Multiplex PCR detection of shiga toxin-producing escherichia coli strains belonging to serogroups o157, o103, o91, o113, o145, o111, and o26 experimentally inoculated in beef carcass swabs, beef trim, and ground beef

Journal of Food Protection

Volumn 74, Issue 2, 2011, Pages 228-239

  Valadez, Angela M ^a   Debroy, Chitrita ^b   Edward, Dudley ^a   Cutter, Catherine N ^a  

^a Department of Food Science ^*  (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHIGA TOXIN;

ANIMAL; ARTICLE; BACTERIAL COUNT; BIOSYNTHESIS; CATTLE; CLASSIFICATION; DISEASE CARRIER; FOOD CONTROL; HUMAN; ISOLATION AND PURIFICATION; MEAT; METABOLISM; METHODOLOGY; MICROBIOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; SEROTYPING; SHIGA TOXIN PRODUCING ESCHERICHIA COLI;

ANIMALS; CATTLE; COLONY COUNT, MICROBIAL; DISEASE RESERVOIRS; FOOD MICROBIOLOGY; HUMANS; MEAT; MEAT PRODUCTS; PHYLOGENY; POLYMERASE CHAIN REACTION; SEROTYPING; SHIGA TOXIN; SHIGA-TOXIGENIC ESCHERICHIA COLI;

ESCHERICHIA COLI;

EID: 79951667389     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-10-386     Document Type: Article

References (52)

1. American Heart Association. 1996. Dietary guidelines for healthy Americans. Circulation 94:1795-1800.
2. Arthur, T. M., J. M. Bosilevac, X. W. Nou, S. D. Shackelford, T. L. Wheeler, M. P. Kent, D. Jaroni, B. Pauling, D. M. Allen, and M. Koohmaraie. 2004. Escherichia coli O157 prevalence and enumeration of aerobic bacteria, enterobacteriaceae, and Escherichia coli O157 at various steps in commercial beef processing plants. J. Food Prot. 67:658-665. (Pubitemid 38449097)
3. Bayardelle, P., and M. Zafarullah. 2002. Development of oligonucleotide primers for the specific PCR-based detection of the most frequent enterobacteriaceae species DNA using wec gene templates. Can. J. Microbiol. 48:113-122. (Pubitemid 34258636)
4. Bell, C. 2002. Approach to the control of entero-haemorrhagic Escherichia coli (EHEC). Int. J. Food Microbiol.78:197-216. (Pubitemid 34879811)
5. Bettelheim, K. A. 2007. The non-O157 Shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit. Rev. Microbiol. 33:67-87. (Pubitemid 46631085)
6. Blais, B. W., R. A. Booth, L. M. Phillippe, and H. Yamazaki. 1997. Effect of temperature and agitation on enrichment of Escherichia coli O157:H7 in ground beef using modified EC broth with novobiocin. Int. J. Food Microbiol. 36:221-225. (Pubitemid 27361714)
7. Bouttier, S., C. Linxe, C. Ntsama, G. Morgant, M. N. Bellon Fontaine, and J. Fourniat. 1997. Attachment of Salmonella choleraesuis choleraesuis to beef muscle and adipose tissues. J. Food Prot. 60:16-22. (Pubitemid 27114808)
8. Brichta-Harhay, D. M., T. M. Arthur, J. M. Bosilevac, M. N. Guerini, N. Kalchayanand, and M. Koohmaraie. 2007. Enumeration of Salmonella and Escherichia coli O157:H7 in ground beef, cattle carcass, hide and faecal samples using direct plating methods. J. Appl. Microbiol. 103:1657-1668. (Pubitemid 47620562)
9. Centers for Disease Control and Prevention. 2006. Outbreaks of Salmonella infections associated with eating Roma tomatoes-United States and Canada, 2004. Morb. Mortal. Wkly. Rep. 55:1-42.
10. Centers for Disease Control and Prevention. 2008. Shiga toxin-producing Escherichia coli: burden and trends. Available at: http://www.cdc.gov/FoodNet/ news/2008/January-FoodNet-News.pdf. Accessed 31 March 2010.
11. Centers for Disease Control and Prevention. 2009. Multistate outbreak of E. coli O157:H7 infections associated with beef from JBS Swift Beef Company. Available at: http://www.cdc.gov/ecoli//0701.html. Accessed 31 March 2010.
12. DebRoy, C., E. Roberts, J. Kundrat, M. A. Davis, C. E. Briggs, and P. M. Fratamico. 2004. Detection of Escherichia coli serogroups O26 and O113 by PCR amplification of the wzx and wzy genes. Appl. Environ. Microbiol. 70:1830-1832. (Pubitemid 38365170)
13. Doering, C., and C. Abbott. 31 July 2009. USDA to expand testing to reduce E. coli in beef. Available at: http://www.reuters.com/article/ idUSTRE56U5N120090731. Accessed 31 March 2010.
14. Feng, L., S. N. Senchenkova, J. Tao, A. S. Shashkov, B. Liu, S. D. Shevelev, P. R. Reeves, J. G. Xu, Y. A. Knirel, and L. Wang. 2005. Structural and genetic characterization of enterohemorrhagic Escherichia coli O145 O antigen and development of an O145 serogroup-specific PCR assay. J. Bacteriol. 187:758-764. (Pubitemid 40096263)
15. Ferguson, A. 2009. USDA should declare non-O157 E. coli an adulterant. Available at: http://www.foodsafetynews.com/2009/10/the-usda-should-declare-non- o157-e-coli-an-adulterant/. Accessed 31 March 2010.
16. Foong, S. C. C., and J. S. Dickson. 2004. Attachment of Listeria monocytogenes on ready-to-eat meats. J. Food Sci. 67:452-462.
17. Fratamico, P. M., C. DebRoy, T. Miyamoto, and Y. H. Liu. 2009. PCR detection of enterohemorrhagic Escherichia coli O145 in food by targeting genes in the E. coli O145 O-antigen gene cluster and the Shiga toxin 1 and Shiga toxin 2 genes. Foodborne Pathog. Dis. 6:605-611.
18. Fratamico, P. M., C. DebRoy, T. P. Strobaugh, and C. Y. Chen. 2005. DNA sequence of the Escherichia coli O103 O-antigen gene cluster and detection of enterohemorrhagic E. coli O103 by PCR amplification of the wzx and wzy genes. Can. J. Microbiol. 51:515-522. (Pubitemid 41641238)
19. Gill, C. O., J. Bryant, and D. Bedard. 1999. The effects of hot water pasteurizing treatments on the appearances and microbiological conditions of beef carcass sides. Food Microbiol. 16:281-289. (Pubitemid 29311363)
20. Goldwater, P. N., and K. A. Bettelheim. 2000. Escherichia coli O group serology of a haemolytic uraemic syndrome (HUS) epidemic. Scand. J. Infect. Dis. 32:385-394. (Pubitemid 30612153)
21. Guerini, M. N., T. Arthur, S. D. Shackelford, and M. Koohmaraie. 2006 Evaluation of Escherichia coli O157:H7 growth media for use in test-and-hold procedures for ground beef processing. J. Food Prot. 69:1007-1011.
22. Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C. G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, T. Yasunaga, S. Kuhara, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8:11-22. (Pubitemid 33617542)
23. Janda, J. M., and S. L. Abbott. 2006. The enterobacteria, 2nd ed. ASM Press, Washington, DC.
24. Jay, J. M., M. Loessner, and D. A. Golden. 2005. Modern food microbiology, 7th ed. Springer Science, New York.
25. Kaper, J. B., J. P. Nataro, and H. L. T. Mobley. 2004. Pathogenic Escherchia coli. Nature Rev. Microbiol. 2:123-140.
26. Kawasaki, S., P. M. Fratamico, N. Horikoshi, Y. Okada, K. Takeshita, T. Sameshima, and S. Kawamoto. 2009. Evaluation of a multiplex PCR system for simultaneous detection of Salmonella spp., Listeria monocytogenes, and Escherichia coli O157:H7 in foods and in food subjected to freezing. Foodborne Pathog. Dis. 6:81-89.
27. Mead, P. S., and P. M. Griffin. 1998. Escherichia coli O157:H7. Lancet 352:1207-1212. (Pubitemid 28458545)
28. 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. (Pubitemid 29493763)
29. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201. (Pubitemid 28046019)
30. O'Hanlon, K. A., T. M. G. Catarame, G. Duffy, I. S. Blair, and D. A. McDowell. 2004. Rapid detection and quantification of E. coli O157/ O26/O111 in minced beef by real-time PCR. J. Appl. Microbiol. 96:1013-1023. (Pubitemid 38582148)
31. Orskov, I., F. Orskov, B. Jann, and K. Jann. 1977. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriol. Rev. 41:667-710. (Pubitemid 8194910)
32. Paton, A. W., and J. C. Paton. 1998. Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlya, rfb(O111), and rfb(O157). J. Clin. Microbiol. 36:598-602. (Pubitemid 28060342)
33. Paton, A. W., and J. C. Paton. 1999. Direct detection of Shiga toxigenic Escherichia coli strains belonging to serogroups O111, O157, and O113 by multiplex PCR. J. Clin. Microbiol. 37:3362-3365. (Pubitemid 29455235)
34. Perelle, S., F. Dilasser, J. Grout, and P. Fach. 2002. Identification of the O-antigen biosynthesis genes of Escherichia coli O91 and development of a O91 PCR serotyping test. J. Appl. Microbiol. 93: 758-764. (Pubitemid 35340876)
35. Perelle, S., F. Dilasser, J. Grout, and P. Fach. 2007. Screening food raw materials for the presence of the world's most frequent clinical cases of Shiga toxin-encoding Escherichia coli O26, O103, O111, O145 and O157. Int. J. Food Microbiol. 113:284-288. (Pubitemid 46123644)
36. Perelle, S., F. Dilasser, J. L. Grout, and P. Fach. 2004. Detection by 59-nuclease PCR of Shiga toxin-producing Escherichia coli O26, O55, O91, O103, O111, O113, O145 and O157:H7, associated with the world's most frequent clinical cases. Mol. Cell. Probes 18:185-192. (Pubitemid 38591610)
37. Pillai, S. D. 2004. Molecular methods for microbial detection, p. 289-301. In R. C. Beier, S. D. Pillai, and T. D. Phillips (ed.), Preharvest and postharvest food safety. Blackwell Publishing, Ltd., College Station, TX.
38. Power, C. A., R. P. Johnson, S. A. McEwen, W. B. McNab, M. W. Griffiths, W. R. Usborne, and S. A. De Grandis. 2000. Evaluation of the reveal and safepath rapid Escherichia coli O157 detection tests for use on bovine feces and carcasses. J. Food Prot. 63:860-866. (Pubitemid 30454168)
39. Rhoades, J. R., G. Duffy, and K. Koutsoumanis. 2009. Prevalence ad concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiol. 26:357-376.
40. Srinivasan, V., B. E. Gillespie, L. T. Nguyen, S. I. Headrick, S. E. Murinda, and S. P. Oliver. 2007. Characterization of antimicrobial resistance patterns and class 1 integrons in Escherichia coli O26 isolated from humans and animals. Int. J. Antimicrob. Agents 29:254-262.
41. Stefan, A., S. Scaramagli, R. Bergami, C. Mazzini, M. Barbanera, S. Perelle, and P. Fach. 2007. Real-time PCR and enzyme-linked fluorescent assay methods for detecting Shiga toxin-producingEscherichia coli in mincemeat samples. Can. J. Microbiol. 53:337-342. (Pubitemid 47110420)
42. Ternent, H. E., G. T. Innocent, L. M. Filshie, D. J. Taylor, W. B. Steele, S. A. McEwen, W. J. Reilly, G. J. Gunn, S. W. J. Reid, and D. J. Mellor. 2004. Frozen storage of Escherichia coli O157 in buffered peptone water and its detection on bovine carcasses. J. Food Prot. 67:40-45. (Pubitemid 38069918)
43. Tozzie, A. E., A. Caprioli, F. Minelli, A. Gianviti, L. De Petris, A. Edefonti, G. Montini, A. Ferretti, T. De Palo, M. Gaido, and G. Rizzoni. 2003. Shiga toxin-producing Escherichia coli infections associated with hemolytic uremic syndrome, Italy, 1988-2000. Emerg. Infect. Dis. 9:106-108. (Pubitemid 36110210)
44. U.S. Department of Agriculture, Food Safety and Inspection Service. 1996 Pathogen reduction: hazard analysis and critical control point (HACCP) systems; final rule. Fed. Regist. 61:38806-38989.
45. U.S. Department of Agriculture, Food Safety and Inspection Service. 2008 Beef trim baseline results and how FSIS will use them. Available at: http://www.fsis.usda.gov/PPT/Beef-Trim-Baseline-040908pt. Accessed 31 March 2010.
46. U.S. Department of Agriculture, Food Safety and Inspection Service. 2008 E. coli O157:H7 laboratory methods and sampling. Available at: http://199.140.94.5/PDF/Sampling-Esteban-101408.pdf. Accessed 31 March 2010.
47. U.S. Department of Agriculture, Food Safety and Inspection Service. 2008 California firm recalls beef products derived from nonambulatory cattle without the benefit of proper inspection. Available at: http://origin-www.fsis.usda.gov/ PDF/Recall-005-2008-Release.pdf. Accessed 13 May 2010.
48. U.S. Department of Agriculture, Food Safety and Inspection Service. 2009 Routine sampling and testing of beef manufacturing trimmings derived from cattle not slaughtered in that establishment (bench trim) for Escherichia coli (E. coli) O157:H7. Available at: http://www.fsis.usda.gov/OPPDE/rdad/FSISNotices/51- 09.pdf. Accessed 31 March 2010.
49. U.S. Department of Agriculture, Food Safety and Inspection Service. 2010 Pennsylvania firm recalls ground beef products due to possible E. coli O26 contamination. Available at: http://www.fsis.usda.gov/News-&-Events/Recall- 050-2010-Release/index.asp. Accessed 11 September 2010.
50. Valadez, A. M. 2010. Development of a multiplex polymerase chain reaction assay for the detection of Escherichia coli serogroups O103, O91, O113, O145, O111, O157, and O26 in beef carcass swabs, beef trim, and ground beef, p. 57-81. M.S. thesis. The Pennsylvania State University, University Park.
51. Wang, L., and P. R. Reeves. 2000. The Escherichia coli O111 and Salmonella enterica O35 gene clusters: gene clusters encoding the same colitose-containing O antigen are highly conserved. J.Bacteriol. 182:5256-5261.
52. Weiner, M. 2008. Development of multiplex PCR assays for identifying and defining the characteristics of Shiga toxin-producing Escherichia coli. Med. Weter. 64:310-313. (Pubitemid 351439826)