Prevalence of coliforms, Salmonella, Listeria, and Campylobacter associated with eggs and the environment of conventional cage and free-range egg production

Poultry Science

Volumn 91, Issue 5, 2012, Pages 1195-1202

  Jones, D R ^a   Anderson, K E ^b   Guard, J Y ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Campylobacter; Egg; Housing; Listeria; Salmonella

Indexed keywords

CAMPYLOBACTER; LISTERIA; LISTERIA INNOCUA; SALMONELLA;

ANIMAL; ANIMAL HOUSING; ANIMAL HUSBANDRY; ARTICLE; CAMPYLOBACTER; CHICKEN; EGG; ENTEROBACTERIACEAE; FOOD CONTROL; ISOLATION AND PURIFICATION; LISTERIA; MICROBIOLOGY;

ANIMAL HUSBANDRY; ANIMALS; CAMPYLOBACTER; CHICKENS; EGGS; ENTEROBACTERIACEAE; ENVIRONMENTAL MICROBIOLOGY; FOOD MICROBIOLOGY; HOUSING, ANIMAL; LISTERIA;

EID: 84930536354     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2011-01795     Document Type: Article

References (33)

1. Allen, K. J., and M. W. Griffiths. 2001. Use of luminescent Campylobacter jejuni ATCC 33291 to assess eggshell colonization and penetration in fresh and retail eggs. J. Food Prot. 64:2058-2062.
2. Anderson, K. E. 2008. Report on pullet rearing period thirty seventh North Carolina layer performance and management test. Vol. 37, No. 2. January 2008. North Carolina State University, Cooperative Extension, Raleigh. Accessed Aug. 8, 2011. http://www.ces.ncsu.edu/depts/poulsci/tech_manuals/layer_reports/37_grow_report.pdf.
3. Anderson, K. E. 2011. Comparison of fatty acid, cholesterol, and vitamin A and E composition in eggs from hens housed in conventional cage and range production facilities. Poult. Sci.90:1600-1608.
4. Aury, K., S. Le Bouquin, M.-T. Toquin, A. Huneau-Salaün, Y. Le Nôtre, V. Allain, I. Petetin, P. Fravalo, and M. Chemaly. 2011. Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks. Prev. Vet. Med. 98:271-278.
5. California Health and Safety Code. 2009. Division 20, Chapter 13.8, Sections 25990-25994. California State Legislature, Sacramento, CA.
6. Callaway, T. R., S. E. Dowd, R. D. Wolcott, Y. Sun, J. L. McReynolds, T. S. Edrington, J. A. Byrd, R. C. Anderson, N. Krueger, and D. J. Nisbet. 2009. Evaluation of bacterial diversity in the cecal contents of laying hens fed various molting diets by using bacterial tag-encoded FLX amplicon pyrosequencing. Poult. Sci. 88:298-302.
7. Cox, N. A., L. J. Richardson, R. J. Buhr, and P. J. Fedorka-Cray. 2009. Campylobacter species occurrence within internal organs and tissues of commercial caged Leghorn laying hens. Poult. Sci. 88:2449-2456.
8. De Vylder, J., S. Van Hoorebeke, R. Ducatelle, F. Pasmans, F. Haesebrouck, J. Dewulf, and F. Van Immerseel. 2009. Effect of the housing system on shedding and colonization of gut and internal organs of laying hens with Salmonella Enteritidis. Poult. Sci. 88:2491-2495.
9. Dipineto, L., A. Gargiulo, T. P. Russo, L. M. De Luca Bossa, L. Borrelli, L. F. Menna, and A. Fioretti. 2011. Campylobacter jejuni, Campylobacter coli, and cytolethal distending toxin genes in laying hens. Avian Dis. 55:103-105.
10. European Council. 1999. Council Directive 1999/74/EC of 19 July 1999: Laying down minimum standards for the protection of laying hens. Off. J. Eur. Communities L203:53-57.
11. Farnell, M. B., R. W. Moore, A. P. McElroy, B. M. Hargis, and D. J. Caldwell. 2001. Effect of prolonged heat stress in Single-Comb White Leghorn hens on progeny resistance to Salmonella Enteritidis organ invasion. Avian Dis. 45:479-485.
12. FDA. 2009. Prevention of Salmonella Enteritidis in shell eggs during production, storage, and transportation; final rule. Accessed June 6, 2011. http://edocket.access.gpo.gov/2009/pdf/E9-16119.pdf.
13. Gast, R. K., B. W. Mitchell, and P. S. Holt. 1998. Airborne transmission of Salmonella Enteritidis infection between groups of chicks in controlled-environment isolation cabinets. Avian Dis. 42:315-320.
14. Golden, N. J., H. H. Marks, M. E. Coleman, C. M. Schroeder, N. E. Bauer, and W. D. Schlosser. 2008. Review of induced molting by feed removal and contamination of eggs with Salmonella enterica serovar Enteritidis. Vet. Microbiol. 131:215-228.
15. Gutierrez, O., C. Zhang, D. J. Caldwell, J. B. Carey, A. L. Cartwright, and C. A. Bailey. 2008. Guar meal diets as an alternative approach to inducing molt and improving Salmonella Enteritidis resistance in late-phase laying hens. Poult. Sci. 87:536-540.
16. Holt, P. S., R. H. Davies, J. Dewulf, R. K. Gast, J. K. Huwe, D. R. Jones, D. Waltman, and K. R. Willian. 2011. The impact of different housing systems on egg safety and quality. Poult. Sci. 90:251-262.
17. Huneau-Salaün, A., M. Chemaly, S. Le Bouquin, F. Lalande, I. Petetin, S. Rouxel, V. Michel, P. Fravalo, and N. Rose. 2009. Risk factors for Salmonella enterica ssp. enterica contamination in 519 French laying hen flocks at the end of the laying period. Prev. Vet. Med. 89:51-58.
18. Jones, D. R., K. E. Anderson, P. A. Curtis, and F. T. Jones. 2002. Microbial contamination in inoculated shell eggs. I. Effects of layer strain and hen age. Poult. Sci. 81:715-720.
19. Jones, D. R., K. E. Anderson, and M. T. Musgrove. 2011. Comparison of environmental and egg microbiology associated with conventional and free-range laying hen management. Poult. Sci.90:2063-2068.
20. Jones, D. R., and M. T. Musgrove. 2007. Pathogen prevalence and microbial levels associated with restricted shell eggs. J. Food Prot. 70:2004-2007.
21. Jones, D. R., M. T. Musgrove, A. B. Caudill, and P. A. Curtis. 2006. Frequency of Salmonella, Campylobacter, Listeria, and Enterobacteriaceae detection in commercially cool water-washed shell eggs. J. Food Saf. 26:264-274.
22. Jones, D. R., M. T. Musgrove, and J. K. Northcutt. 2004. Variations in external and internal microbial populations in shell eggs during extended storage. J. Food Prot. 67:2657-2660.
23. Morales, C. A., R. Gast, and J. Guard-Bouldin. 2006. Linkage of avian and reproductive tract tropism with sequence divergence adjacent to the 5S ribosomal subunit rrfH of Salmonella enterica. FEMS Microbiol. Lett. 264:48-58.
24. Musgrove, M. T., D. R. Jones, J. K. Northcutt, M. A. Harrison, N. A. Cox, K. D. Ingram, and A. J. Hinton Jr. 2005. Recovery of Salmonella from commercial shell eggs by shell rinse and shell crush methodologies. Poult. Sci. 84:1955-1958.
25. Musgrove, M. T., J. K. Northcutt, D. R. Jones, N. A. Cox, and M. A. Harrison. 2008. Enterobacteriaceae and related organisms isolated from shell eggs collected during commercial processing. Poult. Sci. 87:1211-1218.
26. Neill, S. D., J. N. Campbell, and J. J. O'Brien. 1985. Egg penetration by Campylobacter jejuni. Avian Pathol. 14:313-320.
27. SAS Institute. 2002. User's Guide to SAS. Version 9.1. SAS Inst. Inc., Cary, NC.
28. Schwaiger, K., E.-M. V. Schmied, and J. Bauer. 2008. Comparative analysis of antibiotic resistance characteristics of gram-negative bacteria isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Public Hlth. 55:331-341.
29. Schwaiger, K., E.-M. V. Schmied, and J. Bauer. 2010. Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Public Health 57:171-180.
30. Stern, N. J., M. R. S. Clavero, J. S. Bailey, N. A. Cox, and M. C. Robach. 1995. Campylobacter spp. in broilers on the farm and after transport. Poult. Sci. 74:937-941.
31. Sulonen, J., R. Kärenlampi, U. Holma, and M.-L. Hänninen. 2007. Campylobacter in Finnish organic laying hens in autumn 2003 and spring 2004. Poult. Sci. 86:1223-1228.
32. Van Hoorebeke, S., F. Van Immerseel, F. Haesebrouck, R. Ducatelle, and J. Dewulf. 2011. The influence of the housing system on Salmonella infections in laying hens: A review. Zoonoses Public Health 58:304-311.
33. Van Hoorebeke, S., F. Van Immerseel, J. Schulz, J. Hartung, M. Harisberger, L. Barco, A. Ricci, G. Theodoropoulos, E. Xylouri, J. De Vylder, R. Ducatelle, F. Haesebrouck, F. Pasmans, A. de Kruif, and J. Dewulf. 2010. Determination of the within and between flock prevalence and identification of risk factors for Salmonella infections in laying hen flocks housed in conventional and alternative systems. Prev. Vet. Med. 94:94-100.