Rapid inactivation of Salmonella enteritidis on shell eggs by plant-derived antimicrobials

Poultry Science

Volumn 92, Issue 12, 2013, Pages 3228-3235

  Upadhyaya, Indu ^a   Upadhyay, Abhinav ^a   Kollanoor Johny, Anup ^a   Baskaran, Sangeetha Ananda ^a   Mooyottu, Shankumar ^a   Darre, Michael J ^a   Venkitanarayanan, Kumar ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Egg wash; Plant derived antimicrobial; Salmonella enteritidis

Indexed keywords

SALMONELLA ENTERITIDIS;

EID: 84887677369     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2013-03126     Document Type: Article

References (47)

1. Adams, T. B., S. M. Cohen, J. Doull, V. J. Feron, J. I. Goodman, L. J. Marnett, I. C. Munro, P. S. Portoghese, R. L. Smith, W. J. Waddell, and B. M. Wagner. 2004. The FEMA GRAS assessment of cinnamyl derivatives used as flavor ingredients. Food Chem. Toxicol. 42:157-185.
2. Adams, T. B., S. M. Cohen, J. Doull, V. J. Feron, J. I. Goodman, L. J. Marnett, I. C. Munro, P. S. Portoghese, R. L. Smith, W. J. Waddell, and B. M. Wagner. 2005. The FEMA GRAS assessment of hydroxyl- and alkoxy-substituted benzyl derivatives used as flavor ingredients. Food Chem. Toxicol. 43:1241-1271.
3. Allen-Vercoe, E., and M. J. Woodward. 1999. Colonisation of the chicken caecum by afimbriate and aflagellate derivatives of Salmonella enterica serotype Enteritidis. Vet. Microbiol. 69:265-275.
4. Baird-Parker, A. C. 1990. Foodborne salmonellosis. Lancet 336:1231-1235.
5. Braden, C. R. 2006. Salmonella enterica serotype Enteritidis and eggs: A national epidemic in the United States. Clin. Infect. Dis. 43:512-517.
6. Cao, W., Z. W. Zhu, Z. X. Shi, C. Y. Wang, and B. M. Li. 2009. Efficiency of slightly acidic electrolyzed water for inactivation of Salmonella Enteritidis and its contaminated shell eggs. Int. J. Food Microbiol. 130:88-93.
7. Cason, J. A., J. S. Bailey, and N. A. Cox. 1993. Location of Salmonella Typhimurium during incubation and hatching of inoculated eggs. Poult. Sci. 72:2064-2068.
8. Cox, N. A., A. L. J. Richardson, A. D. R. J. Buhr, A. P. J. Fedorka-Cray, B. J. S. Bailey, B. J. L. Wilson, and K. L. Hiett. 2006. Natural presence of Campylobacter spp. in various internal organs of commercial broiler breeder hens. Avian Dis. 50:450-453.
9. Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, R. Gast, T. J. Humphrey, and F. Van Immerseel. 2009. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol. Rev. 33:718-738.
10. Gast, R. K., J. Guard-Bouldin, and P. S. Holt. 2005. The relationship between the duration of fecal shedding and the production of contaminated eggs by laying hens infected with strains of Salmonella Enteritidis and Salmonella Heidelberg. Avian Dis. 49:382-386.
11. Geissman, T. A. 1963. Flavonoid compounds, tannins, lignins and related compounds. Page 265 in Pyrrole Pigments, Isoprenoid compounds and Phenolic Plant Constituents. E. H. Stotz, ed. Elsevier, New York, NY.
12. Howard, Z. R., C. A. O'Bryan, P. G. Crandall, and S. C. Ricke. 2012. Salmonella Enteritidis in shell eggs: Current issues and prospects for control. FRIN 45:755-764.
13. Isman, M. B. 2000. Plant essential oils for pest and disease management. Crop Prot. 19:603-608.
14. Jones, F. T., D. V. Rives, and J. B. Carey. 1995. Salmonella contamination in commercial eggs and an egg production facility. Poult. Sci. 74:753-757.
15. Keller, L. H., C. E. Benson, K. Krotec, and R. J. Eckroade. 1995. Salmonella Enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect. Immun. 63:2443-2449.
16. Knape, K. D., J. B. Carey, R. P. Burgess, Y. M. Kwon, and S. C. Ricke. 1999. Comparison of chlorine with an iodine-based compound on eggshell surface microbial populations in a commercial egg washer. J. Food Saf. 19:185-194.
17. Knape, K. D., C. Chavez, R. P. Burgess, C. D. Coufal, and J. B. Carey. 2002. Comparison of eggshell surface microbial populations for in-line and off-line commercial egg processing facilities. Poult. Sci. 81:695-698.
18. Knowles, J. R., S. Roller, D. B. Murray, and S. Naidu. 2005. Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 71:797-803.
19. Koidis, P., M. Bori, and K. Vareltzis. 2000. Efficacy of ozone treatment to eliminate Salmonella Enteritidis from eggshell surface. Arch. Meat Fish Dairy Sci. 51:4-6.
20. Kollanoor-Johny, A., M. J. Darre, A. M. Donoghue, D. J. Donoghue, and K. Venkitanarayanan. 2010b. Antibacterial effect of transcinnamaldehyde, eugenol, thymol and carvacrol against Salmonella Enteritidis and Campylobacter jejuni in vitro. J. Appl. Poult. Res. 19:237-244.
21. Kollanoor Johny, A., T. A. Hoagland, and K. S. Venkitanarayanan. 2010a. Subinhibitory concentrations of plant molecules increase the sensitivity of Salmonella Typhimurium DT 104 to antibiotics. Foodborne Pathog. Dis. 7:1165-1170.
22. Kollanoor-Johny, A., T. Mattson, S. A. Baskaran, M. A. Amalaradjou, S. Babapoor, B. March, S. Valipe, M. Darre, T. Hoagland, D. Schreiber, M. I. Khan, A. Donoghue, D. Donoghue, and K. Venkitanarayanan. 2012b. Reduction of Salmonella enterica serovar Enteritidis colonization in 20-day-old broiler chickens by the plant-derived compounds trans-cinnamaldehyde and eugenol. Appl. Environ. Microbiol. 78:2981-2987.
23. Kollanoor-Johny, A., A. Upadhyay, S. A. Baskaran, I. Upadhyaya, S. Mooyottu, N. Misra, M. J. Darre, M. I. Khan, A. M. Dono-ghue, D. J. Donoghue, and K. Venkitanarayanan. 2012a. Effect of therapeutic supplementation of the plant compounds transcinnamaldehyde and eugenol on Salmonella enterica Enteritidis colonization in market-age broiler chickens. J. Appl. Poult. Res. 21:816-822.
24. Kuo, F. L., Y. M. Kwon, J. B. Carey, B. M. Hargis, D. P. Krieg, and S. C. Ricke. 1997. Reduction of Salmonella contamination on chicken egg shells by a peroxidase-catalyzed sanitizer. J. Food Sci. 62:873-884.
25. Latimer, H. K., L. A. Jaykus, R. A. Morales, P. Cowen, and D. Crawford-Brown. 2002. Sensitivity analysis of Salmonella Enteritidis levels in contaminated shell eggs using a biphasic growth model. Int. J. Food Microbiol. 75:71-87.
26. Mayes, F. J., and M. A. Takeballi. 1983. Microbial contamination of the hen's egg: A review. J. Food Prot. 46:1092-1098.
27. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
28. Messens, W., K. Grijspeerdt, and L. Herman. 2006. Eggshell penetration of hen's eggs by Salmonella enterica serovar Enteritidis upon various storage conditions. Br. Poult. Sci. 47:554-560.
29. Miyamoto, T., E. Baba, T. Tanaka, K. Sasai, T. Fukata, and A. Arakawa. 1997. Salmonella Enteritidis contamination of eggs from hens inoculated by vaginal, cloacal, and intravenous routes. Avian Dis. 41:296-303.
30. Moats, W. A. 1978. Egg washing-A review. J. Food Prot. 41:919-925.
31. Okamura, M., Y. Kamijima, T. Miyamoto, H. Tani, K. Sasai, and E. Baba. 2001. Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens. Avian Dis. 45:61-69.
32. Padron, M. 1995. Egg dipping in hydrogen peroxide solution to eliminate Salmonella Typhimurium from eggshell membranes. Avian Dis. 39:627-630.
33. Park, C. M., Y. C. Hung, C. S. Lin, and R. E. Brackett. 2005. Efficacy of electrolyzed water in inactivating Salmonella Enteritidis and Listeria monocytogenes on shell eggs. J. Food Prot. 68:986-990.
34. Russell, S. M. 2003. The effect of electrolyzed oxidative water applied using electrostatic spraying on pathogenic and indicator bacteria on the surface of eggs. Poult. Sci. 82:158-162.
35. Salamci, E., S. Kordali, R. Kotan, A. Cakir, and Y. Kaya. 2007. Chemical compositions, antimicrobial and herbicidal effects of essential oils isolated from Turkish Tanacetum aucheranum and Tanacetum chiliophyllum var. chiliophyllum. Biochem. Syst. Ecol. 35:569-581.
36. Scott, T. A., and C. Sweetnam. 1993. Screening sanitizing agents and methods of application for hatching eggs. I. Environmental and user friendliness. J. Appl. Poult. Res. 2:1-6.
37. Shibasaki, I., and N. Kato. 1978. Combined effects on antibacterial activity of fatty acids and their esters against Gram-negative bacteria. Pages 15-24 in Symposium on the Pharmacological Effect of Lipids. J. J. Kabara, ed. The American Oil Chemists' Society, Champaign, IL.
38. Sikkema, J., J. A. M. De Bont, and B. Poolman. 1994. Interactions of cyclic hydrocarbons with biological membranes. J. Biol. Chem. 269:8022-8028.
39. Stern, N. J. 2008. Salmonella species and Campylobacter jejuni cecal colonization model in broilers. Poult. Sci. 87:2399-2403.
40. Stringfellow, K., P. Anderson, D. Caldwell, J. Lee, J. Byrd, J. McReynolds, J. Carey, D. Nisbet, and M. Farnell. 2009. Evaluation of disinfectants commonly used by the commercial poultry industry under simulated field conditions. Poult. Sci. 88:1151-1155.
41. Thiagarajan, D., A. M. Saeed, and E. K. Asem. 1994. Mechanism of transovarian transmission of Salmonella Enteritidis in laying hens. Poult. Sci. 73:89-98.
42. Thiagarajan, D., M. Saeed, J. Turek, and E. Asem. 1996. In vitro attachment and invasion of chicken ovarian granulosa cells by Salmonella Enteritidis phage type 8. Infect. Immun. 64:5015-5021.
43. USDA. 2000. 7 CFR part 56. Egg grading manual. Accessed June 2013. http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004376.
44. USDA. 2012. United States Department of Agriculture-Poultry and Eggs. Background. Accessed May 2013. http://www.ers.usda.gov/topics/animal-products/poultry-eggs/background.aspx.
45. Wang, H., and M. F. Slavik. 1998. Bacterial penetration into eggs washed with various chemicals and stored at different temperatures and times. J. Food Prot. 61:276-279.
46. Wang, S., A. M. Phillippy, K. Deng, X. Rui, Z. Li, M. L. Tortorello, and W. Zhang. 2010. Transcriptomic responses of Salmonella enterica serovars Enteritidis and Typhimurium to chlorine-based oxidative stress. Appl. Environ. Microbiol. 76:5013-5024.
47. Zeidler, G. 2002. Shell eggs and their nutritional value. Pages 1109-1128 in Commercial Chicken Meat and Egg Production. D. D. Bell and W. D. Weaver Jr., ed. Kluwer Academic Publisher, New York, NY.