Development of a cell culture method to isolate and enrich Salmonella enterica serotype enteritidis from shell eggs for subsequent detection by real-time PCR

Applied and Environmental Microbiology

Volumn 75, Issue 16, 2009, Pages 5321-5327

  Day, J B ^a   Basavanna, U ^a   Sharma, S K ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL FEEDING; CELL CULTURE METHODS; CULTURE SYSTEMS; CURRENT TECHNIQUES; DEOXYCHOLATE; DNA SEGMENTS; EUKARYOTIC CELLS; IN-CELL; INTERNATIONAL ORGANIZATION FOR STANDARDIZATIONS; INTRACELLULAR BACTERIA; INTRACELLULAR REPLICATION; LYSATES; MACROPHAGE CELL LINE; MICROBIOLOGICAL METHODS; NOVEL TECHNIQUES; REAL-TIME PCR; SALMONELLA ENTERICA; SEROTYPES; SHELL EGGS; SPECIFIC PRIMERS;

AMINO ACIDS; ANIMAL CELL CULTURE; ANIMALS; CELL MEMBRANES; DNA; FEEDING; GENES; INTERNATIONAL COOPERATION; MACROPHAGES; MICROORGANISMS; MONOLAYERS; NUCLEIC ACIDS; PROBES; STANDARDIZATION;

CELL CULTURE;

DNA;

BACTERIUM; DETECTION METHOD; DNA; EUKARYOTE; GENE EXPRESSION; IDENTIFICATION METHOD; INTERNATIONAL ORGANIZATION; POLYMERASE CHAIN REACTION; PROBE; REAL TIME; RODENT; SHELL; STANDARDIZATION;

ARTICLE; CELL LINE; CELL LYSATE; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE TECHNIQUE; DNA PROBE; EGG SHELL; ENTERITIS; EUKARYOTIC CELL; GENE REPLICATION; ISOLATION PROCEDURE; MACROPHAGE; MICROBIOLOGICAL EXAMINATION; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROTYPE ENTERITIDIS; SEROTYPE;

ANIMALS; CELL LINE; CHICKENS; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; EGGS; FOOD CONTAMINATION; MACROPHAGES; MICE; POLYMERASE CHAIN REACTION; POULTRY DISEASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA; SALMONELLA ENTERICA;

EID: 68549104274     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02422-08     Document Type: Article

References (41)

1. Abolmaaty, A., W. Gu, R. Witkowsky, and R. E. Levin. 2007. The use of activated charcoal for the removal of PCR inhibitors from oyster samples. J. Microbiol. Methods 68:349-352.
2. Anonymous. 2002. Microbiology of food and animal feeding stuffs-horizontal method for the detection of Salmonella. ISO 6579:2002. International Organization for Standardization, Geneva, Switzerland.
3. Blais, B. W., and A. Martinez-Perez. 2008. Detection of group D salmonellae including Salmonella Enteritidis in eggs by polymyxin-based enzyme-linked immunoabsorbent assay. J. Food Prot. 71:392-396.
4. Braden, C. R., P. Fields, N. H. Bean, and R. V. Tauxe. 2002. Salmonella surveillance: annual summary, 2001. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
5. Burr, R., P. Effler, R. Kanenaka, M. Nakata, B. Holland, and F. J. Angulo. 2005. Emergence of Salmonella serotype Enteritidis phage type 4 in Hawaii traced to locally produced eggs. Int. J. Infect. Dis. 9:340-346.
6. Centers for Disease Control and Prevention. 2003. Outbreaks of Salmonella serotype Enteritidis infection associated with eating shell eggs-United States, 1999-2001. MMWR Morb. Mortal. Wkly. Rep. 51:1149-1152.
7. Chan, K., C. C. Kim, and S. Falkow. 2005. Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect. Immun. 73:5438-5449.
8. Clavijo, R. I., C. Loui, G. L. Anderson, L. W. Riley, and S. Lu. 2006. Identification of genes associated with survival of Salmonella enterica serovar Enteritidis in chicken egg albumen. Appl. Environ. Microbiol. 72:1055-1064.
9. Coyle, E. F., S. R. Palmer, C. D. Ribeiro, H. I. Jones, A. J. Howard, L. Ward, and B. Rowe. 1988. Salmonella enteritidis phage type 4 infection: association with hen's eggs. Lancet ii:1295-1297.
10. Day, J. B., and C. A. Lee. 2003. Secretion of the orgC gene product by Salmonella enterica serovar Typhimurium. Infect. Immun. 71:6680-6685.
11. Edwards, R. A., D. M. Schifferli, and S. R. Maloy. 2000. A role for Salmonella fimbriae in interperitoneal infections. Proc. Natl. Acad. Sci. USA 97:1258-1262.
12. Ellingson, J. L., J. L. Anderson, S. A. Carlson, and V. K. Sharma. 2004. Twelve hour real-time PCR technique for the sensitive and specific detection of Salmonella in raw and ready-to-eat meat products. Mol. Cell. Probes 18:51-57.
13. Fierer, J., and D. G. Guiney. 2001. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J. Clin. Investig. 107:775-780.
14. Fink, S. L., and B. T. Cookson. 2007. Pyroptosis and host cell death responses during Salmonella infection. Cell. Microbiol. 9:2562-2570.
15. Fricker, M., U. Messelhausser, U. Busch, S. Scherer, and M. Ehling-Schulz. 2007. Diagnostic real-time PCR assay for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl. Environ. Microbiol. 73:1892-1898.
16. Galán, J. E., and R. Curtiss III. 1989. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86:6383-6387.
17. Gast, R. K., and P. S. Holt. 2001. Multiplication in egg yolk and survival in egg albumen of Salmonella enterica serotype enteritidis strains of phage types 4, 8, 13a, and 14b. J. Food Prot. 64:865-867.
18. Geddes, K., F. Cruz III, and F. Heffron. 2007. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog. 3:2017-2028.
19. Guo, A., M. A. Lasaro, J. C. Sirard, J. P. Kraehenbuhl, and D. M. Schifferli. 2007. Adhesion-dependent binding and uptake of Salmonella enterica serovar Typhimurium by dendritic cells. Microbiology 153:1059-1069.
20. Haraga, A., M. B. Ohlson, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66.
21. Hu, Q., B. Coburn, W. Deng, Y. Li, X. Shi, Q. Lan, B. Wang, B. K. Coombes, and B. B. Finlay. 2008. Salmonella enterica serovar Senftenberg human clinical isolates lacking SPI-1. J. Clin. Microbiol. 46:1330-1336.
22. Kaufman, G. E., G. M. Blackstone, M. C. Vickery, A. K. Bej, J. Bowers, M. D. Bowen, R. F. Meyer, and A. DePaola. 2004. Real-time PCR quantification of Vibrio parahaemolyticus in oysters using an alternative matrix. J. Food Prot. 67:2424-2429.
23. 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.
24. Knodler, L. A., and O. Steele-Mortimer. 2003. Taking possession: biogenesis of the Salmonella containing vacuole. Traffic 4:587-599.
25. Kumar, R., P. K. Surendran, and N. Thampuran. 2008. Evaluation of culture, ELISA and PCR assays for the detection of Salmonella in seafood. Lett. Appl. Microbiol. 46:221-226.
26. Malorny, B., C. Bunge, and R. Helmuth. 2007. A real-time PCR for the detection of Salmonella Enteritidis in poultry meat and consumption eggs. J. Microbiol. Methods 70:245-251.
27. Mozola, M. A., X. Peng, and M. Wendorf. 2007. Evaluation of the GeneQuence DNA hybridization method in conjunction with 24-hour enrichment protocols for detection of Salmonella spp. in select foods: collaborative study. J. AOAC Int. 90:738-755.
28. Munson, T. E., J. P. Schrade, N. B. Bisciello, Jr., L. D. Fantasia, W. H. Hartung, and J. J. O'Conner. 1976. Evaluation of an automated fluorescent antibody procedure for detection of Salmonella in foods and feeds. Appl. Environ. Microbiol. 31:514-521.
29. Ng, S. P., C. O. Tsui, D. Roberts, P. Y. Chau, and M. H. Ng. 1996. Detection and serogroup differentiation of Salmonella spp. in food within 30 hours by enrichment-immunoassay with a T6 antibody capture enzyme-linked immunoabsorbent assay. Appl. Environ. Microbiol. 62:2294-2302.
30. Olsen, J. E., S. Aabo, W. Hill, S. Notemans, K. Wernars, P. E. Granum, T. Popovic, H. N. Rasmussen, and O. Olsvik. 1995. Probes and polymerase chain reaction for detection of food-borne bacterial pathogens. Int. J. Food Microbiol. 28:1-78.
31. Perelle, S., F. Dilasser, B. Malorny, J. Grout, J. Hoorfar, and P. Fach. 2004. Comparison of PCR-ELISA and LightCycler real-time PCR assays for detection of Salmonella spp. in milk and meat samples. Mol. Cell. Probes 18:409-420.
32. Powell, H. A., C. M. Gooding, S. D. Garrett, B. M. Lund, and R. A. McKee. 1994. Proteinase inhibition of the detection of Listeria monocytogenes in milk using the polymerase chain reaction. Lett. Appl. Microbiol. 18:59-61.
33. Rijpens, N. P., G. Jannes, M. Van Asbroeck, R. Rossau, and L. M. Herman. 1996. Direct detection of Brucella spp. in raw milk by PCR and reverse hybridization with 16S-23S rRNA spacer probes. Appl. Environ. Microbiol. 62:1683-1688.
34. Rönner, A. C., and H. Lindmark. 2007. Quantitative detection of Campylobacter jejuni on fresh chicken carcasses by real-time PCR. J. Food Prot. 70:1373-1378.
35. Rossen, L., P. Norskov, K. Holmstrom, and O. F. Rasmussen. 1992. Inhibition of PCR by components of food samples, microbial diagnostic assays and DNA-extraction solutions. Int. J. Food Microbiol. 17:37-45.
36. Seo, K. H., and R. E. Brackett. 2005. Rapid, specific detection of Enterobacter sakazakii in infant formula using a real-time PCR assay. J. Food Prot. 68:59-63.
37. Seo, K. H., I. E. Valentin-Bon, R. E. Bracket, and P. S. Holt. 2004. Rapid, specific detection of Salmonella enteritidis in pooled eggs by real-time PCR. J. Food Prot. 67:864-869.
38. Stephens, N., C. Sault, S. M. Firestone, D. Lightfoot, and C. Bell. 2007. Large outbreaks of Salmonella Typhimurium phage type 135 infections associated with the consumption of products containing raw egg in Tasmania. Commun. Dis. Intell. 31:118-124.
39. U.S. Food and Drug Administration. 2001. Bacteriological analytical manual. http://www.cfsan.fda.gov/∼ebam/bam-toc.html.
40. Wang, L., Y. Li, and A. Mustaphai. 2007. Rapid and simultaneous quantification of Escherichia coli 0157:H7, Salmonella and Shigella in ground beef samples by multiplex real-time PCR and immunomagnetic separation. J. Food Prot. 70:1366-1372.
41. Woodward, M. J., and S. E. Kirwan. 1996. Detection of Salmonella enteritidis in eggs by polymerase chain reaction. Vet. Rec. 138:411-413.