Approaches to prevent and control Campylobacter spp. colonization in broiler chickens: a review

Abstract

Campylobacter, Gram-negative bacteria, is the most common cause of acute bacterial enteritis in human beings, both in developing and developed countries. It is believed that poultry, in particular broiler chickens, is the main host of human infection with Campylobacter. Handling and consumption of contaminated chicken meat are the usual modes of transmission. Prevention and reduction of Campylobacter colonization in poultry farms will cut off the road of infection transmission to humans throughout the food chain. With the incidence of antibiotic resistance and with growing concern about superbugs, the search for natural and safe alternatives will considerably increase in the coming years. In this review, we will discuss the prevalence and risk factors of Campylobacter colonization in broiler chickens and sources of infection. This review also provides extensive and recent approaches to prevent and control Campylobacter colonization in broiler chickens, including biosecurity measures, natural feed/drinking water additives with antimicrobial properties, bacteriocins, bacteriophages, antimicrobial peptides, and vaccination strategies to prevent and control the incidence of human campylobacteriosis.

This is a preview of subscription content, access via your institution.

Data availability

Not applicable.

References

  1. Abd El-Hack ME, Alagawany M (2015) Performance, egg quality, blood profile, immune function, and antioxidant enzyme activities in laying hens fed diets with thyme powder. J Anim Feed Sci 24:127–133

    Google Scholar 

  2. Abd El-Hack ME, Alagawany M, Ragab Farag M, Tiwari R, Karthik K, Dhama K, Adel M (2016) Beneficial impacts of thymol essential oil on health and production of animals, fish and poultry: a review. J Essent Oil Res 28:365–382

    Google Scholar 

  3. Abd El-Hack ME, Mahgoub SA, Hussein MMA, Saadeldin IM (2018a) Improving growth performance and health status of meat-type quail by supplementing the diet with black cumin cold-pressed oil as a natural alternative for antibiotics. Environ Sci Poll Res 25(2):1157–1167

    CAS  Google Scholar 

  4. Abd El-Hack ME, Ashour EA, Elaraby GM, Osman AO, Arif M (2018b) Influences of dietary supplementation of peanut skin powder (Arachis Hypogaea) on growth performance, carcass traits, blood chemistry, antioxidant activity and meat quality of broilers. Anim Prod Sci 58:965–972

    CAS  Google Scholar 

  5. Abd El-Hack ME, Alagawany M, El-Moneim AEA, Mohammed N, Khafaga A, Bin-Jumah M, Othman SI, Allam A, Elnesr S (2020a) Cinnamon (Cinnamomum zeylanicum) oil as a potential alternative to antibiotics in poultry. Antibiotics (Basel) 9(5):210

    CAS  Google Scholar 

  6. Abd El-Hack ME, Abdelnour SA, Taha AE, Khafaga AF, Arif M, Ayasan T, Swelum AA, Abukhalil MH, Alkahtani S, Aleya L, Abdel-Daim MM (2020b) Herbs as thermoregulatory agents in poultry: An overview. Sci Total Env 10, 703:134399

  7. Abd El-Hack ME, Alagawany M, Shaheen H, Samak D, Othman SI, Allam AA, Taha AE, Khafaga AF, Arif M, Osman A (2020c) Ginger and its derivatives as promising alternatives to antibiotics in poultry feed. Animals 10(3):452

    Google Scholar 

  8. Abo Ghanima MM, Elsadek MF, Taha AE, El-Hack A, Mohamed E, Alagawany M, Ahmed BM, Elshafie MM, El-Sabrout K (2020) Effect of housing system and rosemary and cinnamon essential oils on layers performance, egg quality, haematological traits, blood chemistry, immunity, and antioxidant. Animals 10(2):245

    Google Scholar 

  9. Adamczak A, Ożarowski M, Karpiński TM (2020) Antibacterial activity of some flavonoids and organic acids widely distributed in plants. J Clin Med 9(1):109

    CAS  Google Scholar 

  10. Ageitos JM, Sánchez-Pérez A, Calo-Mata P, Villa TG (2017) Antimicrobial peptides (AMPs): ancient compounds that represent novel weapons in the fight against bacteria. Biochem Pharmacol [Internet] 133:117–138

    CAS  Google Scholar 

  11. Alagawany M, Abd El-Hack ME, Farag MR, Tiwari R, Dhama K (2015a) Biological effects and modes of action of carvacrol in animal and poultry production and health—a review. Adv Anim Vet Sci 3:73–84

    Google Scholar 

  12. Alagawany MM, Farag MR, Dhama K, Abd El-Hack ME, Tiwari R, Alam GM (2015b) Mechanisms and beneficial applications of resveratrol as feed additive in animal and poultry nutrition: a review. Int J Pharmacol 11:213–221

    CAS  Google Scholar 

  13. Alagawany M, Abd El-Hack ME, Farag MR, Shaheen HM, Abdel-Latif MA, Noreldin AE, Patra AK (2018) The usefulness of oregano and its derivatives in poultry nutrition. World's Poult Sci J 74(3):463–474

    Google Scholar 

  14. Alagawany M, Elnesr SS, Farag MR, El-Hack A, Mohamed E, Khafaga AF, Taha AE, Tiwari R, Yatoo M, Bhatt P, Marappan G (2019) Use of licorice (Glycyrrhiza glabra) herb as a feed additive in poultry: current knowledge and prospects. Animals. 9(8):536

    Google Scholar 

  15. Alagawany M, Attia Y, Farag MR, Elnesr SS, Nagadi SA, Shafi ME, Khafaga AF, Ohran H, Alaqil AA, Abd El-Hack ME (2020a) The strategy of boosting the immune system of food-producing under CoViD-19 pandemic. Front Vet Sci 7:398. https://doi.org/10.3389/fvets.2020.00398

    Article  Google Scholar 

  16. Alagawany M, Abd El-Hack ME, Farag MR, Shaheen HM, Abdel-Latif MA, Noreldin AE, Khafaga AF (2020b) The applications of Origanum vulgare and its derivatives in human, ruminant and fish nutrition—a review. Ann Anim Sci 20(2):389–407

    CAS  Google Scholar 

  17. Allen VM, Weaver H, Ridley AM, Harris JA, Sharma M, Emery J et al (2008) Sources and spread of thermophilic Campylobacter spp. during partial depopulation of broiler chicken flocks. J Food Prot 71(2):264–270

    CAS  Google Scholar 

  18. Annamalai T, Pina-Mimbela R, Kumar A, Binjawadagi B, Liu Z, Renukaradhya GJ, Rajashekara G (2013) Evaluation of nanoparticle-encapsulated outer membrane proteins for the control of Campylobacter jejuni colonization in chickens. Poult Sci 92:2201–2211

    CAS  Google Scholar 

  19. Barrios PR, Reiersen J, Lowman R, Bisaillon JR, Michel P, Fridriksdottir V et al (2006) Risk factors for Campylobacter spp. colonization in broiler flocks in Iceland. Prev Vet Med 74:264–278

    Google Scholar 

  20. Biswas D, Fernando UM, Reiman CD, Willson PJ, Townsend HGG, Potter AA, Allan BJ (2007) Correlation between in vitro secretion of virulence-associated proteins of Campylobacter jejuni and colonization of chickens. Curr Microbiol [Internet] 54(3):207–212

    CAS  Google Scholar 

  21. Bouwknegt M, van de Giessen AW, Dam-Deisz WD, Havelaar AH, Nagelkerke NJ, Henken AM (2004) Risk factors for the presence of Campylobacter spp. in Dutch broiler flocks. Prev Vet Med 62:35–49

    CAS  Google Scholar 

  22. Buckley AM, Wang J, Hudson DL, Grant AJ, Jones MA, Maskell DJ, Stevens MP (2010) Evaluation of live-attenuated Salmonella vaccines expressing Campylobacter antigens for control of C. jejuni in poultry. Vaccine 28:1094–1105

    CAS  Google Scholar 

  23. Bull SA, Allen VM, Domingue G, Jorgensen F, Frost JA, Ure R et al (2006) Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol 72:645–652

    CAS  Google Scholar 

  24. Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94(3):223–253

    CAS  Google Scholar 

  25. Burt SA, Ojo-Fakunle VTA, Woertman J, Veldhuizen EJA (2014) The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS One 9(4):e93414

    Google Scholar 

  26. Byrd JA, Hargis BM, Caldwell DJ, Bailey RH, Herron KL, McReynolds JL et al (2001) Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poult Sci 80(3):278–283

    CAS  Google Scholar 

  27. Byrne CM, Clyne M, Bourke B (2007) Campylobacter jejuni adhere to and invade chicken intestinal epithelial cells in vitro. Microbiology 153(2):561–569

    CAS  Google Scholar 

  28. Callicott KA, Fridriksdottir V, Reiersen J, Lowman R, Bisaillon JR, Gunnarsson E et al (2006) Lack of evidence for vertical transmission of Campylobacter spp. in chickens. Appl Environ Microbiol 72:5794–5798

    CAS  Google Scholar 

  29. Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM, Roe JM, Azeredo J (2010) The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol 10(1):232

    Google Scholar 

  30. Castillo S, Heredia N, Arechiga-Carvajal E, García S (2014) Citrus extracts as inhibitors of quorum sensing, biofilm formation and motility of. Campylobacter jejuni Food Biotechnol 28(2):106–122

  31. Cawthraw SA, Newell DG (2010) Investigation of the presence and protective effects of maternal antibodies against Campylobacter jejuni in chickens. Avian Dis 54:86–93

    CAS  Google Scholar 

  32. Chaloner G, Wigley P, Humphrey S, Kemmett K, Lacharme-Lora L, Humphrey T, Williams N (2014) Dynamics of dual infection with Campylobacter jejuni strains in chickens reveals distinct strain-to-strain variation in infection ecology. Appl Environ Microbiol 80:6366–6372

    Google Scholar 

  33. Dasti JI, Tareen AM, Lugert R, Zautner AE, Groß U (2010) Campylobacter jejuni: A brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol [Internet] 300(4):205–211

    CAS  Google Scholar 

  34. van Dijk A, Herrebout M, Tersteeg-Zijderveld MHG, Tjeerdsma-van Bokhoven JLM, Bleumink-Pluym N, Jansman AJM et al (2012) Campylobacter jejuni is highly susceptible to killing by chicken host defense peptide cathelicidin-2 and suppresses intestinal cathelicidin-2 expression in young broilers. Vet Microbiol [Internet] 160(3):347–354 Available from: http://www.sciencedirect.com/science/article/pii/S0378113512003434

    Google Scholar 

  35. EFSA Panel on Biological Hazards (BIOHAZ) EP on BH (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(4):2105

    Google Scholar 

  36. Ellis-Iversen J, Ridley A, Morris V, Sowa A, Harris J, Atterbury R et al (2012) Persistent environmental reservoirs on farms as risk factors for Campylobacter in commercial poultry. Epidemiol Infect 140(5):916–924

    CAS  Google Scholar 

  37. El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I (2009) Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Prot 72(4):733–740

    CAS  Google Scholar 

  38. Elvers KT, Morris VK, Newell DG, Allen VM (2011) Molecular tracking, through processing, of Campylobacter strains colonizing broiler flocks. Appl Environ Microbiol 77:5722–5729

    CAS  Google Scholar 

  39. Evans EW, Beach GG, Wunderlich J, Harmon BG (1994) Isolation of antimicrobial peptides from avian heterophils. J Leukoc Biol 56(5):661–665

    CAS  Google Scholar 

  40. Evans EW, Beach FG, Moore KM, Jackwood MW, Glisson JR, Harmon BG (1995) Antimicrobial activity of chicken and turkey heterophil peptides CHP1, CHP2, THP1, and THP3. Vet Microbiol 47(3–4):295–303

    CAS  Google Scholar 

  41. Friedman M, Henika PR, Mandrell RE (2003) Antibacterial activities of phenolic benzaldehydes and benzoic acids against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J Food Prot 66(10):1811–1821

    CAS  Google Scholar 

  42. Gado AR, Ellakany HF, Elbestawy AR, Abd El-Hack ME, Khafaga AF, Taha AE, Arif M, Mahgoub SA (2019) Herbal medicine additives as powerful agents to control and prevent avian influenza virus in poultry—a review. Ann Anim Sci 24:1 (ahead-of-print)

    Google Scholar 

  43. Gahamanyi N, Mboera LEG, Matee MI, Mutangana D, Komba EVG (2020) Prevalence, risk factors, and antimicrobial resistance profiles of thermophilic campylobacter species in humans and animals in Sub-Saharan Africa: a systematic review. Int J Microbiol 2020:1–12

    Google Scholar 

  44. van Gerwe T, Bouma A, Klinkenberg D, Wagenaar JA, Jacobs-Reitsma WF, Stegeman A (2010) Medium chain fatty acid feed supplementation reduces the probability of Campylobacter jejuni colonization in broilers. Vet Microbiol 143:314–318

    Google Scholar 

  45. Ghareeb K, Awad WA, Mohnl M, Porta R, Biarnés M, Böhm J, Schatzmayr G (2012) Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poult Sci 91(8):1825–1832

    CAS  Google Scholar 

  46. Gibbens JC, Pascoe SJS, Evans SJ, Davies RH, Sayers AR (2001) A trial of biosecurity as a means to control Campylobacter infection of broiler chickens. Prev Vet Med 48(2):85–99

    CAS  Google Scholar 

  47. Gracia MI, Millán C, Sánchez J, Guyard-Nicodème M, Mayot J, Carre Y, Csorbai A, Chemaly M, Medel P (2016) Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period: Part B. Poult Sci [Internet] 95(4):886–892

    CAS  Google Scholar 

  48. Guerry P, Poly F, Riddle M, Maue AC, Chen Y-H, Monteiro MA (2012) Campylobacter polysaccharide capsules: virulence and vaccines. Front Cell Infect Microbiol 2:7

    Google Scholar 

  49. Guyard-Nicodème M, Keita A, Quesne S, Amelot M, Poezevara T, Le Berre B et al (2016) Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period1. Poult Sci [Internet] 95(2):298–305

    Google Scholar 

  50. Guyard-Nicodème M, Huneau-Salaün A, Tatone FA, Skiba F, Quentin M, Quesne S et al (2017) Effect of feed additives on productivity and Campylobacter spp. loads in broilers reared under free range conditions. Front Microbiol 8:828

    Google Scholar 

  51. Hansson I, Engvall EO, Vagsholm I, Nyman A (2010) Risk factors associated with the presence of Campylobacter-positive broiler flocks in Sweden. Prev Vet Med 96:114–121

    CAS  Google Scholar 

  52. Herman L, Heyndrickx M, Grijspeerdt K, Vandekerchove D, Rollier I, De ZL (2003) Routes for Campylobacter contamination of poultry meat: Epidemiological study from hatchery to slaughterhouse. Epidemiol Infect 131:1169–1180

    CAS  Google Scholar 

  53. Hermans D, Martel A, Van Deun K, Verlinden M, Van Immerseel F, Garmyn A et al (2010) Intestinal mucus protects Campylobacter jejuni in the ceca of colonized broiler chickens against the bactericidal effects of medium-chain fatty acids. Poult Sci 89(6):1144–1155

    CAS  Google Scholar 

  54. Hermans D, Van Deun K, Martel A, Van Immerseel F, Messens W, Heyndrickx M et al (2011a) Colonization factors of Campylobacter jejuni in the chicken gut. Vet Res 42(1):82

    Google Scholar 

  55. Hermans D, Van Deun K, Messens W, Martel A, Van Immerseel F, Haesebrouck F et al (2011b) Campylobacter control in poultry by current intervention measures ineffective: urgent need for intensified fundamental research. Vet Microbiol 152(3–4):219–228

    Google Scholar 

  56. Hermans D, Martel A, Garmyn A, Verlinden M, Heyndrickx M, Gantois I, Haesebrouck F, Pasmans F (2012a) Application of medium-chain fatty acids in drinking water increases Campylobacter jejuni colonization threshold in broiler chicks. Poult Sci 91(7):1733–1738

    CAS  Google Scholar 

  57. Hermans D, Pasmans F, Messens W, Martel A, Van IF, Rasschaert G et al (2012b) Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector Borne and Zoonotic Diseases 12:89–98

    Google Scholar 

  58. Horrocks SM, Anderson RC, Nielsbet DJ, Ricke SC (2009) Incidence and ecology of Campylobacter jejuni and coli in animals. Anaerobe 15:18–25

    CAS  Google Scholar 

  59. Huang JL, Yin YX, Pan ZM, Zhang G, Zhu AP, Liu XF et al (2010) Intranasal immunization with chitosan/pCAGGS-flaA nanoparticles inhibits Campylobacter jejuni in a White Leghorn model. J Biomed Biotechnol 2010:589476

    Google Scholar 

  60. 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:e01364–e01314

    Google Scholar 

  61. Hussein MMA, Abd El-Hack ME, Mahgoub SA, Saadeldin IM, Swelum AA (2019) Effects of clove (Syzygium aromaticum) oil on quail growth, carcass traits, blood components, meat quality and intestinal microbiota. Poult Sci 98:319–329

    CAS  Google Scholar 

  62. Joerger RD (2003) Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poult Sci 82(4):640–647

    CAS  Google Scholar 

  63. Johnson TJ, Shank JM, Johnson JG (2017) Current and potential treatments for reducing Campylobacter colonization in animal hosts and disease in humans. Front Microbiol 8:487

    Google Scholar 

  64. Jones C (2005) Vaccines based on the cell surface carbohydrates of pathogenic bacteria. An Acad Bras Cienc 77:293–324

    CAS  Google Scholar 

  65. Jonsson ME, Chriel M, Norstrom M, Hofshagen M (2012) Effect of climate and farm environment on Campylobacter spp. colonisation in Norwegian broiler flocks. Prev Vet Med 107:95–104

    Google Scholar 

  66. Kassem II, Sanad Y, Gangaiah D, Lilburn M, LeJeune J, Rajashekara G (2010) Use of bioluminescence imaging to monitor Campylobacter survival in chicken litter. J Appl Microbiol 109:1988–1997

    CAS  Google Scholar 

  67. Kelly C, Gundogdu O, Pircalabioru G, Cean A, Scates P, Linton M, Pinkerton L, Magowan E, Stef L, Simiz E, Pet I, Stewart S, Stabler R, Wren B, Dorrell N, Corcionivoschi N (2017) The in vitro and in vivo effect of carvacrol in preventing Campylobacter infection, colonization and in improving productivity of chicken broilers. Foodborne Pathog Dis 14(6):341–349

    CAS  Google Scholar 

  68. Khafaga AF, Abd El-Hack ME, Taha AE, Elnesr SS, Alagawany M. 2019. The potential modulatory role of herbal additives against Cd toxicity in human, animal, and poultry: A review. Environ Sci Pollut Res. 20;26(5):4588-604.

  69. Kim J, Guk J-H, Mun S-H, An J-U, Kim W, Lee S, Song H, Seong JK, Suh JG, Cho S (2020) The wild mouse (Micromys minutus): reservoir of a novel Campylobacter jejuni strain. Front Microbiol 10:3066

    Google Scholar 

  70. Kishawy A.T.Y., Amer S.A., Mohamed E. Abd El-Hack, Saadeldin I.M., Swelum A.A. The impact of dietary linseed oil and pomegranate peel extract on broiler growth, carcass traits, serum lipid profile, and meat fatty acid, phenol, and flavonoid contents. Asian-Austr J Anim Sci 2019, 32, 1161-08.

  71. Knudsen KN, Bang DD, Andresen LO, Madsen M (2006) Campylobacter jejuni strains of human and chicken origin are invasive in chickens after oral challenge. Avian Dis 50:10–14

    Google Scholar 

  72. Lam KM, DaMassa AJ, Morishita TY, Shivaprasad HL, Bickford AA (1992) Pathogenicity of Campylobacter jejuni for Turkeys and chickens. Avian Dis 36:359–363

    CAS  Google Scholar 

  73. Laniewski P, Kuczkowski M, Chrzastek K, Wozniak A, Wyszynska A, Wieliczko A et al (2014) Evaluation of the immunogenicity of Campylobacter jejuni CjaA protein delivered by Salmonella enterica sv. Typhimurium strain with regulated delayed attenuation in chickens. World J Microbiol Biotechnol 30:281–292

    CAS  Google Scholar 

  74. Layton SL, Morgan MJ, Cole K, Kwon YM, Donoghue DJ, Hargis BM, Pumford NR (2011) Evaluation of Salmonella-vectored Campylobacter peptide epitopes for reduction of Campylobacter jejuni in broiler chickens. Clin Vaccine Immunol 18:449–454

    CAS  Google Scholar 

  75. Line JE, Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Levchuk VP, Svetoch OE, Seal BS, Siragusa GR, 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(3):1094–1100

    CAS  Google Scholar 

  76. de los Santos FS, Donoghue AM, Venkitanarayanan K, Dirain ML, Reyes-Herrera I, Blore PJ et al (2008) Caprylic Acid supplemented in feed reduces enteric Campylobacter jejuni colonization in ten-day-old broiler Chickens1,2. Poult Sci [Internet] 87(4):800–804

    Google Scholar 

  77. Lu T, Marmion M, Ferone M, Wall P, Scannell AGM (2020) On farm interventions to minimise Campylobacter sp p. contamination in chicken. Br Poult Sci https://doi.org/10.1080/00071668.2020.1813253

  78. Mahgoub SAM, Abd El-Hack ME, Saadeldin IM, Hussein MA, Swelum AA, Alagawany M (2019) Impact of Rosmarinus officinalis cold-pressed oil on health, growth performance, intestinal bacterial populations, and immunocompetence of Japanese quail. Poult Sci 89:2139–2149

    Google Scholar 

  79. Medellin-Peña MJ, Wang H, Johnson R, Anand S, Griffiths MW (2007) Probiotics affect virulence-related gene expression in Escherichia coli O157: H7. Appl Environ Microbiol 73(13):4259–4267

    Google Scholar 

  80. Messaoudi S, Kergourlay G, Rossero A, Ferchichi M, Prévost H, Drider D, Manai M, Dousset X (2011) Identification of lactobacilli residing in chicken ceca with antagonism against Campylobacter. Int Microbiol 14(2):103–110

    CAS  Google Scholar 

  81. Messaoudi S, Kergourlay G, Dalgalarrondo M, Choiset Y, Ferchichi M, Prévost H, Pilet MF, Chobert JM, Manai M, Dousset X (2012) Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiol [Internet] 32(1):129–134

    CAS  Google Scholar 

  82. Monk AB, Rees CD, Barrow P, Hagens S, Harper DR (2010) Bacteriophage applications: where are we now? Lett Appl Microbiol 51(4):363–369

    CAS  Google Scholar 

  83. Mortada M, Cosby DE, Shanmugasundaram R, Selvaraj RK (2020) In vivo and in vitro assessment of commercial probiotic and organic acid feed additives in broilers challenged with Campylobacter coli. J Appl Poult Res [Internet] 29(2):435–446

    Google Scholar 

  84. Muller A, Thomas GH, Horler R, Brannigan JA, Blagova E, Levdikov VM et al (2005) An ATP-binding cassette-type cysteine transporter in Campylobacter jejuni inferred from the structure of an extracytoplasmic solute receptor protein. Mol Microbiol 57:143–155

    Google Scholar 

  85. Naiel MAE, Shehata AM, Negm SS, Abd El-Hack ME, Amer MS, Khafaga AF et al (2020) The new aspects of using some safe feed additives on alleviated imidacloprid toxicity in farmed fish: a review. Rev Aquac [Internet] Apr 24; n/a(n/a). Available from. https://doi.org/10.1111/raq.12432

  86. Navarro M, Stanley R, Cusack A, Sultanbawa Y (2015) Combinations of plant-derived compounds against Campylobacter in vitro. J Appl Poult Res [Internet] 24(3):352–363

    CAS  Google Scholar 

  87. Neal-McKinney JM, Samuelson DR, Eucker TP, Nissen MS, Crespo R, Konkel ME (2014) Reducing Campylobacter jejuni colonization of poultry via vaccination. PLoS One 9:e114254

    Google Scholar 

  88. Newell DG, Wagenaar JA (2000) Poultry infections and their control at the farm level. In: Nachamkin I, Blaser MJ (eds) Campylobacter, 2nd edn. ASM Press, Washington, DC, pp 497–509

    Google Scholar 

  89. Nothaft H, Scott NE, Vinogradov E, Liu X, Hu R, Beadle B, Fodor C, Miller WG, Li J, Cordwell SJ, Szymanski CM (2012) Diversity in the protein N-glycosylation pathways among Campylobacter species. Mol Cell Proteomics 11:1203–1219

    Google Scholar 

  90. Nothaft H, Davis B, Lock YY, Perez-Munoz ME, Vinogradov E, Walter J, Coros C, Szymanski CM (2016) Engineering the Campylobacter jejuni N-glycan to create an effective chicken vaccine. Sci Rep 6:26511

    CAS  Google Scholar 

  91. Nothaft H, Perez-Muño ME, Gouveia GJ, Duar RM, Wanford JJ, Lango-Scholey L et al (2017) Co-administration of the Campylobacter jejuni N-glycan based vaccine with probiotics improves vaccine performance in broiler chickens. Appl Environ Microbiol 83. https://doi.org/10.1128/AEM.01523-17

  92. O’Shea EF, Cotter PD, Stanton C, Ross RP, Hill C (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: Bacteriocins and conjugated linoleic acid. Int J Food Microbiol [Internet] 152(3):189–205

    Google Scholar 

  93. Patriarchi A, Fox A, Maunsell B, Fanning S, Bolton D (2011) Molecular characterization and environmental mapping of Campylobacter isolates in a subset of intensive poultry flocks in Ireland. Foodborne Pathog Dis 8:99–108

    CAS  Google Scholar 

  94. Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37(2):156–181

    CAS  Google Scholar 

  95. Powell LF, Lawes JR, Clifton-Hadley FA, Rodgers J, Harris K, Evans SJ et al (2012) The prevalence of Campylobacter spp. in broiler flocks and on broiler carcases, and the risks associated with highly contaminated carcases. Epidemiol Infect 140(12):2233–2246

    CAS  Google Scholar 

  96. Rivoal K, Ragimbeau C, Salvat G, Colin P, 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 71:6216–6227

    CAS  Google Scholar 

  97. Rosenquist H, Nielsen NL, Sommer HM, Nørrung B, Christensen BB (2003) Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol 83(1):87–103

    Google Scholar 

  98. Sahin O, Morishita TY, Zhang Q (2002) Campylobacter colonization in poultry: Sources of infection and modes of transmission. Anim Health Res Rev 3:95–105

    Google Scholar 

  99. Sahin O, Luo N, Huang S, Zhang Q (2003) Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl Environ Microbiol 69:5372–5379

    CAS  Google Scholar 

  100. Salaheen S, Nguyen C, Hewes D, Biswas D (2014) Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni. Food Control 46:174–181

    CAS  Google Scholar 

  101. Santini C, Baffoni L, Gaggia F, Granata M, Gasbarri R, Di Gioia D et al (2010) Characterization of probiotic strains: an application as feed additives in poultry against Campylobacter jejuni. Int J Food Microbiol [Internet] 141:S98–S108

  102. Scallan E, Hoekstra RM, Mahon BE, Jones TF, Griffin PM (2015) An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol Infect 143(13):2795–2804

    CAS  Google Scholar 

  103. Sears A, Baker MG, Wilson N, Marshall J, Muellner P, Campbell DM, Lake RJ, French NP (2011) Marked campylobacteriosis decline after interventions aimed at poultry, New Zealand. Emerg Infect Dis 17(6):1007–1015

    Google Scholar 

  104. Shi C, Sun Y, Liu Z, Guo D, Sun H, Sun Z, Chen S, Zhang W, Wen Q, Peng X, Xia X (2017) Inhibition of Cronobacter sakazakii virulence factors by citral. Sci Rep 7:43243

    CAS  Google Scholar 

  105. Sibanda N, McKenna A, Richmond A, Ricke SC, Callaway T, Stratakos AC, Gundogdu O, Corcionivoschi N (2018) A review of the effect of management practices on Campylobacter prevalence in poultry farms. Front Microbiol 9:2002

    Google Scholar 

  106. Silva J, Leite D, Fernandes M, Mena C, Gibbs PA, Teixeira P (2011) Campylobacter spp. as a foodborne pathogen: a review. Front Microbiol 2:200

    Google Scholar 

  107. Sima F, Stratakos AC, Ward P, Linton M, Kelly C, Pinkerton L, Stef L, Gundogdu O, Lazar V, Corcionivoschi N (2018) A novel natural antimicrobial can reduce the in vitro and in vivo pathogenicity of T6SS positive Campylobacter jejuni and Campylobacter coli chicken isolates. Front Microbiol 9:2139

    Google Scholar 

  108. Sirirak T, Voravuthikunchai SP (2011) Eleutherine americana: a candidate for the control of Campylobacter species. Poult Sci 90(4):791–796

    CAS  Google Scholar 

  109. Sommer HM, Heuer OE, Sorensen AI, Madsen M (2013) Analysis of factors important for the occurrence of Campylobacter in Danish broiler flocks. Prev Vet Med 111:100–111

    CAS  Google Scholar 

  110. Soro AB, Whyte P, Bolton DJ, Tiwari BK (2020) Strategies and novel technologies to control Campylobacter in the poultry chain: a review. Compr Rev Food Sci Food Saf 19:1353–1377

    Google Scholar 

  111. Stern NJ, Cox NA, Musgrove MT (2001) Incidence and levels of Campylobacter in broilers after exposure to an inoculated seeder bird. J Appl Poult Res 10:315–318

    Google Scholar 

  112. Stern NJ, Svetoch EA, Eruslanov BV, Kovalev YN, Volodina LI, Perelygin VV et al (2005) Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. J Food Prot 68(7):1450–1453

    Google Scholar 

  113. Stern NJ, Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Pokhilenko VD, Levchuk VP, Svetoch OE, 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 50:3111–3116

    CAS  Google Scholar 

  114. Stern NJ, Eruslanov BV, Pokhilenko VD, Kovalev YN, Volodina LL, Perelygin VV, Mitsevich EV, Mitsevich IP, Borzenkov VN, Levchuk VP, Svetoch OE, Stepanshin YG, Svetoch EA (2008) Bacteriocins reduce Campylobacter jejuni colonization while bacteria producing bacteriocins are ineffective. Microb Ecol Health Dis 20(2):74–79

    CAS  Google Scholar 

  115. Svetoch EA, Stern NJ (2010) Bacteriocins to control Campylobacter spp. in poultry—a review. Poult Sci 89(8):1763–1768

    CAS  Google Scholar 

  116. Svetoch EA, Stern NJ, Eruslanov BV, Kovalev YN, Volodina LI, Perelygin VV et al (2005) Isolation of Bacillus circulans and Paenibacillus polymyxa strains inhibitory to Campylobacter jejuni and characterization of associated bacteriocins. J Food Prot 68(1):11–17

    CAS  Google Scholar 

  117. Szymanski CM, St Michael F, Jarrell HC, Li JJ, Gilbert M, Larocque S et al (2003) Detection of conserved N-linked glycans and phase-variable lipooligosaccharides and capsules from campylobacter cells by mass spectrometry and high-resolution magic angle spinning NMR spectroscopy. J Biol Chem 278:24509–24520

    CAS  Google Scholar 

  118. Tabashsum Z, Peng M, Salaheen S, Comis C, Biswas D (2018) Competitive elimination and virulence property alteration of Campylobacter jejuni by genetically engineered Lactobacillus casei. Food Control [Internet] 85:283–291

    CAS  Google Scholar 

  119. Tabashsum Z, Peng M, Kahan E, Rahaman SO, Biswas D (2019) Effect of conjugated linoleic acid overproducing Lactobacillus with berry pomace phenolic extracts on Campylobacter jejuni pathogenesis. Food Funct 10(1):296–303

    CAS  Google Scholar 

  120. Theoret JR, Coope KK, Zekarias B, Roland KL, Law BF, Curtiss R et al (2012) The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination. Clin Vaccine Immunol 19:1426–1431

    CAS  Google Scholar 

  121. Umar S, Maiyah AT, Mushtaq A (2016) Campylobacter infections in poultry: update on challenges and potential immune interventions. World's Poul Sci J 72(2):381–390

    Google Scholar 

  122. Upadhyay A, Arsi K, Upadhyaya I, Donoghue AM, Donoghue DJ (2019) Natural and environmentally friendly strategies for controlling Campylobacter jejuni colonization in poultry, survival in poultry products and infection in humans. Food Safety in Poultry Meat Production. Springer, In, pp 67–93

    Google Scholar 

  123. Van Alphen LB, Burt SA, Veenendaal AKJ, Bleumink-Pluym NMC, Van Putten JPM (2012) The natural antimicrobial carvacrol inhibits Campylobacter jejuni motility and infection of epithelial cells. PLoS One 7(9)

  124. Van de Giessen AW, Tilburg J, Ritmeester WS, Van Der Plas J (1998) Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol Infect 121(1):57–66

    Google Scholar 

  125. Wagenaar JA, Van Bergen MAP, Mueller MA, Wassenaar TM, Carlton RM (2005) Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109(3–4):275–283

    Google Scholar 

  126. Wagle BR, Upadhyay A, Arsi K, Shrestha S, Venkitanarayanan K, Donoghue AM et al (2017) Application of β-resorcylic acid as potential antimicrobial feed additive to reduce Campylobacter colonization in broiler chickens. Front Microbiol 8:599

    Google Scholar 

  127. Wagle BR, Upadhyay A, Upadhyaya I, Shrestha S, Arsi K, Liyanage R, Venkitanarayanan K, Donoghue DJ, Donoghue AM (2019) Trans-cinnamaldehyde, eugenol and carvacrol reduce Campylobacter jejuni biofilms and modulate expression of select genes and proteins. Front Microbiol 10:1837

    Google Scholar 

  128. Widders PR, Thomas LM, Long KA, Tokhi MA, Panaccio M, Apos E (1998) The specificity of antibody in chickens immunised to reduce intestinal colonisation with Campylobacter jejuni. Vet Microbiol 64:39–50

    CAS  Google Scholar 

  129. Willis WL, Reid L (2008) Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni Presence1. Poult Sci [Internet] 87(4):606–611. Available from: http://www.sciencedirect.com/science/article/pii/S0032579119388327

  130. Wittwer M, Keller J, Wassenaar TM, Stephan R, Howald D, Regula G, Bissig-Choisat B (2005) Genetic diversity and antibiotic resistance patterns in a Campylobacter population isolated from poultry farms in Switzerland. Appl Environ Microbiol 71:2840–2847

    CAS  Google Scholar 

  131. Wyszynska A, Raczko A, Lis M, Jagusztyn-Krynicka EK (2004) Oral immunization of chickens with avirulent Salmonella vaccine strain carrying C. jejuni 72Dz/92 cjaA gene elicits specific humoral immune response associated with protection against challenge with wild-type Campylobacter. Vaccine 22:1379–1389

    CAS  Google Scholar 

  132. Zhang L, Gallo RL (2016) Antimicrobial peptides. Curr Biol [Internet] 26(1):R14–R19

    CAS  Google Scholar 

  133. Zhang Q, Sahin O (2013) Campylobacteriosis. In: Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair VL (eds) Diseases of poultry, 13th edn. Wiley, Ames, IA, pp 737–750

    Google Scholar 

  134. Zhang D, Nie S, Xie M, Hu J (2020) Antioxidant and antibacterial capabilities of phenolic compounds and organic acids from Camellia oleifera cake. Food Sci Biotechnol 29(1):17–25

    CAS  Google Scholar 

Download references

Acknowledgments

Authors thank their respective universities and institutes for their support.

Author information

Affiliations

Authors

Contributions

All the authors (M.E.A.E-H., M.T.E-S., A.M.S., M.A., V.K.P., G.E-S.B., A.F.K. and A.R.E.) were equally contributed to the conception, design, analysis, and interpretation of data. All authors have read and agreed to the final version of the manuscript.

Corresponding authors

Correspondence to Mohamed E. Abd El-Hack or Mohamed T. El-Saadony.

Ethics declarations

Ethical approval

Not applicable because it is a review article and has no experiments.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Competing interests

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Philipp Gariguess

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abd El-Hack, M.E., El-Saadony, M.T., Shehata, A.M. et al. Approaches to prevent and control Campylobacter spp. colonization in broiler chickens: a review. Environ Sci Pollut Res 28, 4989–5004 (2021). https://doi.org/10.1007/s11356-020-11747-3

Download citation

Keywords

  • Campylobacter
  • Poultry
  • Feed additives
  • Antimicrobial
  • Vaccination