Sadeyen JR, Salmon N, Rothwell L, Young J, Poh TY, Stevens M, Smith J, Burt D, Swaggerty C and Kogut M, 2009. Towards the selection of chickens resistant to Salmonella and Campylobacter infections. Bull Mem Acad R Med Belg, 164, 17–25; discussion 25‐6. [PubMed] [Google Scholar]
- Kapperud G, Skjerve E, Vik L, Hauge K, Lysaker A, Aalmen I, Ostroff SM and Potter M, 1993. Epidemiological investigation of risk factors for Campylobacter colonization in Norwegian broiler flocks. Epidemiol Infect, 111, 245–55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keener KM, Bashor MP, Curtis PA, Sheldon BW and Kathariou S, 2004. Comprehensive review of Campylobacter and poultry processing. Comprehensive Reviews in Food Science and Food Safety, 3, 105–16. [DOI] [PubMed] [Google Scholar]
- Kemp GK, Aldrich ML, Guerra ML and Schneider KR, 2001. Continuous online processing of fecal‐and ingesta‐contaminated poultry carcasses using an acidified sodium chlorite antimicrobial intervention. J Food Prot, 64, 807–12. [DOI] [PubMed] [Google Scholar]
- Kemp GK, Aldrich ML and Waldroup AL, 2000. Acidified sodium chlorite antimicrobial treatment of broiler carcasses. Journal of Food Protection, 63, 1087–92. [DOI] [PubMed] [Google Scholar]
- Kemp R, Leatherbarrow AJ, Williams NJ, Hart CA, Clough HE, Turner J, Wright EJ and French NP, 2005. Prevalence and genetic diversity of Campylobacter spp. in environmental water samples from a 100‐square‐kilometer predominantly dairy farming area. Appl Environ Microbiol, 71, 1876–82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kennedy C and Miller J, 2004. A chilling technique for processing chicken more safely and efficiently. Food Science and Technology, 18 (1) 30–32. [Google Scholar]
- Kiess AS, Kenney PB and Nayak RR, 2007. Campylobacter detection in commercial turkeys. Br Poult Sci, 48, 567–72. [DOI] [PubMed] [Google Scholar]
- Kim C, Hung YC and Russell SM, 2005. Efficacy of electrolyzed water in the prevention and removal of fecal material attachment and its microbicidal effectiveness during simulated industrial poultry processing. Poult Sci, 84, 1778–84. [DOI] [PubMed] [Google Scholar]
- King V, Bavetsia A and Bumstead N, 1993. Effect of host lineage on the virulence of Campylobacter jejuni/coli in the chick embryo model. FEMS Microbiol Lett, 106, 271–4. [DOI] [PubMed] [Google Scholar]
- Kitis M, 2004. Disinfection of wastewater with peracetic acid: A review. Environment International, 30, 47–55. [DOI] [PubMed] [Google Scholar]
- Klein G, Reich F, Beckmann L and Atanassova V, 2007. Quantification of thermophilic Campylobacter spp. in broilers during meat processing. Antonie Van Leeuwenhoek, 92, 267–73. [DOI] [PubMed] [Google Scholar]
- Lake R, Hudson A, Cressey P and Bayne G (Report of the Institute of Environmental Science and Research Limited) , 2007. Quantitative risk model: Campylobacter spp. in the poultry food chain. 1–91.
- Lastovica A and Allos BM, 2008. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and Campylobacter coli . In: Campylobacter, Nachamkin, I , Szymanski, C , Blaser, M (eds.) ASM Press, Washington, DC, USA. [Google Scholar]
- Li Y, Yang H and Swem BL, 2002. Effect of high‐temperature inside‐outside spray on survival of Campylobacter jejuni attached to prechill chicken carcasses. Poult Sci, 81, 1371–7. [DOI] [PubMed] [Google Scholar]
- Lin J, 2009. Novel approaches for Campylobacter control in poultry. Foodborne Pathogens and Disease, 6, 755–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindblom GB, Sjorgren E and Kaijser B, 1986. Natural Campylobacter colonization in chickens raised under different environmental conditions. J Hyg (Lond), 96, 385–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindqvist R and Lindblad M, 2008. Quantitative risk assessment of thermophilic Campylobacter spp. and cross‐contamination during handling of raw broiler chickens evaluating strategies at the producer level to reduce human campylobacteriosis in sweden. Int J Food Microbiol, 121, 41–52. [DOI] [PubMed] [Google Scholar]
- Line JE, Bailey JS, Cox NA, Stern NJ and Tompkins T, 1998. Effect of yeast‐supplemented feed on Salmonella and Campylobacter populations in broilers. Poult Sci, 77, 405–10. [DOI] [PubMed] [Google Scholar]
- Line JE, Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Levchuk VP, Svetoch OE, Seal BS, Siragusa GR and Stern NJ, 2008. Isolation and purification of enterocin e‐760 with broad antimicrobial activity against gram‐positive and gram‐negative bacteria. Antimicrob Agents Chemother, 52, 1094–100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loc Carrillo C, Atterbury RJ, El‐Shibiny A, Connerton PL, Dillon E, Scott A and Connerton IF, 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Applied and Environmental Microbiology, 71, 6554–63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowman R, Reiersen J, Tco Jonsson, Gunnarsson A, Bisaillon JG and Daoadottir Sc, 2009. Iceland: 2008 pilot year fly netting ventilation inlets of 35 broiler houses to reduce flyborne transmission of Campylobacter spp. to flocks. 15th International Workshop on Campylobacter , Helicobacter and Related Organisms, September 2–5, 2009, Niigata, Japan. [Google Scholar]
- Luber P and Bartelt E, 2007. Enumeration of Campylobacter spp. on the surface and within chicken breast fillets. J Appl Microbiol, 102, 313–8. [DOI] [PubMed] [Google Scholar]
- Luning PA, Bango L, Kussaga J, Rovira J and Marcelis WJ, 2008. Comprehensive analysis and differentiated assessment of food safety control systems: A diagnostic instrument. Trends in Food Science & Technology, 19, 522–34. [Google Scholar]
- Lyngstad TM, Jonsson ME, Hofshagen M and Heier BT, 2008. Risk factors associated with the presence of Campylobacter species in Norwegian broiler flocks. Poult Sci, 87, 1987–94. [DOI] [PubMed] [Google Scholar]
- Mangen MJJ, Havelaar AH, Bernsen RAJAM, Koningsveld RV and Wit GAD, 2005. The costs of human Campylobacter infections and sequelae in the Netherlands: A DALY and cost‐of‐illness approach. Acta Agricultura Scandinavica. Section C, Food Economics, 2, 35–51. [Google Scholar]
- McCrea BA, Tonooka KH, VanWorth C, Boggs CL, Atwill ER and Schrader JS, 2006. Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poult Sci, 85, 136–43. [DOI] [PubMed] [Google Scholar]
- McDowell SWJ, MenzieS FD, McBride SH, Oza A, McKenna JP, Gordon AW and Neillab SD, 2008. Campylobacter spp. in conventional broiler flocks in northern ireland: Epidemiology and risk factors. Preventive Veterinary Medicine, 84, 261–76. [DOI] [PubMed] [Google Scholar]
- McDowell SWJ, Menzies FD, McBride SH, Oza AN, McKenna JP, Gordon AW and Neill SD, 2007. Campylobacter spp. in commercial broiler flocks: Epidemiology and risk factors. Society for Veterinary Epidemiology and Preventive Medicine. Proceedings of a meeting held at Dipoli, Helsinki/Espoo, Finland, 28–30 March 2007, 84–97.
- Mead GC, 2000. Prospects for ‘competitive exclusion’ treatment to control Salmonella and other foodborne pathogens in poultry. Vet J, 159, 111–23. [DOI] [PubMed] [Google Scholar]
- Mead GC, 2004. Poultry meat processing and quality. Woodhead Publishing Ltd., Cambridge, UK, xiii + 388 pp. ISBN 1–85573‐727‐2. [Google Scholar]
- Mead GC, Adams BW and Parry RT, 1975. Effectiveness of in‐plant chlorination in poultry‐processing. British Poultry Science, 16, 517–26. [DOI] [PubMed] [Google Scholar]
- Mead GC, Hudson WR and Hinton MH, 1995. Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with Campylobacter . Epidemiol Infect, 115, 495–500. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mead GC, Norris AP and Bratchell N, 1989. Differentiation of Staphylococcus aureus from freshly slaughtered poultry and strains endemic to processing plants by biochemical and physiological tests. Journal of Applied Bacteriology, 66, 153–59. [DOI] [PubMed] [Google Scholar]
- Mead GC, Scott MJ, Humphrey TJ and McAlpine K, 1996. Observations on the control of Campylobacter jejuni infection of poultry by ‘competitive exclusion’. Avian Pathol, 25, 69–79. [DOI] [PubMed] [Google Scholar]
- Meremaee K, Elias P, Tamme T, Kramarenko T, Lillenberg M, Karus A, Hanninen M‐L and Roasto M, 2010. The occurrence of Campylobacter spp. in Estonian broiler chicken production in 2002–2007. Food Control, 21, 272–75. [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, 120–31. [DOI] [PubMed] [Google Scholar]
- Mills A and Phillips CA, 2003. Campylobacter jejuni and the human food chain: A possible source. Nutrition & Food Science, 33, 197–202. [Google Scholar]
- Milnes AS, Stewart I, Clifton‐Hadley FA, Davies RH, Newell DG, Sayers AR, Cheasty T, Cassar C, Ridley A, Cook AJ, Evans SJ, Teale CJ, Smith RP, McNally A, Toszeghy M, Futter R, Kay A and Paiba GA, 2008. Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect, 136, 739–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mohyla P, Bilgili SF, Oyarzabal OA, Warf CC and Kemp GK, 2007. Application of acidified sodium chlorite in the drinking water to control Salmonella serotype Typhimurium and Campylobacter jejuni in commercial broilers. J Appl Poult Res, 16, 45–51. [Google Scholar]
- Musgrove MT, Cason JA, Fletcher DL, Stern NJ, Cox NA and Bailey JS, 1997. Effect of cloacal plugging on microbial recovery from partially processed broilers. Poult Sci, 76, 530–3. [DOI] [PubMed] [Google Scholar]
- Nadeau E, Messier S and Quessy S, 2003. Comparison of Campylobacter isolates from poultry and humans: Association between in vitro virulence properties, biotypes, and pulsed‐field gel electrophoresis clusters. Appl Environ Microbiol, 69, 6316–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nauta M and Christensen B, 2011. The impact of consumer phase models in microbial risk analysis. Risk Analysis, 31, 255–65. [DOI] [PubMed] [Google Scholar]
- Nauta M, Hill A, Rosenquist H, Brynestad S, Fetsch A, van der Logt P, Fazil A, Christensen B, Katsma E, Borck B and Havelaar A, 2009a. A comparison of risk assessments on Campylobacter in broiler meat. Int J Food Microbiol, 129, 107–23. [DOI] [PubMed] [Google Scholar]
- Nauta M, Jacobs‐Reitsma W, Evers EG, Van Pelt W and Havelaar A 2005a. Risk assessment of Campylobacter in the Netherlands via broiler meat and other routes. RIVM Report. www.rivm.nl/bibliotheek/rapporten/250911006.pdf (accessed 16/12/2010).
- Nauta M, van der Fels‐Klerx I and Havelaar A, 2005b. A poultry‐processing model for quantitative microbiological risk assessment. Risk Anal, 25, 85–98. [DOI] [PubMed] [Google Scholar]
- Nauta MJ, Fischer AR, van Asselt ED, de Jong AE, Frewer LJ and de Jonge R, 2008. Food safety in the domestic environment: The effect of consumer risk information on human disease risks. Risk Anal, 28, 179–92. [DOI] [PubMed] [Google Scholar]
- Nauta MJ, Wal FJvd, Putirulan FF, Post J, Kassteele Jvd and Bolder NM, 2009b. Evaluation of the “Testing and scheduling” Strategy for control of Campylobacter in broiler meat in the Netherlands. International Journal of Food Microbiology, 134, 216–22. [DOI] [PubMed] [Google Scholar]
- Neubauer C, Bibl D, Szolgyenyi W, Jauk V, Schmidt M, Gabler C and Vasicek L, 2005. Epidemiological investigation of Campylobacter spp. in Austrian broiler flocks: Prevalence and risk factors. Wiener Tierarztliche Monatsschrift, 92, 4–10. [Google Scholar]
- Newell D, Allen V, Elvers KT, Dorfper D, Hanssen I, Jones P, James S, Gittins J, Stern N, Davies RH, Connerton I, Pearson D and Salvat G 2008. A critical review of interventions and strategies (both biosecurity and non‐biosecurity) to reduce Campylobacter on the poultry farm. [DOI] [PMC free article] [PubMed]
- Newell DG and Fearnley C, 2003. Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol, 69, 4343–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Newell DG, Shreeve JE, Toszeghy M, Domingue G, Bull S, Humphrey T and Mead G, 2001. Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl Environ Microbiol, 67, 2636–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Newell DG and Wagenaar JA, 2000. Poultry infections and their control at the farm level. In: Campylobacter, 2nd ed. Nachamkin I and Blaser MJ. American Society for Microbiology, Washington, D.C., 497–509. [Google Scholar]
- Nicholson FA, Groves SJ and Chambers BJ, 2005. Pathogen survival during livestock manure storage and following land application. Bioresour Technol, 96, 135–43. [DOI] [PubMed] [Google Scholar]
- Nijdam E, Delezie E, Lambooij E, Nabuurs MJA, Decuypere E and Stegeman JA, 2005. Feed withdrawal of broilers before transport changes plasma hormone and metabolite concentrations. Poultry Science, 84, 1146–52. [DOI] [PubMed] [Google Scholar]
- Nijdam E, Lambooij E, Nabuurs MJA, Decuypere E and Stegeman JA, 2006. Influences of feeding conventional and semisynthetic diets and transport of broilers on weight gain, digestive tract mass, and plasma hormone and metabolite concentrations. Poultry Science, 85, 1652–59. [DOI] [PubMed] [Google Scholar]
- Northcutt J, Smith D, Ingram KD, Hinton A, Jr. and Musgrove M, 2007. Recovery of bacteria from broiler carcasses after spray washing with acidified electrolyzed water or sodium hypochlorite solutions. Poult Sci, 86, 2239–44. [DOI] [PubMed] [Google Scholar]
- Northcutt JK, Buhr RJ, Berrang ME and Fletcher DL, 2003. Effects of replacement finisher feed and length of feed withdrawal on broiler carcass yield and bacteria recovery. Poult Sci, 82, 1820–4. [DOI] [PubMed] [Google Scholar]
- Northcutt JK, Savage SI and Vest LR, 1997. Relationship between feed withdrawal and viscera condition of broilers. Poultry Science, 76, 410–14. [DOI] [PubMed] [Google Scholar]
- Northcutt JK, Smith DP, Musgrove MT, Ingram KD and Hinton A, Jr. , 2005. Microbiological impact of spray washing broiler carcasses using different chlorine concentrations and water temperatures. Poult Sci, 84, 1648–52. [DOI] [PubMed] [Google Scholar]
- Nylen G, Dunstan F, Palmer SR, Andersson Y, Bager F, Cowden J, Feierl G, Galloway Y, Kapperud G, Megraud F, Molbak K, Petersen LR and Ruutu P, 2002. The seasonal distribution of Campylobacter infection in nine European countries and New Zealand. Epidemiol Infect, 128, 383–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ogata N, 2007. Denaturation of protein by chlorine dioxide: Oxidative modification of tryptophan and tyrosine residues. Biochemistry, 46, 4898–911. [DOI] [PubMed] [Google Scholar]
- Oosterom J, Dewilde GJA, Deboer E, Deblaauw LH and Karman H, 1983. Survival of Campylobacter‐jejuni during poultry‐processing and pig slaughtering. Journal of Food Protection, 46, 702–&. [DOI] [PubMed] [Google Scholar]
- Oyarzabal OA, Hawk C, Bilgili SF, Warf CC and Kemp GK, 2004. Effects of postchill application of acidified sodium chlorite to control Campylobacter spp. and Escherichia coli on commercial broiler carcasses. J Food Prot, 67, 2288–91. [DOI] [PubMed] [Google Scholar]
- Park H, Hung YC and Brackett RE, 2002. Antimicrobial effect of electrolyzed water for inactivating Campylobacter jejuni during poultry washing. Int J Food Microbiol, 72, 77–83. [DOI] [PubMed] [Google Scholar]
- Pearson AD, Greenwood M, Healing TD, Rollins D, Shahamat M, Donaldson J and Colwell RR, 1993. Colonization of broiler chickens by waterborne Campylobacter jejuni . Appl Environ Microbiol, 59, 987–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petersen L, Nielsen EM, Engberg J, On SL and Dietz HH, 2001a. Comparison of genotypes and serotypes of Campylobacter jejuni isolated from Danish wild mammals and birds and from broiler flocks and humans. Appl Environ Microbiol, 67, 3115–21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petersen L, Nielsen EM and On SL, 2001b. Serotype and genotype diversity and hatchery transmission of Campylobacter jejuni in commercial poultry flocks. Vet Microbiol, 82, 141–54. [DOI] [PubMed] [Google Scholar]
- Peyrat MB, Soumet C, Maris P and Sanders P, 2008. Recovery of Campylobacter jejuni from surfaces of poultry slaughterhouses after cleaning and disinfection procedures: Analysis of a potential source of carcass contamination. Int J Food Microbiol, 124, 188–94. [DOI] [PubMed] [Google Scholar]
- Pordesimo LO, Wilkerson EG, Womac AR and Cutter CN, 2002. Process engineering variables in the spray washing of meat and produce. Journal of Food Protection, 65, 222–37. [DOI] [PubMed] [Google Scholar]
- Purnell G, Mattick K and Humphrey T, 2004. The use of ‘hot wash’ treatments to reduce the number of pathogenic and spoilage bacteria on raw retail poultry. Journal of Food Engineering, 62, 29–36. [Google Scholar]
- Puterflam J, Bouvarel I, Ragot O and Drouet M, 2005. Contamination of broiler breeding farms by Campylobacter: Is this inevitable? Sciences & Techniques Avicoles, 53, 12–19. [Google Scholar]
- Ramabu SS, Boxall NS, Madie P and Fenwick SG, 2004. Some potential sources for transmission of Campylobacter jejuni to broiler chickens. Lett Appl Microbiol, 39, 252–6. [DOI] [PubMed] [Google Scholar]
- Ramirez GA, Sarlin LL, Caldwell DJ, Yezak CR, Hume ME, Corrier DE, Deloach JR and Hargis BM, 1997. Effect of feed withdrawal on the incidence of Salmonella in the crops and ceca of market age broiler chickens. Poultry Science, 76, 654–56. [DOI] [PubMed] [Google Scholar]
- Rasschaert G, Houf K and De Zutter L, 2007. External contamination of Campylobacter‐free flocks after transport in cleaned and disinfected containers. J Food Prot, 70, 40–6. [DOI] [PubMed] [Google Scholar]
- Rathgeber BM, MacIsaac JL and MacKenzie ME, 2007. Feeding turkeys a highly digestible supplement during preslaughter feed withdrawal. Poultry Science, 86, 2029–33. [DOI] [PubMed] [Google Scholar]
- Refregier‐Petton J, Rose N, Denis M and Salvat G, 2001. Risk factors for Campylobacter spp. contamination in French broiler‐chicken flocks at the end of the rearing period. Prev Vet Med, 50, 89–100. [DOI] [PubMed] [Google Scholar]
- 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 . Int J Food Microbiol, 127, 116–20. [DOI] [PubMed] [Google Scholar]
- Richardson SD, Thruston AD, Caughran TV, Chen PH, Collette TW, Schenck KM, Lykins BW, Rav‐Acha C and Glezer V, 2000. Identification of new drinking water disinfection by‐products from ozone, chlorine dioxide, chloramine, and chlorine. Water Air and Soil Pollution, 123, 95–102. [Google Scholar]
- Ridley AM, Allen VM, Sharma M, Harris JA and Newell DG, 2008a. Real‐time PCR approach for detection of environmental sources of Campylobacter strains colonizing broiler flocks. Appl Environ Microbiol, 74, 2492–504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ridley AM, Morris VK, Cawthraw SA, Ellis‐Iversen J, Harris JA, Kennedy EM, Newell DG and Allen VM, 2011. Longitudinal molecular epidemiological study of thermophilic Campylobacters on one conventional broiler chicken farm. Appl. Environ. Microbiol., 77, 98–107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ridley AM, Toszeghy MJ, Cawthraw SA, Wassenaar TM and Newell DG, 2008b. Genetic instability is associated with changes in the colonization potential of Campylobacter jejuni in the avian intestine. J Appl Microbiol, 105, 95–104. [DOI] [PubMed] [Google Scholar]
- Riedel CT, Brndsted L, Rosenquist H, Haxgart SN and Christensen BB, 2009. Chemical decontamination of Campylobacter jejuni on chicken skin and meat. Journal of Food Protection, 72, 1173–80. [DOI] [PubMed] [Google Scholar]
- Rigby CE, Pettit JR, Baker MF, Bentley AH, Salomons MO and Lior H, 1980. Sources of Salmonellae in an uninfected commercially‐processed broiler flock. Canadian Journal of Comparative Medicine‐Revue Canadienne De Medecine Comparee, 44, 267–74. [PMC free article] [PubMed] [Google Scholar]
- Ring M, Zychowska MA and Stephan R, 2005. Dynamics of Campylobacter spp. spread investigated in 14 broiler flocks in Switzerland. Avian Dis, 49, 390–6. [DOI] [PubMed] [Google Scholar]
- 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 broiler farms and comparison with isolates of various origins. Appl Environ Microbiol, 71, 6216–27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Romero Barrios P, Reiersen J, Lowman R, Bisaillon JR, Michel P, Fridriksdottir V, Gunnarsson E, Stern N, Berke O, McEwen S and Martin W, 2006. Risk factors for Campylobacter spp. colonization in broiler flocks in Iceland. Prev Vet Med, 74, 264–78. [DOI] [PubMed] [Google Scholar]
- Rosef O, Rettedal G and Lageide L, 2001. Thermophilic Campylobacters in surface water: A potential risk of campylobacteriosis. Int J Environ Health Res, 11, 321–7. [DOI] [PubMed] [Google Scholar]
- 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, 1742–50. [DOI] [PubMed] [Google Scholar]
- Rosenquist H, Nielsen NL, Sommer HM, Norrung B and Christensen BB, 2003. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol, 83, 87–103. [DOI] [PubMed] [Google Scholar]
- Rosenquist H, Sommer HM, Nielsen NL and Christensen BB, 2006. The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter . Int J Food Microbiol, 108, 226–32. [DOI] [PubMed] [Google Scholar]
- Russa AD, Bouma A, Vernooij JC, Jacobs‐Reitsma W and Stegeman JA, 2005. No association between partial depopulation and Campylobacter spp. colonization of Dutch broiler flocks. Lett Appl Microbiol, 41, 280–5. [DOI] [PubMed] [Google Scholar]
- Sahin O, Luo N, Huang S and Zhang Q, 2003. Effect of Campylobacter‐specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl Environ Microbiol, 69, 5372–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sampers I, Habib I, De Zutter L, Dumoulin A and Uyttendaele M, 2010. Survival of Campylobacter spp. in poultry meat preparations subjected to freezing, refrigeration, minor salt concentration, and heat treatment. International Journal of Food Microbiology, 137, 147–53. [DOI] [PubMed] [Google Scholar]
- Sandberg M, Hofshagen M, Ostensvik O, Skjerve E and Innocent G, 2005. Survival of Campylobacter on frozen broiler carcasses as a function of time. Journal of Food Protection, 68, 1600–05. [DOI] [PubMed] [Google Scholar]
- SCF (European Commission) , 1986. Reports of the scientific committee for food eighteenth series. Brussels, Belgium. ec.europa.eu/food/fs/sc/scf/reports/scf_reports_18.pdf (accessed 02/03/2011). [Google Scholar]
- Schneider KR, Kemp GK and Aldrich ML, 2002. Antimicrobial treatment of air chilled broiler carcasses: Acidified sodium chlorite antimicrobial treatment of air chilled broiler carcasses. Dairy, Food and Environmental Sanitation, 22, 102–08. [Google Scholar]
- Scott AE, Timms AR, Connerton PL, Loc Carrillo C, Adzfa Radzum K and Connerton IF, 2007. Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathog, 3 (8), e119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SCVPH (European Commission) , 2003. The evaluation of antimicrobial treatments for poultry carcasses. Brussels, Belgium. ec.europa.eu/food/fs/sc/scv/out63_en.pdf (accessed 16/12/2010). [Google Scholar]
- Shane SM, Montrose MS and Harrington KS, 1985. Transmission of Campylobacter jejuni by the housefly (musca domestica). Avian Dis, 29, 384–91. [PubMed] [Google Scholar]
- Shanker S, Lee A and Sorrell TC, 1986. Campylobacter jejuni in broilers: The role of vertical transmission. J Hyg (Lond), 96, 153–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shreeve JE, Toszeghy M, Pattison M and Newell DG, 2000. Sequential spread of Campylobacter infection in a multipen broiler house. Avian Dis, 44, 983–8. [PubMed] [Google Scholar]
- Shreeve JE, Toszeghy M, Ridley A and Newell DG, 2002. The carry‐over of Campylobacter isolates between sequential poultry flocks. Avian Dis, 46, 378–85. [DOI] [PubMed] [Google Scholar]
- Skanseng B, Kaldhusdal M, Moen B, Gjevre AG, Johannessen GS, Sekelja M, Trosvik P and Rudi K, 2010. Prevention of intestinal Campylobacter jejuni colonization in broilers by combinations of in‐feed organic acids. Journal of Applied Microbiology, 109, 1265–73. [DOI] [PubMed] [Google Scholar]
- Slader J, Domingue G, Jorgensen F, McAlpine K, Owen RJ, Bolton FJ and Humphrey TJ, 2002. Impact of transport crate reuse and of catching and processing on Campylobacter and Salmonella contamination of broiler chickens. Appl Environ Microbiol, 68, 713–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slavik MF, Kim JW, Pharr MD, Raben DP, Tsai S and Lobsinger CM, 1994. Effect of trisodium phosphate on Campylobacter attached to post‐chill chicken carcasses. Journal of Food Protection, 57, 324–26. [DOI] [PubMed] [Google Scholar]
- Smith JL and Bayles D, 2007. Postinfectious irritable bowel syndrome: A long‐term consequence of bacterial gastroenteritis. J Food Prot, 70, 1762–9. [DOI] [PubMed] [Google Scholar]
- Smith K, Reimers N, Barnes HJ, Lee BC, Siletzky R and Kathariou S, 2004. Campylobacter colonization of sibling turkey flocks reared under different management conditions. J Food Prot, 67, 1463–8. [DOI] [PubMed] [Google Scholar]
- Smulders FJ, 1995. Preservation by microbial decontamination, the surface treatment of meats by organic acids. In: New methods of food preservation. Gould KG. Aspen Publishers, London, 253–82. [Google Scholar]
- Smulders FJM, Barendsen P, Vanlogtestijn JG, Mossel DAA and Vandermarel GM, 1986. Review ‐ lactic‐acid ‐ considerations in favor of its acceptance as a meat decontamininant. Journal of Food Technology, 21, 419–36. [Google Scholar]
- Snelling WJ, Stern NJ, Lowery CJ, Moore JE, Gibbons E, Baker C and Dooley JS, 2008. Colonization of broilers by Campylobacter jejuni internalized within Acanthamoeba castellanii . Arch Microbiol, 189, 175–9. [DOI] [PubMed] [Google Scholar]
- Sofos JN and Busta FF, 1992. Chemical food preservatives. In: Principles and practice of disinfection, preservation and sterilisation. Russell AD, Hugo WB and Ayliffe GAJ. Blackwell Scientific Publications, Oxford, 351–97. [Google Scholar]
- Solis de Los Santos F, Donoghue AM, Venkitanarayanan K, Dirain ML, Reyes‐Herrera I, Blore PJ and Donoghue DJ, 2008a. Caprylic acid supplemented in feed reduces enteric Campylobacter jejuni colonization in ten‐day‐old broiler chickens. Poult Sci, 87, 800–4. [DOI] [PubMed] [Google Scholar]
- Solis de los Santos F, Donoghue AM, Venkitanarayanan K, Reyes‐Herrera I, Metcalf JH, Dirain ML, Aguiar VF, Blore PJ and Donoghue DJ, 2008b. Therapeutic supplementation of caprylic acid in feed reduces Campylobacter jejuni colonization in broiler chicks. Appl Environ Microbiol, 74, 4564–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Solis de los Santos F, Hume M, Venkitanarayanan K, Donoghue AM, Hanning I, Slavik MF, Aguiar VF, Metcalf JH, Reyes‐Herrera I, Blore PJ and Donoghue DJ, 2010. Caprylic acid reduces enteric Campylobacter colonization in market‐aged broiler chickens but does not appear to alter cecal microbial populations. J Food Prot, 73, 251–7. [DOI] [PubMed] [Google Scholar]
- Sparks NHC, 2009. The role of the water supply system in the infection and control of Campylobacter in chicken. Worlds Poultry Science Journal, 65, 459–73. [Google Scholar]
- Stapleton K, Cawthraw SA, Cooles SW, Coldham NG, La Ragione RM, Newell DG and Ridley AM, 2010. Selecting for development of fluoroquinolone resistance in a Campylobacter jejuni strain 81116 in chickens using various enrofloxacin treatment protocols. Journal of Applied Microbiology, 109, 1132–38. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Clavero MR, Bailey JS, Cox NA and Robach MC, 1995. Campylobacter spp. In broilers on the farm and after transport. Poult Sci, 74, 937–41. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Cox NA, Bailey JS, Berrang ME and Musgrove MT, 2001a. Comparison of mucosal competitive exclusion and competitive exclusion treatment to reduce Salmonella and Campylobacter spp. colonization in broiler chickens. Poultry Science, 80, 156–60. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Fedorka‐Cray P, Bailey JS, Cox NA, Craven SE, Hiett KL, Musgrove MT, Ladely S, Cosby D and Mead GC, 2001b. Distribution of Campylobacter spp. in selected US poultry production and processing operations. Journal of Food Protection, 64, 1705–10. [DOI] [PubMed] [Google Scholar]
- Stern NJ and Line JE, 2009. Enumeration of Campylobacter spp., Escherichia coli, and Salmonella in broiler carcass rinses before and after simulated transport in artificial ice for 24 hours. Journal of Food Protection, 72, 1099–101. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Meinersmann RJ and Dickerson HW, 1990. Influence of antibody treatment of Campylobacter jejuni on the dose required to colonize chicks. Avian Dis, 34, 595–601. [PubMed] [Google Scholar]
- Stern NJ and Pretanik S, 2006. Counts of Campylobacter spp. on us broiler carcasses. Journal of Food Protection, 69, 1034–39. [DOI] [PubMed] [Google Scholar]
- Stern NJ and Robach MC, 2003. Enumeration of Campylobacter spp. in broiler feces and in corresponding processed carcasses. J Food Prot, 66, 1557–63. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Robach MC, Coxa NA and Musgrove MT, 2002. Effect of drinking water chlorination on Campylobacter spp. colonization of broilers. Avian Diseases, 46, 401–04. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Svetoch EA, Eruslanov BV, Kovalev YN, Volodina LI, Perelygin VV, Mitsevich EV, Mitsevich IP and Levchuk VP, 2005. Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. Journal of Food Protection, 68, 1450–53. [DOI] [PubMed] [Google Scholar]
- Stern NJ, Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Pokhilenko VD, Levchuk VP, Svetoch OE and Seal BS, 2006. Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother, 50, 3111–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stopforth JD, O'Connor R, Lopes M, Kottapalli B, Hill WE and Samadpour M, 2007. Validation of individual and multiple‐sequential interventions for reduction of microbial populations during processing of poultry carcasses and parts. Journal of Food Protection, 70, 1393–401. [DOI] [PubMed] [Google Scholar]
- Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Borzenkov VN, Levchuk VP, Svetoch OE, Kovalev YN, Stepanshin YG, Siragusa GR, Seal BS and Stern NJ, 2008. Diverse antimicrobial killing by Enterococcus faecium E 50–52 bacteriocin. J Agric Food Chem, 56, 1942–8. [DOI] [PubMed] [Google Scholar]
- Takahashi R, Shahada F, Chuma T and Okamoto K, 2006. Analysis of Campylobacter spp. contamination in broilers from the farm to the final meat cuts by using restriction fragment length polymorphism of the polymerase chain reaction products. Int J Food Microbiol, 110, 240–5. [DOI] [PubMed] [Google Scholar]
- Thomas LM, Long KA, Good RT, Panaccio M and Widders PR, 1997. Genotypic diversity among Campylobacter jejuni isolates in a commercial broiler flock. Appl Environ Microbiol, 63, 1874–77. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson KL and Applegate TJ, 2006. Feed withdrawal alters small‐intestinal morphology and mucus of broilers. Poultry Science, 85, 1535–40. [DOI] [PubMed] [Google Scholar]
- Thompson KL and Applegate TJ, 2008. Optimizing feed withdrawal programs. Purdue University Extension, AS‐576‐W. www.ces.purdue.edu/extmedia/AS/AS_576_W.pdf (accessed 10/05/2011).
- Thomson JE, Bailey JS, Cox NA, Posey DA and Carson MO, 1979. Salmonella on broiler carcasses as affected by fresh‐water input rate and chlorination of chiller water. Journal of Food Protection, 42, 954–&. [DOI] [PubMed] [Google Scholar]
- 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 . Appl Environ Microbiol, 72, 522–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trachoo N and Frank JF, 2002. Effectiveness of chemical sanitizers against Campylobacter jejuni‐containing biofilms. J Food Prot, 65, 1117–21. [DOI] [PubMed] [Google Scholar]
- Tustin J, Laberge K, Michel P, Reiersen J, Dađadóttir S, Briem H, Harđardóttir H, Kristinsson K, Gunnarsson E, Friđriksdóttir V and Georgsson F, 2011. A national epidemic of campylobacteriosis in Iceland, lessons learned. Zoonoses and Public Health. Blackwell Publishing Ltd. [DOI] [PubMed] [Google Scholar]
- van de Giessen A, Mazurier SI, Jacobs‐Reitsma W, Jansen W, Berkers P, Ritmeester W and Wernars K, 1992. Study on the epidemiology and control of Campylobacter jejuni in poultry broiler flocks. Appl Environ Microbiol, 58, 1913–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van de Giessen AW, Bloemberg BP, Ritmeester WS and Tilburg JJ, 1996. Epidemiological study on risk factors and risk reducing measures for Campylobacter infections in Dutch broiler flocks. Epidemiol Infect, 117, 245–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van de Giessen AW, Tilburg JJ, Ritmeester WS and van der Plas J, 1998. Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol Infect, 121, 57–66. [DOI] [PMC free article] [PubMed] [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 Pathol, 37, 379–83. [DOI] [PubMed] [Google Scholar]
- Vandekinderen I, Devlieghere F, Van Camp J, Kerkaert B, Cucu T, Ragaert P, De Bruyne J and De Meulenaer B, 2009. Effects of food composition on the inactivation of foodborne microorganisms by chlorine dioxide. International Journal of Food Microbiology, 131, 138–44. [DOI] [PubMed] [Google Scholar]
- Wagenaar JA, Van Bergen MA, Mueller MA, Wassenaar TM and Carlton RM, 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol, 109, 275–83. [DOI] [PubMed] [Google Scholar]
- Waldenstrom J, Broman T, Carlsson I, Hasselquist D, Achterberg RP, Wagenaar JA and Olsen B, 2002. Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds. Appl Environ Microbiol, 68, 5911–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang WL, Powers BW, Leuchtefeld NW and Blaser MJ, 1983. Effects of disinfectants on Campylobacter jejuni . Appl Environ Microbiol, 45, 1202–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warriss PD, Wilkins LJ, Brown SN, Phillips AJ and Allen V, 2004. Defaecation and weight of the gastrointestinal tract contents after feed and water withdrawal in broilers. British Poultry Science, 45, 61–66. [DOI] [PubMed] [Google Scholar]
- Wedderkopp A, Rattenborg E and Madsen M, 2000. National surveillance of Campylobacter in broilers at slaughter in Denmark in 1998. Avian Dis, 44, 993–9. [PubMed] [Google Scholar]
- Wesley IV, Rostagno M, Hurd HS and Trampel DW, 2009. Prevalence of Campylobacter jejuni and Campylobacter coli in market‐weight turkeys on‐farm and at slaughter. Journal of Food Protection, 72, 43–48. [DOI] [PubMed] [Google Scholar]
- Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, Hudson MJ and Roderick PJ, 1999. Study of infectious intestinal disease in England: Rates in the community, presenting to general practice, and reported to national surveillance. The infectious intestinal disease study executive. BMJ, 318, 1046–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whyte P, Collins JD, McGill K, Monahan C and O'Mahony H, 2001a. The effect of transportation stress on excretion rates of Campylobacters in market‐age broilers. Poult Sci, 80, 817–20. [DOI] [PubMed] [Google Scholar]
- Whyte P, Collins JD, McGill K, Monahan C and O'Mahony H, 2001b. Quantitative investigation of the effects of chemical decontamination procedures on the microbiological status of broiler carcasses during processing. Journal of Food Protection, 64, 179–83. [DOI] [PubMed] [Google Scholar]
- Whyte P, McGill K and Collins JD, 2003. An assessment of steam pasteurization and hot water immersion treatments for the microbiological decontamination of broiler carcasses. Food Microbiology, 20, 111–17. [Google Scholar]
- Whyte R, Hudson JA and Graham C, 2006. Campylobacter in chicken livers and their destruction by pan frying. Letters in Applied Microbiology, 43, 591–95. [DOI] [PubMed] [Google Scholar]
- Willis WL, Murray C and Raczkowski CW, 1996. The influence of feed and water withdrawal on Campylobacter jejuni detection and yield of broilers. J. Appl. Poultry Res, 5, 210–14. [Google Scholar]
- Woldemariam E, Bouma A, Vernooij JC and Stegeman A, 2008. The sensitivity and specificity of fecal and cecal culture for the detection of Campylobacter in Dutch broiler flocks quantified by bayesian analysis. Int J Food Microbiol, 121, 308–12. [DOI] [PubMed] [Google Scholar]
- Zeitoun AAM and Debevere JM, 1990. The effect of treatment with buffered lactic‐acid on microbial decontamination and on shelf‐life of poultry. International Journal of Food Microbiology, 11, 305–11. [DOI] [PubMed] [Google Scholar]
- Zhao T and Doyle MP, 2006. Reduction of Campylobacter jejuni on chicken wings by chemical treatments. Journal of Food Protection, 69, 762–67. [DOI] [PubMed] [Google Scholar]
- Zuidhof MJ, McGovern RH, Schneider BL, Feddes JJR, Robinson FE, Korver DR and Goonewardene LA, 2004. Effects of feed withdrawal and livehaul on body weight, gut clearance, and contamination of broiler caracasses. Journal of Applied Poultry Research, 13, 472–80. [Google Scholar]
