Development of a quantitative real time PCR assay to detect and enumerate Escherichia coli O157 and O26 serogroups in bovine recto-anal swabs

Journal of Microbiological Methods

Volumn 114, Issue , 2015, Pages 9-15

  Lawal, Dolapo ^a,b   Burgess, Catherine ^a   McCabe, Evonne ^a   Whyte, Paul ^b   Duffy, Geraldine ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cattle; Enumeration; PCR; Quantification; RAJ; Real time

Indexed keywords

NOVOBIOCIN; CULTURE MEDIUM;

ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIUM IDENTIFICATION; BOVINAE; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI O157; ESCHERICHIA COLI O26; FECES ANALYSIS; MICROBIOLOGICAL EXAMINATION; MOST PROBABLE NUMBER; NONHUMAN; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECTO ANAL SWAB; RFBE GENE; SENSITIVITY ANALYSIS; SEROTYPE; WZX GENE; ANAL CANAL; ANIMAL; BACTERIAL LOAD; BOVINE; CHEMISTRY; CULTURE MEDIUM; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; EVALUATION STUDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROZYGOTE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES; RECTUM; SENSITIVITY AND SPECIFICITY; TIME FACTOR; VETERINARY;

BOS; BOVINAE; ESCHERICHIA COLI;

ANAL CANAL; ANIMALS; BACTERIAL LOAD; CARRIER STATE; CATTLE; CULTURE MEDIA; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; RECTUM; SENSITIVITY AND SPECIFICITY; SEROGROUP; TIME FACTORS;

EID: 84928544177     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2015.04.005     Document Type: Article

References (64)

1. Almeida C., Sousa J., Rocha R., Cerqueira L., Fanning S., Azevedo N., VieiRa M. Detection of Escherichia coli O157 by peptide nucleic acid fluorescence in situ hybridisation (PNA-FISH) and comparison to a standard culture method. Appl. Environ. Microbiol. 2013, 79:6293-6300.
2. Arthur T.M., Brichta-Harhay D.M., Bosilevac J.M., Kalchayanand N., Shackelford S.D., Wheeler T.L., Koohmaraie M. Super shedding of Escherichia coli O157:H7 by cattle and the impact on beef carcass contamination. Meat Sci. 2010, 86(1):32-37.
3. Arthur T.M., Ahmed R., Chase-Topping M., Kalchayanand N., Schmidt J.W., Bono J.L. Characterization of Escherichia coli O157:H7 strains isolated from supershedding cattle. Appl. Environ. Microbiol. 2013, 79(14):4294-4303.
4. Ayaz N.D., Gencay Y.E., Erol I. Prevalence and molecular characterization of sorbitol fermenting and non-fermenting Escherichia coli O157:H7(+)/H7(-) isolated from cattle at slaughterhouse and slaughterhouse wastewater. Int. J. Food Microbiol. 2014, 174:31-38.
5. Bhaduri S., Cottrell B. Sample preparation methods for PCR detection of Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on beef chuck shoulder using a single enrichment medium. Mol. Cell. Probes 2001, 15(5):267-274.
6. Brichta-Harhay D.M., Arthur T.M., Bosilevac J.M., Guerini M.N., Kalchayanand N., Koohmaraie M. Enumeration of Salmonella and Escherichia coli O157:H7 in ground beef, cattle carcass, hide and faecal samples using direct plating methods. J. Appl. Microbiol. 2007, 103(5):1657-1668.
7. Catarame T.M., O'Hanlon K.A., Duffy G., Sheridan J.J., Blair I.S., McDowell D.A. Optimization of enrichment and plating procedures for the recovery of Escherichia coli O111 and O26 from minced beef. J. Appl. Microbiol. 2003, 95(5):949-957.
8. Chase-Topping M., Gally D., Low C., Matthews L., Woolhouse M. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat. Rev. Microbiol. 2008, 6(12):904-912.
9. Cobbold R.N., Hancock D.D., Rice D.H., Berg J., Stilborn R., Hovde C.J., Besser T.E. Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl. Environ. Microbiol. 2007, 73(5):1563-1568.
10. Conrad C.C., Stanford K., McAllister T.A., Thomas J., Reuter T. Further development of sample preparation and detection methods for O157 and the top 6 non-O157 STEC serogroups in cattle feces. J. Microbiol. Methods 2014, 105:22-30.
11. Doyle M., Schoeni J. Isolation of Escherichia coli O157:H7 from retail fresh meats and poultry. Appl. Environ. Microbiol. 1987, 53:2394-2396.
12. Duffy G., Sheridan J.J., Buchanan R.L., McDowell D.A., Blair I.S. The effect of aeration, initial inoculum and meat microflora on the growth kinetics of Listeria monocytogenes in selective enrichment broths. Food Microbiol. 1994, 11(5):429-438.
13. Duffy G., Cummins E., Nally P., O' Brien S., Butler F. A review of quantitative microbial risk assessment in the management of Escherichia coli O157:H7 on beef. Meat Sci. 2006, 74(1):76-88.
14. Duffy L.L., Small A., Fegan N. Concentration and prevalence of Escherichia coli O157 and Salmonella serotypes in sheep during slaughter at two Australian abattoirs. Aust. Vet. J. 2010, 88(10):399-404.
15. EFSA The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J. 2014, 12(2):3547.
16. Fegan N., Higgs G., Vanderlinde P., Desmarchelier P. Enumeration of Escherichia coli O157 in cattle faeces using most probable number technique and automated immunomagnetic separation. Lett. Appl. Microbiol. 2004, 38(1):56-59.
17. Fitzmaurice J., Duffy G., Kilbride B., Sheridan J.J., Carroll C., Maher M. Comparison of a membrane surface adhesion recovery method with an IMS method for use in a polymerase chain reaction method to detect Escherichia coli O157:H7 in minced beef. J. Microbiol. Methods 2004, 59(2):243-252.
18. Foster G., Hopkins G.F., Gunn G.J., Ternent H.E., Thomson-Carter F., Knight H.I., Graham D.J., Edge V., Synge B.A. A comparison of two pre-enrichment media prior to immunomagnetic separation for the isolation of E. coli O157 from bovine faeces. J. Appl. Microbiol. 2003, 95(1):155-159.
19. Fratamico P.M., Bagi L.K. Detection of Shiga toxin-producing Escherichia coli in ground beef using the GeneDisc real-time PCR system. Front. Cell. Infect. Microbiol. 2012, 2:152.
20. Fricker M., Messelha U., Busch U., Scherer S., Ehling-Schulz M. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl. Environ. Microbiol. 2007, 73(6):1892-1898.
21. Gordillo R., Rodriguez A., Werning M.L., Bermudez E., Rodriguez M. Quantification of viable Escherichia coli O157:H7 in meat products by duplex real-time PCR assays. Meat Sci. 2014, 96:964-970.
22. Guerini M.N., Arthur T.M., Shackelford S.D., Koohmaraie M. Evaluation of Escherichia coli O157:H7 growth media for use in test-and-hold procedures for ground beef processing. J. Food Prot. 2006, 69(5):1007-1011.
23. Guy R.A., Tremblay D., Beausoleil L., Harel J., Champagne M.J. Quantification of E. coli O157 and STEC in feces of farm animals using direct multiplex real time PCR (qPCR) and a modified most probable number assay comprised of immunomagnetic bead separation and qPCR detection. J. Microbiol. Methods 2014, 99:44-53.
24. Han Y., Linton R.H., Nelson P.E. Effects of recovery, plating, and inoculation methods on quantification of Escherichia coli O157:H7 and Listeria monocytogenes from strawberries. J. Food Prot. 2004, 67(11):2436-2442.
25. Hara-Kudo Y., Konuma H., Nakagawa H., Kumagai S. Escherichia coli O26 detection from foods using an enrichment procedure and an immunomagnetic separation method. Lett. Appl. Microbiol. 2000, 30(2):151-154.
26. Hedman J., Rådström P. Overcoming inhibition in real-time diagnostic PCR. Methods Mol. Biol. 2013, 17-48. Humana Press. M. Wilks (Ed.).
27. Heuvelink A.E., van den Biggelaar F.L., de Boer E., Herbes R.G., Melchers W.J., Huis in 't Veld J.H., Monnens L.A. Isolation and characterization of verocytotoxin-producing Escherichia coli O157 strains from Dutch cattle and sheep. Clin. Microbiol. 1998, 36(4):878-882.
28. Ibekwe A.M., Grieve C.M. Detection and quantification of Escherichia coli O157:H7 in environmental samples by real-time PCR. J. Appl. Microbiol. 2003, 94(3):421-431.
29. ISO: 13136 Microbiology of Food and Animal Feed - Real-time Polymerase Chain Reaction (PCR)-based Method for the Detection of Food-borne Pathogens - Horizontal Method for the Detection of Shiga Toxin Producing Escherichia coli (STEC) and the Determination of O157, O111, O26, O102 and O145 Serogroups 2012.
30. ISO: 16654 Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection of Escherichia coli O157 2001, International Standard Organisation.
31. Jasson V., Rajkovic A., Baert L., Debevere J., Uyttendaele M. Comparison of enrichment conditions for rapid detection of low numbers of sublethally injured Escherichia coli O157 in food. J. Food Prot. 2009, 72(9):1862-1868.
32. Kalchayanand N., Arthur T.M., Bosilevac J.M., Wells J.E., Wheeler T.L. Chromogenic agar medium for detection and isolation of Escherichia coli serogroups O26, O45, O103, O111, O121, and O145 from fresh beef and cattle feces. J. Food Prot. 2013, 76(2):192-199.
33. Kaper J.B., Nataro J.P., Mobley H.L.T. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2(2):123-140.
34. Karmali M.A., Gannon V., Sargeant J.M. Verocytotoxin-producing Escherichia coli (VTEC). Vet. Microbiol. 2010, 140(3-4):360-370.
35. Kramer N., Lofstrom C., Vigre H., Hoorfar J., Bunge C., Malorny B. A novel strategy to obtain quantitative data for modelling: combined enrichment and real-time PCR for enumeration of Salmonellae from pig carcasses. Int. J. Food Microbiol. 2011, 145:86-95.
36. Kudva I.T., Hovde C.J., John M. Adherence of non-O157 Shiga toxin-producing Escherichia coli to bovine recto-anal junction squamous epithelial cells appears to be mediated by mechanisms distinct from those used by O157. Foodborne Pathog. Dis. 2013, 10(4):375-381.
37. Lim J., Li J.W., Sheng H., Besser T.E., Potter K. Escherichia coli O157:H7 Colonization at the Rectoanal Junction of Long-duration Culture-positive Cattle 2007, 73:1380-1382.
38. Low J.C., McKendrick I.J., McKechnie C., Fenlon D., Naylor S.W., Currie C., Smith D.G., Allison L., Gally D.L. Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl. Environ. Microbiol. 2005, 71(1):93-97.
39. Luedtke B.E., Bono J.L., Bosilevac J.M. Evaluation of real time PCR assays for the detection and enumeration of enterohemorrhagic Escherichia coli directly from cattle feces. J. Microbiol. Methods 2014, 105:72-79.
40. Ma D., Alberti M., Lynch C., Nikaido H., Hearst J.E. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 1996, 19(1):101-112.
41. Mancusi R., Trevisani M. Enumeration of verocytotoxigenic Escherichia coli (VTEC) O157 and O26 in milk by quantitative PCR. Int. J. Food Microbiol. 2014, 184:121-127.
42. Nauta M., Dufrenne J. Variability in growth characteristics of different E. coli O157:H7 isolates, and its implications for predictive microbiology. Quant. Microbiol. 1999, 1(2):137-155.
43. Naylor S.W., Low J.C., Besser T.E., Mahajan A., Gunn G.J., Pearce M.C., McKendrick I.J., Smith D.G., Gally D.L. Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect. Immun. 2003, 71(3):1505-1512.
44. O'Brien S.B., Duffy G., Daly D., Sheridan J.J., Blair I.S., McDowell D.A. Detection and recovery rates achieved using direct plate and enrichment/immunomagnetic separation methods for Escherichia coli O157: H7 in minced beef and on bovine hide. Lett. Appl. Microbiol. 2005, 41(1):88-93.
45. O'Hanlon K.A., Catarame T.M., Duffy G., Blair I.S., McDowell D.A. RAPID detection and quantification of E. coli O157/O26/O111 in minced beef by real-time PCR. J. Appl. Microbiol. 2004, 96(5):1013-1023.
46. Omisakin F., MacRae M., Ogden I.D., Strachan N.J. Concentration and prevalence of Escherichia coli O157 in cattle feces at slaughter. Appl. Environ. Microbiol. 2003, 69(5):2444-2447.
47. Opel K.L., Chung D., McCord B.R. A study of PCR inhibition mechanisms using real time PCR. J. Forensic Sci. 2010, 55(1):25-33.
48. Oses S.M., Rantsiou K., Cocolin L., Jaime I., Rovira J. Prevalence and quantification of Shiga-toxin producing Escherichia coli along the lamb food chain by quantitative PCR. Int. J. Food Microbiol. 2010, 141(Suppl. 1):163-169.
49. Perelle S., Dilasser F., Grout J., Fach P. Detection by 5'-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 2004, 18(3):185-192.
50. Pos K.M. Drug transport mechanism of the AcrB efflux pump. Biochim. Biophys. Acta 2009, 1794(5):782-793.
51. Rapp D., Waller J., Brightwell G., Muirhead R. Lyophilization prior to direct DNA extraction from bovine feces improves the quantification of Escherichia coli O157:H7 and Campylobacter jejuni▿. Appl. Environ. Microbiol. 2010, 76(5):1686-1688.
52. Rice D.H., Sheng H.Q., Wynia S.A., Hovde C.J. Rectoanal mucosal swab culture is more sensitive than fecal culture and distinguishes Escherichia coli O157:H7-colonized cattle and those transiently shedding the same organism. J. Clin. Microbiol. 2003, 41(11):4924-4929.
53. Robinson S.E., Wright E.J., Williams N.J., Hart C.A., French N.P. Development and application of a spiral plating method for the enumeration of Escherichia coli O157 in bovine faeces. J. Appl. Microbiol. 2004, 97(3):581-589.
54. Savoye F., Rozand C., Bouvier M., Gleizal A., Thevenot D. Optimized enrichment for the detection of Escherichia coli O26 in French raw milk cheeses. Lett. Appl. Microbiol. 2011, 52(6):603-609.
55. Sharma V.K. Detection and quantitation of enterohemorrhagic Escherichia coli O157, O111, and O26 in beef and bovine feces by real-time polymerase chain reaction. J. Food Prot. 2002, 65(9):1371-1380.
56. Smith R.P., Paiba G.A., Ellis-Iversen J. Longitudinal study to investigate VTEC O157 shedding patterns in young cattle. Res. Vet. Sci. 2010, 88(3):411-414.
57. Stephens T.P., Loneragan G.H., Chaney W.E., Branham L.A., Brashears M.M. Development and validation of a most-probable-number immunomagnetic separation methodology of enumerating Escherichia coli O157 in cattle feces. J. Food Prot. 2007, 70(5):1072-1075.
58. Thomas K.M., McCann M.S., Collery M.M., Logan A., Whyte P., McDowell D.A., Duffy G. Tracking verocytotoxigenic Escherichia coli O157, O26, O111, O103 and O145 in Irish cattle. Int. J. Food Microbiol. 2012, 153(3):288-296.
59. Tutenel A.V., Pierard D., Van Hoof J., De Zutter L. Molecular characterization of Escherichia coli O157 contamination routes in a cattle slaughterhouse. J. Food Prot. 2003, 66(9):1564-1569.
60. Verstraete K., Van Coillie E., Werbrouck H., Van Weyenberg S., Herman L., Del-Favero J., De Rijk P., De Zutter L., Joris M.A., Heyndrickx M., De Reu K. A qPCR assay to detect and quantify Shiga toxin-producing E. coli (STEC) in cattle and on farms: a potential predictive tool for STEC culture-positive farms. Toxins (Basel) 2014, 6(4):1201-1221.
61. Vimont A., Vernozy-Rozand C., Delignette-Muller M.L. Isolation of E. coli O157:H7 and non-O157 STEC in different matrices: review of the most commonly used enrichment protocols. Lett. Appl. Microbiol. 2006, 42(2):102-108.
62. Wang L., Li Y., Mustaphai A. Rapid and simultaneous quantitation of Escherichia coli O157:H7, Salmonella, and Shigella in ground beef by multiplex real-time PCR and immunomagnetic separation. J. Food Prot. 2007, 70(6):1366-1372.
63. Wang L., Li P., Zhang Z., Chen Q., Aguilar Z.P., Xu H., Yang L., Xu F., Lai W., Xiong Y., Wei H. Rapid and accurate detection of viable Escherichia coli O157:H7 in milk using a combined IMS, sodium deoxycholate, PMA and real-time quantitative PCR process. Food Control 2014, 36(1):119-125.
64. Weagant S.D., Jinneman K.C., Yoshitomi K.J., Zapata R., Fedio W.M. Optimization and evaluation of a modified enrichment procedure combined with immunomagnetic separation for detection of E. coli O157:H7 from artificially contaminated alfalfa sprouts. Int. J. Food Microbiol. 2011, 149(3):209-217.