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.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abedon S (2011) Phage therapy pharmacology: calculating phage dosing. Adv Appl Microbiol 77:1–40. https://doi.org/10.1016/B978-0-12-387044-5.00001-7
Abedon ST (2011b) Lysis from without. Bacteriophage 1:46–49. https://doi.org/10.4161/bact.1.1.13980
Abedon ST (2014) Phage therapy: eco-physiological pharmacology. Scientifica 2014:581639. https://doi.org/10.1155/2014/581639
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.0.000470
Aksyuk AA, Rossmann MG (2011) Bacteriophage assembly. Viruses 3:172–203. https://doi.org/10.3390/v3030172
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.69.10.6302-6306.2003
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.69.8.4511-4518.2003
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.71.8.4885-4887.2005
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.02057-14
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.7b00240
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.2007.11.003
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.2016.79
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.0094690
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.2019.118601
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/s10439-019-02435-6
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.x
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/10.1186/1471-2180-10-232
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.2008.05.001
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.70.7.3877-3883.2004
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.x
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.00184-06
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.01111-19
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.2009.07.002
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.2013.09.001
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
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
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.2011.2105
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.2012.2615
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.2016.4565
EFSA (2019) The European union one health 2018 zoonoses report. EFSA J 17(12):5926. https://doi.org/10.2903/j.efsa.2019.5926
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
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-72.4.733
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/nature21049
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
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.2018.00296
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.2016.08.026
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.0078543
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.0078543
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/10.1111/1462-2920.13284
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.2018.00082
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.2014.08.015
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.69.8.5032-5036.2003
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 61:1764–1771
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
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.0114785
Hazeleger WC, Wouters JA, Rombouts FM, Abee T (1998) Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl Environ Microbiol 64:3917–3922
Hirsch K (2010) Entwicklung von Minimierungsstrategien für Campylobacter im Geflügel durch Anwendung von Bakteriophagen. Doctoral thesis, University of Veterinary Medicine Hannover, Foundation, Hannover
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
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.2012.00011
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.2014.00744
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)70007-1
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.1008193
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/mps2010018
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.2013.06.024
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.12849
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.76.11.5557-5564.2002
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.02703-13
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.0094782
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.2016.06.001
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
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):132–140
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_14
Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327. https://doi.org/10.1038/nrmicro2315
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-x
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-090110-102908
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.2019.09.018
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/microorganisms8020282
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.14120
Lin J (2009) Novel approaches for Campylobacter control in poultry. Foodborne Pathog Dis 6:755–765. https://doi.org/10.1089/fpd.2008.0247
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.2016.01908
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1:111–114. https://doi.org/10.4161/bact.1.2.14590
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
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/BST20130127
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/s10096-012-1733-4
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.x
Moye ZD, Woolston J, Sulakvelidze A (2018) Bacteriophage applications for food production and processing. Viruses 10(4):205. https://doi.org/10.3390/v10040205
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.01090-10
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.2010.01.021
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
Oechslin F (2018) Resistance development to bacteriophages occurring during bacteriophage therapy. Viruses 10(7):351. https://doi.org/10.3390/v10070351
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/10.4172/1747-0862.1000049
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):141–147
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/s00705-018-3845-3
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/evv174
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.2016.04.020
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.53078
Quinn PJ (2011) Veterinary Microbiology and Microbial Disease. Campylobacter and Helicobacter species. Blackwell Publishing Ltd., West Sussex, UK
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.2008.06.018
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.2019.00476
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.2017.06.010
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)00317-3
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/v10060332
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/10.1099/00222615-47-2-123
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.x
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.0030119
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.130200
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.02704-10
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/v11050468
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.0116287
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.05276-11
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
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.70.3.1735-1743.2004
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/s00253-003-1438-9
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.12770
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/10.1186/1471-2164-11-214
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.2005.06.002
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.185.3.779-787.2003
Young KD, Young R (1982) Lytic action of cloned phi X174 gene E. J Virol. 44:993–1002. https://doi.org/10.1128/JVI.44.3.993-1002.1982
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.2016.10.033
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).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Kittler, S., Steffan, S., Peh, E., Plötz, M. (2021). Phage Biocontrol of Campylobacter: A One Health Approach. In: Backert, S. (eds) Fighting Campylobacter Infections. Current Topics in Microbiology and Immunology, vol 431. Springer, Cham. https://doi.org/10.1007/978-3-030-65481-8_6
Download citation
DOI: https://doi.org/10.1007/978-3-030-65481-8_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-65480-1
Online ISBN: 978-3-030-65481-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)