Campylobacter and Arcobacter species in food-producing animals: prevalence at primary production and during slaughter

  • Nompumelelo Shange
  • Pieter GouwsEmail author
  • Louwrens C. Hoffman


The Campylobacter and Arcobacter genera encompass closely related species that are ubiquitous in nature and are harboured in the gastrointestinal tract of many animals, including food-producing animals (cattle, sheep, pigs and poultry). In humans Campylobacter spp. is the cause of most of the gastroenteritis cases worldwide and in more severe cases the infection can result in Guillian Barré syndrome. Similarly, Arcobacter species can cause gastroenteritis as well as bacteraemia. Infections in humans can be induced by the consumption of contaminated vegetables, meat, milk and water. However, food originating from animals, especially meat, has been recognised as a source of infection, in fact, poultry meat and meat products have been globally reported as the main source of infection. It is clear that food-producing animals are important reservoirs for Campylobacter and Arcobacter species, which implies successful colonisation of the gastrointestinal tract at primary production and contamination during the slaughter process. During slaughter the evisceration step has been recognised as the most likely point of contamination, as accidental spillage of intestinal fluid and rapture of gastrointestinal tract can occur. Therefore, improper hygienic practices can ultimately allow for the contamination of finished/retail products intended for human consumption. This literature review will seek to explore the infection of food-producing animals with Campylobacter and Arcobacter species at primary production and contamination during the slaughter of food-producing animals.


Arcobacter species Contamination Campylobacter species Food-producing animals Primary production Slaughter process 



This work is based on the research supported by the South African Research Chairs Initiative (SARChI) and partly funded by the South African Department of Science and Technology (UID Number: 84633), as administered by the National Research Foundation (NRF) of South Africa and partly by the Department of Trade and Industry’s THRIP program (THRIP/64/19/04/2017) with Stellenbosch University as partner. Any opinions, findings and conclusions or recommendations expressed in this material are that of the author(s) and the National Research Foundation does not accept any liability in this regard.


  1. Allos BM, Lastovica AJ (2011) Campylobacter infections. In: Guerrant RL, Walker DH, Weller PF (ed) Tropical infectious diseases: principles, pathogens and practise, 3rd edn. Saunders/Elsevier, PhiladelphiaGoogle Scholar
  2. Arun AI, Irshad TS (2013) Scalding and its significance in livestock slaughter and wholesome meat production. Int J Livest Res 3:45–53Google Scholar
  3. Atabay HI, Wainø M, Madsen M (2006) Detection and diversity of various Arcobacter species in Danish poultry. Int J Food Microbiol 109:139–145. CrossRefPubMedGoogle Scholar
  4. Avrain L, Allain L, Vernozy-Rozand C, Kempf I (2003) Disinfectant susceptibility testing of avian and swine Campylobacter isolates by a filtration method. Vet Microbiol 96:35–40. CrossRefPubMedGoogle Scholar
  5. Balogu TV, Nwaugo VO, Onyeagba RA (2014) Persistence and biofilm assessment of Campylobacter jejuni in poultry abattoir. Niger Food J 32:54–61. CrossRefGoogle Scholar
  6. Banting G, Figueras SMJ (2017) Part three. Specific excreted pathogens: environmental and Epidemiology aspects. Accessed 8 Aug 2018
  7. Berrang ME, Dickens JA (2000) Presence and level of Campylobacter spp. on broiler carcasses throughout the processing plant. J Appl Poult Res 9:43–47. CrossRefGoogle Scholar
  8. Bily L, Petton J, Lalande F, Rouxel S, Denis M, Chemaly M, Salvat G, Fravalo P (2010) Quantitative and qualitative evaluation of Campylobacter spp. contamination of turkey cecal contents and carcasses during and following the slaughtering process. J Food Prot 73:1212–1218. CrossRefPubMedGoogle Scholar
  9. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ (1988) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157:472–479. CrossRefPubMedGoogle Scholar
  10. Bogantes EV, Fallas-Padilla KL, Rodríguez-Rodríguez CE, Jaramillo HF, Echandi MLA (2015) Zoonotic Species of the genus Arcobacter in poultry from different regions of Costa Rica. J Food Prot 78:808–811. CrossRefPubMedGoogle Scholar
  11. Bolton DJ, Pearce RA, Sheridan JJ, Blair IS, McDowell DA, Harrington D (2002) Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. J Appl Microbiol 92:893–902. CrossRefPubMedGoogle Scholar
  12. Bouwknegt M, Van De Giessen AW, Dam-Deisz WDC, Havelaar AH, Nagelkerke NJD, Henken AM (2004) Risk factors for the presence of Campylobacter spp. in Dutch broiler flocks. Prev Vet Med 62:35–49. CrossRefPubMedGoogle Scholar
  13. Bratz K, Bücker R, Gölz G, Zakrzewski SS, Janczyk P, Nöckler K, Alter T (2013) Experimental infection of weaned piglets with Campylobacter coli - Excretion and translocation in a pig colonisation trial. Vet Microbiol 162:136–143. CrossRefPubMedGoogle Scholar
  14. Callicott KA, Frioriksdóttir V, Reiersen J, Lowman R, Bisaillon JR, Gunnarsson E, Berndtson E, Hiett KL, Needleman DS, Stern NJ (2006) Lack of evidence for vertical transmission of Campylobacter spp. in chickens. Appl Environ Microbiol 72:5794–5798. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Carrique-Mas JJ, Bryant JE, Cuong NV et al (2014) An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiol Infect 142:1425–1436. CrossRefPubMedGoogle Scholar
  16. Çelİk E, Sağlam AG, Çelebİ Ö, Otlu S (2018) Isolation of Arcobacter spp. from domestic ducks and geese and identification of the recovered isolates by using molecular method. Turk J Vet Anim Sci 42:1–6. CrossRefGoogle Scholar
  17. Červenka L, Malíková Z, Zachová I, Vytřasová J (2004) The effect of acetic acid, citric acid, and trisodium citrate in combination with different levels of water activity on the growth of Arcobacter butzleri in culture. Folia Microbiol 49:8–12. CrossRefGoogle Scholar
  18. Chokboonmongkol C, Patchanee P, Gölz G, Zessin KH, Alter T (2013) Prevalence, quantitative load, and antimicrobial resistance of Campylobacter spp. from broiler ceca and broiler skin samples in Thailand. Poult Sci 92:462–467. CrossRefPubMedGoogle Scholar
  19. Collado L, Figueras MJ (2011) Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 24:174–192. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Colles FM, Dingle KE, Cody AJ, Maiden MCJ (2008a) Comparison of Campylobacter populations in wild geese with those in starlings and free-range poultry on the same farm. Appl Environ Microbiol 74:3583–3590CrossRefGoogle Scholar
  21. Colles FM, Jones TA, McCarthy ND, Sheppard SK et al (2008b) Campylobacter infection of broiler chickens in a free-range environment. Environ Microbiol 10:2042–2050CrossRefGoogle Scholar
  22. Córdoba-Calderón O, Redondo-Solano M, Castro-Arias E, Arias-EchandI ML (2017) Arcobacter isolation from minced beef samples in Costa Rica. J Food Prot 80:775–778CrossRefGoogle Scholar
  23. CoşAnsu S, 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. J Food Process Pres 34:98–113CrossRefGoogle Scholar
  24. Cox ANA, Stern NJ, Wilson JL, Musgrove MT, Buhr RJ (2002) Isolation of Campylobacter spp. from semen samples of commercial broiler breeder roosters. Avian Dis 46:717–720CrossRefGoogle Scholar
  25. De Smet S, De Zutter L, Debruyne L, Vangroenweghe F, Vandamme P, Houf K (2011a) Arcobacter population dynamics in pigs on farrow-to-finish farms. Appl Environ Microbiol 77:1732–1738CrossRefGoogle Scholar
  26. De Smet S, De Zutter L, Van Hende J, Houf K (2010) Arcobacter contamination on pre- and post-chilled bovine carcasses and in minced beef at retail. J Appl Microbiol 108:299–305. CrossRefPubMedGoogle Scholar
  27. De Smet S, Vandamme P, De Zutter L, On SLW, Douidah L, Houf K (2011) Ar cobacter trophiarum sp. nov., isolated from fattening pigs. Int J Syst Evol Microbiol 61:356–361. CrossRefPubMedGoogle Scholar
  28. Dekker D, Eibach D, Boahen KG, Akenten CW, Pfeifer Y, Zautner AE, Mertens E, Krumkamp R, Jaeger A, Flieger A, Owusu-Dabo E, May J (2019) Fluoroquinolone-Resistant Salmonella enterica, Campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog Dis 16:1–7. CrossRefGoogle Scholar
  29. Denis M, Henrique E, Chidaine B, Tircot A, Bougeard S, Fravalo P (2011) Campylobacter from sows in farrow-to-finish pig farms: risk indicators and genetic diversity. Vet Microbiol 154:163–170. CrossRefPubMedGoogle Scholar
  30. Díaz-Sánchez S, Moriones AM, Casas F, Höfle U (2004) Prevalence of Escherichia coli, Salmonella sp. and Campylobacter sp. in the intestinal flora of farm-reared, restocked and wild red-legged partridges (Alectoris rufa): Is restocking using farm-reared birds a risk? Eur J Wildl Res 3:129–134. CrossRefGoogle Scholar
  31. Dipineto L, Gargiulo A, Bossa LMDL, Cuomo A, Santaniello A, Sensale M, Menna LF, Fioretti A (2008) Survey of thermotolerant Campylobacter in pheasant (Phasianus colchicus). Ital J Anim Sci 7:401–403. CrossRefGoogle Scholar
  32. Duffy LL, Osmond-McLeod MJ, Judy J, King T (2018) Investigation into the antibacterial activity of silver, zinc oxide and copper oxide nanoparticles against poultry-relevant isolates of Salmonella and Campylobacter. Food Control 92:293–300. CrossRefGoogle Scholar
  33. EFSA (2011) Scientific Opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J 9:1–141. CrossRefGoogle Scholar
  34. Eifert JD, Castle RM, Pierson FW, Larsen CT, Hackney CR (2003) Comparison of sampling techniques for detection of Arcobacter butzleri from chickens. Poult Sci 82:1898–1902. CrossRefPubMedGoogle Scholar
  35. Elmali M, Can HY (2016) Occurence and antimicrobial resistance of Arcobacter species in food and slaughterhouse samples. Food Sci Technol 37:280–285. CrossRefGoogle Scholar
  36. Enokimoto M, Kubo M, Bozono Y, Mieno Y, Misawa N (2007) Enumeration and identification of Campylobacter species in the liver and bile of slaughtered cattle. Int J Food Microbiol 118:259–263. CrossRefPubMedGoogle Scholar
  37. Evans SJ, Sayers AR (2000) A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Prev Vet Med 46:209–223. CrossRefPubMedGoogle Scholar
  38. Federighi M (2017) How to control Campylobacter in poultry farms?: an overview of the main strategies. In: Manafi M, Poult Science. InTechOpen, CroatiaGoogle Scholar
  39. Fernandez H, Villanueva MP, Mansilla I, Gonzalez M, Latif F (2015) Arcobacter butzleri and A. cryaerophilus in human, animals and food sources, in southern Chile. Braz J Microbiol 46:145–147CrossRefGoogle Scholar
  40. Figueroa G, Troncoso M, Ĺopez C, Rivas P, Toro M (2009) Occurrence and enumeration of Campylobacter spp. during the processing of Chilean broilers. BMC Microbiol 9:1–6. CrossRefGoogle Scholar
  41. Food Standards Australia New Zealand (2013) Assessment of microbiological hazards associated with the four main meat species. Accessed 15 Feb 2017
  42. Giacometti F, Lucchi A, Di Francesco A, Delogu M, Grilli E, Guarniero I, Stancampiano L, Manfreda G, Merialdi G, Serraino A (2015) Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii circulation in a dairy farm and sources of milk contamination. Appl Environ Microbiol 81:5055–5063. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Gill CO, Harris LM (1982) Contamination of red-meat carcasses by Campylobacter fetus subsp. jejuni. Appl Environ Microbiol 43:977–980PubMedPubMedCentralGoogle Scholar
  44. González M, Mikkelä A, Tuominen P, Ranta J, Hakkinen M, Hänninen M, Llarena A (2016) Risk assessment of Campylobacter spp. in Finland. Accessed 8 Feb 2017
  45. Gormley FJ, Bailey RA, Watson KA, McAdam J, Avendaño S, Stanley WA, Koerhuis ANM (2014) Campylobacter colonization and proliferation in the broiler chicken upon natural field challenge is not affected by the bird growth rate or breed. Appl Environ Microbiol 80:6733–6738CrossRefGoogle Scholar
  46. Gouws PA, Shange N, Hoffman LC (2017) Microbial quality of springbok (Antidorcas marsupialis) meat in relation to harvesting and production process. In: Paulsen P, Bauer A, Smulders FJM (ed) Game meat hygiene: food safety and security.Academic Publishers, WageningenGoogle Scholar
  47. Grau FH (1988) Campylobacter jejuni and Campylobacter hyointestinalis in the intestinal tract and on the carcasses of calves and cattle. J Food Prot 51:857–861. CrossRefPubMedGoogle Scholar
  48. Grove-White DH, Leatherbarrow AJH, Cripps PJ, Diggle PJ, French NP (2014) Temporal and farm-management-associated variation in faecal pat prevalence of Arcobacter spp. in ruminants. Epidemiol Infect 142:861–870CrossRefGoogle Scholar
  49. Gwimi PB, Faleke OO, Salihu MD, Magaji AA, Abubakar MB, Nwankwo IO, Ibitoye EB (2015) Prevalence of Campylobacter species in fecal samples of pigs and humans from Zuru Kebbi State, Nigeria. Int J One Health 1:1–5CrossRefGoogle Scholar
  50. Hald T, Aspinall W, Devleesschauwer B, Cooke R, Corrigan T, Havelaar AH, Gibb HJ, Torgerson PR, Kirk MD, Angulo FJ, Lake RJ, Speybroeck N, Hoffmann S (2016) World Health Organization estimates of the relative contributions of food to the burden of disease due to selected foodborne hazards: A structured expert elicitation. PLoS ONE 11:1–35. CrossRefGoogle Scholar
  51. Hamidi K (2018) How do Rodents play role in transmission of foodborne diseases? Int J Food Sci Nutr 6:10–13CrossRefGoogle Scholar
  52. Haruna M, Sasaki Y, Murakami M, Mori T, Asai T, Ito K, Yamada Y (2013) Prevalence and antimicrobial resistance of Campylobacter isolates from beef cattle and pigs in Japan. J Vet Med Sci 75:625–628CrossRefGoogle Scholar
  53. Hassan AK (2017) Detection and identification of Arcobacter species in poultry in Assiut Governorate, Upper Egypt. J Adv Vet Res 7:53–58CrossRefGoogle Scholar
  54. Ho HTK, Lipman LJA, Gaastra W (2008) The introduction of Arcobacter spp. in poultry slaughterhouses. Int J Food Microbiol 125:223–229. CrossRefPubMedGoogle Scholar
  55. Ho TKH, Lipman LJA, Van Der Graaf-Van Bloois L, Van Bergen M, Gaastra W (2006) Potential routes of acquisition of Arcobacter species by piglets. Vet Microbiol 114:123–133CrossRefGoogle Scholar
  56. Horrocks SM, Anderson RC, Nisbet DJ, Ricke SC (2009) Incidence and ecology of Campylobacter jejuni and coli in animals. Anaerobe 15:18–25CrossRefGoogle Scholar
  57. Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N, Kipar A, Humphrey T, Wigley P (2014) Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. mBio 5:1–7. CrossRefGoogle Scholar
  58. Humphrey T, O’Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: A food production perspective. Int J Food Microbiol 117:237–257. CrossRefPubMedGoogle Scholar
  59. Johnsen G, Zimmerman K, Lindstedt BA, Vardund T, Herikstad H, Kapperud G (2006) Intestinal carriage of Campylobacter jejuni and Campylobacter coli among cattle from South Western Norway and comparative genotyping of bovine and human isolates by amplified-fragment length polymorphism. Acta Vet Scand 48:4–9. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM (2015) Global epidemiology of Campylobacter infection. Clin Microbiol Rev 28:687–720. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kalupahana RS, Kottawatta SA, Somarathne S (2018) Weather correlates of Campylobacter prevalence in broilers at slaughter under tropical conditions in Sri Lanka. Epidemiol infect 56:1–8. CrossRefGoogle Scholar
  62. Karikari AB, Obiri-Danso K, Frimpong EH, Krogfelt KA (2017) Antibiotic resistance of Campylobacter recovered from faeces and carcasses of healthy livestock. Biomed Res Int 2017:1–9. CrossRefGoogle Scholar
  63. Keener KM, Bashor MP, Curtis PA, Sheldon BW, Kathariou S (2004) Comprehensive review of Campylobacter and poultry processing. Compr Rev Food Sci Food Saf 3:105–116. CrossRefGoogle Scholar
  64. Khoshbakht R, Tabatabaei M, Shirzad Aski H, Seifi S (2014) Occurrence of Arcobacter in Iranian poultry and slaughterhouse samples implicates contamination by processing equipment and procedures. Br Poult Sci 55:732–736. CrossRefPubMedGoogle Scholar
  65. King T, Osmond-McLeod MJ, Duffy LL (2018) Nanotechnology in the food sector and potential applications for the poultry industry. Trends Food Sci Technol 72:62–73. CrossRefGoogle Scholar
  66. Lastovica AJ, On LW, Zhang L (2014) The family Campylobacteraceae. In: Rosenberg E et al (ed) The prokaryotes-Deltaproteobacteria and Epsilonproteobacteria. Springer, BerlinGoogle Scholar
  67. Lindmark H, Diedrich IC, Andersson L, Lindqvist R, Engvall EO (2006) Distribution of Campylobacter genotypes on broilers during slaughter. J food Prot 69:2902–2907. CrossRefPubMedGoogle Scholar
  68. Ling YE, Aziz SA, Abu J (2011) Occurrence of Campylobacter and Salmonella spp. in Ostrich. J Vet Malaysia 24:6–8Google Scholar
  69. Lipman L, Ho H, Gaastra W (2008) The presence of Arcobacter species in breeding hens and eggs from these hens. Poult Sci 87:2404–2407. CrossRefPubMedGoogle Scholar
  70. Louwen R, van Baarlen P, van Vliet AHM, van Belkum A, Hays JP, Endtz HP (2012) Campylobacter bacteremia: A rare and under-reported event? Eur J Microbiol Immunol 2:76–87. CrossRefGoogle Scholar
  71. Luber P, Brynestad S, Topsch D, Scherer K, Bartelt E (2006) Quantification of Campylobacter species cross-contamination during handling of contaminated fresh chicken parts in kitchens. Appl Environ Microbiol 72:66–70. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Luque I, Tarradas C, Herrera-León S, Gómez-Laguna J, Hernández M, Maldonado A, Astorga RJ, Morales-Partera AM, Cardoso-Toset F (2018) Prevalence and diversity of Salmonella spp., Campylobacter spp., and Listeria monocytogenes in two free-range pig slaughterhouses. Food Control 92:208–215. CrossRefGoogle Scholar
  73. Maramski A (2012) Prevalence of Campylobacter spp. in pig Slaughter carcasses during the processing. Trakia J Sci 10:62–67Google Scholar
  74. Maridor ML, Denis M, Lalande F et al (2008) Experimental infection of specific pathogen-free pigs with Campylobacter: excretion in faeces and transmission to non-inoculated pigs. Vet Microbiol 131:309–317. CrossRefGoogle Scholar
  75. Merga JY, Williams NJ, Miller WG, Leatherbarrow AJH, Bennett M, Hall N, Ashelford KE, Winstanley C (2013) Exploring the diversity of Arcobacter butzleri from cattle in the UK using MLST and whole genome sequencing. PLoS ONE 8:1–12. CrossRefGoogle Scholar
  76. Mohan HV, Rathore RS, Dhama K et al (2014) Prevalence of Arcobacter spp. in humans, animals and foods of animal origin in India based on cultural isolation, antibiogram, PCR and multiplex PCR detection. Asian J Anim Vet Adv 9:452–466. CrossRefGoogle Scholar
  77. Newell DG, Elvers KT, Dopfer D, Hansson I, Jones P, James S, Gittins J, Stern NJ, Davies R, Connerton I, Pearson D, Salvat Allen VM (2011) Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol 77:8605–8614. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Oporto B, Esteban JI, Aduriz G, Juste RA, Hurtado A (2007) Prevalence and strain diversity of thermophilic Campylobacters in cattle, sheep and swine farms. J Appl Microbiol 103:977–984. CrossRefPubMedGoogle Scholar
  79. Osiriphun S, Iamtaweejaloen P, Kooprasertying P, Koetsinchai W, Tuitemwong K, Erickson LE, Tuitemwong P (2011) Exposure assessment and process sensitivity analysis of the contamination of Campylobacter in poultry products. Poult Sci 90:1562–1573. CrossRefPubMedGoogle Scholar
  80. Padungtod P, Kaneene JB (2005) Campylobacter in food animals and humans in Northern Thailand. J Food Prot 68:2519–2526. CrossRefPubMedGoogle Scholar
  81. Park SF (2002) The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 74:177–188. CrossRefPubMedGoogle Scholar
  82. Pearce RA, Wallace FM, Call JE, Dudley RL, Oser A, Yoder L, Sheridan JJ, Luchansky JB (2003) Prevalence of Campylobacter within a swine slaughter and processing facility. J Food Prot 66:1550–1556. CrossRefPubMedGoogle Scholar
  83. Percivalle E, Monzillo V, Pauletto A, Marone P, Imberti R (2016) Colistin inhibits E. coli O157:H7 Shiga-like toxin release, binds endotoxins and protects Vero cells. New Microbiol 39:119–123. CrossRefPubMedGoogle Scholar
  84. Perko-Mäkelä P, Isohanni P, Katzav M, Lund M, Hänninen ML, Lyhs U (2009) A longitudinal study of Campylobacter distribution in a turkey production chain. Acta Vet Scand 51:1–10. CrossRefGoogle Scholar
  85. Peyrat MB, Soumet C, Maris P, Sanders P (2008) Phenotypes and genotypes of Campylobacter strains isolated after cleaning and disinfection in poultry slaughterhouses. Vet Microbiol 128:313–326. CrossRefPubMedGoogle Scholar
  86. Prince Milton AA, Agarwal RK, Priya GB et al (2017) Prevalence of Campylobacter jejuni and Campylobacter coli in captive wildlife species in India. Iranian J Vet Res 18:177–182. CrossRefGoogle Scholar
  87. Ramonaitė S, Rokaitytė A, Tamulevičienė E, Malakauskas A, Alter T, Malakauskas M (2013) Prevalence, quantitative load and genetic diversity of Campylobacter spp. in dairy cattle herds in Lithuania. Acta Vet Scand 55:87. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Rasschaert G, Houf K, Van Hende J, De Zutter L (2006) Campylobacter contamination during poultry slaughter in Belgium. J Food Prot 69:27–33. CrossRefPubMedGoogle Scholar
  89. Reich F, Atanassova V, Haunhorst E, Klein G (2008) The effects of Campylobacter numbers in caeca on the contamination of broiler carcasses with Campylobacter. Int J Food Microbiol 127:116–120. CrossRefPubMedGoogle Scholar
  90. Ridley AM, Morris VK, Cawthraw SA, Ellis-Iversen J, Harris JA, Kennedy EM, Newell DG, Allen VM (2011) Longitudinal molecular epidemiological study of thermophilic Campylobacters on one conventional broiler chicken farm. Appl Environ Microbiol 77:98–107. CrossRefPubMedGoogle Scholar
  91. Rosenquist H, Sommer HM, Nielsen NL, Christensen BB (2006) The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter. Int J Food Microbiol 108:226–232. CrossRefPubMedGoogle Scholar
  92. Rotariu O, Dallas JF, Ogden ID et al (2009) Spatiotemporal homogeneity of Campylobacter subtypes from cattle and sheep across North Eastern and South Western Scotland. Appl Environ Microbiol 75:6275–6281. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Sahin O, Kassem II, Shen Z, Lin J, Rajashekara G, Zhang Q (2015) Campylobacter in poultry: Ecology and potential interventions. Avian Dis 59:185–200. CrossRefPubMedGoogle Scholar
  94. Sahin O, Kobalka P, Zhang Q (2003) Detection and survival of Campylobacter in chicken eggs. J Appl Microbiol 95:1070–1079. CrossRefPubMedGoogle Scholar
  95. Samie A, Obi CL, Barrett LJ, Powell SM, Guerrant RL (2007) Prevalence of Campylobacter species, Helicobacter pylori and Arcobacter species in stool samples from the Venda region, Limpopo, South Africa: studies using molecular diagnostic methods. J Infect 54:558–566. CrossRefPubMedGoogle Scholar
  96. Schets FM, Jacobs-Reitsma WF, Van der Plaats RQJ et al (2017) Prevalence and types of Campylobacter on poultry farms and in their direct environment. J Water Health 15:849–862. CrossRefPubMedGoogle Scholar
  97. Seguino A, Chintoan-Uta C (2017) Campylobacter spp. carriage in wild game pheasants (Phasianus colchicus) in Scotland and its relevance to public health. In: Paulsen P, Bauer A, Smulders FJM (ed) Game meat hygiene: Food safety and security. Academic Publishers, WageningenGoogle Scholar
  98. Seliwiorstow T, Baré J, Van Damme I, Uyttendaele M, De Zutter L (2015) Campylobacter carcass contamination throughout the slaughter process of Campylobacter-positive broiler batches. Int J Food Microbiol 194:25–31. CrossRefPubMedGoogle Scholar
  99. Semaan EH, Dib H, Mrad R, Chami C, Jalkh R (2014) Dynamic of Campylobacter species contamination along a poultry slaughtering chain. Ital J Food Saf 3:185–187. CrossRefGoogle Scholar
  100. Shirzad Aski H, Tabatabaei M, Khoshbakht R, Raeisi M (2016) Occurrence and antimicrobial resistance of emergent Arcobacter spp. isolated from cattle and sheep in Iran. Comp Immunol Microbiol Infect Dis 44:37–40. CrossRefPubMedGoogle Scholar
  101. Sibanda N, McKenna A, Richmond A, Ricke SC, Callaway T, Stratakos AC, Gundogdu OC (2004) A Review of the effect of management practices on Campylobacter prevalence in poultry farms. Int J Poult Sci 3:129–134. CrossRefGoogle Scholar
  102. Skarp CPA, Hänninen ML, Rautelin HIK (2016) Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 22:103–109. CrossRefPubMedGoogle Scholar
  103. Snelling WJ, Matsuda M, Moore JE, Dooley JSG (2005) Under the microscope: Campylobacter jejuni. Lett Appl Microbiol 41:297–302. CrossRefPubMedGoogle Scholar
  104. Son I, Englen MD, Berrang ME, Fedorka-Cray PJ, Harrison MA (2007) Prevalence of Arcobacter and Campylobacter on broiler carcasses during processing. Int J Food Microbiol 113:16–22. CrossRefGoogle Scholar
  105. Sproston EL, Ogden ID, MacRae M et al (2011) Temporal variation and host association in the Campylobacter population in a longitudinal ruminant farm study. Appl Environ Microbiol 77:6579–6586. CrossRefPubMedPubMedCentralGoogle Scholar
  106. Stanley K, Jones K (2003) Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol 94:104S–113S. CrossRefPubMedGoogle Scholar
  107. Stanley KN, Wallace JS, Currie JE, Diggle PJ, Jone K (1998) The seasonal variation of thermophilic Campylobacters in beef cattle, dairy cattle and calves. J Appl Microbiol 85:472–480. CrossRefPubMedGoogle Scholar
  108. Stephens CP, On SLW, Gibson JA (1998) An outbreak of infectious hepatitis in commercially reared ostriches associated with Campylobacter coli and Campylobacter jejuni. Vet Microbiol 61:183–190. CrossRefPubMedGoogle Scholar
  109. Thépault A, Poezevara T, Quesne S, Rose V, Chemaly M, Rivoal K (2018) Prevalence of thermophilic Campylobacter in cattle production at slaughterhouse level in France and link between C. jejuni bovine strains and Campylobacteriosis. Front Microbiol 9:1–9. CrossRefGoogle Scholar
  110. Umar S, Maiyah AT, Mushtaq A (2016) Campylobacter infections in poultry: Update on challenges and potential immune interventions. Worlds Poult Sci J 72:381–390. CrossRefGoogle Scholar
  111. Van Driessche E, Houf K (2007a) Discrepancy between the occurrence of Arcobacter in chickens and broiler carcass contamination. Poult Sci 86:744–751. CrossRefPubMedGoogle Scholar
  112. Van Driessche E, Houf K (2007b) Characterization of the Arcobacter contamination on Belgian pork carcasses and raw retail pork. Int J Food Microbiol 118:20–26. CrossRefPubMedGoogle Scholar
  113. Van Driessche E, Houf K, Vangroenweghe F, De Zutter L, Van Hoof J (2005) Prevalence, enumeration and strain variation of Arcobacter species in the faeces of healthy cattle in Belgium. Vet Microbiol 105:149–154. CrossRefPubMedGoogle Scholar
  114. Van Driessche E, Houf K, Vangroenweghe F, Nollet N, De Zutter L, Vandamme P, Van Hoof J (2004) Occurrence and strain diversity of Arcobacter species isolated from healthy Belgian pigs. Res Microbiol 155:662–666. CrossRefPubMedGoogle Scholar
  115. Vandenberg O, Dediste A, Houf K, Ibekwem S, Souayah H, Cadranel S, Douat N, Zissis G, Butzler J (2004) Arcobacter species in humans. Emerg Infect Dis 10:1863–1867. CrossRefPubMedPubMedCentralGoogle Scholar
  116. Vandeplas S, Marcq C, Dauphin RD, Beckers Y, Thonart P, Théwis A (2008) Contamination of poultry flocks by the human pathogen Campylobacter spp. and strategies to reduce its prevalence at the farm level. Biotechnol Agron Soc Environ 12:317–334Google Scholar
  117. Wagenaar JA, Mevius DJ, Havelaar AH (2006) Campylobacter in primary animal production and control strategies to reduce the burden of human Campylobacteriosis. Rev Sci Tech 25:581–594. CrossRefPubMedGoogle Scholar
  118. Weber R, Auerbach M, Jung A, Glünder G (2014) Campylobacter infections in four poultry species in respect of frequency, onset of infection and seasonality. Berl Münch tierärztl Wochenschr 127:257–266. CrossRefPubMedGoogle Scholar
  119. Wesley IV, Baetz AL (1996) Natural and experimental infections of Arcobacter in poultry. Poult Sci 78:536–545. CrossRefGoogle Scholar
  120. Whyte P, Collins JD, McGill K, Monahan C, O’Mahony H (2001) The effect of transportation stress on excretion rates of Campylobacters in market-age broilers. Poult Sci 80:817–820. CrossRefPubMedGoogle Scholar
  121. Wieczorek K, Denis E, Osek J (2009) Occurrence of four major food-borne pathogens in cattle slaughtered in Poland. Bull Vet Inst Pulawy 53:439–444. CrossRefGoogle Scholar
  122. Workman SN, Mathison GE, Marc C, Lavoie MC (2005) Pet dogs and chicken meat as reservoirs of Campylobacter spp. in Barbados’s pet dogs and chicken meat as reservoirs of Campylobacter spp. in Barbados. J Clin Microbiol 43:2642–2650. CrossRefPubMedPubMedCentralGoogle Scholar
  123. Ziprin RL, Young CR, Stanker LH, Hume ME, Konkel ME, Konkelb ME (1999) The Absence of Cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein. Avian Dis 43:586–589. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Nompumelelo Shange
    • 1
    • 2
  • Pieter Gouws
    • 1
    • 3
    Email author
  • Louwrens C. Hoffman
    • 2
    • 4
  1. 1.Department of Food ScienceStellenbosch UniversityStellenboschSouth Africa
  2. 2.Department of Animal SciencesStellenbosch UniversityStellenboschSouth Africa
  3. 3.Centre for Food SafetyStellenbosch UniversityStellenboschSouth Africa
  4. 4.Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation (QAAFI)The University of QueenslandBrisbaneAustralia

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