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Natural and Environmentally Friendly Strategies for Controlling Campylobacter jejuni Colonization in Poultry, Survival in Poultry Products and Infection in Humans

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Food Safety in Poultry Meat Production

Abstract

Campylobacter jejuni is a major foodborne pathogen that causes severe gastrointestinal illness in humans characterized by abdominal cramps, pyrexia, and diarrhea. Although livestock, and particularly poultry, are the most common source, recent evidence suggests that environmental reservoirs (soil, water) play an important role in its transmission leading to product contamination and human infections. Antibiotics such as macrolides and fluoroquinolones are commonly used for treating campylobacteriosis in humans; however, there are reports of development of resistance to these drugs, and several resistance-imparting genes have been identified in Campylobacter. This increase in antibiotic resistance in the pathogen has fueled research exploring the potential of various alternative strategies to prevent food contamination and reduce Campylobacter infections in humans.

Our laboratory has extensively studied the efficacy of several phytochemicals and probiotics for controlling C. jejuni both at preharvest and postharvest stages. Results from our research and several other labs suggest that some of the plant-based compounds, probiotic strains, and bacteriophages have significant antimicrobial efficacy against C. jejuni and could improve food safety at various stages in food supply chain. This chapter discusses the potential of alternative approaches using phytochemicals, probiotic bacteria, and bacteriophages for controlling C. jejuni colonization in reservoir hosts, persistence in processing areas, survival in food products, and infections in humans. In addition, mechanistic studies delineating their potential mechanism(s) of actions are highlighted.

Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by the USDA and does not imply its approval to the exclusion of other products that may be suitable.

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References

  • Aguiar, V. F., Donoghue, A. M., Arsi, K., Reyes-Herrera, I., Metcalf, J. H., de los Santos, F. S., et al. (2013). Targeting motility properties of bacteria in the development of probiotic cultures against Campylobacter jejuni in broiler chickens. Foodborne Pathogens and Disease, 10(5), 435–441.

    Google Scholar 

  • Ahmed, M. U., Dunn, L., & Ivanova, E. P. (2012). Evaluation of current molecular approaches for genotyping of Campylobacter jejuni strains. Foodborne Pathogens and Disease, 9(5), 375–385.

    Google Scholar 

  • Alemka, A., Clyne, M., Shanahan, F., Tompkins, T., Corcionivoschi, N., & Bourke, B. (2010). Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infection and Immunity, 78(6), 2812–2822.

    Google Scholar 

  • Amour, C., Gratz, J., Mduma, E., Svensen, E., Rogawski, E. T., McGrath, M., et al. (2016). Epidemiology and impact of Campylobacter infection in children in 8 low-resource settings: Results from the MAL-ED study. Clinical Infectious Diseases, 63(9), 1171–1179.

    Google Scholar 

  • Anjorin, T. S., Salako, E. A., & Makun, H. A. (2013). Control of toxigenic fungi and mycotoxins with phytochemicals: Potentials and challenges. In Mycotoxin and food safety in developing countries. Rijeka, Croatia: InTech.

    Google Scholar 

  • Armon, R., Araujo, R., Kott, Y., Lucena, F., & Jofre, J. (1997). Bacteriophages of enteric bacteria in drinking water, comparison of their distribution in two countries. Journal of Applied Microbiology, 83(5), 627–633.

    Google Scholar 

  • Arsi, K., Donoghue, A. M., Venkitanarayanan, K., Kollanoor-Johny, A., Fanatico, A. C., Blore, P. J., et al. (2014). The efficacy of the natural plant extracts, thymol and carvacrol against Campylobacter colonization in broiler chickens. Journal of Food Safety, 34, 321–325.

    Google Scholar 

  • Arsi, K., Donoghue, A. M., Woo-Ming, A., Blore, P. J., & Donoghue, D. J. (2015a). The efficacy of selected probiotic and prebiotic combinations in reducing Campylobacter colonization in broiler chickens. Journal of Applied Poultry Research, 24(3), 327–334.

    Google Scholar 

  • Arsi, K., Donoghue, A. M., Woo-Ming, A., Blore, P. J., & Donoghue, D. J. (2015b). Intracloacal inoculation, an effective screening method for determining the efficacy of probiotic bacterial isolates against Campylobacter colonization in broiler chickens. Journal of Food Protection, 78(1), 209–213.

    Google Scholar 

  • Atterbury, R. J., Connerton, P. L., Dodd, C. E., Rees, C. E., & Connerton, I. F. (2003a). Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Applied and Environmental Microbiology, 69(10), 6302–6306.

    Google Scholar 

  • Atterbury, R. J., Connerton, P. L., Dodd, C. E., Rees, C. E., & Connerton, I. F. (2003b). Isolation and characterization of Campylobacter bacteriophages from retail poultry. Applied and Environmental Microbiology, 69(8), 4511–4518.

    Google Scholar 

  • Azizkhani, M., Misaghi, A., Basti, A. A., Gandomi, H., & Hosseini, H. (2013). Effects of Zataria multiflora Boiss. essential oil on growth and gene expression of enterotoxins A, C and E in Staphylococcus aureus ATCC 29213. International Journal of Food Microbiology, 163(2), 159–165.

    Google Scholar 

  • Bereswill, S., Ekmekciu, I., Escher, U., Fiebiger, U., Stingl, K., & Heimesaat, M. M. (2017). Lactobacillus johnsonii ameliorates intestinal, extra-intestinal and systemic pro-inflammatory immune responses following murine Campylobacter jejuni infection. Scientific Reports, 7(1), 2138.

    Google Scholar 

  • Bezek, K., Kurinčič, M., Knauder, E., Klančnik, A., Raspor, P., Bucar, F., et al. (2016). Attenuation of adhesion, biofilm formation and quorum sensing of Campylobacter jejuni by Euodia ruticarpa. Phytotherapy Research, 30(9), 1527–1532.

    Google Scholar 

  • Bigwood, T., Hudson, J. A., Billington, C., Carey-Smith, G. V., & Heinemann, J. A. (2008). Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiology, 25(2), 400–406.

    Google Scholar 

  • Bilia, A. R., Guccione, C., Isacchi, B., Righeschi, C., Firenzuoli, F., & Bergonzi, M. C. (2014). Essential oils loaded in nanosystems: A developing strategy for a successful therapeutic approach. Evidence-based Complementary and Alternative Medicine, 2014, 1–14.

    Google Scholar 

  • Blaser, M. J., & Engberg, J. (2008). Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In I. Nachamkin, C. Szymanski, & M. Blaser (Eds.), Campylobacter (3rd ed., pp. 99–121). Washington, DC: ASM Press.

    Google Scholar 

  • Brisbin, J. T., Gong, J., & Sharif, S. (2008). Interactions between commensal bacteria and the gut-associated immune system of the chicken. Animal Health Research Reviews, 9(1), 101–110.

    Google Scholar 

  • Brown, K., DeCoffe, D., Molcan, E., & Gibson, D. L. (2012). Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients, 4(8), 1095–1119.

    Google Scholar 

  • Bronowski, C., James, C. E. and Winstanley, C., 2014. Role of environmental survival in transmission of Campylobacter jejuni. FEMS microbiology letters, 356(1), 8–19.

    Google Scholar 

  • Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology, 94(3), 223–253.

    Google Scholar 

  • Candela, M., Perna, F., Carnevali, P., Vitali, B., Ciati, R., Gionchetti, P., et al. (2008). Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: Adhesion properties, competition against enteropathogens and modulation of IL-8 production. International Journal of Food Microbiology, 125(3), 286–292.

    Google Scholar 

  • Capparelli, R., Ventimiglia, I., Roperto, S., Fenizia, D., & Iannelli, D. (2006). Selection of an Escherichia coli O157: H7 bacteriophage for persistence in the circulatory system of mice infected experimentally. Clinical Microbiology and Infection, 12(3), 248–253.

    Google Scholar 

  • Cargill News Report. (2016). Essential oils key to Cargill’s comprehensive approach to reducing antibiotics in poultry. https://www.cargill.com/news/releases/2016/NA31925706.jsp

  • Carrillo, C. L., Atterbury, R. J., El-Shibiny, A., Connerton, P. L., Dillon, E., Scott, A., et al. (2005). Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Applied and Environmental Microbiology, 71(11), 6554–6563.

    Google Scholar 

  • Carvalho, C. M., Gannon, B. W., Halfhide, D. E., Santos, S. B., Hayes, C. M., Roe, J. M., et al. (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 Microbiology, 10(1), 232.

    Google Scholar 

  • 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 Biotechnology, 28(2), 106–122.

    Google Scholar 

  • Castillo, S., Heredia, N., & García, S. (2015). 2 (5H)-Furanone, epigallocatechin gallate, and a citric-based disinfectant disturb quorum-sensing activity and reduce motility and biofilm formation of Campylobacter jejuni. Folia Microbiologica, 60(1), 89–95.

    Google Scholar 

  • Cava-Roda, R. M., Taboada-Rodríguez, A., Valverde-Franco, M. T., & Marín-Iniesta, F. (2012). Antimicrobial activity of vanillin and mixtures with cinnamon and clove essential oils in controlling Listeria monocytogenes and Escherichia coli O157: H7 in milk. Food and Bioprocess Technology, 5(6), 2120–2131.

    Google Scholar 

  • CDC. (2014). Campylobacter. Available online at: https://www.cdc.gov/foodsafety/diseases/campylobacter/

  • CDC. (2017). Antibiotic resistance in campylobacter. Available online at: https://www.cdc.gov/campylobacter/campy-antibiotic-resistance.html

  • Chambers, J. R., & Gong, J. (2011). The intestinal microbiota and its modulation for Salmonella control in chickens. Food Research International, 44(10), 3149–3159.

    Google Scholar 

  • Chaveerach, P., Lipman, L. J. A., & Van Knapen, F. (2004). Antagonistic activities of several bacteria on in vitro growth of 10 strains of Campylobacter jejuni/coli. International Journal of Food Microbiology, 90(1), 43–50.

    Google Scholar 

  • Dasti, J. I., Tareen, A. M., Lugert, R., Zautner, A. E., & Groß, U. (2010). Campylobacter jejuni: A brief overview on pathogenicity-associated factors and disease-mediating mechanisms. International Journal of Medical Microbiology, 300(4), 205–211.

    Google Scholar 

  • Ding, W. K., & Shah, N. P. (2009). An improved method of microencapsulation of probiotic bacteria for their stability in acidic and bile conditions during storage. Journal of Food Science, 74(2), M53–M61.

    Google Scholar 

  • Donelli, G., Vuotto, C., & Mastromarino, P. (2013). Phenotyping and genotyping are both essential to identify and classify a probiotic microorganism. Microbial Ecology in Health and Disease, 24(1), 20105.

    Google Scholar 

  • Donoghue, A. M., Venkitanarayanan, K., Arsi, K., Woo-Ming, A., Upadhyaya, I., Kollanoor-Johny, A., et al. (2015). Organic poultry: Developing natural solutions for reducing pathogens and improving production. In: Proceedings of the Organic Agricultural Conference Proceedings (pp. 1–5).

    Google Scholar 

  • Doyle, M. P., & Erickson, M. C. (2006). Reducing the carriage of foodborne pathogens in livestock and poultry. Poultry Science, 85(6), 960–973.

    Google Scholar 

  • Duckworth, D. H., & Gulig, P. A. (2002). Bacteriophages. BioDrugs, 16(1), 57–62.

    Google Scholar 

  • Duncan, S. H., Belenguer, A., Holtrop, G., Johnstone, A. M., Flint, H. J., & Lobley, G. E. (2007). Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Applied and Environmental Microbiology, 73(4), 1073–1078.

    Google Scholar 

  • 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 Journal, 9, 2105–2246.

    Google Scholar 

  • Ekmekciu, I., von Klitzing, E., Fiebiger, U., Neumann, C., Bacher, P., Scheffold, A., et al. (2017). The probiotic compound VSL# 3 modulates mucosal, peripheral, and systemic immunity following murine broad-spectrum antibiotic treatment. Frontiers in Cellular and Infection Microbiology, 7, 167.

    Google Scholar 

  • 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. Journal of Food Protection, 72, 733–740.

    Google Scholar 

  • Engberg, J., Aarestrup, F. M., Taylor, D. E., Gerner-Smidt, P., & Nachamkin, I. (2001). Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: Resistance mechanisms and trends in human isolates. Emerging Infectious Diseases, 7, 24–34. https://doi.org/10.3201/eid0701.010104

    Google Scholar 

  • Felis, G. E., & Dellaglio, F. (2007). Taxonomy of lactobacilli and bifidobacteria. Current Issues in Intestinal Microbiology, 8(2), 44.

    Google Scholar 

  • Fernández, H., Vera, F., Villanueva, M. P., & García, A. (2008). Occurrence of Campylobacter species in healthy well-nourished and malnourished children. Brazilian Journal of Microbiology, 39(1), 56–58.

    Google Scholar 

  • Fiorentin, L., Vieira, N. D., & Barioni Jr., W. (2005). Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathology, 34(3), 258–263.

    Google Scholar 

  • Food Drug Administration. (2012). Code of federal regulations title 21 Part 172. Available online at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.cfm?CFRPart1/4172

  • Food Drug Administration. (2013). Everything Added to Food in the United States (EAFUS). Doc. No. 3045–2, 4-dihydroxybenzoic acid. Available online at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.cfm?

  • Food Drug Administration. (2015). Use of nanomaterials in food for animals. https://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM401508.pdf

  • Fooks, L. J., & Gibson, G. R. (2002). Probiotics as modulators of the gut flora. British Journal of Nutrition, 88(Suppl 1), S39–S49.

    Google Scholar 

  • Friedman, C. R. (2000). Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter (pp. 121–138). Washington, DC: ASM International.

    Google Scholar 

  • Fuller, R. (1989). Probiotics in man and animals. The Journal of Applied Bacteriology, 66, 365–378.

    Google Scholar 

  • Gauthier, R. (2003). Poultry therapeutics: New alternatives in nuevas alternativas en therapeutica aviar. In XVIII Latin American poultry congress 2003, Bolivia.

    Google Scholar 

  • Gautier, M., Rouault, A., Sommer, P., & Briandet, R. (1995). Occurrence of Propionibacterium freudenreichii bacteriophages in swiss cheese. Applied and Environmental Microbiology, 61(7), 2572–2576.

    Google Scholar 

  • Ghosh, S., Dai, C., Brown, K., Rajendiran, E., Makarenko, S., Baker, J., et al. (2011). Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. American Journal of Physiology-Gastrointestinal and Liver Physiology, 301(1), G39–G49.

    Google Scholar 

  • Gibreel, A., Kos, V. N., Keelan, M., Trieber, C. A., Levesque, S., Michaud, S., et al. (2005). Macrolide resistance in Campylobacter jejuni and Campylobacter coli: Molecular mechanism and stability of the resistance phenotype. Journal of Antimicrobial Chemotherapy, 49, 2753–2759. https://doi.org/10.1128/AAC.49.7.2753-2759.2005

    Google Scholar 

  • Gibreel, A., & Taylor, D. E. (2006). Macrolide resistance in Campylobacter jejuni and Campylobacter coli. Journal of Antimicrobial Chemotherapy, 58, 243–255. https://doi.org/10.1093/jac/dkl210

    Google Scholar 

  • Gillespie, I. A., O’Brien, S. J., Adak, G. K., Tam, C. C., Frost, J. A., Bolton, F. J., et al. (2003). Point source outbreaks of Campylobacter jejuni infection--are they more common than we think and what might cause them? Epidemiology and Infection, 130(3), 367.

    Google Scholar 

  • Goode, D., Allen, V. M., & Barrow, P. A. (2003). Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Applied and Environmental Microbiology, 69(8), 5032–5036.

    Google Scholar 

  • Guerin-Danan, C., Chabanet, C., Pedone, C., Popot, F., Vaissade, P., Bouley, C., et al. (1998). Milk fermented with yogurt cultures and Lactobacillus casei compared with yogurt and gelled milk: Influence on intestinal microflora in healthy infants. The American Journal of Clinical Nutrition, 67(1), 111–117.

    Google Scholar 

  • Gul, P., & Bakht, J. (2015). Antimicrobial activity of turmeric extract and its potential use in food industry. Journal of Food Science and Technology, 52(4), 2272–2279.

    Google Scholar 

  • Gutierrez, J., Barry-Ryan, C., & Bourke, P. (2008). The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. International Journal of Food Microbiology, 124(1), 91–97.

    Google Scholar 

  • Haddad, N., Burns, C. M., Bolla, J. M., Prévost, H., Fédérighi, M., & Drider, D. (2009). Long-term survival of Campylobacter jejuni at low temperatures is dependent on polynucleotide phosphorylase activity. Applied and Environmental Microbiology, 75(23), 7310–7318.

    Google Scholar 

  • Hampton, T. (2013). Report reveals scope of US antibiotic resistance threat. JAMA, 310(16), 1661–1663.

    Google Scholar 

  • Handy, R. D., & Shaw, B. J. (2007). Toxic effects of nanoparticles and nanomaterials: Implications for public health, risk assessment and the public perception of nanotechnology. Health Risk Society, 9(2), 125–144.

    Google Scholar 

  • Hanning, I., Jarquin, R., & Slavik, M. (2008). Campylobacter jejuni as a secondary colonizer of poultry biofilms. Journal of Applied Microbiology, 105(4), 1199–1208.

    Google Scholar 

  • Harborne, J. R. (1993). Introduction to ecological biochemistry (4th ed.). London: Elsevier.

    Google Scholar 

  • Hermans, D., Martel, A., Van Deun, K., Van Immerseel, F., Heyndrickx, M., Haesebrouck, F., et al. (2011a). The cinnamon-oil ingredient trans-cinnamaldehyde fails to target Campylobacter jejuni strain KC 40 in the broiler chicken cecum despite marked in vitro activity. Journal of Food Protection, 74(10), 1729–1734.

    Google Scholar 

  • Hermans, D., Pasmans, F., Messens, W., Martel, A., Van Immerseel, F., Rasschaert, G., et al. (2012). Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector-Borne and Zoonotic Diseases, 12(2), 89–98.

    Google Scholar 

  • Hermans, D., Van Deun, K., Martel, A., Van Immerseel, F., Messens, W., Heyndrickx, M., et al. (2011b). Colonization factors of Campylobacter jejuni in the chicken gut. Veterinary Research, 42(1), 82.

    Google Scholar 

  • Higgins, J. P., Higgins, S. E., Guenther, K. L., Huff, W., Donoghue, A. M., Donoghue, D. J., et al. (2005). Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poultry Science, 84(7), 1141–1145.

    Google Scholar 

  • Hilbert, F., Scherwitzel, M., Paulsen, P., & Szostak, M. P. (2010). Survival of Campylobacter jejuni under conditions of atmospheric oxygen tension with the support of Pseudomonas spp. Applied and Environmental Microbiology, 76(17), 5911–5917.

    Google Scholar 

  • Ho, K. (2001). Bacteriophage therapy for bacterial infections: Rekindling a memory from the pre-antibiotics era. Perspectives in Biology and Medicine, 44(1), 1–16.

    Google Scholar 

  • Holzapfel, W. H., Geisen, R., & Schillinger, U. (1995). Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. International Journal of Food Microbiology, 24(3), 343–362.

    Google Scholar 

  • Huff, W. E., Huff, G. R., Rath, N. C., Balog, J. M., & Donoghue, A. M. (2005). Alternatives to antibiotics: Utilization of bacteriophage to treat colibacillosis and prevent foodborne pathogens. Poultry Science, 84(4), 655–659.

    Google Scholar 

  • Hyldgaard, M., Mygind, T., & Meyer, R. L. (2012). Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components. Frontiers in Microbiology, 3, 12.

    Google Scholar 

  • Isman, M. B. (2000). Plant essential oils for pest and disease management. Crop Protection, 19(8), 603–608.

    Google Scholar 

  • Janež, N., & Loc-Carrillo, C. (2013). Use of phages to control Campylobacter spp. Journal of Microbiological Methods, 95(1), 68–75.

    Google Scholar 

  • Joshua, G. P., Guthrie-Irons, C., Karlyshev, A. V., & Wren, B. W. (2006). Biofilm formation in Campylobacter jejuni. Microbiology, 152(2), 387–396.

    Google Scholar 

  • Kaakoush, N. O., Castaño-Rodríguez, N., Mitchell, H. M., & Man, S. M. (2015). Global epidemiology of Campylobacter infection. Clinical Microbiology Reviews, 28(3), 687–720.

    Google Scholar 

  • Kechagia, M., Basoulis, D., Konstantopoulou, S., Dimitriadi, D., Gyftopoulou, K., Skarmoutsou, N., et al. (2013). Health benefits of probiotics: A review. ISRN Nutrition, 2013, 7.

    Google Scholar 

  • Kennedy, D. O., & Wightman, E. L. (2011). Herbal extracts and phytochemicals: Plant secondary metabolites and the enhancement of human brain function. Advances in Nutrition, 2(1), 32–50.

    Google Scholar 

  • Kittler, S., Fischer, S., Abdulmawjood, A., Glünder, G., & Klein, G. (2013). Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. Applied and Environmental Microbiology, 79(23), 7525–7533.

    Google Scholar 

  • Koh, C. L., Sam, C. K., Yin, W. F., Tan, L. Y., Krishnan, T., Chong, Y. M., et al. (2013). Plant-derived natural products as sources of anti-quorum sensing compounds. Sensors, 13(5), 6217–6228.

    Google Scholar 

  • Kollanoor Johny, A., Darre, M. J., Donoghue, A. M., Donoghue, D. J., & Venkitanarayanan, K. (2010). Antibacterial effect of trans-cinnamaldehyde, eugenol, carvacrol, and thymol on Salmonella Enteritidis and Campylobacter jejuni in chicken cecal contents in vitro. Journal of Applied Poultry Research, 19(3), 237–244.

    Google Scholar 

  • Kollanoor-Johny, A., Upadhyay, A., Baskaran, S. A., Upadhyaya, I., Mooyottu, S., Mishra, N., et al. (2012). Effect of therapeutic supplementation of the plant compounds trans-cinnamaldehyde and eugenol on Salmonella enterica serovar Enteritidis colonization in market-age broiler chickens 1 2. Journal of Applied Poultry Research, 21(4), 816–822.

    Google Scholar 

  • Kovács, J. K., Felső, P., Makszin, L., Pápai, Z., Horváth, G., Ábrahám, H., et al. (2016). Antimicrobial and virulence-modulating effects of clove essential oil on the foodborne pathogen Campylobacter jejuni. Applied and Environmental Microbiology, 82(20), 6158–6166.

    Google Scholar 

  • Kuroki, S., Saida, T., Nukina, M., Haruta, T., Yoshioka, M., Kobayashi, Y., et al. (1993). Campylobacter jejuni strains from patients with guillain-barré syndrome belong mostly to penner serogroup 19 and contain β-N-acetylglucosamine residues. Annals of Neurology, 33(3), 243–247.

    Google Scholar 

  • Leriche, V., & Carpentier, B. (2000). Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms. Journal of Applied Microbiology, 88(4), 594–605.

    Google Scholar 

  • Li, J., Dong, J., Qiu, J. Z., Wang, J. F., Luo, M. J., Li, H. E., et al. (2011). Peppermint oil decreases the production of virulence-associated exoproteins by Staphylococcus aureus. Molecules, 16(2), 1642–1654.

    Google Scholar 

  • Lin, J. (2009). Novel approaches for Campylobacter control in poultry. Foodborne Pathogens and Disease, 6(7), 755–765.

    Google Scholar 

  • Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C. M., & Zhang, Q. (2009). Antibiotic resistance in Campylobacter: Emergence, transmission and persistence. Future Microbiology, 4(2), 189–200.

    Google Scholar 

  • Magajna, B. A., & Schraft, H. (2015). Campylobacter jejuni biofilm cells become viable but non-culturable (VBNC) in low nutrient conditions at 4C more quickly than their planktonic counterparts. Food Control, 50, 45–50.

    Google Scholar 

  • Mai, V., Ukhanova, M., Visone, L., Abuladze, T., & Sulakvelidze, A. (2010). Bacteriophage administration reduces the concentration of Listeria monocytogenes in the gastrointestinal tract and its translocation to spleen and liver in experimentally infected mice. International Journal of Microbiology, 2010, 624234.

    Google Scholar 

  • Maura, D., Galtier, M., Le Bouguénec, C., & Debarbieux, L. (2012). Virulent bacteriophages can target O104: H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrobial Agents and Chemotherapy, 56(12), 6235–6242.

    Google Scholar 

  • Maynard, A. D., Aitken, R. J., Butz, T., Colvin, V., Donaldson, K., Oberdörster, G., et al. (2006). Safe handling of nanotechnology. Nature, 444(7117), 267–269.

    Google Scholar 

  • Merril, C. R., Scholl, D., & Adhya, S. L. (2003). The prospect for bacteriophage therapy in Western medicine. Nature Reviews. Drug Discovery, 2(6), 489.

    Google Scholar 

  • Meunier, M., Guyard‐Nicodème, M., Dory, D. and Chemaly, M., (2016). Control strategies against C ampylobacter at the poultry production level: biosecurity measures, feed additives and vaccination. Journal of Applied Microbiology, 120(5),1139–1173.

    Google Scholar 

  • Moore-Neibel, K., Gerber, C., Patel, J., Friedman, M., & Ravishankar, S. (2012). Antimicrobial activity of lemongrass oil against Salmonella enterica on organic leafy greens. Journal of Applied Microbiology, 112(3), 485–492.

    Google Scholar 

  • Morishita, T. Y., Aye, P. P., Harr, B. S., Cobb, C. W., & Clifford, J. R. (1997). Evaluation of an avian-specific probiotic to reduce the colonization and shedding of Campylobacter jejuni in broilers. Avian Diseases, 41(4), 850–855.

    Google Scholar 

  • Murphy, C., Carroll, C., & Jordan, K. N. (2006). Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. Journal of Applied Microbiology, 100(4), 623–632.

    Google Scholar 

  • Nachamkin, I., Szymanski, C. M., & Blaser, M. J. (2008). Campylobacter (3rd ed.). Washington, DC: ASM Press.

    Google Scholar 

  • National Research Council. (2007). Toxicity testing in the 21st century: A vision and a strategy. Washington, DC: National Academies Press.

    Google Scholar 

  • Ncube, B., Finnie, J. F., & Van Staden, J. (2012). In vitro antimicrobial synergism within plant extract combinations from three South African medicinal bulbs. Journal of Ethnopharmacology, 139(1), 81–89.

    Google Scholar 

  • Negi, P. S. (2012). Plant extracts for the control of bacterial growth: Efficacy, stability and safety issues for food application. International Journal of Food Microbiology, 156(1), 7–17.

    Google Scholar 

  • Nielsen, E. M., Engberg, J., Fussing, V., Petersen, L., Brogren, C. H., & On, S. L. (2000). Evaluation of phenotypic and genotypic methods for subtyping Campylobacter jejuni isolates from humans, poultry, and cattle. Journal of Clinical Microbiology, 38(10), 3800–3810.

    Google Scholar 

  • Newell, D. G., Elvers, K. T., Dofper, D., Hansson, I., Jones, P., James, S., Gittins, J., Stern, N. J., Davies, R., Connerton, I. and Pearson, D. (2011). A critical review of biosecurity-based interventions and strategies to reduce Campylobacter on the poultry farm. Applied and Environmental Microbiology, AEM-01090.

    Google Scholar 

  • Nikkhahi, F., Dallal, M. M. S., Alimohammadi, M., Foroushani, A. R., Rajabi, Z., Fardsanei, F., et al. (2017). Phage therapy: Assessment of the efficacy of a bacteriophage isolated in the treatment of salmonellosis induced by Salmonella Enteritidis in mice. Gastroenterology and Hepatology from Bed to Bench, 10(2), 131.

    Google Scholar 

  • Nishiyama, K., Seto, Y., Yoshioka, K., Kakuda, T., Takai, S., Yamamoto, Y., et al. (2014). Lactobacillus gasseri SBT2055 reduces infection by and colonization of Campylobacter jejuni. PLoS One, 9(9), e108827.

    Google Scholar 

  • Oakley, B. B., Lillehoj, H. S., Kogut, M. H., Kim, W. K., Maurer, J. J., Pedroso, A., et al. (2014). The chicken gastrointestinal microbiome. FEMS Microbiology Letters, 360(2), 100–112.

    Google Scholar 

  • Oh, E., McMullen, L. M., Chui, L., & Jeon, B. (2017). Differential survival of hyper-aerotolerant Campylobacter jejuni under different gas conditions. Frontiers in Microbiology, 8, 954.

    Google Scholar 

  • Olkkola, S., Culebro, A., Juntunen, P., Hänninen, M. L., & Rossi, M. (2016). Functional genomics in Campylobacter coli identified a novel streptomycin resistance gene located in a hypervariable genomic region. Microbiology, 162(7), 1157–1166.

    Google Scholar 

  • Olszak, T., An, D., Zeissig, S., Vera, M. P., Richter, J., Franke, A., et al. (2012). Microbial exposure during early life has persistent effects on natural killer T cell function. Science, 336(6080), 489–493.

    Google Scholar 

  • On, S. L. (2001). Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: Current status, future prospects and immediate concerns. Journal of Applied Microbiology, 90(S6), 1S–15S.

    Google Scholar 

  • Orquera, S., Gölz, G., Hertwig, S., Hammerl, J., Sparborth, D., Joldic, A., et al. (2012). Control of Campylobacter spp. and Yersinia enterocolitica by virulent bacteriophages. Journal of Molecular and Genetic Medicine, 6, 273.

    Google Scholar 

  • Ouwehand, A. C., Derrien, M., de Vos, W., Tiihonen, K., & Rautonen, N. (2005). Prebiotics and other microbial substrates for gut functionality. Current Opinion in Biotechnology, 16(2), 212–217.

    Google Scholar 

  • Parisi, C., Vigani, M., & Rodríguez-Cerezo, E. (2015). Agricultural nanotechnologies: What are the current possibilities? Nano Today, 10(2), 124–127.

    Google Scholar 

  • Park, S. H., Lee, S. I., & Ricke, S. C. (2016). Microbial populations in naked neck chicken ceca raised on pasture flock fed with commercial yeast cell wall prebiotics via an Illumina MiSeq platform. PLoS One, 11(3), e0151944.

    Google Scholar 

  • Parsaeimehr, M., Basti, A. A., Radmehr, B., Misaghi, A., Abbasifar, A., Karim, G., et al. (2010). Effect of Zataria multiflora boiss. Essential oil, nisin, and their combination on the production of enterotoxin C and α-hemolysin by Staphylococcus aureus. Foodborne Pathogens and Disease, 7(3), 299–305.

    Google Scholar 

  • Persson, T., Hansen, T. H., Rasmussen, T. B., Skindersø, M. E., Givskov, M., & Nielsen, J. (2005). Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Organic & Biomolecular Chemistry, 3(2), 253–262.

    Google Scholar 

  • Pintar, K. D., Christidis, T., Thomas, M. K., Anderson, M., Nesbitt, A., Keithlin, J., et al. (2015). A systematic review and meta-analysis of the Campylobacter spp. prevalence and concentration in household pets and petting zoo animals for use in exposure assessments. PLoS One, 10(12), e0144976.

    Google Scholar 

  • Plummer, P., Sahin, O., Burrough, E., Sippy, R., Mou, K., Rabenold, J., et al. (2012). Critical role of LuxS in the virulence of Campylobacter jejuni in a guinea pig model of abortion. Infection and Immunity, 80(2), 585–593.

    Google Scholar 

  • Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalog established by metagenomic sequencing. Nature, 464(7285), 59.

    Google Scholar 

  • Qiu, J., Wang, D., Xiang, H., Feng, H., Jiang, Y., Xia, L., et al. (2010). Subinhibitory concentrations of thymol reduce enterotoxins A and B and α-hemolysin production in Staphylococcus aureus isolates. PLoS One, 5(3), e9736.

    Google Scholar 

  • Qiu, J., Wang, J., Luo, H., Du, X., Li, H., Luo, M., et al. (2011). The effects of subinhibitory concentrations of costus oil on virulence factor production in Staphylococcus aureus. Journal of Applied Microbiology, 110(1), 333–340.

    Google Scholar 

  • Reeser, R. J., Medler, R. T., Billington, S. J., Jost, B. H., & Joens, L. A. (2007). Characterization of Campylobacter jejuni biofilms under defined growth conditions. Applied and Environmental Microbiology, 73(6), 1908–1913.

    Google Scholar 

  • Reichling, J. (2010). Plant-Microbe Interactions and Secondary Metabolites with Antibacterial, Antifungal and Antiviral Properties. In Annual plant reviews volume 39: Functions and biotechnology of plant secondary metabolites (2nd ed., pp. 214–347). Oxford, UK: Blackwell.

    Google Scholar 

  • Reuter, M., Mallett, A., Pearson, B. M., & van Vliet, A. H. (2010). Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Applied and Environmental Microbiology, 76(7), 2122–2128.

    Google Scholar 

  • Ricke, S. C. (2015). Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems 1. Poultry Science, 94(6), 1411–1418.

    Google Scholar 

  • Rohwer, F. (2003). Global phage diversity. Cell, 113(2), 141.

    Google Scholar 

  • Romero-Barrios, P., Hempen, M., Messens, W., Stella, P., & Hugas, M. (2013). Quantitative microbiological risk assessment (QMRA) of food-borne zoonoses at the European level. Food Control, 29(2), 343–349.

    Google Scholar 

  • Rosenquist, H., Nielsen, N. L., Sommer, H. M., Nørrung, B., & Christensen, B. B. (2003). Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology, 83(1), 87–103.

    Google Scholar 

  • Saint-Cyr, M. J., Guyard-Nicodème, M., Messaoudi, S., Chemaly, M., Cappelier, J. M., Dousset, X., et al. (2016). Recent advances in screening of anti-Campylobacter activity in probiotics for use in poultry. Frontiers in Microbiology, 7, 553.

    Google Scholar 

  • Sanders, M. E., & Marco, M. L. (2010). Food formats for effective delivery of probiotics. Annual Review of Food Science and Technology, 1, 65–85.

    Google Scholar 

  • Sanders, S. Q., Boothe, D. H., Frank, J. F., & Arnold, J. W. (2007). Culture and detection of Campylobacter jejuni within mixed microbial populations of biofilms on stainless steel. Journal of Food Protection, 70(6), 1379–1385.

    Google Scholar 

  • Santiesteban-López, A., Palou, E., & López-Malo, A. (2007). Susceptibility of food-borne bacteria to binary combinations of antimicrobials at selected aw and pH. Journal of Applied Microbiology, 102(2), 486–497.

    Google Scholar 

  • 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. International Journal of Food Microbiology, 141, S98–S108.

    Google Scholar 

  • Sarker, S. A., McCallin, S., Barretto, C., Berger, B., Pittet, A. C., Sultana, S., et al. (2012). Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology, 434(2), 222–232.

    Google Scholar 

  • Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Diseases, 17(1), 7.

    Google Scholar 

  • Scharff, R. L. (2012). Economic burden from health losses due to foodborne illness in the United States. Journal of Food Protection, 75(1), 123–131.

    Google Scholar 

  • Schroeder, B. O., & Bäckhed, F. (2016). Signals from the gut microbiota to distant organs in physiology and disease. Nature Medicine, 22(10), 1079–1089.

    Google Scholar 

  • Serban, D. E. (2014). Gastrointestinal cancers: Influence of gut microbiota, probiotics and prebiotics. Cancer Letters, 345, 258–270.

    Google Scholar 

  • Sergeant, M. J., Constantinidou, C., Cogan, T. A., Bedford, M. R., Penn, C. W., & Pallen, M. J. (2014). Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One, 9(3), e91941.

    Google Scholar 

  • Shin, H., Lee, J. H., Kim, H., Choi, Y., Heu, S., & Ryu, S. (2012). Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica serovar Typhimurium. PLoS One, 7(8), e43392.

    Google Scholar 

  • Shrestha, S., Donoghue, A., Arsi, K., Upadhyay, A., Wagle, B. R., Venkitanarayanan, K., et al. 2017. A carvacrol wash and/or a chitosan-based coating reduced Campylobacter jejuni on chicken wingettes. In Poultry Science Association Annual Meeting, Orlando, FL

    Google Scholar 

  • Si, W., Gong, J., Chanas, C., Cui, S., Yu, H., Caballero, C., et al. (2006). In vitro assessment of antimicrobial activity of carvacrol, thymol and cinnamaldehyde towards Salmonella serotype Typhimurium DT104: Effects of pig diets and emulsification in hydrocolloids. Journal of Applied Microbiology, 101(6), 1282–1291.

    Google Scholar 

  • Sillankorva, S. M., Oliveira, H., & Azeredo, J. (2012). Bacteriophages and their role in food safety. International Journal of Microbiology, 2012, 863945.

    Google Scholar 

  • Sime-Ngando, T. (2014). Environmental bacteriophages: Viruses of microbes in aquatic ecosystems. Frontiers in Microbiology, 5, 355.

    Google Scholar 

  • Simões, M., Simoes, L. C., & Vieira, M. J. (2010). A review of current and emergent biofilm control strategies. LWT-Food Science and Technology, 43(4), 573–583.

    Google Scholar 

  • Siringan, P., Connerton, P. L., Payne, R. J., & Connerton, I. F. (2011). Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Applied and Environmental Microbiology, 77(10), 3320–3326.

    Google Scholar 

  • Skarp, C. P. A., Hänninen, M. L., & Rautelin, H. I. K. (2016). Campylobacteriosis: The role of poultry meat. Clinical Microbiology and Infection, 22(2), 103–109.

    Google Scholar 

  • Smrekar, F., Ciringer, M., Peterka, M., Podgornik, A., & Štrancar, A. (2008). Purification and concentration of bacteriophage T4 using monolithic chromatographic supports. Journal of Chromatography B, 861(2), 177–180.

    Google Scholar 

  • Sonnenburg, J. L., Xu, J., Leip, D. D., Chen, C. H., Westover, B. P., Weatherford, J., et al. (2005). Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science, 307(5717), 1955–1959.

    Google Scholar 

  • Stern, N. J., Cox, N. A., Musgrove, M. T., & Park, C. M. (2001). Incidence and levels of Campylobacter in broilers after exposure to an inoculated seeder bird. Journal of Applied Poultry Research, 10(4), 315–318.

    Google Scholar 

  • Sulakvelidze, A., & Barrow, P. (2005). Phage therapy in animals and agribusiness. In E. Kutter & A. Sulakvelidze (Eds.), Bacteriophages: Biology and applications (pp. 335–380). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Sulakvelidze, A. K., & Kutter, E. (2005). Bacteriophage therapy in humans. In Bacteriophages: Biology and applications (pp. 381–436). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Taboada, E. N., Clark, C. G., Sproston, E. L., & Carrillo, C. D. (2013). Current methods for molecular typing of Campylobacter species. Journal of Microbiological Methods, 95(1), 24–31.

    Google Scholar 

  • Tang, Y., Sahin, O., Pavlovic, N., LeJeune, J., Carlson, J., Wu, Z., et al. (2017). Rising fluoroquinolone resistance in Campylobacter isolated from feedlot cattle in the United States. Scientific Reports, 7, 494.

    Google Scholar 

  • Tareb, R., Bernardeau, M., Gueguen, M., & Vernoux, J. P. (2013). In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. Journal of Medical Microbiology, 62(4), 637–649.

    Google Scholar 

  • Tassou, C. C., Drosinos, E. H., & Nychas, G. J. E. (1995). Effects of essential oil from mint (Mentha piperita) on Salmonella enteritidis and Listeria monocytogenes in model food systems at 4 and 10 C. Journal of Applied Microbiology, 78(6), 593–600.

    Google Scholar 

  • Teh, K. H., Flint, S., & French, N. (2010). Biofilm formation by Campylobacter jejuni in controlled mixed-microbial populations. International Journal of Food Microbiology, 143(3), 118–124.

    Google Scholar 

  • Thomrongsuwannakij, T., Chuanchuen, R., & Chansiripornchai, N. (2016). Identification of competitive exclusion and its ability to protect against Campylobacter jejuni in broilers. The Thai Journal of Veterinary Medicine, 46(2), 279–286.

    Google Scholar 

  • Thongson, C., Davidson, P. M., Mahakarnchanakul, W., & Weiss, J. (2004). Antimicrobial activity of ultrasound-assisted solvent-extracted spices. Letters in Applied Microbiology, 39(5), 401–406.

    Google Scholar 

  • Trachoo, N., & Frank, J. F. (2002). Effectiveness of chemical sanitizers against Campylobacter jejuni–containing biofilms. Journal of Food Protection, 65(7), 1117–1121.

    Google Scholar 

  • Trigui, H., Paquet, V. E., Charette, S. J., & Faucher, S. P. (2016). Packaging of Campylobacter jejuni into multilamellar bodies by the ciliate Tetrahymena pyriformis. Applied and Environmental Microbiology, 82(9), 2783–2790.

    Google Scholar 

  • Upadhyay, A., Arsi, K., Wagle, B. R., Upadhyaya, I., Shrestha, S., Donoghue, A. M., et al. (2017a). Trans-Cinnamaldehyde, Carvacrol, and Eugenol Reduce Campylobacter jejuni Colonization Factors and Expression of Virulence Genes in Vitro. Frontiers in Microbiology, 8, 713.

    Google Scholar 

  • Upadhyay, A., Johny, A. K., Amalaradjou, M. A. R., Baskaran, S. A., Kim, K. S., & Venkitanarayanan, K. (2012). Plant-derived antimicrobials reduce Listeria monocytogenes virulence factors in vitro, and down-regulate expression of virulence genes. International Journal of Food Microbiology, 157(1), 88–94.

    Google Scholar 

  • Upadhyay, A., Upadhyaya, I., Kollanoor-Johny, A., & Venkitanarayanan, K. (2013). Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food Microbiology, 36(1), 79–89.

    Google Scholar 

  • Upadhyay, A., Wagle, B. R., Shrestha, S., Upadhyaya, I., Arsi, K., Bhargava, K., et al. 2017b. Antimicrobial wash with Trans-cinnamaldehyde nanoemulsion reduces Campylobacter jejuni on chicken skin. In Poultry Science Association Annual Meeting, Orlando, FL.

    Google Scholar 

  • Upadhyaya, I., Upadhyay, A., Kollanoor-Johny, A., Mooyottu, S., Baskaran, S. A., Yin, H. B., et al. (2015). In-feed supplementation of trans-cinnamaldehyde reduces layer-chicken egg-borne transmission of Salmonella enterica serovar Enteritidis. Applied and Environmental Microbiology, 81(9), 2985–2994.

    Google Scholar 

  • Van Alphen, L. B., Burt, S. A., Veenendaal, A. K., Bleumink-Pluym, N. M., & Van Putten, J. P. (2012). The natural antimicrobial carvacrol inhibits Campylobacter jejuni motility and infection of epithelial cells. PLoS One, 7(9), e45343.

    Google Scholar 

  • Venkitanarayanan, K., Kollanoor-Johny, A., Darre, M. J., Donoghue, A. M., & Donoghue, D. J. (2013). Use of plant-derived antimicrobials for improving the safety of poultry products. Poultry Science, 92(2), 493–501.

    Google Scholar 

  • Wagenaar, J. A., French, N. P., & Havelaar, A. H. (2013). Preventing Campylobacter at the source: Why is it so difficult? Clinical Infectious Diseases, 57(11), 1600–1606.

    Google Scholar 

  • Wagenaar, J. A., Newell, D. G., Kalupahana, R. S., & Mughini-Gras, L. (2015). Campylobacter: Animal reservoirs, human infections, and options for control. In Zoonoses-Infections Affecting Humans and Animals (pp. 159–177). Dordrecht, Netherlands: Springer.

    Google Scholar 

  • Wagenaar, J. A., Van Bergen, M. A., Mueller, M. A., Wassenaar, T. M., & Carlton, R. M. (2005). Phage therapy reduces Campylobacter jejuni colonization in broilers. Veterinary Microbiology, 109(3), 275–283.

    Google Scholar 

  • Wagle, B. R., Donoghue, A. M., Arsi, K., Upadhyay, A., Shrestha, S., Blore, P.J., et al. (2016). Eugenol wash and chitosan-based coating reduces Campylobacter jejuni counts on poultry products. In Poultry Science Association Annual Meeting, New Orleans, LA.

    Google Scholar 

  • Wagle, B. R., Upadhyay, A., Arsi, K., Shrestha, S., Venkitanarayanan, K., Donoghue, A. M., et al. (2017a). Application of β-resorcylic acid as potential antimicrobial feed additive to reduce Campylobacter colonization in broiler chickens. Frontiers in Microbiology, 8, 599.

    Google Scholar 

  • Wagle, B. R., Upadhyay, A., Arsi, K., Upadhyaya, I., Shrestha, S., Blore, P.J., et al. (2017b). Phytochemicals reduce biofilm formation and inactivates mature biofilm of Campylobacter jejuni. In Poultry Science Association Annual Meeting, Orlando, FL.

    Google Scholar 

  • Wagner, R. D., Johnson, S. J., & Kurniasih Rubin, D. (2009). Probiotic bacteria are antagonistic to Salmonella enterica and Campylobacter jejuni and influence host lymphocyte responses in human microbiota-associated immunodeficient and immunocompetent mice. Molecular Nutrition & Food Research, 53(3), 377–388.

    Google Scholar 

  • Wassenaar, T. M., & Newell, D. G. (2000). Genotyping of Campylobacter spp. Applied and Environmental Microbiology, 66(1), 1–9.

    Google Scholar 

  • Weber-Dąbrowska, B., Mulczyk, M., & Górski, A. (2001). Bacteriophage therapy of bacterial infections: An update of our institute’s experience. In Inflammation (pp. 201–209). Dordrecht, Netherlands: Springer.

    Google Scholar 

  • Wine, E., Gareau, M. G., Johnson-Henry, K., & Sherman, P. M. (2009). Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. FEMS Microbiology Letters, 300(1), 146–152.

    Google Scholar 

  • Woo-Ming, A., Arsi, K., Donoghue, A. M., Moyle, J. R., & Donoghue, D. J. (2016). Efficacy of natural cranberry extracts against Campylobacter colonization in poultry. International Journal of Food Engineering, 2, 66–70.

    Google Scholar 

  • Yin, H. B., Chen, C. H., Kollanoor-Johny, A., Darre, M. J., & Venkitanarayanan, K. (2015). Controlling Aspergillus flavus and Aspergillus parasiticus growth and aflatoxin production in poultry feed using carvacrol and trans-cinnamaldehyde. Poultry Science, 94(9), 2183–2190.

    Google Scholar 

  • Young, K. T., Davis, L. M., & DiRita, V. J. (2007). Campylobacter jejuni: Molecular biology and pathogenesis. Nature Reviews. Microbiology, 5(9), 665.

    Google Scholar 

  • Zhao, T., Doyle, M. P., & Zhao, P. (2004). Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Applied and Environmental Microbiology, 70(7), 3996–4003.

    Google Scholar 

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Upadhyay, A., Arsi, K., Upadhyaya, I., Donoghue, A.M., Donoghue, D.J. (2019). Natural and Environmentally Friendly Strategies for Controlling Campylobacter jejuni Colonization in Poultry, Survival in Poultry Products and Infection in Humans. In: Venkitanarayanan, K., Thakur, S., Ricke, S. (eds) Food Safety in Poultry Meat Production. Food Microbiology and Food Safety(). Springer, Cham. https://doi.org/10.1007/978-3-030-05011-5_4

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