ORIGINAL ARTICLE
Eugenol as an antimicrobial wash treatment reduces Campylobacter jejuni in postharvest poultry
Basanta R. Wagle,
Komala Arsi,
Sandip Shrestha,
Abhinav Upadhyay,
Indu Upadhyaya,
Kanika Bhargava,
Annie Donoghue,
Dan J. Donoghue,
Basanta R. Wagle
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorKomala Arsi
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorSandip Shrestha
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorAbhinav Upadhyay
Department of Animal Science, University of Connecticut, Storrs, Connecticut
Search for more papers by this authorIndu Upadhyaya
School of Agriculture, Tennessee Tech University, Cookeville, Tennessee
Search for more papers by this authorKanika Bhargava
Department of Human Environmental Sciences, University of Central Oklahoma, Edmond, Oklahoma
Search for more papers by this authorAnnie Donoghue
Poultry Production and Product Safety Research Unit, ARS, USDA, Fayetteville, Arkansas
Search for more papers by this authorCorresponding Author
Dan J. Donoghue
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Correspondence
Dan J. Donoghue, Department of Poultry Science, University of Arkansas, O 408, 1260 W Maple St, Fayetteville, AR.
Email: [email protected]
Search for more papers by this authorBasanta R. Wagle,
Komala Arsi,
Sandip Shrestha,
Abhinav Upadhyay,
Indu Upadhyaya,
Kanika Bhargava,
Annie Donoghue,
Dan J. Donoghue,
Basanta R. Wagle
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorKomala Arsi
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorSandip Shrestha
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Search for more papers by this authorAbhinav Upadhyay
Department of Animal Science, University of Connecticut, Storrs, Connecticut
Search for more papers by this authorIndu Upadhyaya
School of Agriculture, Tennessee Tech University, Cookeville, Tennessee
Search for more papers by this authorKanika Bhargava
Department of Human Environmental Sciences, University of Central Oklahoma, Edmond, Oklahoma
Search for more papers by this authorAnnie Donoghue
Poultry Production and Product Safety Research Unit, ARS, USDA, Fayetteville, Arkansas
Search for more papers by this authorCorresponding Author
Dan J. Donoghue
Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas
Correspondence
Dan J. Donoghue, Department of Poultry Science, University of Arkansas, O 408, 1260 W Maple St, Fayetteville, AR.
Email: [email protected]
Search for more papers by this authorFunding information: USDA-NIFA-OREI, Grant/Award Number: 2017-51300-26815
Abstract
The efficacy of the natural plant-derived compound, eugenol (EG), as an antimicrobial wash treatment to reduce Campylobacter jejuni in postharvest poultry was investigated. The antimicrobial efficacy of EG was studied as a suspension, emulsion, or nanoemulsion treatment (two trials each). In each trial, chicken skin samples were inoculated with C. jejuni (∼7.2 Log CFU/sample), washed with treatments (0, 0.125, 0.25, 0.5, 1, or 2% EG corresponds to 0, 7.61, 15.22, 30.45, 60.90, or 121.8 mM, respectively) for 1 min, drip dried for 2 min, and then processed at 0, 8, and 24 hr of refrigerated storage (n = 5 samples/treatment/time point). All doses of the EG suspension consistently reduced C. jejuni counts with the greatest reduction (>2.0 Log CFU/sample) for the 2% dose when compared with controls (p < .05). EG emulsions or nanoemulsions did not provide any additional reduction in C. jejuni when compared to EG suspension. Our results suggest that EG could be an effective postharvest intervention strategy for reducing C. jejuni contamination on poultry products.
Practical Applications
Campylobacter jejuni, a leading cause of foodborne illness in humans, is strongly associated with the consumption of contaminated poultry products. Interventions reducing C. jejuni contamination in poultry would reduce the risk of subsequent human infections. In this study, the antimicrobial efficacy of eugenol was studied in three different delivery systems; suspension, emulsion, or nanoemulsion. Our results demonstrated that eugenol was effective in reducing C. jejuni counts on chicken skin and can be used as a potential strategy to reduce Campylobacter on poultry products.
REFERENCES
- Abd-Elsalam, K. A., & Khokhlov, A. R. (2015). Eugenol oil nanoemulsion: Antifungal activity against Fusarium oxysporum f. sp. vasinfectum and phytotoxicity on cottonseeds. Applied Nanoscience, 5(2), 255–265.
- Achen, M., Morishita, T. Y., & Ley, E. C. (1998). Shedding and colonization of Campylobacter jejuni in broilers from day-of-hatch to slaughter age. Avian Diseases, 42, 732–737.
- Arsi, K., Donoghue, A. M., Venkitanarayanan, K., Kollanoor-Johny, A., Fanatico, A. C., Blore, P. J., & Donoghue, D. J. (2014). The efficacy of the natural plant extracts, thymol and carvacrol against Campylobacter colonization in broiler chickens. Journal of Food Safety, 34(4), 321–325.
- Bauermeister, L. J., Bowers, J. W., Townsend, J. C., & McKee, S. R. (2008). Validating the efficacy of peracetic acid mixture as an antimicrobial in poultry chillers. Journal of Food Protection, 71(6), 1119–1122.
- Beery, J. T., Hugdahl, M. B., & Doyle, M. P. (1988). Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Applied and Environmental Microbiology, 54(10), 2365–2370.
- Bhargava, K., Conti, D. S., da Rocha, S. R., & Zhang, Y. (2015). Application of an oregano oil nanoemulsion to the control of foodborne bacteria on fresh lettuce. Food Microbiology, 47, 69–73.
- Bilgili, S. F., Conner, D. E., Pinion, J. L., & Tamblyn, K. C. (1998). Broiler skin color as affected by organic acids: Influence of concentration and method of application. Poultry Science, 77(5), 752–757.
- Birk, T., Grønlund, A. C., Christensen, B. B., Knøchel, S., Lohse, K., & Rosenquist, H. (2010). Effect of organic acids and marination ingredients on the survival of Campylobacter jejuni on meat. Journal of Food Protection, 73(2), 258–265.
- Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P., & Blaser, M. J. (1988). Experimental Campylobacter jejuni infection in humans. Journal of Infectious Diseases, 157(3), 472–479.
- Borges, A., Abreu, A. C., Dias, C., Saavedra, M. J., Borges, F., & Simões, M. (2016). New perspectives on the use of phytochemicals as an emergent strategy to control bacterial infections including biofilms. Molecules, 21(7), 877.
- Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods—A review. International Journal of Food Microbiology, 94(3), 223–253.
- Calo, J. R., Crandall, P. G., O'Bryan, C. A., & Ricke, S. C. (2015). Essential oils as antimicrobials in food systems–a review. Food Control, 54, 111–119.
- Chantarapanont, W., Berrang, M., & Frank, J. F. (2003). Direct microscopic observation and viability determination of Campylobacter jejuni on chicken skin. Journal of Food Protection, 66(12), 2222–2230.
- Devi, K. P., Nisha, S. A., Sakthivel, R., & Pandian, S. K. (2010). Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. Journal of Ethnopharmacology, 130(1), 107–115.
- Danis, K., Di Renzi, M., O'Neill, W., Smyth, B., McKeown, P., Foley, B., … Devine, M. (2009). Risk factors for sporadic Campylobacter infection: An all-Ireland case-control study. Eurosurveillance, 14(7), 19123.
- Donsì, F., Annunziata, M., Sessa, M., & Ferrari, G. (2011). Nanoencapsulation of essential oils to enhance their antimicrobial activity in foods. LWT Food Science and Technology, 44(9), 1908–1914.
- Donsì, F., Annunziata, M., Vincensi, M., & Ferrari, G. (2012). Design of nanoemulsion-based delivery systems of natural antimicrobials: Effect of the emulsifier. Journal of Biotechnology, 159(4), 342–350.
- EFSA Panel on Biological Hazards (BIOHAZ). (2014). Scientific opinion on the evaluation of the safety and efficacy of peroxyacetic acid solutions for reduction of pathogens on poultry carcasses and meat. EFSA Journal, 12(3), 3599.
10.2903/j.efsa.2014.3599 Google Scholar
- Friedman, M., Henika, P. R., & Mandrell, R. E. (2002). Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. Journal of Food Protection, 65(10), 1545–1560.
- Friedman, C. R., Hoekstra, R. M., Samuel, M., Marcus, R., Bender, J., Shiferaw, B., … Carter, M. (2004). Risk factors for sporadic Campylobacter infection in the United States: A case-control study in FoodNet sites. Clinical Infectious Diseases, 38, S285–S296.
- Gill, A. O., & Holley, R. A. (2004). Mechanisms of bactericidal action of cinnamaldehyde against listeria monocytogenes and of eugenol against L. monocytogenes and Lactobacillus sakei. Applied and Environmental Microbiology, 70(10), 5750–5755.
- Gill, A. O., & Holley, R. A. (2006). Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. International Journal of Food Microbiology, 108(1), 1–9.
- Ghosh, V., Mukherjee, A., & Chandrasekaran, N. (2013). Ultrasonic emulsification of food-grade nanoemulsion formulation and evaluation of its bactericidal activity. Ultrasonics Sonochemistry, 20(1), 338–344.
- 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.
- Gracia, M. I., Millan, C., Sanchez, J., Guyard-Nicodeme, M., Mayot, J., Carre, Y., … Medel, P. (2016). Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period: Part B. Poultry Science, 95(4), 886–892.
- Gradel, K. O., Nielsen, H. L., Schønheyder, H. C., Ejlertsen, T., Kristensen, B., & Nielsen, H. (2009). Increased short-and long-term risk of inflammatory bowel disease after Salmonella or Campylobacter gastroenteritis. Gastroenterology, 137(2), 495–501.
- Guyard-Nicodeme, M., Keita, A., Quesne, S., Amelot, M., Poezevara, T., Le Berre, B., … Chemaly, M. (2016). Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period. Poultry Science, 95(2), 298–305.
- Hermans, D., Van Deun, K., Messens, W., Martel, A., Van Immerseel, F., Haesebrouck, F., … Pasmans, F. (2011). Campylobacter control in poultry by current intervention measures ineffective: Urgent need for intensified fundamental research. Veterinary Microbiology, 152(3–4), 219–228.
- Holley, R. A., & Patel, D. (2005). Improvement in shelf-life and safety of perishable foods by plant essential oils and smoke antimicrobials. Food Microbiology, 22(4), 273–292.
- Jang, K., Kim, M., Ha, S., Kim, K., Lee, K., Chung, D., … Kim, K. (2007). Morphology and adhesion of Campylobacter jejuni to chicken skin under varying conditions. Journal of Microbiology and Biotechnology, 17(2), 202–206.
- Khan, A., Allen, K., & Wang, X. (2015). Effect of type I and type II antioxidants on oxidative stability, microbial growth, pH, and color in raw poultry meat. Food and Nutrition Sciences, 6(16), 1541–1551.
- Kim, S. A., Park, S. H., Lee, S. I., Owens, C. M., & Ricke, S. C. (2017). Assessment of chicken carcass microbiome responses during processing in the presence of commercial antimicrobials using a next generation sequencing approach. Scientific Reports, 7, 43354.
- Kim, C. R., & Marshall, D. L. (2000). Quality evaluation of refrigerated chicken wings treated with organic acids. Journal of Food Quality, 23(3), 327–335.
- 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.
- Line, J. E. (2001). Development of a selective differential agar for isolation and enumeration of Campylobacter spp. Journal of Food Protection, 64(11), 1711–1715.
- Mangen, M. J., Havelaar, A. H., Haagsma, J. A., & Kretzschmar, M. E. E. (2016). The burden of Campylobacter-associated disease in six European countries. Microbial Risk Analysis, 2, 48–52.
- Marder, E. P., Cieslak, P. R., Cronquist, A. B., Dunn, J., Lathrop, S., Rabatsky-Ehr, T., … Zansky, S. (2017). Incidence and trends of infections with pathogens transmitted commonly through food and the effect of increasing use of culture-independent diagnostic tests on surveillance-foodborne diseases active surveillance network, 10 US sites, 2013-2016. MMWR. Morbidity and Mortality Weekly Report, 66(15), 397–403.
- Mattson, T. E., Johny, A. K., Amalaradjou, M. A. R., More, K., Schreiber, D. T., Patel, J., & Venkitanarayanan, K. (2011). Inactivation of Salmonella spp. on tomatoes by plant molecules. International Journal of Food Microbiology, 144(3), 464–468.
- Mehyar, G., Blank, G., Han, J. H., Hydamaka, A., & Holley, R. A. (2005). Effectiveness of trisodium phosphate, lactic acid and commercial anti-microbials against pathogenic bacteria on chicken skin. Food Protection Trends, 25(5), 351–362.
- Nagel, G. M., Bauermeister, L. J., Bratcher, C. L., Singh, M., & McKee, S. R. (2013). Salmonella and Campylobacter reduction and quality characteristics of poultry carcasses treated with various antimicrobials in a post-chill immersion tank. International Journal of Food Microbiology, 165(3), 281–286.
- Nauta, M. J., Johannessen, G., Adame, L. L., Williams, N., & Rosenquist, H. (2016). The effect of reducing numbers of Campylobacter in broiler intestines on human health risk. Microbial Risk Analysis, 2, 68–77.
- Ostertag, F., Weiss, J., & McClements, D. J. (2012). Low-energy formation of edible nanoemulsions: Factors influencing droplet size produced by emulsion phase inversion. Journal of Colloid and Interface Science, 388(1), 95–102.
- Pechacek, N., Osorio, M., Caudill, J., & Peterson, B. (2015). Evaluation of the toxicity data for peracetic acid in deriving occupational exposure limits: A minireview. Toxicology Letters, 233(1), 45–57.
- Pei, R. S., Zhou, F., Ji, B. P., & Xu, J. (2009). Evaluation of combined antibacterial effects of eugenol, cinnamaldehyde, thymol, and carvacrol against E. coli with an improved method. Journal of Food Science, 74(7), M379–M383.
- Riedel, C. T., Brøndsted, L., Rosenquist, H., Haxgart, S. N., & Christensen, B. B. (2009). Chemical decontamination of Campylobacter jejuni on chicken skin and meat. Journal of Food Protection, 72(6), 1173–1180.
- SCVPH. (1998). Report of the Scientific Committee on Veterinary Measures relating to Public Health (SCVPH) on benefits and limitations of antimicrobial treatments for poultry carcasses. Retrieved from https://ec.europa.eu/food/sites/food/files/safety/docs/sci-com_scv_out14_en.pdf.
- Shafiq, S., & Shakeel, F. (2010). Stability and self-nanoemulsification efficiency of ramipril nanoemulsion containing labrasol and plurol oleique. Clinical Research and Regulatory Affairs, 27(1), 7–12.
10.3109/10601330903571691 Google Scholar
- Shah, P., Bhalodia, D., & Shelat, P. (2010). Nanoemulsion: A pharmaceutical review. Systematic Reviews in Pharmacy, 1(1), 24.
- Shrestha, S., Arsi, K., Wagle, B. R., Donoghue, A. M., & Donoghue, D. J. (2017). The ability of select probiotics to reduce enteric Campylobacter colonization in broiler chickens. International Journal of Poultry Science, 16, 37–42.
10.3923/ijps.2017.37.42 Google Scholar
- Speranza, P., Ribeiro, A. P. B., Cunha, R. L., Macedo, J. A., & Macedo, G. A. (2015). Influence of emulsion droplet size on antimicrobial activity of interesterified Amazonian oils. LWT Food Science and Technology, 60(1), 207–212.
- Spiller, R. C. (2007). Role of infection in irritable bowel syndrome. Journal of Gastroenterology, 42(17), 41–47.
- Thormar, H., Hilmarsson, H., Thráinsson, J. H., Georgsson, F., Gunnarsson, E., & Dadadottir, S. (2011). Treatment of fresh poultry carcases with emulsions of glycerol monocaprate (monocaprin) to reduce contamination with Campylobacter and psychrotrophic bacteria. British Poultry Science, 52(1), 11–19.
- Upadhyay, A., Upadhyaya, I., Karumathil, D. P., Yin, H. B., Nair, M. S., Bhattaram, V., … Venkitanarayanan, K. (2015). Control of Listeria monocytogenes on skinless frankfurters by coating with phytochemicals. LWT Food Science and Technology, 63(1), 37–42.
- Upadhyaya, I., Upadhyay, A., Kollanoor-Johny, A., Baskaran, S. A., Mooyottu, S., Darre, M. J., & Venkitanarayanan, K. (2013). Rapid inactivation of Salmonella Enteritidis on shell eggs by plant-derived antimicrobials. Poultry Science, 92(12), 3228–3235.
- USDA FSIS. (2015). Changes to the Salmonella and Campylobacter verification-testing program: Proposed tella and Campylobacter in not-ready-to-eat comminuted chicken and Turkey products and raw chicken parts and related agency verification procedures and other changes to agency sampling. Federal Register, 80, 3940–3950.
- USDA FSIS. (2017). Table of safe and suitable ingredients: Antimicrobial update. Retrieved from https://www.fsis.usda.gov/wps/wcm/connect/24346cbd-ad28-4223-8db1-55f067ce3879/7120.1-Antimicrobials.pdf?MOD=AJPERES.
- 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, the Netherlands: Springer.
10.1007/978-94-017-9457-2_6 Google Scholar
- Wagle, B. R., Arsi, K., Upadhyay, A., Shrestha, S., Venkitanarayanan, K., Donoghue, A. M., & Donoghue, D. J. (2017). β-Resorcylic acid, a phytophenolic compound, reduces Campylobacter jejuni in postharvest poultry. Journal of Food Protection, 80(8), 1243–1251.
- Zainol, S., Basri, M., Basri, H. B., Shamsuddin, A. F., Abdul-Gani, S. S., Karjiban, R. A., & Abdul-Malek, E. (2012). Formulation optimization of a palm-based nanoemulsion system containing levodopa. International Journal of Molecular Sciences, 13(10), 13049–13064.
- Zhao, T., & Doyle, M. P. (2006). Reduction of Campylobacter jejuni on chicken wings by chemical treatments. Journal of Food Protection, 69(4), 762–767.
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