L. monocytogenes in a cheese processing facility: Learning from contamination scenarios over three years of sampling

International Journal of Food Microbiology

Volumn 189, Issue , 2014, Pages 98-105

  Ruckerl I ^a,b   Muhterem Uyar, M ^a,b   Muri Klinger, S ^a   Wagner, K H ^b   Wagner, M ^a   Stessl, B ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Contamination scenario; Food processing; Listeria monocytogenes

Indexed keywords

BENZALKONIUM CHLORIDE; HYDROGEN PEROXIDE; PERACETIC ACID;

ARTICLE; AUSTRIA; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIUM ISOLATE; CHEESE; CLEANING; COOLING; FOOD CONTAMINATION; FOOD PROCESSING; FOOD STORAGE; GENOTYPE; HUMIDITY; LEARNING; LISTERIA MONOCYTOGENES; MINIMUM INHIBITORY CONCENTRATION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PH; PULSED FIELD GEL ELECTROPHORESIS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; STORAGE TEMPERATURE; WATER VAPOR;

CONTAMINATION SCENARIO; FOOD PROCESSING; LISTERIA MONOCYTOGENES;

CHEESE; DISINFECTANTS; ELECTROPHORESIS, GEL, PULSED-FIELD; FOOD CONTAMINATION; FOOD HANDLING; FOOD MICROBIOLOGY; GENOTYPE; HUMANS; LISTERIA MONOCYTOGENES; MULTILOCUS SEQUENCE TYPING; PHYLOGENY;

EID: 84906075974     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.08.001     Document Type: Article

References (60)

1. Alessandria V., Rantsiou K., Dolci P., Cocolin L. Molecular methods to assess Listeria monocytogenes route of contamination in a dairy processing plant. Int. J. Food Microbiol. 2010, 141:S156-S162.
2. Almeida G., Magalhães R., Carneiro L., Santos I., Silva J., Ferreira V., Hogg T., Teixeira P. Foci of contamination of Listeria monocytogenes in different cheese processing plants. Int. J. Food Microbiol. 2013, 167:303-309.
3. Anonymous Guidelines on sampling the food processing area and equipment for the detection of Listeria monocytogenes 2012, 1-15. (http://www.ansespro.fr/eurl-listeria/Documents/LIS-Cr-201213D1.pdf; accessed on: 05.12.2013).
4. Asperger H., Wagner M., Brandl E. An approach towards public health and foodborne human listeriosis-the Austrian Listeria monitoring. Berl. Munch. Tierarztl. Wochenschr. 2001, 114:446-452.
5. Berrang M.E., Frank J.F. Generation of airborne Listeria innocua from model floor drains. J. Food Prot. 2012, 75:1328-1331.
6. Bubert A., Hein I., Rauch M., Lehner A., Yoon B., Goebel W., Wagner M. Detection and differentiation of Listeria spp. by a single reaction based on multiplex PCR. Appl. Environ. Microbiol. 1999, 65:4688-4692.
7. Carpentier B., Cerf O. Review-persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145:1-8.
8. Chambel L., Sol M., Fernandes I., Barbosa M., Zilhão I., Barata B., Jordan S., Perni S., Shama G., Adrião A. Occurrence and persistence of Listeria spp. in the environment of ewe and cow's milk cheese dairies in Portugal unveiled by an integrated analysis of identification, typing and spatial-temporal mapping along production cycle. Int. J. Food Microbiol. 2007, 116:52-63.
9. Cooper J.E., Feil E.J. Multilocus sequence typing-what is resolved?. Trends Microbiol. 2004, 12:373-377.
10. Dal Bello B., Cocolin L., Zeppa G., Field D., Cotter P.D., Hill C. Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in cottage cheese. Int. J. Food Microbiol. 2012, 153:58-65.
11. Doumith M., Buchrieser C., Glaser P., Jacquet C., Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J. Clin. Microbiol. 2004, 42:3819-3822.
12. Dufour C. Application of EC regulation no. 2073/2005 regarding Listeria monocytogenes in ready-to-eat foods in retail and catering sectors in Europe. Food Control 2011, 22:1491-1494.
13. European Commission (EC) Commission Regulation No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Communities 2005, 1-29. (p 9. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2005R2073:20071227:EN:PDF; accessed on: 05.04.2014).
14. Ferreira V., Barbosa J., Stasiewicz M., Vongkamjan K., Moreno Switt A., Hogg T., Gibbs P., Teixeira P., Wiedmann M. Diverse geno- and phenotypes of persistent Listeria monocytogenes isolates from fermented meat sausage production facilities in Portugal. Appl. Environ. Microbiol. 2011, 77:2701-2715.
15. Fox E., Hunt K., O'Brien M., Jordan K. Listeria monocytogenes in Irish Farmhouse cheese processing environments. Int. J. Food Microbiol. 2011, 145(Suppl. 1):S39-S45.
16. Freitag N.E., Port G.C., Miner M.D. Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 2009, 7:623-628.
17. Fretz R., Pichler J., Sagel U., Much P., Ruppitsch W., Pietzka A.T., Stoger A., Huhulescu S., Heuberger S., Appl G., Werber D., Stark K., Prager R., Flieger A., Karpiskova R., Pfaff G., Allerberger F. Update: multinational listeriosis outbreak due to 'Quargel', a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009-2010. Euro Surveill. 2010, 15:19543.
18. Garrido V., García-Jalón I., Vitas A.I. Temperature distribution in Spanish domestic refrigerators and its effect on Listeria monocytogenes growth in sliced ready-to-eat ham. Food Control 2010, 21:896-901.
19. Gilmour M.W., Graham M., Van Domselaar G., Tyler S., Kent H., Trout-Yakel K.M., Larios O., Allen V., Lee B., Nadon C. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 2010, 11:120.
20. Holch A., Webb K., Lukjancenko O., Ussery D., Rosenthal B.M., Gram L. Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6years apart. Appl. Environ. Microbiol. 2013, 79:2944-2951.
21. Huson D.H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 1998, 14:68-73. (Oxford, England).
22. Institute Pasteur L. monocytogenes MLST database. PF8 genotyping of pathogens and public health platform (accessed on: 05.04.2014). http://www.pasteur.fr/recherche/genopole/PF8/mlst/Lmono.html.
23. ISO 11290-1 Microbiology of food and animal feeding stuffs-horizontal method for the detection and enumeration of Listeria monocytogenes - Part 1: Detection, 1996/Amd 1:2004 1996, International Organisation for Standardisation, Geneva.
24. ISO 11290-2 Microbiology of food and animal feeding stuffs - Horizontal method for the detection and enumeration of Listeria monocytogenes - Part 2: Enumeration method 1998, International Organisation for Standardisation, Geneva.
25. Jackson K., Biggerstaff M., Tobin-D'Angelo M., Sweat D., Klos R., Nosari J., Garrison O., Boothe E., Saathoff-Huber L., Hainstock L. Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant. Hispanic women. J. Food Prot. 2011, 74:949-953.
26. Kastbjerg V.G., Gram L. Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Int. J. Food Microbiol. 2012, 160:11-15.
27. Koch J., Dworak R., Prager R., Becker B., Brockmann S., Wicke A., Wichmann-Schauer H., Hof H., Werber D., Stark K. Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006-2007. Foodborne Pathog. Dis. 2010, 7:1581-1584.
28. Lambertz S.T., Ivarsson S., Lopez-Valladares G., Sidstedt M., Lindqvist R. Subtyping of Listeria monocytogenes isolates recovered from retail ready-to-eat foods, processing plants and listeriosis patients in Sweden 2010. Int. J. Food Microbiol. 2013, 166:186-192.
29. Lehto M., Kuisma R., Määttä J., Kymäläinen H., Mäki M. Hygienic level and surface contamination in fresh-cut vegetable production plants. Food Control 2011, 22:469-475.
30. Lomonaco S., Verghese B., Gerner-Smidt P., Tarr C., Gladney L., Joseph L., Katz L., Turnsek M., Frace M., Chen Y., Brown E., Meinersmann R., Berrang M., Knabel S. Novel epidemic clones of Listeria monocytogenes, United States, 2011. Emerg. Infect. Dis. 2013, 19:147-150.
31. Luber P., Crerar S., Dufour C., Farber J., Datta A., Todd E.C. Controlling Listeria monocytogenes in ready-to-eat foods: working towards global scientific consensus and harmonization-recommendations for improved prevention and control. Food Control 2011, 22:1535-1549.
32. Malley T.J., Stasiewicz M.J., Grohn Y.T., Roof S., Warchocki S., Nightingale K., Wiedmann M. Implementation of statistical tools to support identification and management of persistent Listeria monocytogenes contamination in smoked fish processing plants. J. Food Prot. 2013, 76:796-811.
33. Mammina C., Parisi A., Guaita A., Aleo A., Bonura C., Nastasi A., Pontello M. Enhanced surveillance of invasive listeriosis in the Lombardy region, Italy, in the years 2006-2010 reveals major clones and an increase in serotype 1/2a. BMC Infect. Dis. 2013, 13. (152-2334-13-152).
34. Marklinder I., Lindblad M., Eriksson L., Finnson A., Lindqvist R. Home storage temperatures and consumer handling of refrigerated foods in Sweden. J. Food Prot. 2004, 67:2570-2577.
35. McLaughlin J., Mitchell R.T., Smerdon W.J., Jewell K. Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. Int. J. Food Microbiol. 2004, 92:15-33.
36. Mereghetti L., Quentin R., Marquet-Van Der Mee N., Audurier A. Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 2000, 66:5083-5086.
37. Møller S.M., Bertram H.C., Andersen U., Lillevang S.K., Rasmussen A., Hansen T.B. Physical sample structure as predictive factor in growth modeling of Listeria innocua in a white cheese model system. Food Microbiol. 2013, 36:90-102.
38. Nilsson R.E., Ross T., Bowman J.P. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int. J. Food Microbiol. 2011, 150:14-24.
39. Ortiz S., López V., Villatoro D., López P., Dávila J.C., Martínez-Suárez J.V. A 3-year surveillance of the genetic diversity and persistence of Listeria monocytogenes in an Iberian pig slaughterhouse and processing plant. Foodborne Pathog. Dis. 2010, 7:1177-1184.
40. Parisi A., Latorre L., Fraccalvieri R., Miccolupo A., Normanno G., Caruso M., Santagada G. Occurrence of Listeria spp. in dairy plants in Southern Italy and molecular subtyping of isolates using AFLP. Food Control 2013, 29:91-97.
41. Pricope L., Nicolau A., Wagner M., Rychli K. The effect of sublethal concentrations of benzalkonium chloride on invasiveness and intracellular proliferation of Listeria monocytogenes. Food Control 2012, 31:230-235.
42. PubMLST (accessed: 05.12.2013). http://pubmlst.org/analysis/.
43. Ragon M., Wirth T., Hollandt F., Lavenir R., Lecuit M., Le Monnier A., Brisse S. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 2008, 4:1-14.
44. Reij M.W., Den Aantrekker E.D. Recontamination as a source of pathogens in processed foods. Int. J. Food Microbiol. 2004, 91:1-11.
45. Rodrigues D., Cerca N., Teixeira P., Oliveira R., Ceri H., Azeredo J. Listeria monocytogenes and Salmonella enterica Enteritidis biofilms susceptibility to different disinfectants and stress-response and virulence gene expression of surviving cells. Microb. Drug Resist. 2011, 17:181-189.
46. Rotariu O., Thomas D.J.I., Goodburn K.E., Hutchison M.L., Strachan N.J. Smoked salmon industry practices and their association with Listeria monocytogenes. Food Control 2014, 35:284-292.
47. Rousseaux S., Olier M., Lemaitre J.P., Piveteau P., Guzzo J. Use of PCR-restriction fragment length polymorphism of inlA for rapid screening of Listeria monocytogenes strains deficient in the ability to invade Caco-2 cells. Appl. Environ. Microbiol. 2004, 70:2180-2185.
48. Ryan S., Begley M., Hill C., Gahan C.G. A five-gene stress survival islet (SSI-1) that contributes to the growth of Listeria monocytogenes in suboptimal conditions. J. Appl. Microbiol. 2010, 109:984-995.
49. Schoder D., Rossmanith P., Glaser K., Wagner M. Fluctuation in contamination dynamics of L. monocytogenes in quargel (acid curd cheese) lots recalled during the multinational listeriosis outbreak 2009/2010. Int. J. Food Microbiol. 2012, 157:326-331.
50. Schoder D., Stessl B., Szakmary-Brändle K., Rossmanith P., Wagner M. Population diversity of Listeria monocytogenes in quargel (acid curd cheese) lots recalled during the multinational listeriosis outbreak 2009/2010. Food Microbiol. 2013, 39:68-73.
51. Schoder D., Skandamis P., Wagner M. Assessing in-house monitoring efficiency by tracing contamination rates in cheese lots recalled during an outbreak of listeriosis in Austria. Int. J. Food Microbiol. 2013, 167:353-358.
52. Stessl B., Fricker M., Fox E., Karpiskova R., Demnerova K., Jordan K., Ehling-Schulz M., Wagner M. Collaborative survey on the colonization of different types of cheese processing facilities with Listeria monocytogenes. Foodborne Pathog. Dis. 2013, (Ahead of print). 10.1089/fpd.2013.1578.
53. Tasara T., Stephan R. Cold stress tolerance of Listeria monocytogenes: a review of molecular adaptive mechanisms and food safety implications. J. Food Prot. 2006, 69:1473-1484.
54. Tenover F.C., Arbeit R.D., Goering R.V., Mickelsen P.A., Murray B.E., Persing D.H., Swaminathan B. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 1995, 33:2233.
55. Todd E.C.D., Notermans S. Surveillance of listeriosis and its causative pathogen, Listeria monocytogenes. Food Control 2011, 22:1484-1490.
56. Van Houdt R., Michiels C.W. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 2010, 109:1117-1131.
57. Walsh P.S., Metzger D.A., Higushi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 1991, 10:506-513.
58. Wang Y., Zhao A., Zhu R., Lan R., Jin D., Cui Z., Wang Y., Li Z., Wang Y., Xu J. Genetic diversity and molecular typing of Listeria monocytogenes in China. BMC Microbiol. 2012, 12:119.
59. Williams S.K., Roof S., Boyle E.A., Burson D., Thippareddi H., Geornaras I., Sofos J.N., Wiedmann M., Nightingale K. Molecular ecology of Listeria monocytogenes and other Listeria species in small and very small ready-to-eat meat processing plants. J. Food Prot. 2011, 74:63-77.
60. Yde M., Naranjo M., Mattheus W., Stragier P., Pochet B., Beulens K., De Schrijver K., Van den Branden D., Laisnez V., Flipse W., Leclercq A., Lecuit M., Dierick K., Bertrand S. Usefulness of the European Epidemic Intelligence Information System in the management of an outbreak of listeriosis, Belgium, 2011. Euro Surveill. 2012, 17:20279.