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Phage Biocontrol of Campylobacter: A One Health Approach

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Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 431)

Abstract

Human infections by Campylobacter species are among the most reported bacterial gastrointestinal diseases in the European Union and worldwide with severe outcomes in rare cases. Considering the transmission routes and farm animal reservoirs of these zoonotic pathogens, a comprehensive One Health approach will be necessary to reduce human infection rates. Bacteriophages are viruses that specifically infect certain bacterial genera, species, strains or isolates. Multiple studies have demonstrated the general capacity of phage treatments to reduce Campylobacter loads in the chicken intestine. However, phage treatments are not yet approved for extensive use in the agro-food industry in Europe. Technical inconvenience is mainly related to the efficacy of phages, depending on the optimal choice of phages and their combination, as well as application route, concentration and timing. Additionally, regulatory uncertainties have been a major concern for investment in commercial phage-based products. This review addresses the question as to how phages can be put into practice and can help to solve the issue of human campylobacteriosis in a sustainable One Health approach. By compiling the reported findings from the literature in a standardized manner, we enabled inter-experimental comparisons to increase our understanding of phage infection in Campylobacter spp. and practical on-farm studies. Further, we address some of the hurdles that still must be overcome before this new methodology can be adapted on an industrial scale. We envisage that phage treatment can become an integrated and standardized part of a multi-hurdle anti-bacterial strategy in food production. The last part of this chapter deals with some of the issues raised by legal authorities, bringing together current knowledge on Campylobacter-specific phages and the biosafety requirements for approval of phage treatment in the food industry.

Keywords

Phage safety One health Field trials Campylobacter phages Phage therapy 

Notes

Acknowledgements

This work was supported by the German Federal Ministry of Education and Research (BMBF) through the zoonoses research consortium PAC-Campylobacter (project IP5/01KI1725E).

References

  1. Abedon S (2011) Phage therapy pharmacology: calculating phage dosing. Adv Appl Microbiol 77:1–40.  https://doi.org/10.1016/B978-0-12-387044-5.00001-7CrossRefPubMedGoogle Scholar
  2. Abedon ST (2011b) Lysis from without. Bacteriophage 1:46–49.  https://doi.org/10.4161/bact.1.1.13980
  3. Abedon ST (2014) Phage therapy: eco-physiological pharmacology. Scientifica 2014:581639.  https://doi.org/10.1155/2014/581639CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aidley J, Sørensen MCH, Bayliss CD, Brondsted L (2017) Phage exposure causes dynamic shifts in the expression states of specific phase-variable genes of Campylobacter jejuni. Microbiology 163:911–919.  https://doi.org/10.1099/mic.0.000470CrossRefPubMedGoogle Scholar
  5. Aksyuk AA, Rossmann MG (2011) Bacteriophage assembly. Viruses 3:172–203.  https://doi.org/10.3390/v3030172
  6. Atterbury RJ, Connerton PL, Dodd CE, Rees CE, Connerton IF (2003) Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl Environ Microbiol 69:6302–6306.  https://doi.org/10.1128/AEM.69.10.6302-6306.2003CrossRefPubMedPubMedCentralGoogle Scholar
  7. Atterbury RJ, Connerton PL, Dodd CE, Rees CE, Connerton IF (2003) Isolation and characterization of Campylobacter bacteriophages from retail poultry. Appl Environ Microbiol 69:4511–4518.  https://doi.org/10.1128/aem.69.8.4511-4518.2003CrossRefPubMedPubMedCentralGoogle Scholar
  8. Atterbury RJ, Dillon E, Swift C, Connerton PL, Frost JA, Dodd CE, Rees CE, Connerton IF (2005) Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol 71:4885–4887.  https://doi.org/10.1128/AEM.71.8.4885-4887.2005CrossRefPubMedPubMedCentralGoogle Scholar
  9. Baldvinsson SB, Sørensen MC, Vegge CS, Clokie MR, Brondsted L (2014) Campylobacter jejuni motility is required for infection of the flagellotropic bacteriophage F341. Appl Environ Microbiol 80:7096–7106.  https://doi.org/10.1128/AEM.02057-14CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bari SMN, Walker FC, Cater K, Aslan B, Hatoum-Aslan A (2017) Strategies for editing virulent staphylococcal phages using CRISPR-Cas10. ACS Synth Biol 6:2316–2325.  https://doi.org/10.1021/acssynbio.7b00240CrossRefPubMedGoogle Scholar
  11. Bigwood T, Hudson JA, Billington C, Carey-Smith GV, Heinemann JA (2008) Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiol 25:400–406.  https://doi.org/10.1016/j.fm.2007.11.003CrossRefPubMedGoogle Scholar
  12. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL (2016) Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10:2854–2866.  https://doi.org/10.1038/ismej.2016.79CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bull JJ, Vegge CS, Schmerer M, Chaudhry WN, Levin BR (2014) Phenotypic resistance and the dynamics of bacterial escape from phage control. PLoS ONE 9(4):e94690.  https://doi.org/10.1371/journal.pone.0094690CrossRefPubMedPubMedCentralGoogle Scholar
  14. Carrigy NB, Liang L, Wang H, Kariuki S, Nagel TE, Connerton IF, Vehring R (2019) Spray-dried anti-Campylobacter bacteriophage CP30A powder suitable for global distribution without cold chain infrastructure. Int J Pharm 569:118601.  https://doi.org/10.1016/j.ijpharm.2019.118601CrossRefPubMedGoogle Scholar
  15. Carrigy NB, Liang L, Wang H, Kariuki S, Nagel TE, Connerton IF, Vehring R (2020) Trileucine and Pullulan improve anti-Campylobacter bacteriophage stability in engineered spray-dried microparticles. Ann Biomed Eng 48:1169–1180.  https://doi.org/10.1007/s10439-019-02435-6CrossRefPubMedGoogle Scholar
  16. Carvalho C, Susano M, Fernandes E, Santos S, Gannon B, Nicolau A, Gibbs P, Teixeira P, Azeredo J (2010) Method for bacteriophage isolation against target Campylobacter strains. Lett Appl Microbiol 50:192–197.  https://doi.org/10.1111/j.1472-765X.2009.02774.xCrossRefPubMedGoogle Scholar
  17. 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 10:232.  https://doi.org/10.1186/1471-2180-10-232CrossRefPubMedPubMedCentralGoogle Scholar
  18. Comeau AM, Hatfull GF, Krisch HM, Lindell D, Mann NH, Prangishvili D (2008) Exploring the prokaryotic virosphere. Res Microbiol 159:306–313.  https://doi.org/10.1016/j.resmic.2008.05.001CrossRefPubMedGoogle Scholar
  19. Connerton PL, Loc Carrillo CM, Swift C, Dillon E, Scott A, Rees CE, Dodd CE, Frost J, Connerton IF (2004) Longitudinal study of Campylobacter jejuni bacteriophages and their hosts from broiler chickens. Appl. Environ. Microbiol. 70:3877–3883.  https://doi.org/10.1128/AEM.70.7.3877-3883.2004CrossRefPubMedPubMedCentralGoogle Scholar
  20. Connerton PL, Timms AR, Connerton IF (2011) Campylobacter bacteriophages and bacteriophage therapy. J. Appl Microbiol 111:255–265.  https://doi.org/10.1111/j.1365-2672.2011.05012.xCrossRefPubMedGoogle Scholar
  21. Coward C, Grant AJ, Swift C, Philp J, Towler R, Heydarian M, Frost JA, Maskell DJ (2006) Phase-variable surface structures are required for infection of Campylobacter jejuni by bacteriophages. Appl Environ Microbiol 72:4638–4647.  https://doi.org/10.1128/AEM.00184-06CrossRefPubMedPubMedCentralGoogle Scholar
  22. Crippen CS, Lee YJ, Hutinet G, Shajahan A, Sacher JC, Azadi P, de Crecy-Lagard V, Weigele PR, Szymanski CM (2019) Deoxyinosine and 7-deaza-2-deoxyguanosine as carriers of genetic information in the DNA of Campylobacter viruses. J Virol 93(23):e01111–19. https://doi.org/ARTNe01111-1910.1128/JVI.01111-19Google Scholar
  23. 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 300:205–211.  https://doi.org/10.1016/j.ijmm.2009.07.002CrossRefPubMedGoogle Scholar
  24. Denes T, Wiedmann M (2014) Environmental responses and phage susceptibility in foodborne pathogens: implications for improving applications in food safety. Curr Opin Biotechnol 26:45–49.  https://doi.org/10.1016/j.copbio.2013.09.001CrossRefPubMedGoogle Scholar
  25. Denou E, Bruttin A, Barretto C, Ngom-Bru C, Brussow H, Zuber S (2009) T4 phages against Escherichia coli diarrhea: potential and problems. Virology 388:21–30.  https://doi.org/10.1016/j.virol.2009.03.009
  26. EFSA (2009) Scientific opinion on “The use and mode of action of bacteriophages in food production". EFSA J 2(26):1076.  https://doi.org/10.2903/j.efsa.2009.1076
  27. 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(4):2105.  https://doi.org/10.2903/j.efsa.2011.2105CrossRefGoogle Scholar
  28. EFSA (2012) Scientific opinion on the evaluation of the safety and efficacy of ListexTM P100 for the removal of Listeria monocytogenes surface contamination of raw fish. EFSA J 10(3):2615.  https://doi.org/10.2903/j.efsa.2012.2615CrossRefGoogle Scholar
  29. EFSA (2016) Evaluation of the safety and efficacy of ListexTMP100 forreduction of pathogens on different ready-to-eat (RTE) food products. EFSA J 14(8):4565.  https://doi.org/10.2903/j.efsa.2016.4565CrossRefGoogle Scholar
  30. EFSA (2019) The European union one health 2018 zoonoses report. EFSA J 17(12):5926.  https://doi.org/10.2903/j.efsa.2019.5926CrossRefGoogle Scholar
  31. EG (2017) Commission Regulation (EU) 2017/1495 amending Regulation (EC) No 2073/2005 as regards Campylobacter in broiler carcases. Available from https://eur-lex.europa.eu/eli/reg/2017/1495/oj
  32. 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 72:733–740.  https://doi.org/10.4315/0362-028x-72.4.733CrossRefPubMedGoogle Scholar
  33. Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A, Peleg Y, Melamed S, Leavitt A, Savidor A, Albeck S, Amitai G, Sorek R (2017) Communication between viruses guides lysis-lysogeny decisions. Nature 541:488–493.  https://doi.org/10.1038/nature21049CrossRefPubMedPubMedCentralGoogle Scholar
  34. FDA (2003) Quantitative assessment of relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready to eat foods. US food and drug administration center for food safety and applied nutrition. Available fromhttps://www.fda.gov/food/cfsan-risk-safety-assessments/quantitative-assessment-relative-risk-public-health-foodborne-listeria-monocytogenes-among-selected
  35. Fernandez L, Gutierrez D, Rodriguez A, Garcia P (2018) Application of bacteriophages in the agro-food sector: a long way toward approval. Front Cell Infect Microbiol 8:296.  https://doi.org/10.3389/fcimb.2018.00296CrossRefPubMedPubMedCentralGoogle Scholar
  36. Firlieyanti AS, Connerton PL, Connerton IF (2016) Campylobacters and their bacteriophages from chicken liver: the prospect for phage biocontrol. Int J Food Microbiol 237:121–127.  https://doi.org/10.1016/j.ijfoodmicro.2016.08.026CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fischer S, Kittler S, Klein G, Glunder G (2013) Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLoS ONE 8(10):e78543.  https://doi.org/10.1371/journal.pone.0078543CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fischer S, Kittler S, Klein G, Glünder G (2013) Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLoS ONE 8(10):e78543.  https://doi.org/10.1371/journal.pone.0078543CrossRefPubMedPubMedCentralGoogle Scholar
  39. Galtier M, De Sordi L, Maura D, Arachchi H, Volant S, Dillies MA, Debarbieux L (2016) Bacteriophages to reduce gut carriage of antibiotic resistant uropathogens with low impact on microbiota composition. Environ Microbiol 18(7):2237–2245.  https://doi.org/10.1111/1462-2920.13284CrossRefPubMedGoogle Scholar
  40. Gencay YE, Sørensen MCH, Wenzel CQ, Szymanski CM, Brøndsted L (2018) Phase variable expression of a single phage receptor in Campylobacter jejuni NCTC12662 influences sensitivity toward several diverse CPS-dependent phages. Front Microbiol 9:82.  https://doi.org/10.3389/fmicb.2018.00082CrossRefPubMedPubMedCentralGoogle Scholar
  41. Gölz G, Rosner B, Hofreuter D, Josenhans C, Kreienbrock L, Lowenstein A, Schielke A, Stark K, Suerbaum S, Wieler LH, Alter T (2014) Relevance of Campylobacter to public health—the need for a one health approach. Int J Med Microbiol 304:817–823.  https://doi.org/10.1016/j.ijmm.2014.08.015CrossRefPubMedGoogle Scholar
  42. Goode D, Allen VM, Barrow PA (2003) Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microbiol 69:5032–5036.  https://doi.org/10.1128/aem.69.8.5032-5036.2003CrossRefPubMedPubMedCentralGoogle Scholar
  43. Grant CC, Konkel ME, Cieplak W Jr, Tompkins LS (1993) Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect Immun 61:1764–1771CrossRefGoogle Scholar
  44. Hagens S, Loessner MJ (2010) Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol 11:58–68.  https://doi.org/10.2174/138920110790725429
  45. Hammerl JA, Jackel C, Alter T, Janzcyk P, Stingl K, Knuver MT, Hertwig S (2014) Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLoS ONE 9(12):e114785.  https://doi.org/10.1371/journal.pone.0114785CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hazeleger WC, Wouters JA, Rombouts FM, Abee T (1998) Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl Environ Microbiol 64:3917–3922CrossRefGoogle Scholar
  47. Hirsch K (2010) Entwicklung von Minimierungsstrategien für Campylobacter im Geflügel durch Anwendung von Bakteriophagen. Doctoral thesis, University of Veterinary Medicine Hannover, Foundation, HannoverGoogle Scholar
  48. Hobbs Z, Abedon ST (2016) Diversity of phage infection types and associated terminology: the problem with ‘Lytic or lysogenic’. FEMS Microbiol Lett 363(7).  https://doi.org/10.1093/femsle/fnw047
  49. Holst Sørensen MC, van Alphen LB, Fodor C, Crowley SM, Christensen BB, Szymanski CM, Brondsted L (2012) Phase variable expression of capsular polysaccharide modifications allows Campylobacter jejuni to avoid bacteriophage infection in chickens. Front Cell Infect Microbiol 2:11.  https://doi.org/10.3389/fcimb.2012.00011CrossRefPubMedGoogle Scholar
  50. Hooton SPT, Connerton IF (2015) Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harboring a CRISPR-like Cas4 protein. Front Microbiol 5:744.  https://doi.org/10.3389/Fmicb.2014.00744CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248.  https://doi.org/10.1016/S0065-2164(10)70007-1CrossRefPubMedGoogle Scholar
  52. Islam MZ, Fokine A, Mahalingam M, Zhang Z, Garcia-Doval C, van Raaij MJ, Rossmann MG, Rao VB (2019) Molecular anatomy of the receptor binding module of a bacteriophage long tail fiber. PLoS Pathog. 15(12):e1008193.  https://doi.org/10.1371/journal.ppat.1008193CrossRefPubMedPubMedCentralGoogle Scholar
  53. Jackel C, Hammerl JA, Hertwig S (2019) Campylobacter phage isolation and characterization: what we have learned so far. Methods Protoc 2(1):18.  https://doi.org/10.3390/mps2010018CrossRefPubMedCentralGoogle Scholar
  54. Janez N, Loc-Carrillo C (2013) Use of phages to control Campylobacter spp. J Microbiol Methods 95:68–75.  https://doi.org/10.1016/j.mimet.2013.06.024CrossRefPubMedGoogle Scholar
  55. Javed MA, van Alphen LB, Sacher J, Ding W, Kelly J, Nargang C, Smith DF, Cummings RD, Szymanski CM (2015) A receptor-binding protein of Campylobacter jejuni bacteriophage NCTC 12673 recognizes flagellin glycosylated with acetamidino-modified pseudaminic acid. Mol Microbiol. 95:101–115.  https://doi.org/10.1111/mmi.12849CrossRefPubMedGoogle Scholar
  56. Kasman LM, Kasman A, Westwater C, Dolan J, Schmidt MG, Norris JS (2002) Overcoming the phage replication threshold: a mathematical model with implications for phage therapy. J Virol 76(11):5557–5564.  https://doi.org/10.1128/jvi.76.11.5557-5564.2002CrossRefPubMedPubMedCentralGoogle Scholar
  57. Kittler S, Fischer S, Abdulmawjood A, Glünder G, Klein G (2013) Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. Appl Environ Microbiol 79:7525–7533.  https://doi.org/10.1128/AEM.02703-13CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kittler S, Fischer S, Abdulmawjood A, Glünder G, Klein G (2014) Colonisation of a phage susceptible Campylobacter jejuni population in two phage positive broiler flocks. PLoS ONE 9(4):e94782.  https://doi.org/10.1371/journal.pone.0094782CrossRefPubMedPubMedCentralGoogle Scholar
  59. Kittler S, Wittmann J, Mengden RALP, Klein G, Rohde C, Lehnherr H (2017) The use of bacteriophages as one-health approach to reduce multidrug-resistant bacteria. Sus Chem Pharm 5:80–83.  https://doi.org/10.1016/j.scp.2016.06.001CrossRefGoogle Scholar
  60. Kittler S, Mengden R, Korf IHE, Bierbrodt A, Wittmann J, Plötz M, Jung A, Lehnherr T, Rohde C, Lehnherr H, Klein G, Kehrenberg C (2020) Impact of bacteriophage-supplemented drinking water on the E. coli population in the chicken gut. Pathogens 9(4):293.  https://doi.org/10.3390/pathogens9040293
  61. Klein G, Jansen W, Kittler S, Reich F (2015) Mitigation strategies for Campylobacter spp. in broiler at pre-harvest and harvest level. Berl Munch Tierarztl Wochenschr 128(3–4):132–140Google Scholar
  62. Kutter E (2009) Phage host range and efficiency of plating. Methods Mol Biol 501:141–149.  https://doi.org/10.1007/978-1-60327-164-6_14CrossRefPubMedGoogle Scholar
  63. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327.  https://doi.org/10.1038/nrmicro2315CrossRefPubMedGoogle Scholar
  64. Lee S, Lee J, Ha J, Choi Y, Kim S, Lee H, Yoon Y, Choi KH (2016) Clinical relevance of infections with zoonotic and human oral species of Campylobacter. J Microbiol 54:459–467.  https://doi.org/10.1007/s12275-016-6254-xCrossRefPubMedGoogle Scholar
  65. Lertsethtakarn P, Ottemann KM, Hendrixson DR (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 65:389–410.  https://doi.org/10.1146/annurev-micro-090110-102908CrossRefPubMedPubMedCentralGoogle Scholar
  66. Lewis R, Hill C (2019) Overcoming barriers to phage application in food and feed. Curr Opin Biotechnol 61:38–44.  https://doi.org/10.1016/j.copbio.2019.09.018CrossRefPubMedGoogle Scholar
  67. Liang L, Carrigy NB, Kariuki S, Muturi P, Onsare R, Nagel T, Vehring R, Connerton PL, Connerton IF (2020) Development of a lyophilization process for Campylobacter bacteriophage storage and transport. Microorganisms 8(2):282.  https://doi.org/10.3390/microorganisms8020282CrossRefPubMedCentralGoogle Scholar
  68. Liang L, Connerton IF (2018) FlhF(T368A) modulates motility in the bacteriophage carrier state of Campylobacter jejuni. Mol Microbiol 110:616–633.  https://doi.org/10.1111/mmi.14120CrossRefPubMedPubMedCentralGoogle Scholar
  69. Lin J (2009) Novel approaches for Campylobacter control in poultry. Foodborne Pathog Dis 6:755–765.  https://doi.org/10.1089/fpd.2008.0247CrossRefPubMedPubMedCentralGoogle Scholar
  70. Lis L, Connerton IF (2016) The minor flagellin of Campylobacter jejuni (FlaB) confers defensive properties against bacteriophage infection. Front Microbiol 7:1908.  https://doi.org/10.3389/fmicb.2016.01908CrossRefPubMedPubMedCentralGoogle Scholar
  71. Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1:111–114.  https://doi.org/10.4161/bact.1.2.14590CrossRefPubMedPubMedCentralGoogle Scholar
  72. Loc Carrillo C, Atterbury RJ, el-Shibiny A, Connerton PL, Dillon E, Scott A, Connerton IF (2005) Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71:6554-6563.  https://doi.org/10.1128/AEM.71.11.6554-6563.2005
  73. Louwen R, van Baarlen P (2013) Are bacteriophage defence and virulence two sides of the same coin in Campylobacter jejuni? Biochem Soc Trans 41:1475–1481.  https://doi.org/10.1042/BST20130127CrossRefPubMedGoogle Scholar
  74. Louwen R, Horst-Kreft D, de Boer AG, van der Graaf L, de Knegt G, Hamersma M, Heikema AP, Timms AR, Jacobs BC, Wagenaar JA, Endtz HP, van der Oost J, Wells JM, Nieuwenhuis EE, van Vliet AH, Willemsen PT, van Baarlen P, van Belkum A (2013) A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barre syndrome. Eur J Clin Microbiol Inf Dis 32:207–226.  https://doi.org/10.1007/s10096-012-1733-4CrossRefGoogle Scholar
  75. Mondigler M, Vögele RT, Heller KJ (1995) Overproduced and purified receptor binding protein pb5 of bacteriophage T5 binds to the T5 receptor protein FhuA. FEMS Microbiol Lett 130:293–300.  https://doi.org/10.1111/j.1574-6968.1995.tb07734.xCrossRefPubMedGoogle Scholar
  76. Moye ZD, Woolston J, Sulakvelidze A (2018) Bacteriophage applications for food production and processing. Viruses 10(4):205.  https://doi.org/10.3390/v10040205CrossRefPubMedCentralGoogle 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 G, Allen VM (2011) Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol 77:8605–8614.  https://doi.org/10.1128/AEM.01090-10CrossRefPubMedPubMedCentralGoogle Scholar
  78. Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse H (2010) Food-borne diseases—the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 139(Suppl 1):S3-15.  https://doi.org/10.1016/j.ijfoodmicro.2010.01.021CrossRefPubMedPubMedCentralGoogle Scholar
  79. Nowaczek A, Urban-Chmiel R, Dec M, Puchalski A, Stepien-Pysniak D, Marek A, Pyzik E (2019) Campylobacter spp. and bacteriophages from broiler chickens: characterization of antibiotic susceptibility profiles and lytic bacteriophages. Microbiol Open 8:e784.  https://doi.org/10.1002/mbo3.784
  80. Oechslin F (2018) Resistance development to bacteriophages occurring during bacteriophage therapy. Viruses 10(7):351.  https://doi.org/10.3390/v10070351CrossRefPubMedCentralGoogle Scholar
  81. Orquera S, Golz G, Hertwig S, Hammerl J, Sparborth D, Joldic A, Alter T (2012) Control of Campylobacter spp. and Yersinia enterocolitica by virulent bacteriophages. J Mol Genet Med 6:273–278.  https://doi.org/10.4172/1747-0862.1000049CrossRefPubMedPubMedCentralGoogle Scholar
  82. Orquera S, Hertwig S, Alter T, Hammerl JA, Jirova A, Golz G (2015) Development of transient phage resistance in Campylobacter coli against the group II phage CP84. Berl Munch Tierarztl Wochenschr 12(3–4):141–147Google Scholar
  83. O’Sullivan L, Lucid A, Neve H, Franz CMAP, Bolton D, McAuliffe O, Paul Ross R, Coffey A (2018) Comparative genomics of Cp8viruses with special reference to Campylobacter phage vB_CjeM_los1, isolated from a slaughterhouse in Ireland. Arch Virol 163:2139–2154.  https://doi.org/10.1007/s00705-018-3845-3CrossRefPubMedGoogle Scholar
  84. Pearson BM, Louwen R, van Baarlen P, van Vliet AH (2015) Differential distribution of type II CRISPR-Cas systems in agricultural and nonagricultural Campylobacter coli and Campylobacter jejuni isolates correlates with lack of shared environments. Genome Biol Evol 7(9):2663–2679.  https://doi.org/10.1093/gbe/evv174CrossRefPubMedPubMedCentralGoogle Scholar
  85. Pereira C, Moreirinha C, Lewicka M, Almeida P, Clemente C, Cunha Â, Delgadillo I, Romalde JL, Nunes ML, Almeida A (2016) Bacteriophages with potential to inactivate Salmonella Typhimurium: use of single phage suspensions and phage cocktails. Virus Res 220:179–192.  https://doi.org/10.1016/j.virusres.2016.04.020CrossRefPubMedGoogle Scholar
  86. Pyenson NC, Marraffini LA (2020) Co-evolution within structured bacterial communities results in multiple expansion of CRISPR loci and enhanced immunity. Elife 9:e53078.  https://doi.org/10.7554/eLife.53078CrossRefPubMedPubMedCentralGoogle Scholar
  87. Quinn PJ (2011) Veterinary Microbiology and Microbial Disease. Campylobacter and Helicobacter species. Blackwell Publishing Ltd., West Sussex, UKGoogle Scholar
  88. 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.  https://doi.org/10.1016/j.ijfoodmicro.2008.06.018CrossRefPubMedGoogle Scholar
  89. Richards PJ, Connerton PL, Connerton IF (2019) Phage biocontrol of Campylobacter jejuni in chickens does not produce collateral effects on the gut microbiota. Front Microbiol 10:476.  https://doi.org/10.3389/fmicb.2019.00476CrossRefPubMedPubMedCentralGoogle Scholar
  90. Román S, Sánchez-Siles LM, Siegrist M (2017) The importance of food naturalness for consumers: results of a systematic review. Trends Food Sci Technol 67:44–57.  https://doi.org/10.1016/j.tifs.2017.06.010CrossRefGoogle Scholar
  91. Rosenquist H, Nielsen NL, Sommer HM, Norrung B, Christensen BB (2003) Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol 83:87–103.  https://doi.org/10.1016/s0168-1605(02)00317-3CrossRefPubMedGoogle Scholar
  92. Sacher JC, Flint A, Butcher J, Blasdel B, Reynolds HM, Lavigne R, Stintzi A, Szymanski CM (2018) Transcriptomic analysis of the Campylobacter jejuni response to T4-like phage NCTC 12673 infection. Viruses 10(6):322.  https://doi.org/10.3390/v10060332CrossRefGoogle Scholar
  93. Sails AD, Wareing DR, Bolton FJ, Fox AJ, Curry A (1998) Characterisation of 16 Campylobacter jejuni and C. coli typing bacteriophages. J Med Microbiol 47:123–128.  https://doi.org/10.1099/00222615-47-2-123CrossRefPubMedGoogle Scholar
  94. Scott AE, Timms AR, Connerton PL, El-Shibiny A, Connerton IF (2007) Bacteriophage influence Campylobacter jejuni types populating broiler chickens. Environ Microbiol 9:2341–2353.  https://doi.org/10.1111/j.1462-2920.2007.01351.xCrossRefPubMedGoogle Scholar
  95. Scott AE, Timms AR, Connerton PL, Loc Carrillo C, Adzfa Radzum K, Connerton IF (2007) Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Path 3(8):e119.  https://doi.org/10.1371/journal.ppat.0030119CrossRefGoogle Scholar
  96. Siringan P, Connerton PL, Cummings NJ, Connerton IF (2014) Alternative bacteriophage life cycles: the carrier state of Campylobacter jejuni. Open Biol 4:130200.  https://doi.org/10.1098/rsob.130200CrossRefPubMedPubMedCentralGoogle Scholar
  97. Siringan P, Connerton PL, Payne RJ, Connerton IF (2011) Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Appl Environ Microbiol 77:3320–3326.  https://doi.org/10.1128/AEM.02704-10CrossRefPubMedPubMedCentralGoogle Scholar
  98. Sommer J, Trautner C, Witte AK, Fister S, Schoder D, Rossmanith P, Mester PJ (2019) Don’t shut the stable door after the phage has bolted-the importance of bacteriophage inactivation in food environments. Viruses 11(5):468.  https://doi.org/10.3390/v11050468CrossRefPubMedCentralGoogle Scholar
  99. Sørensen MC, Gencay YE, Birk T, Baldvinsson SB, Jäckel C, Hammerl JA, Vegge CS, Neve H, Brøndsted L (2015) Primary isolation strain determines both phage type and receptors recognised by Campylobacter jejuni bacteriophages. PLoS ONE 10(1):e0116287.  https://doi.org/10.1371/journal.pone.0116287CrossRefPubMedPubMedCentralGoogle Scholar
  100. Sørensen MC, van Alphen LB, Harboe A, Li J, Christensen BB, Szymanski CM, BrøndstedL, (2011) Bacteriophage F336 recognizes the capsular phosphoramidate modification of Campylobacter jejuni NCTC11168. J Bacteriol 193:6742–6749.  https://doi.org/10.1128/JB.05276-11CrossRefPubMedPubMedCentralGoogle Scholar
  101. Soundararajan M, von Bünau R, Oelschlaeger TA (2019) K5 capsule and lipopolysaccharide are important in resistance to T4 phage attack in probiotic E. coli Strain Nissle 1917. Front Microbiol 10:2783.  https://doi.org/10.3389/fmicb.2019.02783
  102. Sturino JM, Klaenhammer TR (2004) Antisense RNA targeting of primase interferes with bacteriophage replication in Streptococcus thermophilus. Appl Environ Microbiol 70:1735–1743.  https://doi.org/10.1128/aem.70.3.1735-1743.2004CrossRefPubMedPubMedCentralGoogle Scholar
  103. Tanji Y, Shimada T, Yoichi M, Miyanaga K, Hori K, Unno H (2004) Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 64:270–274.  https://doi.org/10.1007/s00253-003-1438-9CrossRefPubMedGoogle Scholar
  104. Thung TY, Lee E, Mahyudin NA, Radzi CWJWM, Mazlan N, Tan CW, Radu S (2020) Partial characterization and in vitro evaluation of a lytic bacteriophage for biocontrol of Campylobacter jejuni in mutton and chicken meat. J Food Safety 40:e12770.  https://doi.org/10.1111/jfs.12770CrossRefGoogle Scholar
  105. Timms AR, Cambray-Young J, Scott AE, Petty NK, Connerton PL, Clarke L, Seeger K, Quail M, Cummings N, Maskell DJ, Thomson NR, Connerton IF (2010) Evidence for a lineage of virulent bacteriophages that target Campylobacter. BMC Genom 11:214.  https://doi.org/10.1186/1471-2164-11-214CrossRefGoogle Scholar
  106. Wagenaar JA, Van Bergen MA, Mueller MA, Wassenaar TM, Carlton RM (2005) Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109:275–283.  https://doi.org/10.1016/j.vetmic.2005.06.002CrossRefPubMedGoogle Scholar
  107. Wang IN, Deaton J, Young R (2003) Sizing the holin lesion with an endolysin-beta-galactosidase fusion. J Bacteriol 185:779–787.  https://doi.org/10.1128/jb.185.3.779-787.2003CrossRefPubMedPubMedCentralGoogle Scholar
  108. Young KD, Young R (1982) Lytic action of cloned phi X174 gene E. J Virol. 44:993–1002.  https://doi.org/10.1128/JVI.44.3.993-1002.1982CrossRefPubMedPubMedCentralGoogle Scholar
  109. Zampara A, Sørensen MC, Elsser-Gravensen A, Brøndsted L (2017) Significance of phage-host interactions for biocontrol of Campylobacter jejuni in food. Food Control 73:1169–1175.  https://doi.org/10.1016/j.foodcont.2016.10.033CrossRefGoogle Scholar

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© The Author(s), under exclusive license to Springer Nature Switzerland AG 2021

Authors and Affiliations

  1. 1.Institute for Food Quality and Food Safety, University of Veterinary Medicine Hannover, FoundationHannoverGermany

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