Evaluation of viability-qPCR detection system on viable and dead Salmonella serovar Enteritidis

Journal of Microbiological Methods

Volumn 103, Issue , 2014, Pages 131-137

  Barbau Piednoir, Elodie ^a,b   Mahillon, Jacques ^a   Pillyser, Julie ^b   Coucke, Wim ^b   Roosens, Nancy H ^b   Botteldoorn, Nadine ^b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

Author keywords

Detection; Propidium monoazide; Real time PCR; Salmonella; SYBR Green

Indexed keywords

PROPIDIUM MONOAZIDE; REAGENT; UNCLASSIFIED DRUG; AZIDE; PROPIDIUM IODIDE;

ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL VIABILITY; BACTERIUM CULTURE; CELL DEATH; CELL KILLING; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SALMONELLA ENTERITIDIS; VIABILITY POLYMERASE CHAIN REACTION; ANALOGS AND DERIVATIVES; DRUG EFFECTS; GENETICS; MICROBIAL VIABILITY; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR ENTERITIDIS; SALMONELLA INFECTIONS; SENSITIVITY AND SPECIFICITY;

AZIDES; MICROBIAL VIABILITY; PROPIDIUM; REAL-TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS; SENSITIVITY AND SPECIFICITY;

EID: 84902959036     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2014.06.003     Document Type: Article

References (64)

1. Banihashemi A., Van Dyke M.I., Huck P.M. Long-amplicon propidium monoazide-PCR enumeration assay to detect viable Campylobacter and Salmonella. J. Appl. Microbiol 2012, 10.1111/j.1365-2672.2012.05382.x.
2. Barbau-Piednoir E., Roosens N.H., Bertrand S., Mahillon J., Botteldoorn N. SYBR®Green qPCR Salmonella detection system allowing discrimination at the genus, species and subspecies levels. Appl. Microbiol. Biotechnol. 2013, 97:9811-9824. 10.1007/s00253-013-5234-x.
3. Bustin S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 2000, 25:169-193.
4. Cawthorn D.M., Witthuhn R.C. Selective PCR detection of viable Enterobacter sakazakii cells utilizing propidium monoazide or ethidium bromide monoazide. J. Appl. Microbiol. 2008, 105:1178-1185. 10.1111/j.1365-2672.2008.03851.x.
5. Coffman G.L., Gaubatz J.W., Yielding K.L., Yielding L.W. Demonstration of specific high affinity binding sites in plasmid DNA by photoaffinity labeling with an ethidium analog. J. Biol. Chem. 1982, 257:13205-13207.
6. Commission of the European Communities Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs 2005.
7. Commission of the European Communities Commission Regulation (EU) No 209/2013 of 11 March 2013 amending Regulation (EC) No 2073/2005 as regards microbiological criteria for sprouts and the sampling rules for poultry carcases and fresh poultry meat 2013.
8. Dinu L.D., Bach S. Detection of viable but non-culturable Escherichia coli O157:H7 from vegetable samples using quantitative PCR with propidium monoazide and immunological assays. Food Control 2013, 31:268-273. 10.1016/j.foodcont.2012.10.020.
9. EFSA: European Food Safety Authority and ECDC: European Centre for Disease Prevention and Control The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA J. 2014, 12:3547. 10.2903/j.efsa.2014.3547.
10. Elizaquivel P., Sanchez G., Aznar R. Application of propidium monoazide quantitative PCR for selective detection of live Escherichia coli O157:H7 in vegetables after inactivation by essential oils. Int. J. Food Microbiol. 2012, 159:115-121. 10.1016/j.ijfoodmicro.2012.08.006.
11. Elizaquivel P., Sanchez G., Selma M.V., Aznar R. Application of propidium monoazide-qPCR to evaluate the ultrasonic inactivation of Escherichia coli O157:H7 in fresh-cut vegetable wash water. Food Microbiol. 2012, 30:316-320. 10.1016/j.fm.2011.10.008.
12. Elizaquivel P., Sanchez G., Aznar R. Quantitative detection of viable foodborne E.coli O157:H7, Listeria monocytogenes and Salmonella in fresh-cut vegetables combining propidium monoazide and real-time PCR. Food Control 2012, 25:704-708. 10.1016/j.foodcont.2011.12.003.
13. Fittipaldi M., Codony F., Adrados B., Camper A.K., Morato J. Viable real-time PCR in environmental samples: can all data be interpreted directly?. Microb. Ecol 2010, 10.1007/s00248-010-9719-1.
14. Fittipaldi M., Nocker A., Codony F. Progress in understanding preferential detection of live cells using viability dyes in combination with DNA amplification. J. Microbiol. Meth. 2012, 91:276-289. 10.1016/j.mimet.2012.08.007.
15. Gonzalez-Escalona N., Hammack T.S., Russell M., Jacobson A.P., De Jesus A.J., Brown E.W., Lampel K.A. Detection of live Salmonella sp. cells in produce by a TaqMan-based quantitative reverse transcriptase real-time PCR targeting invA mRNA. Appl. Environ. Microbiol. 2009, 75:3714-3720. 10.1128/AEM.02686-08.
16. ISO: International Organization for Standardization ISO 11290-1:1996 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Listeria monocytogenes - Part 1: Detection Method 1996.
17. ISO: International Organization for Standardization ISO 11290-2:1996 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Listeria monocytogenes - Part 2: Enumeration Method 1996.
18. ISO: International Organization for Standardization ISO 16654:2001 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection Escherichia coli O157 2001.
19. ISO: International Organization for Standardization ISO 6579:2002 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection of Salmonella spp 2002.
20. ISO: International Organization for Standardization ISO 10272-1:2006 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Campylobacter spp. - Part 1: Detection Method 2006.
21. ISO: International Organization for Standardization ISO 10272-2:2006 - Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Campylobacter spp. - Part 2: Colony-count Technique 2006.
22. ISO: International Organization for Standardization ISO/TS 13136:2012 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, O103 and O145 Serogroups 2012.
23. 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. Appl. Environ. Microbiol. 2010, 76:5097-5104. 10.1128/AEM.00411-10.
24. Kim S.Y., Ko G. Using propidium monoazide to distinguish between viable and nonviable bacteria, MS2 and murine norovirus. Lett. Appl. Microbiol 2012, 10.1111/j.1472-765X.2012.03276.x.
25. Kobayashi H., Oethinger M., Tuohy M.J., Hall G.S., Bauer T.W. Distinction between intact and antibiotic-inactivated bacteria by real-time PCR after treatment with propidium monoazide. J. Orthop. Res. 2010, 28:1245-1251. 10.1002/jor.21108.
26. Kralik P., Nocker A., Pavlik I. Mycobacterium avium subsp. paratuberculosis viability determination using F57 quantitative PCR in combination with propidium monoazide treatment. Int. J. Food Microbiol. 2010, 141(Suppl. 1):S80-S86. 10.1016/j.ijfoodmicro.2010.03.018.
27. Li B., Chen J.Q. Development of a sensitive and specific qPCR assay in conjunction with propidium monoazide for enhanced detection of live Salmonella spp. in food. BMC Microbiol. 2013, 13:273. 10.1186/1471-2180-13-273.
28. Li M., Zhao G., Liu J., Gao X., Zhang Q. Effect of different heat treatments on the degradation of Salmonella nucleic acid. J. Food Saf. 2013, 33:536-544. 10.1111/jfs.12086.
29. Liang Z., Keeley A. Comparison of propidium monoazide-quantitative PCR and reverse transcription quantitative PCR for viability detection of fresh Cryptosporidium oocysts following disinfection and after long-term storage in water samples. Water Res. 2012, 46:5941-5953. 10.1016/j.watres.2012.08.014.
30. Liang N., Dong J., Luo L., Li Y. Detection of viable Salmonella in lettuce by propidium monoazide real-time PCR. J. Food Sci. 2011, 76:M234-M237. 10.1111/j.1750-3841.2011.02123.x.
31. Liu Y., Mustapha A. Detection of viable Escherichia coli O157:H7 in ground beef by propidium monoazide real-time PCR. Int. J. Food Microbiol. 2014, 170C:48-54. 10.1016/j.ijfoodmicro.2013.10.026.
32. Lovdal T., Hovda M.B., Börkblom B., Moller S.G. Propidium monoazide combined with real-time quantitative PCR underestimates heat-killed Listeria innocua. J. Microbiol. Meth. 2011, 85:164-169. 10.1016/j.mimet.2011.01.027.
33. Luo J.F., Lin W.T., Guo Y. Method to detect only viable cells in microbial ecology. Appl. Microbiol. Biotechnol. 2010, 86:377-384. 10.1007/s00253-009-2373-1.
34. Mamlouk K., Mace S., Guilbaud M., Jaffres E., Ferchichi M., Prevost H., Pilet M.F., Dousset X. Quantification of viable Brochothrix thermosphacta in cooked shrimp and salmon by real-time PCR. Food Microbiol. 2012, 30:173-179. 10.1016/j.fm.2011.09.012.
35. Martin B., Raurich S., Garriga M., Aymerich T. Effect of amplicon length in propidium monoazide quantitative PCR for the enumeration of viable cells of Salmonella in cooked ham. Food Anal. Methods 2013, 10.1007/s12161-012-9460-0.
36. Masters C.I., Shallcross J.A., Mackey B.M. Effect of stress treatments on the detection of Listeria monocytogenes and enterotoxigenic Escherichia coli by the polymerase chain reaction. J. Appl. Bacteriol. 1994, 77:73-79.
37. McIngvale S.C., Elhanafi D., Drake M.A. Optimization of reverse transcriptase PCR to detect viable Shiga-toxin-producing Escherichia coli. Appl. Environ. Microbiol. 2002, 68:799-806. 10.1128/AEM.68.2.799-806.2002.
38. Misumi M., Tanaka N. Mechanism of inhibition of translocation by kanamycin and viomycin: a comparative study with fusidic acid. Biochem. Biophys. Res. Commun. 1980, 92:647-654. 10.1016/0006-291X(80)90382-4.
39. Nkuipou-Kenfack E., Engel H., Fakih S., Nocker A. Improving efficiency of viability-PCR for selective detection of live cells. J. Microbiol. Methods 2013, 93:20-24. 10.1016/j.mimet.2013.01.018.
40. Nocker A., Camper A.K. Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Appl. Environ. Microbiol. 2006, 72:1997-2004. 10.1128/AEM.72.3.1997-2004.2006.
41. Nocker A., Camper A.K. Novel approaches toward preferential detection of viable cells using nucleic acid amplification techniques. FEMS Microbiol. Lett. 2009, 291(2):137-142.
42. 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. J. Microbiol. Methods 2006, 67:310-320. 10.1016/j.mimet.2006.04.015.
43. Nocker A., Sossa K.E., Camper A.K. Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 2007, 70:252-260. 10.1016/j.mimet.2007.04.014.
44. Pacholewicz E., Swart A., Lipman L.J., Wagenaar J.A., Havelaar A.H., Duim B. Propidium monoazide does not fully inhibit the detection of dead Campylobacter on broiler chicken carcasses by qPCR. J. Microbiol. Methods 2013, 10.1016/j.mimet.2013.06.003.
45. Pan Y., Breidt F. Enumeration of viable Listeria monocytogenes cells by real-time PCR with propidium monoazide and ethidium monoazide in the presence of dead cells. Appl. Environ. Microbiol. 2007, 73:8028-8031. 10.1128/AEM.01198-07.
46. Postollec F., Falentin H., Pavan S., Combrisson J., Sohier D. Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 2011, 28:848-861. 10.1016/j.fm.2011.02.008.
47. Rudi K., Naterstad K., Dromtorp S.M., Holo H. Detection of viable and dead Listeria monocytogenes on gouda-like cheeses by real-time PCR. Lett. Appl. Microbiol. 2005, 40:301-306. 10.1111/j.1472-765X.2005.01672.x.
48. Schnetzinger F., Pan Y., Nocker A. Use of propidium monoazide and increased amplicon length reduce false-positive signals in quantitative PCR for bioburden analysis. Appl. Microbiol. Biotechnol 2013, 10.1007/s00253-013-4711-6.
49. Shapiro H.M. Parameters and probes. Practical Flow Cytometry 2003, John Wileys & Sons. Inc., Hoboken, New Jersey, USA. 4th edition, 10.1002/0471722731.ch7.
50. Singh G., Vajpayee P., Bhatti S., Ronnie N., Shah N., McClure P., Shanker R. Determination of viable Salmonellae from potable and source water through PMA assisted qPCR. Ecotoxicol. Environ. Saf. 2013, 93:121-127. 10.1016/j.ecoenv.2013.02.017.
51. Soejima T., Iida K., Qin T., Taniai H., Seki M., Takade A., Yoshida S. Photoactivated ethidium monoazide directly cleaves bacterial DNA and is applied to PCR for discrimination of live and dead bacteria. Microbiol. Immunol. 2007, 51:763-775.
52. Soejima T., Minami J., Iwatsuki K. Rapid propidium monoazide PCR assay for the exclusive detection of viable Enterobacteriaceae cells in pasteurized milk. J. Dairy Sci. 2012, 95:3634-3642. 10.3168/jds.2012-5360.
53. Trevors J.T. Can dead bacterial cells be defined and are genes expressed after cell death?. J. Microbiol. Meth. 2012, 90:25-29. 10.1016/j.mimet.2012.04.004.
54. van Frankenhuyzen J.K., Trevors J.T., Lee H., Flemming C.A., Habash M.B. Molecular pathogen detection in biosolids with a focus on quantitative PCR using propidium monoazide for viable cell enumeration. J. Microbiol. Meth. 2011, 87:263-272. 10.1016/j.mimet.2011.09.007.
55. Wang H., Gill C.O., Yang X. Use of sodium lauroyl sarcosinate (sarkosyl) in viable real-time PCR for enumeration of Escherichia coli. J. Microbiol. Meth. 2014, 98:89-93. 10.1016/j.mimet.2014.01.004.
56. 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, 36:119-125. 10.1016/j.foodcont.2013.08.011.
57. Waring M.J. Complex formation between ethidium bromide and nucleic acids. J. Mol. Biol. 1965, 13:269-282.
58. 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. J. Microbiol. Methods 2005, 60:315-323. 10.1016/j.mimet.2004.10.003.
59. Yanez M.A., Nocker A., Soria-Soria E., Murtula R., Martinez L., Catalan V. Quantification of viable Legionella pneumophila cells using propidium monoazide combined with quantitative PCR. J. Microbiol. Meth. 2011, 85:124-130. 10.1016/j.mimet.2011.02.004.
60. Yang X., Badoni M., Gill C.O. Use of propidium monoazide and quantitative PCR for differentiation of viable Escherichia coli from E. coli killed by mild or pasteurizing heat treatments. Food Microbiol. 2011, 28:1478-1482. 10.1016/j.fm.2011.08.013.
61. Yang Y., Wan C., Xu H., Lai W., Xiong Y., Xu F., You X., Xu H., Aguilar Z.P., Sun J., Wei H. Development of a multiplexed PCR assay combined with propidium monoazide treatment for rapid and accurate detection and identification of three viable Salmonella enterica serovars. Food Control 2012, 28:456-462. 10.1016/j.foodcont.2012.05.061.
62. Yang X., Badoni M., Wang H., Gill C.O. Effects of mild and pasteurizing heat treatments on survival of generic and verotoxigenic Escherichia coli from beef enrichment cultures. Food Control 2014, 39:100-104.
63. Yaron S., Matthews K.R. A reverse transcriptase-polymerase chain reaction assay for detection of viable Escherichia coli O157:H7 investigation of specific target genes. J. Appl. Microbiol. 2002, 92:633-640. 10.1046/j.1365-2672.2002.01563.x.
64. Zhu R.G., Li T.P., Jia Y.F., Song L.F. Quantitative study of viable Vibrio parahaemolyticus cells in raw seafood using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 2012, 10.1016/j.mimet.2012.05.019.