Swab sample preparation and viable real-time PCR methodologies for the recovery of Escherichia coli, Staphylococcus aureus or Listeria monocytogenes from artificially contaminated food processing surfaces

Food Control

Volumn 24, Issue 1-2, 2012, Pages 86-94

  Martinon, A ^a   Cronin, U P ^a   Quealy, J ^b   Stapleton, A ^b   Wilkinson, M G ^a  

^a UNIVERSITY OF LIMERICK   (Ireland)

^b Dawn Fresh Foods   (Ireland)

Author keywords

Bacteria; PMA; Real time PCR; Swab; Viable

Indexed keywords

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; STAPHYLOCOCCUS AUREUS;

EID: 80055099846     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2011.09.007     Document Type: Article

References (71)

1. Anonymous Council directive 93/43/EEC of 14 June 1993 on the hygiene of foodstuffs 1993, Official Journal of the European Communities, Brussels, Belgium. E. Commission (Ed.).
2. Anonymous EC Decision 2001/471/EC - Commission decision of 8 June 2001 laying down rules for the regular checks on the general hygiene carried out by the operators in establishments according to Directive 64/433/EEC on health conditions for the production and marketing of fresh meat and Directive 71/118/EEC on health problems affecting the production and placing on the market of fresh poultry meat 2001, Official Journal of the European Communities, Brussels, Belgium. E. Commission (Ed.).
3. Anonymous ISO 18593:2004-Microbiology of food and animal feeding stuffs - Horizontal methods for sampling techniques from surfaces using contact plates and swabs. Geneva, Switzerland 2004.
4. Anonymous Reagent D - version 2.0-For the elimination of DNA from dead cells to avoid false-positive PCR results 2008, Biotecon Diagnostics, Potsdam, Germany.
5. Bae S., Wuertz S. Rapid decay of host-specific fecal bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide. Water Research 2009, 43(19):4850-4859.
6. Bazaco M.C., Eifert J.D., Williams R.C., Kathariou S. Quantitative recovery of Listeria monocytogenes and select Salmonella serotypes from environmental sample media. Journal of Aoac International 2007, 90(1):250-257.
7. Brakstad O.G., Aasbakk K., Maeland J.A. Detection of Staphylococcus aureus by Polymerase Chain Reaction, Amplification of the nuc gene. Journal of Clinical Microbiology 1992, 30(7):1654-1660.
8. Birch L., Dawson C.E., Cornett J.H., Keer J.T. A comparison of nucleic acid amplification techniques for the assessment of bacterial viability. Letters in Applied Microbiology 2001, 33(4):296-301.
9. Bogosian G., Bourneuf E.V. A matter of bacterial life and death. Embo Reports 2001, 2(9):770-774.
10. Bolton P.H., Kearns D.R. Spectroscopic properties of ethidium monoazide - fluorescent photoaffinity label for nucleic acids. Nucleic Acids Research 1978, 5(12):4891-4903.
11. Brown M.H., Baird-Parker A.C. The microbiological examination of meat. Meat microbiology 1982, Applied Science Publishers, London, England. M.H. Brown (Ed.).
12. Cox L.J., Kleiss T., Cordier J.L., Cordellana C., Konkel P., Pedrazzini C., et al. Listeria spp. in food processing, non-food and domestic environments. Food Microbiology 1989, 6(1):49-61.
13. Dancer S.J. How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals. Journal of Hospital Infection 2004, 56(1):10-15.
14. Davidson C.A., Griffith C.J., Peters A.C., Fielding L.M. Evaluation of two methods for monitoring surface cleanliness - ATP bioluminescence and traditional hygiene swabbing. Luminescence 1999, 14(1):33-38.
15. Elizaquível P., Sánchez G., Salón N., Cerveró J., Aznar R. Specific detection of viable foodborne pathogenic bacteria in fresh-cut vegetables. foodInnova 2010 2010, Universidad Politechnica de Valencia.
16. Fedio W.M., Wendakoon C.N., Zapata R., Carrillo C., Browning P. Comparison of petrifilm (TM) staph express count system with the bacteriological analytical manual direct-plating method for enumeration of Staphylococcus aureus in artificially contaminated hard cheese. Journal of Aoac International 2008, 91(5):1138-1141.
17. Ferraz, M. A., Cerqueira, M., & Souza, M. R. Evaluation of Enterobacteriaceae in the powdered milk production chain using both traditional (ISO 21528:2) and rapid (3 M (TM) Petrifilm (TM)) methods. Annals of Microbiology, 60(2), 373-376.
18. Fittipaldi M., Codony F., Adrados B., Camper A., Morató J. Viable real-time PCR in environmental samples: can all data be interpreted directly?. Microbial Ecology 2010, 61(1):7-12.
19. Flekna G., Stefanic P., Wagner M., Smulders F.J.M., Mozina S.S., Hein I. Insufficient differentiation of live and dead Campylobacter jejuni and Listeria monocytogenes cells by ethidium monoazide (EMA) compromises EMA/real-time PCR. Research in Microbiology 2007, 158(5):405-412.
20. Fuster-Valls N., Hernadez-Herrero M., Marin-De-Mateo M., Rodriguez-Jerez J.J. Effect of different environmental conditions on the bacteria survival on stainless steel surfaces. Food Control 2008, 19(3):308-314.
21. Garcia-Cayuela T., Tabasco R., Pelaez C., Requena T. Simultaneous detection and enumeration of viable lactic acid bacteria and bifidobacteria in fermented milk by using propidium monoazide and real-time PCR. International Dairy Journal 2009, 19(6-7):405-409.
22. Griffith C. Improving surface sampling and detection of contamination. Handbook of hygiene control in the food industry 2005, Woodhead Publishing in Food Science and Technology, Cambridge, England. H.L.M. Lelieveld, M.A. Mostert, J. Holah (Eds.).
23. Griffith C.J., Cooper R.A., Gilmore J., Davies C., Lewis M. An evaluation of hospital cleaning regimes and standards. Journal of Hospital Infection 2000, 45(1):19-28.
24. Holah J. Cleaning and disinfection. Hygiene in food processing 2003, J. Woodhead Publishing Ltd, Cambridge, England. H.L.M. Lelieveld, M.A. Mostert, J. Holah (Eds.).
25. Josefsen M.H., Lofstrom C., Hansen T.B., Christensen L.S., Olsen J.E., Hoorfar J. Rapid quantification of viable Campylobacter bacteria on chicken carcasses, using real-time PCR and propidium monoazide treatment, as a tool for quantitative risk assessment. Applied and Environmental Microbiology 2010, 76(15):5097-5104.
26. Josephson K.L., Gerba C.P., Pepper I.L. Polymerase chain reaction detection of non viable bacterial pathogens. Applied and Environmental Microbiology 1993, 59(10):3513-3515.
27. Knight I.T. Molecular genetic methods for detection and identification of viable but nonculturable microorganisms. Noncultivable microorganisms in the environment 2000, 77-86. ASM Press, Washington DC, USA. CR.R, GD.J (Eds.).
28. Kobayashi H., Oethinger M., Tuohy M.J., Hall G.S., Bauer T.W. Improving clinical significance of PCR: use of propidium monoazide to distinguish viable from dead Staphylococcus aureus and Staphylococcus epidermidis. Journal of Orthopaedic Research 2009, 27(9):1243-1247.
29. Kobayashi H., Oethinger M., Tuohy M.J., Hall G.S., Bauer T.W. Unsuitable distinction between viable and dead Staphylococcus aureus and Staphylococcus epidermidis by ethidium bromide monoazide. Letters in Applied Microbiology 2009, 48(5):633-638.
30. Kusumaningrum H.D., Riboldi G., Hazeleger W.C., Beumer R.R. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. International Journal of Food Microbiology 2003, 85(3):227-236.
31. Luo J.F., Lin W.T., Guo Y. Method to detect only viable cells in microbial ecology. Applied Microbiology and Biotechnology 2010, 86(1):377-384.
32. Martinon A., Cronin U.P., Wilkinson M.G. Comparison of in-house and commercial real-time PCR systems for the detection of Enterobacteriaceae and their evaluation within an interlaboratory study using infant formula samples. Food Analytical Methods 2011, 10.1007/s12161-12010-19188-12167.
33. Martinon A., Cronin U.P., Wilkinson M.G. Development of defined microbial population standards using fluorescence activated cell sorting for the absolute quantification of S. aureus using real-time PCR. Molecular Biotechnology 2011, 10.1007/s12033-12011-19417-12033.
34. Martinon A., Wilkinson M.G. Selection of optimal primer sets for use in a duplex SYBR Green-based real time PCR protocol for the detection of L. monocytogenes and S. aureus in foods. Journal of Food Safety 2011, 10.1111/j.1745-4565.2011.00301.x.
35. Mattila T., Manninen M., Kylasiurola A.L. Effect of cleaning-in-place disinfectants on wild bacterial strains isolated from a milking line. Journal of Dairy Research 1990, 57(1):33-39.
36. McKillip J.L., Jaykus L.A., Drake M. rRNA stability in heat-killed and UV-irradiated enterotoxigenic Staphylococcus aureus and Escherichia coli O157: H7. Applied and Environmental Microbiology 1998, 64(11):4264-4268.
37. Miles A.A., Misra S.S., Irwin J.O. The estimation of the bactericidal power of the blood. Journal of Hygiene 1938, 38:732-749.
38. Moore G., Griffith C. A comparison of surface sampling methods for detecting coliforms on food contact surfaces. Food Microbiology 2002, 19(1):65-73.
39. Moore G., Griffith C. A comparison of traditional and recently developed methods for monitoring surface hygiene within the food industry: an industry trial. International Journal of Environmental Health Research 2002, 12(4):317-329.
40. Moore G., Griffith C. Factors influencing recovery of microorganisms from surfaces by use of traditional hygiene swabbing. Dairy, Food, and Environmental Sanitation 2002, 22(6):410-421.
41. Moore G., Griffith C. Problems associated with traditional hygiene swabbing: the need for in-house standardization. Journal of Applied Microbiology 2007, 103(4):1090-1103.
42. Mossel D.A.A., Jansen J.T., Struijk C.B. Microbiological safety assurance applied to smaller catering operations world-wide. From angst through ardour to assistance and achievement - the facts. Food Control 1999, 10(3):195-211.
43. Nakano S., Kobayashi T., Funabiki K., Matsumura A., Nagao Y., Yamada T. Development of a PCR assay for detection of Enterobacteriaceae in foods. Journal of Food Protection 2003, 66(10):1798-1804.
44. Nocker A., Camper A.K. Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Applied and Environmental Microbiology 2006, 72(3):1997-2004.
45. Nocker A., Cheung C.Y., Camper A.K. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. Journal of Microbiological Methods 2006, 67(2):310-320.
46. Nocker A., Richter-Heitmann T., Montijn R., Schuren F., Kort R. Discrimination between live and dead cells in bacterial communities from environmental water samples analyzed by 454 pyrosequencing. International Microbiology 2010, 13(2):59-65.
47. Nocker A., Sossa K.E., Camper A.K. Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. Journal of Microbiological Methods 2007, 70(2):252-260.
48. Nocker A., Sossa-Fernandez P., Burr M.D., Camper A.K. Use of propidium monoazide for live/dead distinction in microbial ecology. Applied and Environmental Microbiology 2007, 73(16):5111-5117.
49. Nogva H.K., Dromtorp S.M., Nissen H., Rudi K. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5 '-nuclease PCR. Biotechniques 2003, 34(4):804.
50. Nogva H.K., Rudi K., Naterstad K., Holck A., Lillehaug D. Application of 5'-nuclease PCR for quantitative detection of Listeria monocytogenes in pure cultures, water, skim milk, and unpasteurized whole milk. Applied and Environmental Microbiology 2000, 66(10):4266-4271.
51. Nyachuba D.G., Donnelly C.W. Comparison of 3M (TM) Petrifilm (TM) environmental Listeria plates against standard enrichment methods for the detection of Listeria monocytogenes of epidemiological significance from environmental surfaces. Journal of Food Science 2007, 72(9):346-354.
52. Pan Y., Breidt F., Kathariou S. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Applied and Environmental Microbiology 2006, 72(12):7711-7717.
53. Paulsen P., Borgetti C., Schopf E., Smulders F.J.M. Enumeration of Enterobacteriaceae in various foods with a new automated most-probable-number method compared with Petrifilm and international organization for standardization procedures. Journal of Food Protection 2008, 71(2):376-379.
54. Poimenidou S., Belessi C.A., Giaouris E.D., Gounadaki A.S., Nychas G.J.E., Skandamis P.N. Listeria monocytogenes attachment to and detachment from stainless steel surfaces in a simulated Dairy processing environment. Applied and Environmental Microbiology 2009, 75(22):7182-7188.
55. Rudi K., Moen B., Dromtorp S.M., Holck A.L. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Applied and Environmental Microbiology 2005, 71(2):1018-1024.
56. Rudi K., Naterstad K., Dromtorp S.M., Holo H. Detection of viable and dead Listeria monocytogenes on gouda-like cheeses by real-time PCR. Letters in Applied Microbiology 2005, 40(4):301-306.
57. Scheu P.M., Berghof K., Stahl U. Detection of pathogenic and spoilage micro-organisms in food with the polymerase chain reaction. Food Microbiology 1998, 15(1):13-31.
58. Scott E., Bloomfield S.F. The survival and transfer of microbial contamination via cloths, hands and utensils. Journal of Applied Bacteriology 1990, 68(3):271-278.
59. Sharma M., Anand S.K. Bacterial biofilm on food contact surfaces: a review. Journal of Food Science and Technology-Mysore 2002, 39(6):573-593.
60. Sheridan G.E.C., Masters C.I., Shallcross J.A., Mackey B.M. Detection of mRNA by reverse transcription PCR as an indicator of viability in Escherichia coli cells. Applied and Environmental Microbiology 1998, 64(4):1313-1318.
61. Silva B.O., Caraviello D.Z., Rodrigues A.C., Ruegg P.L. Evaluation of petrifilm for the isolation of Staphylococcus aureus from milk samples. Journal of Dairy Science 2005, 88(8):3000-3008.
62. Szewzyk U., Szewzyk R., Manz W., Schleifer K.H. Microbiological safety of drinking water. Annual Review of Microbiology 2000, 54:81-127.
63. Tassinari A.R., Noda P.K., Franco G.M., Landgraf M., Destro M.T. Express evaluation - an evaluation of 3M petrifilm staph express count system for enumerating coagulase-positive Staphylococcus. Food Quality Magazine 2006.
64. Varma M., Field R., Stinson M., Rukovets B., Wymer L., Hauglanda R. Quantitative real-time PCR analysis of total and propidium monoazide-resistant fecal indicator bacteria in wastewater. Water Research 2009, 43(19):4790-4801.
65. Verran J., Boyd R.D., Hall K., West R.H. Microbiological and chemical analyses of stainless steel and ceramics subjected to repeated soiling and cleaning treatments. Journal of Food Protection 2001, 64(9):1377-1387.
66. Vicosa G.N., Moraes P.M., Yamazi A.K., Nero L.A. Enumeration of coagulase and thermonuclease-positive Staphylococcus spp. in raw milk and fresh soft cheese: an evaluation of Baird-Parker agar, Rabbit Plasma Fibrinogen agar and the Petrifilm (TM) Staph Express count system. Food Microbiology 2010, 27(4):447-452.
67. Wang S.S., Levin R.E. Discrimination of viable Vibrio vulnificus cells from dead cells in real-time PCR. Journal of Microbiological Methods 2006, 64(1):1-8.
68. Wang Z., Spadoro J. Determination of target copy number of quantitative standards used in PCR-based diagnostic assays. Gene Quantification 1998, 31-44. Birkhäuser, Carlsbad, USA. F. Ferré (Ed.).
69. Wilks S.A., Michels H., Keevil C.W. The survival of Escherichia coli O157 on a range of metal surfaces. International Journal of Food Microbiology 2005, 105(3):445-454.
70. Wilks S.A., Michels H.T., Keevil C.W. Survival of Listeria monocytogenes Scott A on metal surfaces: implications for cross-contamination. International Journal of Food Microbiology 2006, 111(2):93-98.
71. Wolffs P., Norling B., Radstrom P. Risk assessment of false-positive quantitative real-time PCR results in food, due to detection of DNA originating from dead cells. Journal of Microbiological Methods 2005, 60(3):315-323.