External contamination of broilers by Campylobacter spp. increases from the farm to the slaughterhouse

References

• Adria Development. 2018. “CampyFood Agar Method for the Detection of Campylobacter Spp. In Raw Meat Products, Meat-based Products and Production Environmental Samples.” Certification organism: AFNOR certification. https://nf-validation.afnor.org/wp-content/uploads/2014/03/Synt-BIO-12-30-05-10_en.pdf
   Google Scholar
• Agunos, A., L. Waddell, D. Léger, and E. Taboada. 2014. “A Systematic Review Characterizing On-Farm Sources of Campylobacter Spp. For Broiler Chickens.” PloS ONE 9 (8): e104905. doi:10.1371/journal.pone.0104905.
   PubMed Web of Science ®Google Scholar
• Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. “Fitting Linear Mixed-Effects Models Using Lme4.” Journal of Statistical Software 67 (1): 1–48. doi:10.18637/jss.v067.i01.
   Web of Science ®Google Scholar
• Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. Stevens, and J. S. White. 2009. “Generalized Linear Mixed Models: A Practical Guide for Ecology and Evolution.” Trends in Ecology & Evolution 24 (3): 127–135. doi:10.1016/j.tree.2008.10.008.
   PubMed Web of Science ®Google Scholar
• Borck Høg, B., H. M. Sommer, L. S. Larsen, A. I. Sørensen, B. David, M. Hofshagen, and H. Rosenquist. 2016. “Farm Specific Risk Factors for Campylobacter Colonisation in Danish and Norwegian Broilers.” Preventive Veterinary Medicine 130: 137–145. doi:10.1016/j.prevetmed.2016.04.002.
   PubMed Web of Science ®Google Scholar
• Brooks, M. E., K. Kristensen, K. J. van Benthem, A. Magnusson, C. W. Berg, A. Nielsen, H. J. Skaug, M. Maechler, and B. M. Bolker. 2017. “glmmTMB Balances Speed and Flexibility among Packages for Zero-inflated Generalized Linear Mixed Modeling.” The R Journal 9 (2): 378–400. doi:10.32614/RJ-2017-066.
   Google Scholar
• Bull, S. A., A. Thomas, T. Humphrey, J. Ellis-Iversen, A. J. Cook, R. Lovell, and F. Jorgensen. 2008. “Flock Health Indicators and Campylobacter Spp. In Commercial Housed Broilers Reared in Great Britain.” Applied and Environmental Microbiology 74 (17): 5408–5413. doi:10.1128/AEM.00462-08.
   PubMed Web of Science ®Google Scholar
• Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. M. Hargis. 1998. “Effect of Feed Withdrawal on Campylobacter in the Crops of Market-age Broiler Chickens.” Avian Diseases 42 (4): 802–806. doi:10.2307/1592719.
   PubMed Web of Science ®Google Scholar
• Carreira, A. C., L. Clemente, T. Rocha, A. Tavares, M. Geraldes, M. J. Barahona, A. Botelho, and M. V. Cunha. 2012. “Comparative Genotypic and Antimicrobial Susceptibility Analysis of Zoonotic Campylobacter Species Isolated from Broilers in a Nationwide Survey, Portugal.” Journal of Food Protection 75 (12): 2100–2109. doi:10.4315/0362-028X.JFP-12-183.
   PubMed Web of Science ®Google Scholar
• Choo, L. C., A. A. Saleha, S. S. Wai, and N. Fauziah. 2011. “Isolation of Campylobacter and Salmonella from Houseflies (Musca Domestica) in a University Campus and a Poultry Farm in Selangor, Malaysia.” Tropical Biomedicine 28 (1): 16–20.
   PubMed Web of Science ®Google Scholar
• Chowdhury, S., M. Sandberg, G. E. Themudo, and A. K. Ersboll. 2012. “The Effect of Presence of Infected Neighbouring Farms for the Campylobacter Infection Status in Danish Broiler Farms.” Spatial and Spatio-temporal Epidemiology 3 (4): 311–322. doi:10.1016/j.sste.2012.06.001.
   PubMedGoogle Scholar
• Damjanova, I., M. Jakab, T. Farkas, J. Meszaros, Z. Galantai, I. Turcsanyi, A. Bistyak, et al. 2011. “From Farm to Fork Follow-up of Thermotolerant Campylobacters Throughout the Broiler Production Chain and in Human Cases in a Hungarian County during a Ten-months Period.” International Journal of Food Microbiology 150 (2–3): 95–102. doi:10.1016/j.ijfoodmicro.2011.07.011.
   PubMed Web of Science ®Google Scholar
• Di Martino, G., A. Piccirillo, M. Giacomelli, D. Comin, A. Gallina, K. Capello, F. Buniolo, C. Montesissa, and L. Bonfanti. 2018. “Microbiological, Chemical and Physical Quality of Drinking Water for Commercial Turkeys: A Cross-sectional Study.” Poultry Science 97 (8): 2880–2886. doi:10.3382/ps/pey130.
   PubMed Web of Science ®Google Scholar
• Duarte, A., A. Santos, V. Manageiro, A. Martins, M. J. Fraqueza, M. Canica, F. C. Domingues, and M. Oleastro. 2014. “Human, Food and Animal Campylobacter Spp. Isolated in Portugal: High Genetic Diversity and Antibiotic Resistance Rates.” International Journal of Antimicrobial Agents 44 (4): 306–313. doi:10.1016/j.ijantimicag.2014.06.012.
   PubMed Web of Science ®Google Scholar
• ECDC (European Centre for Disease Prevention and Control) and EFSA (European Food Safety Authority). 2017. “The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2016.” EFSA Journal 15 (12): 5077. doi:10.2903/j.efsa.2017.5077.
   Web of Science ®Google Scholar
• EFSA (European Food Safety Authority). 2010. “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 8 (3): 1503. doi:10.2903/j.efsa.2010.1503.
   Google Scholar
• Ellis-Iversen, J., A. Ridley, V. Morris, A. Sowa, J. Harris, R. Atterbury, N. Sparks, and V. Allen. 2012. “Persistent Environmental Reservoirs on Farms as Risk Factors for Campylobacter in Commercial Poultry.” Epidemiology & Infection 140 (5): 916–924. doi:10.1017/S095026881100118X.
   PubMed Web of Science ®Google Scholar
• Fraqueza, M. J., A. Martins, A. C. Borges, M. H. Fernandes, M. J. Fernandes, Y. Vaz, R. J. Bessa, and A. S. Barreto. 2014. “Antimicrobial Resistance among Campylobacter Spp. Strains Isolated from Different Poultry Production Systems at Slaughterhouse Level.” Poultry Science 93 (6): 1578–1586. doi:10.3382/ps.2013-03729.
   PubMed Web of Science ®Google Scholar
• Georgiev, M., W. Beauvais, and J. Guitian. 2017. “Effect of Enhanced Biosecurity and Selected On-farm Factors on Campylobacter Colonization of Chicken Broilers.” Epidemiology & Infection 145 (3): 553–567. doi:10.1017/S095026881600251X.
   PubMed Web of Science ®Google Scholar
• Guerin, M. T., W. Martin, J. Reiersen, O. Berke, S. A. McEwen, J. R. Bisaillon, and R. Lowman. 2007. “A Farm-level Study of Risk Factors Associated with the Colonization of Broiler Flocks with Campylobacter Spp. In Iceland, 2001–2004.” Acta Veterinaria Scandinavica 49 (1): 18. doi:10.1186/1751-0147-49-18.
   PubMedGoogle Scholar
• Guerin, M. T., C. Sir, J. M. Sargeant, L. Waddell, A. M. O’Connor, R. W. Wills, R. H. Bailey, and J. A. Byrd. 2010. “The Change in Prevalence of Campylobacter on Chicken Carcasses during Processing: A Systematic Review.” Poultry Science 89 (5): 1070–1084. doi:10.3382/ps.2009-00213.
   PubMed Web of Science ®Google Scholar
• Hald, B., H. Skovgard, K. Pedersen, and H. Bunkenborg. 2008. “Influxed Insects as Vectors for Campylobacter Jejuni and Campylobacter Coli in Danish Broiler Houses.” Poultry Science 87 (7): 1428–1434. doi:10.3382/ps.2007-00301.
   PubMed Web of Science ®Google Scholar
• Hansson, I., M. Ederoth, L. Andersson, I. Vågsholm, and E. Olsson Engvall. 2005. “Transmission of Campylobacter Spp. To Chickens during Transport to Slaughter.” Journal of Applied Microbiology 99 (5): 1149–1157. doi:10.1111/j.1365-2672.2005.02689.x.
   PubMed Web of Science ®Google Scholar
• ISO 10272-1. 2017. Microbiology of the Food Chain - Horizontal Method for Detection and Enumeration of Campylobacter Spp. - Part 1: Detection Method. 2nd ed. Geneva, Switzerland: International Organisation for Standardisation (ISO).
   Google Scholar
• ISO 16140-2. 2016. Microbiology of the Food Chain - Method Validation - Part 2: Protocol for the Validation of Alternative (Proprietary) Methods against a Reference Method. Geneva, Switzerland: International Organisation for Standardisation (ISO).
   Google Scholar
• Lawes, J. R., A. Vidal, F. A. Clifton-Hadley, R. Sayers, J. Rodgers, L. Snow, S. J. Evans, and L. F. Powell. 2012. “Investigation of Prevalence and Risk Factors for Campylobacter in Broiler Flocks at Slaughter: Results from a UK Survey.” Epidemiology & Infection 140 (10): 1725–1737. doi:10.1017/S0950268812000982.
   PubMed Web of Science ®Google Scholar
• McCrea, B. A., K. H. Tonooka, C. VanWorth, C. L. Boggs, E. R. Atwill, and J. S. Schrader. 2006. “Prevalence of Campylobacter and Salmonella Species on Farm, after Transport, and at Processing in Specialty Market Poultry.” Poultry Science 85 (1): 136–143. doi:10.1093/ps/85.1.136.
   PubMed Web of Science ®Google Scholar
• Northcutt, J. K., R. J. Buhr, M. E. Berrang, and D. L. Fletcher. 2003. “Effects of Replacement Finisher Feed and Length of Feed Withdrawal on Broiler Carcass Yield and Bacteria Recovery.” Poultry Science 82 (11): 1820–1824. doi:10.1093/ps/82.11.1820.
   PubMed Web of Science ®Google Scholar
• Pauwels, J., B. Taminiau, G. P. Janssens, M. De Beenhouwer, L. Delhalle, G. Daube, and F. Coopman. 2015. “Cecal Drop Reflects the Chickens’ Cecal Microbiome, Fecal Drop Does Not.” Journal of Microbiological Methods 117: 164–170. doi:10.1016/j.mimet.2015.08.006.
   PubMed Web of Science ®Google Scholar
• Pearson, A. D., M. Greenwood, T. D. Healing, D. Rollins, M. Shahamat, J. Donaldson, and R. R. Colwell. 1993. “Colonization of Broiler Chickens by Waterborne Campylobacter Jejuni.” Applied and Environmental Microbiology 59 (4): 987–996. doi:10.1128/AEM.59.4.987-996.1993.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2018. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
   Google Scholar
• Rasschaert, G., K. Houf, and L. De Zutter. 2007. “External Contamination of Campylobacter-free Flocks after Transport in Cleaned and Disinfected Containers.” Journal of Food Protection 70 (1): 40–46. doi:10.4315/0362-028X-70.1.40.
   PubMed Web of Science ®Google Scholar
• Ridley, A., V. Morris, J. Gittins, S. Cawthraw, J. Harris, S. Edge, and V. Allen. 2011. “Potential Sources of Campylobacter Infection on Chicken Farms: Contamination and Control of Broiler-harvesting Equipment, Vehicles and Personnel.” Journal of Applied Microbiology 111 (1): 233–244. doi:10.1111/j.1365-2672.2011.05038.x.
   PubMed Web of Science ®Google Scholar
• Seliwiorstow, T., J. Baré, D. Berkvens, I. Van Damme, M. Uyttendaele, and L. De Zutter. 2016. “Identification of Risk Factors for Campylobacter Contamination Levels on Broiler Carcasses during the Slaughter Process.” International Journal of Food Microbiology 226: 26–32. doi:10.1016/j.ijfoodmicro.2016.03.010.
   PubMed Web of Science ®Google Scholar
• Slader, J., G. Domingue, F. Jorgensen, K. McAlpine, R. J. Owen, F. J. Bolton, and T. J. Humphrey. 2002. “Impact of Transport Crate Reuse and of Catching and Processing on Campylobacter and Salmonella Contamination of Broiler Chickens.” Applied and Environmental Microbiology 68 (2): 713–719. doi:10.1128/AEM.68.2.713-719.2002.
   PubMed Web of Science ®Google Scholar
• Smith, S., L. L. Messam, J. Meade, J. Gibbons, K. McGill, D. Bolton, and P. Whyte. 2016. “The Impact of Biosecurity and Partial Depopulation on Campylobacter Prevalence in Irish Broiler Flocks with Differing Levels of Hygiene and Economic Performance.” Infection Ecology & Epidemiology 6: 31454. doi:10.3402/iee.v6.31454.
   PubMedGoogle Scholar
• Sparks, N. H. C. 2009. “The Role of the Water Supply System in the Infection and Control of Campylobacter in Chicken.” World’s Poultry Science Journal 65 (3): 459–474. doi:10.1017/S0043933909000324.
   Web of Science ®Google Scholar
• Stafford, R. J., P. Schluter, M. Kirk, A. Wilson, L. Unicomb, R. Ashbolt, and J. Gregory. 2007. “A Multi-centre Prospective Case-control Study of Campylobacter Infection in Persons Aged 5 Years and Older in Australia.” Epidemiology & Infection 135 (6): 978–988. doi:10.1017/S0950268806007576.
   PubMed Web of Science ®Google Scholar
• Stafford, R. J., P. J. Schluter, A. J. Wilson, M. D. Kirk, G. Hall, and L. Unicomb. 2008. “Population-attributable Risk Estimates for Risk Factors Associated with Campylobacter Infection, Australia.” Emerging Infectious Diseases 14 (6): 895–901. doi:10.3201/eid1406.071008.
   PubMed Web of Science ®Google Scholar
• Stern, N. J., M. R. Clavero, J. S. Bailey, N. A. Cox, and M. C. Robach. 1995. “Campylobacter Spp. In Broilers on the Farm and after Transport.” Poultry Science 74 (6): 937–941. doi:10.3382/ps.0740937.
   PubMed Web of Science ®Google Scholar
• Tam, C. C., C. D. Higgins, K. R. Neal, L. C. Rodrigues, S. E. Millership, and S. J. O’Brien. 2009. “Chicken Consumption and Use of Acid-suppressing Medications as Risk Factors for Campylobacter Enteritis, England.” Emerging Infectious Diseases 15 (9): 1402–1408. doi:10.3201/eid1509.080773.
   PubMed Web of Science ®Google Scholar
• Torralbo, A., C. Borge, A. Allepuz, I. Garcia-Bocanegra, S. K. Sheppard, A. Perea, and A. Carbonero. 2014. “Prevalence and Risk Factors of Campylobacter Infection in Broiler Flocks from Southern Spain.” Preventive Veterinary Medicine 114 (2): 106–113. doi:10.1016/j.prevetmed.2014.01.019.
   PubMed Web of Science ®Google Scholar
• Venables, W. N., and B. D. Ripley. 2002. Modern Applied Statistics with S. 4 ed. New York: Springer-Verlag.
   Google Scholar
• Vondrakova, L., J. Pazlarova, and K. Demnerova. 2014. “Detection, Identification and Quantification of Campylobacter Jejuni, Coli and Lari in Food Matrices All at once Using Multiplex qPCR.” Gut Pathogens 6: 12. doi:10.1186/1757-4749-6-12.
   PubMed Web of Science ®Google Scholar
• Whyte, P., J. D. Collins, K. McGill, C. Monahan, and H. O’Mahony. 2001. “The Effect of Transportation Stress on Excretion Rates of Campylobacters in Market-age Broilers.” Poultry Science 80 (6): 817–820. doi:10.1093/ps/80.6.817.
   PubMed Web of Science ®Google Scholar
• Yamazaki-Matsune, W., M. Taguchi, K. Seto, R. Kawahara, K. Kawatsu, Y. Kumeda, M. Kitazato, M. Nukina, N. Misawa, and T. Tsukamoto. 2007. “Development of a Multiplex PCR Assay for Identification of Campylobacter Coli, Campylobacter Fetus, Campylobacter Hyointestinalis Subsp. Hyointestinalis, Campylobacter Jejuni, Campylobacter Lari and Campylobacter Upsaliensis.” Journal of Medical Microbiology 56: 1467–1473. doi:10.1099/jmm.0.47363-0.
   PubMed Web of Science ®Google Scholar