Broiler farming practices using new or re-used bedding, inclusive of free-range, have no impact on Campylobacter levels, species diversity, Campylobacter community profiles and Campylobacter bacteriophages

Helene Nalini Chinivasagam; Wiyada Estella; Damien Finn; David G. Mayer; Hugh Rodrigues; Ibrahim Diallo; Helene Nalini Chinivasagam; Wiyada Estella; Damien Finn; David G. Mayer; Hugh Rodrigues; Ibrahim Diallo

doi:10.3934/microbiol.2024002

AIMS Microbiology

2024, Volume 10, Issue 1: 12-40. doi: 10.3934/microbiol.2024002

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Broiler farming practices using new or re-used bedding, inclusive of free-range, have no impact on Campylobacter levels, species diversity, Campylobacter community profiles and Campylobacter bacteriophages

1.
Department of Agriculture and Fisheries, Eco Sciences Precinct, Dutton Park QLD 4102, Australia
2.
Department of Agriculture and Fisheries, Biosecurity Sciences Laboratory, Coopers Plains QLD 4108

Received: 03 August 2023 Revised: 27 November 2023 Accepted: 25 December 2023 Published: 16 January 2024

A multi-stage option to address food-safety can be produced by a clearer understanding of Campylobacter's persistence through the broiler production chain, its environmental niche and its interaction with bacteriophages. This study addressed Campylobacter levels, species, genotype, bacteriophage composition/ levels in caeca, litter, soil and carcasses across commercial broiler farming practices to inform on-farm management, including interventions.

Broilers were sequentially collected as per company slaughter schedules over two-years from 17 farms, which represented four commercially adopted farming practices, prior to the final bird removal (days 39–53). The practices were conventional full clean-out, conventional litter re-use, free-range–full cleanout and free-range–litter re-use. Caeca, litter and soil collected on-farm, and representative carcases collected at the processing plant, were tested for Campylobacter levels, species dominance and Campylobacter bacteriophages. General community profiling via denaturing gradient gel electrophoresis of the flaA gene was used to establish the population relationships between various farming practices on representative Campylobacter isolates. The farming practice choices did not influence the high caeca Campylobacter levels (log 7.5 to log 8.5 CFU/g), the carcass levels (log 2.5 to log 3.2 CFU/carcass), the C. jejuni/C. coli dominance and the on-farm bacteriophage presence/levels. A principal coordinate analysis of the flaA distribution for farm and litter practices showed strong separation but no obvious farming practice related grouping of Campylobacter. Bacteriophages originated from select farms, were not practice-dependent, and were detected in the environment (litter) only if present in the birds (caeca).

This multifaceted study showed no influence of farming practices on on-farm Campylobacter dynamics. The significance of this study means that a unified on-farm risk-management could be adopted irrespective of commercial practice choices to collectively address caeca Campylobacter levels, as well as the potential to include Campylobacter bacteriophage biocontrol. The impact of this study means that there are no constraints in re-using bedding or adopting free-range farming, thus contributing to environmentally sustainable (re-use) and emerging (free-range) broiler farming choices.
- Campylobacter,
- bacteriophages,
- broiler,
- litter,
- free-range,
- re-use
Citation: Helene Nalini Chinivasagam, Wiyada Estella, Damien Finn, David G. Mayer, Hugh Rodrigues, Ibrahim Diallo. Broiler farming practices using new or re-used bedding, inclusive of free-range, have no impact on Campylobacter levels, species diversity, Campylobacter community profiles and Campylobacter bacteriophages[J]. AIMS Microbiology, 2024, 10(1): 12-40. doi: 10.3934/microbiol.2024002

Related Papers:

Abstract

A multi-stage option to address food-safety can be produced by a clearer understanding of Campylobacter's persistence through the broiler production chain, its environmental niche and its interaction with bacteriophages. This study addressed Campylobacter levels, species, genotype, bacteriophage composition/ levels in caeca, litter, soil and carcasses across commercial broiler farming practices to inform on-farm management, including interventions.

Broilers were sequentially collected as per company slaughter schedules over two-years from 17 farms, which represented four commercially adopted farming practices, prior to the final bird removal (days 39–53). The practices were conventional full clean-out, conventional litter re-use, free-range–full cleanout and free-range–litter re-use. Caeca, litter and soil collected on-farm, and representative carcases collected at the processing plant, were tested for Campylobacter levels, species dominance and Campylobacter bacteriophages. General community profiling via denaturing gradient gel electrophoresis of the flaA gene was used to establish the population relationships between various farming practices on representative Campylobacter isolates. The farming practice choices did not influence the high caeca Campylobacter levels (log 7.5 to log 8.5 CFU/g), the carcass levels (log 2.5 to log 3.2 CFU/carcass), the C. jejuni/C. coli dominance and the on-farm bacteriophage presence/levels. A principal coordinate analysis of the flaA distribution for farm and litter practices showed strong separation but no obvious farming practice related grouping of Campylobacter. Bacteriophages originated from select farms, were not practice-dependent, and were detected in the environment (litter) only if present in the birds (caeca).

This multifaceted study showed no influence of farming practices on on-farm Campylobacter dynamics. The significance of this study means that a unified on-farm risk-management could be adopted irrespective of commercial practice choices to collectively address caeca Campylobacter levels, as well as the potential to include Campylobacter bacteriophage biocontrol. The impact of this study means that there are no constraints in re-using bedding or adopting free-range farming, thus contributing to environmentally sustainable (re-use) and emerging (free-range) broiler farming choices.

Acknowledgments

The financial support of the Rural Industries Research and Development Corporation (Agrifutures Australia) (RIRDC Project Number: No PRJ-006238), Chicken Meat Program is gratefully acknowledged. The publication of this work was made possible by the support of the Queensland Department of Agriculture and Fisheries (DAF), Australia. We gratefully acknowledge both integrator companies and all farmers for their participation. The support of Professor Ian Connerton (University of Nottingham, United Kingdom) with the bacteriophage work is gratefully acknowledged. We gratefully acknowledge Dr. Craig Billington (Institute of Environmental Science and Research, Christchurch, New Zealand) for reviewing the manuscript and providing valuable comments. The technical support of Caitlin Weyand is acknowledged. Dr. Kathy Crew is acknowledged for the preparation of the EM image of Campylobacter bacteriophage.

Conflict of interest

The authors declare no conflict of interest.

Author contributions

HC with industry collaborators designed the study, administered the project, curated the data, and wrote the original version. HC, WE, DF, HR, DM and ID all provided input into methodologies, farm and laboratory experiments. HC, DM and DF analysed the data. HC, DF, DM, and ID contributed to the final manuscript. All authors contributed to the article and approved the submission.

References

[1]	Gržinić G, Piotrowicz-Cieślak A, Klimkowicz-Pawlas A, et al. (2022) Intensive poultry farming: A review of the impact on the environment and human health. Sci Total Environ 160014. https://doi.org/10.1016/j.scitotenv.2022.160014
[2]	Runge GA, Blackall PJ, Casey KD (2007) Chicken litter issues associated with sourcing and use. Canberra: Rural Industries Research and Development Corporation.
[3]	Pepper CM, Dunlop MW (2022) An industry survey on litter management and re-use practices of Australian meat chicken growers. Animal Prod Sci 62: 401-408. https://doi.org/10.1071/AN21222
[4]	Chinivasagam HN, Estella W, Rodrigues H, et al. (2022) Re-used or new bedding are not drivers of Salmonella levels and serovar emergence in commercially farmed broilers in Australia. Front Sustainable Food Syst 6: 816181. https://doi.org/10.3389/fsufs.2022.816181
[5]	Barker KJ, Coufal CD, Purswell JL, et al. (2011) In-house windrowing of a commercial broiler farm during the summer months and its effect on litter composition. J Appl Poult Res 20: 168-180. https://doi.org/10.3382/japr.2010-00242
[6]	Macklin KS, Hess JB, Bilgili SF (2008) In-house windrow composting and its effects on foodborne pathogens. J Appl Poult Res 17: 121-127. https://doi.org/10.3382/japr.2007-00051
[7]	Chinivasagam HN Re-use of chicken litter across broiler cycles – managing the food-borne pathogen risk, Final Report, Project No: 05-16, Poultry CRC, Australia (2009). Available from: http://www.poultryhub.org/wp-content/uploads/2012/07/Final-Report-05-16.pdf
[8]	Chinivasagam HN, Tran T, Blackall PJ (2012) Impact of the Australian litter re-use practice on Salmonella in the broiler farming environment. Food Res Int 45: 891-896. https://doi.org/10.1016/j.foodres.2011.06.014
[9]	Chinivasagam HN, Estella W, Rodrigues H, et al. (2016) On-farm Campylobacter and Escherichia coli in commercial broiler chickens: Re-used bedding does not influence Campylobacter emergence and levels across sequential farming cycles. Poult Sci 95: 1105-1115. https://doi.org/10.3382/ps/pew003
[10]	Singh M, Cowieson AJ (2013) Range use and pasture consumption in free-range poultry production. Animal Prod Sci 53: 1202-1208. https://doi.org/10.1071/AN13199
[11]	Pumtang-on P, Mahony TJ, Hill RA, et al. (2020) Investigation of Campylobacter colonization in three Australian commercial free-range broiler farms. Poult Sci 100891. https://doi.org/10.1016/j.psj.2020.12.004
[12]	Rothrock MJ, Gibson KE, Micciche AC, et al. (2019) Pastured poultry production in the united states: strategies to balance system sustainability and environmental impact. Front Sustainable Food Syst 3: 10.3389. https://doi.org/10.3389/fsufs.2019.00074
[13]	Xu X, Rothrock MJ, Mohan A, et al. (2021) Using farm management practices to predict Campylobacter prevalence in pastured poultry farms. Poult Sci 100. https://doi.org/10.1016/j.psj.2021.101122
[14]	Golden CE, Rothrock MJ, Mishra A (2021) Mapping foodborne pathogen contamination throughout the conventional and alternative poultry supply chains. Poult Sci 100: 101157. https://doi.org/10.1016/j.psj.2021.101157
[15]	Shaughnessy RG, Meade KG, Cahalane S, et al. (2009) Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet Immunol Immunopathol 132: 191-198. https://doi.org/10.1016/j.vetimm.2009.06.007
[16]	Line JE, Hiett KL, Guard-Bouldin J, et al. (2010) Differential carbon source utilization by Campylobacter jejuni 11168 in response to growth temperature variation. J Microbiol Methods 80: 198-202. https://doi.org/10.1016/j.mimet.2009.12.011
[17]	European Food Safety Authority.The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J (2016) 14: e04634. https://doi.org/10.2903/j.efsa.2016.4634
[18]	Lake RJ, Campbell DM, Hathaway SC, et al. (2021) Source attributed case-control study of campylobacteriosis in New Zealand. Int J Infect Dis 103: 268-277. https://doi.org/10.1016/j.ijid.2020.11.167
[19]	D'Lima CB, Miller WG, Mandrell RE, et al. (2007) Clonal population structure and specific genotypes of multidrug-resistant Campylobacter coli from turkeys. Appl Environ Microbiol 73: 2156-2164. https://doi.org/10.1128/AEM.02346-06
[20]	Tam CC, O'Brien SJ, Adak GK, et al. (2003) Campylobacter coli - an important foodborne pathogen. J Infect 47: 28-32. https://doi.org/10.1016/S0163-4453(03)00042-2
[21]	Zhang J, Konkel ME, Gölz G, et al. (2022) Editorial: Campylobacter-associated food safety. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.1038128
[22]	NNDSS Annual Report Working Group.Australia's notifiable disease status, 2015: Annual report of the national notifiable diseases surveillance system. Commun Dis Intell (2019) . https://doi.org/10.33321/cdi.2019.43.6
[23]	Centre for Disease Control and PreventionNational centre for emerging and zoonotic infectious diseases (Campyloacter) (2015). Available from: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/campylobacter/
[24]	Nastasijevic I, Proscia F, Boskovic Cabrol M, et al. (2020) The European Union control strategy for Campylobacter spp. in the broiler meat chain. J Food Safety 40: e12819. https://doi.org/10.1111/jfs.12819
[25]	Ingmer H (2011) Challenges of Campylobacter jejuni in poultry production. IntJ Food Microbiol 145: S110-S110. https://doi.org/10.1016/j.ijfoodmicro.2010.12.015
[26]	Lee MD, Newell DG (2006) Invited Minireview: Campylobacter in poultry: filling an ecological niche. Avian Dis 50: 1-9. https://doi.org/10.1637/7474-111605R.1
[27]	Diaz Carrasco J, Redondo L, Casanova N, et al. (2022) The role of farm environment and management in shaping the gut microbiota of poultry. Gut Microbiota, Immunity, and Health in Production Animals, The Microbiomes of Humans, Animals, Plants, and the Environment.Springer Nature Switzerland 193-224. https://doi.org/10.1007/978-3-030-90303-9_10
[28]	Amit-Romach E, Sklan D, Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83: 1093-1098. https://doi.org/10.1093/ps/83.7.1093
[29]	Shane SM, Stern MJ (2003) Campylobacter infection. Diseases of Poultry. Ames: Iowa State University Press 615-630.
[30]	Van Deun K, Pasmans F, Ducatelle R, et al. (2008) Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut. Vet Microbiol 130: 285-297. https://doi.org/10.1016/j.vetmic.2007.11.027
[31]	Colles FM, Hedges SJ, Dixon R, et al. (2021) Parallel sequencing reveals Campylobacter spp. In commercial meat chickens less than 8 days old. Appl Environ Microbiol 87: e01060-01021. https://doi.org/10.1128/AEM.01060-21
[32]	Cox NA, Richardson LJ, Maurer JJ, et al. (2012) Evidence for horizontal and vertical transmission in Campylobacter passage from hen to her progeny. J Food Prot 75: 1896-1902. https://doi.org/10.4315/0362-028.JFP-11-322
[33]	Newell DG, Fearnley C (2003) Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol 69: 4343-4351. https://doi.org/10.1128/AEM.69.8.4343-4351.2003
[34]	Brown PE, Christensen OF, Clough HE, et al. (2004) Frequency and spatial distribution of environmental Campylobacter spp. Appl Environ Microbiol 70: 6501-6511. https://doi.org/10.1128/AEM.70.11.6501-6511.2004
[35]	Colles FM, McCarthy ND, Layton R, et al. (2011) The prevalence of Campylobacter amongst a free-range broiler breeder flock was primarily affected by flock age. PloS One 6: e22825. https://doi.org/10.1371/journal.pone.0022825
[36]	Shanker S, Lee A, Sorrell TC (1990) Horizontal transmission of Campylobacter jejuni amongst broiler chicks: Experimental studies. Epidemiol Infect 104: 101-110. https://doi.org/10.1017/S0950268800054571
[37]	Ridley AM, Morris VK, Cawthraw SA, et al. (2011) A longitudinal molecular epidemiological study of thermophilic campylobacters on one conventional broiler farm. Appl Environ Microbiol 77: 98-107. https://doi.org/10.1128/AEM.01388-10
[38]	Sandberg M, Sørensen LL, Steenberg B, et al. (2015) Risk factors for Campylobacter colonization in Danish broiler flocks, 2010 to 2011. Poult Sci 94: 447-453. https://doi.org/10.3382/ps/peu065
[39]	Koutsoumanis K, Allende A, Alvarez-Ordonez A, et al. (2020) Update and review of control options for Campylobacter in broilers at primary production. EFSA J 18: 6090-6090. https://doi.org/10.2903/j.efsa.2020.6090
[40]	Jorgensen F, Ellis-Iversen J, Rushton S, et al. (2011) Influence of season and geography on Campylobacter jejuni and C. coli Subtypes in housed broiler flocks reared in Great Britain. Appl Environ Microbiol 77: 3741-3748. https://doi.org/10.1128/AEM.02444-10
[41]	Zbrun MV, Olivero CR, Soto LP, et al. (2022) Impact of farm-level strategies against thermotolerant Campylobacter in broiler chickens, using a quantitative risk assessment model and meta-analysis. Zoonoses Public Health 00: 1-17. https://doi.org/10.1111/zph.12930
[42]	Hermans D, Van Deun K, Messens W, et al. (2011) Campylobacter control in poultry by current intervention measures ineffective: Urgent need for intensified fundamental research. Vet Microbiol 152: 219-228. https://doi.org/10.1016/j.vetmic.2011.03.010
[43]	El-Shibiny A, Connerton PL, Connerton IF (2005) Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens. Appl Environ Microbiol 71: 1259-1266. https://doi.org/10.1128/AEM.71.3.1259-1266.2005
[44]	Sillankorva SM, Oliveira H, Azeredo J (2012) Bacteriophages and their role in food safety. Intl J Microbiol 2012: 863945. https://doi.org/10.1155/2012/863945
[45]	Mahony J, McAuliffe O, Ross RP, et al. (2011) Bacteriophages as biocontrol agents of food pathogens. Curr Opin Biotechnol 22: 157-163. https://doi.org/10.1016/j.copbio.2010.10.008
[46]	Hudson JA, Billington C, Carey-Smith G, et al. (2005) Bacteriophages as biocontrol agents in food. J Food Protect 68: 426-437. https://doi.org/10.4315/0362-028X-68.2.426
[47]	Weitz JS, Poisot T, Meyer JR, et al. (2013) Phage–bacteria infection networks. Trends in Microbiol 21: 82-91. https://doi.org/10.1016/j.tim.2012.11.003
[48]	El-Shibiny A, Scott A, Timms A, et al. (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
[49]	Callaway TR, Edrington TS, Brabban A, et al. (2010) Occurrence of Salmonella-specific bacteriophages in swine feces collected from commercial farms. Foodborne Pathog Dis 7: 851-856. https://doi.org/10.1089/fpd.2009.0512
[50]	Olson EG, Micciche AC, Rothrock MJ, et al. (2022) Application of bacteriophages to limit campylobacter in poultry production. Front Microbiol 12: 458721-458721. https://doi.org/10.3389/fmicb.2021.458721
[51]	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
[52]	Furuta M, Nasu T, Umeki K, et al. (2017) Characterization and application of lytic bacteriophages against Campylobacter jejuni isolated from poultry in Japan. Biocontrol Sci 22: 213-221. https://doi.org/10.4265/bio.22.213
[53]	Nowaczek A, Urban-Chmiel R, Dec M, et al. (2019) Campylobacter spp. and bacteriophages from broiler chickens: Characterization of antibiotic susceptibility profiles and lytic bacteriophages. MicrobiologyOpen 8: e784. https://doi.org/10.1002/mbo3.784
[54]	Kittler S, Fischer S, Abdulmawjood A, et al. (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
[55]	Chinivasagam HN, Estella W, Maddock L, et al. (2020) Bacteriophages to control Campylobacter in commercially farmed broiler chickens, in australia. Front Microbiol 11: 632. https://doi.org/10.3389/fmicb.2020.00632
[56]	Chinivasagam HN A “proof of concept” study to control Campylobacter using bacteriophages Poultry CRC (2017). Available from: https://www.poultryhub.org/content/uploads/2017/05/3.1.6-Chinivasagam-Final-Report.pdf
[57]	Chinivasagam HN, Estella W, Cockerill SA, et al. (2020) Moving from concept to control; use of phages for Campylobacter reduction. AgriFutures Australia Publication No. 20–110 . https://www.agrifutures.com.au/wp-content/uploads/2020/11/20-110.pdf
[58]	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
[59]	Hakeem MJ, Lu X (2021) Survival and control of Campylobacter in poultry production environment. Front Cell Infect Microbiol 10: 615049. https://doi.org/10.3389/fcimb.2020.615049
[60]	Alter T, Reich F (2021) Management strategies for prevention of Campylobacter Infections through the poultry food chain: a european perspective. Fighting Campylobacter Infections: Towards a One Health Approach. Cham: Springer International Publishing 79-102. https://doi.org/10.1007/978-3-030-65481-8_4
[61]	Reichelt B, Szott V, Epping L, et al. (2022) Transmission pathways of campylobacter spp. at broiler farms and their environment in Brandenburg, Germany. Front Microbiol 13: 982693. https://doi.org/10.3389/fmicb.2022.982693
[62]	Free Range Egg & Poultry Australia (FREPA)FREPA, range care, chicken meat bird standards (2012). http://www.frepa.com.au/standards/meat-standards/.
[63]	Best EL, Powell EJ, Swift C, et al. (2003) Applicability of a rapid duplex real-time PCR assay for speciation of Campylobacter jejuni and Campylobacter coli directly from culture plates. FEMS Microbiol Lett 229: 237-241. https://doi.org/10.1016/S0378-1097(03)00845-0
[64]	Leblanc-Maridor M, Garenaux A, Beaudeau F, et al. (2011) Quantification of Campylobacter spp. in pig feces by direct real-time PCR with an internal control of extraction and amplification. J Microbiol Methods 85: 53-61. https://doi.org/10.1016/j.mimet.2011.01.013
[65]	Hein I, Mach RL, Farnleitner AH, et al. (2003) Application of single-strand conformation polymorphism and denaturing gradient gel electrophoresis for fla sequence typing of Campylobacter jejuni. J Microbiol Methods 52: 305-313. https://doi.org/10.1016/S0167-7012(02)00183-5
[66]	Najdenski H, Heyndrickx M, Herman L, et al. (2008) Fla-DGGE analysis of Campylobacter jejuni and Campylobacter coli in cecal samples of broilers without cultivation. Vet Microbiol 127: 196-202. https://doi.org/10.1016/j.vetmic.2007.08.002
[67]	Chen YH, Kocherginskaya SA, Lin Y, et al. (2005) Biochemical and mutational analyses of a unique clamp loader complex in the archaeon Methanosarcina acetivorans. J Biol Chem 280: 41852-41863. https://doi.org/10.1074/jbc.M508684200
[68]	Kocherginskaya SA (2005) Denaturing gradient gel electrophoresis. Methods in gut microbial ecology for ruminants. Amsterdam: International Atomic Energy Agency, Springer Academic Press 119-128. https://doi.org/10.1007/1-4020-3791-0_9
[69]	R Core TeamR: A language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria (2013).
[70]	Oksanen J, Guillaume Blanchet F, Friendly M, et al. Package ‘vegan’: Community Ecology Package (2019).
[71]	Atterbury RJ, Connerton PL, Dodd CER, et al. (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
[72]	GenStatGenStat for Windows, Release 19.1. VSN International Ltd., Oxford (2018).
[73]	McCullagh P, Nelder JA (1989) Generalized Linear Models (2nd ed.). London: Chapman and Hall. https://doi.org/10.1007/978-1-4899-3242-6
[74]	International Committee on Taxonomy of VirusesICTV Taxonomy history: Campylobacter virus CP81 (2018).
[75]	Mota-Gutierrez J, Lis L, Lasagabaster A, et al. (2022) Campylobacter spp. prevalence and mitigation strategies in the broiler production chain. Food Microbiol 104: 103998. https://doi.org/10.1016/j.fm.2022.103998
[76]	Scott AE, Timms AR, Connerton PL, et al. (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
[77]	Scott A, Timms A, Connerton P, et al. (2007) Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathog 3: 1142-1151. https://doi.org/10.1371/journal.ppat.0030119
[78]	Klancnik A, Guzej B, Jamnik P, et al. (2009) Stress response and pathogenic potential of Campylobacter jejuni cells exposed to starvation. Res Microbiol 160: 345-352. https://doi.org/10.1016/j.resmic.2009.05.002
[79]	Daczkowska-Kozon EG, Sawicki W, Skotarczak K (2010) The caeca-niche supporting survival of Campylobacter spp. in commercially reared broiler chickens. Pol J Food Nutr Sci 60: 265-271.
[80]	Hansson I, Pudas N, Harbom B, et al. (2010) Within-flock variations of Campylobacter loads in caeca and on carcasses from broilers. Int J Food Microbiol 141: 51-55. https://doi.org/10.1016/j.ijfoodmicro.2010.04.019
[81]	Allen VM, Ridley AM, Harris JA, et al. (2011) Influence of production system on the rate of onset of Campylobacter colonization in chicken flocks reared extensively in the United Kingdom. Br Poult Sci 52: 30-39. https://doi.org/10.1080/00071668.2010.537306
[82]	Valeris-Chacin R, Pieters M, Hwang H, et al. (2021) Association of broiler litter microbiome composition and Campylobacter isolation. Front Vet Sci 8: 654927. https://doi.org/10.3389/fvets.2021.654927
[83]	Hanning I, Biswas D, Herrera P, et al. (2010) Prevalence and characterization of Campylobacter jejuni Isolated from pasture flock poultry. J Food Sci 75: M496-M502. https://doi.org/10.1111/j.1750-3841.2010.01747.x
[84]	Nesbit EG, Gibbs P, Dreesen DW, et al. (2001) Epidemiologic features of Campylobacter jejuni isolated from poultry broiler houses and surrounding environments as determined by use of molecular strain typing. Am J Vet Res 62: 190-194. https://doi.org/10.2460/ajvr.2001.62.190
[85]	Meinersmann RJ, Helsel LO, Fields PI, et al. (1997) Discrimination of Campylobacter jejuni isolates by fla gene sequencing. J Clin Microbiol 35: 2810-2814. https://doi.org/10.1128/jcm.35.11.2810-2814.1997
[86]	Wieczorek K, Wolkowicz T, Osek J (2019) flaA-SVR based genetic diversity of multiresistant Campylobacter jejuni isolated from chickens and humans. Front Microbiol 10: 1176. https://doi.org/10.3389/fmicb.2019.01176
[87]	Colles FM, Dingle KE, Cody AJ, et al. (2008) Comparison of Campylobacter populations in wild geese with those in starlings and free-range poultry on the same farm. Appl Environ Microbiol 74: 3583-3590. https://doi.org/10.1128/AEM.02491-07
[88]	Meinersmann RJ, Phillips RW, Hiett KL, et al. (2005) Differentiation of Campylobacter populations as demonstrated by flagellin short variable region sequences. Appl Environ Microbiol 71: 6368-6374. https://doi.org/10.1128/AEM.71.10.6368-6374.2005
[89]	Ahmed MU, Dunn L, Ivanova EP (2012) Evaluation of current molecular approaches for genotyping of Campylobacter jejuni strains. Foodborne Pathog Dis 9: 375-385. https://doi.org/10.1089/fpd.2011.0988
[90]	Manning G, Duim B, Wassenaar T, et al. (2001) Evidence for a genetically stable strain of Campylobacter jejuni. Appl Environ Microbiol 67: 1185-1189. https://doi.org/10.1128/AEM.67.3.1185-1189.2001
[91]	Sheppard SK, McCarthy ND, Falush D, et al. (2008) Convergence of Campylobacter species: Implications for bacterial evolution. Science 320: 237-239. https://doi.org/10.1126/science.1155532
[92]	Sheppard SK, Dallas JF, Wilson DJ, et al. (2010) Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland. PLoS ONE 5: e15708. https://doi.org/10.1371/journal.pone.0015708
[93]	Sheppard SK, Colles FM, McCarthy ND, et al. (2011) Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol Ecol 20: 3484-3490. https://doi.org/10.1111/j.1365-294X.2011.05179.x
[94]	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. https://doi.org/10.3389/fmicb.2017.00487
[95]	Pasquali F, De Cesare A, Manfreda G, et al. (2011) Campylobacter control strategies in European poultry production. Worlds Poult Sci J 67: 5-18. https://doi.org/10.1017/S0043933911000018
[96]	Premaratne A, Zhang H, Wang R, et al. (2021) Phage biotechnology to mitigate antimicrobial resistance in agriculture. Sustainable Agriculture Reviews 49: Mitigation of Antimicrobial Resistance Vol 2 Natural and Synthetic Approaches Springer International Publishing, Cham . https://doi.org/10.1007/978-3-030-58259-3_9
[97]	Loc Carrillo CM, Connerton PL, Pearson T, et al. (2007) Free-range layer chickens as a source of Campylobacter bacteriophage. Antonie van Leeuwenhoek 92: 275-284. https://doi.org/10.1007/s10482-007-9156-4
[98]	Connerton PL, Loc Carrillo CM, Swift C, et al. (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
[99]	Atterbury RJ, Dillon E, Swift C, et al. (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
[100]	Baker MG, Grout L, Wilson N (2021) Update on the campylobacter epidemic from chicken meat in New Zealand: The urgent need for an upgraded regulatory response. Epidemiol Infect 149: e30. https://doi.org/10.1017/S095026882000299X

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