Microbial background flora in small-scale cheese production facilities does not inhibit growth and surface attachment of Listeria monocytogenes

Journal of Dairy Science

Volumn 96, Issue 10, 2013, Pages 6161-6171

  Schirmer, B C T ^a   Heir, E ^a   Moretro T ^a   Skaar, I ^b   Langsrud, S ^a  

^a NOFIMA   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Cheese; Flora; Listeria monocytogenes; Small scale

Indexed keywords

BACTERIA (MICROORGANISMS); CHRYSEOBACTERIUM; LACTOCOCCUS; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; MICROBACTERIUM; PSEUDOMONAS PUTIDA; PSYCHROBACTER; PSYCHROBACTER SP.; RHODOCOCCUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS EQUORUM;

BRINE; INORGANIC SALT;

ANTIBIOSIS; BACTERIA; BACTERIUM ADHERENCE; CHEESE; FOOD CONTROL; FOOD SAFETY; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; MICROBIOLOGY; MICROFLORA; NORWAY; PHYSIOLOGY; YEAST;

ANTIBIOSIS; BACTERIA; BACTERIAL ADHESION; CHEESE; FOOD MICROBIOLOGY; FOOD SAFETY; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; MICROBIOTA; NORWAY; SALTS; YEASTS;

EID: 84884350148     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2012-6395     Document Type: Article

References (50)

1. Bell C., Kyriakides A. Outbreaks: Causes and lessons to be learnt. Listeria: A Practical Approach to the Organism and its Control in Foods 2005, Blackwell Publishing Ltd., Oxford, UK, Pages 28-31. 2nd.
2. Bemrah N., Sanaa M., Cassin M.H., Griffiths M.W., Cerf O. Quantitative risk assessment of human listeriosis from consumption of soft cheese made from milk. Prev. Vet. Med. 1998, 37:129-145.
3. Bergdoll M.S. Staphylococcus aureus. Foodborne Bacterial Pathogens 1989, 463-523. Marcel Dekker Inc., New York, NY. M.P. Doyle (Ed.).
4. Bille J., Blanc D.S., Schmid H., Boubaker K., Baumgartner A., Siegrist H.H., Tritten M.L., Lienhard R., Berner D., Anderau R., Treboux M., Ducommun J.M., Malinverni R., Genné D., Erard P.H., Waespi U. Outbreak of human listeriosis associated with tomme cheese in northwest Switzerland, 2005. Euro Surveill. 2006, 11:91-93.
5. Bockelmann V., Willems P., Rademaker J., Noordman W., Heller K.J. Cultures for surface ripening of smeared soft cheese. Kieler Milchwirtschaftliche Forschungsberichte 2003, 55:277-299.
6. Bore E., Langsrud S. Characterization of micro-organisms isolated from dairy industry after cleaning and fogging disinfection with alkyl amine and peracetic acid. J. Appl. Microbiol. 2005, 98:96-105.
7. Bremer P.J., Monk I., Osborne C.M. Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. J. Food Prot. 2001, 64:1369-1376.
8. Carpentier B., Chassaing D. Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. Int. J. Food Microbiol. 2004, 97:111-122.
9. Carrique-Mas J.J., Hökeberg I., Andersson Y., Arneborn M., Tham W., Danielsson-Tham M.-L., Osterman B., Leffler M., Steen M., Eriksson E., Hedin G., Giesecke J. Febrile gastroenteritis after eating on-farm manufactured fresh cheese-An outbreak of listeriosis?. Epidemiol. Infect. 2003, 130:79-86.
10. Di Bonaventura G., Piccolomini R., Paludi D., D'Orio V., Vergara A., Conter M., Ianieri A. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: Relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 2008, 104:1552-1561.
11. Fretz R., Pichler J., Sagel U., Much P., Ruppitsch W., Pietzka A.T., Stöger A., Huhulescu S., Heuberger S., Appl G., Werber D., Stark K., Prager R., Flieger A., Karpíšková 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:pii:19543.
12. Fricker M., Skånseng B., Rudi K., Stessl B., Ehling-Schulz M. Shift from farm to dairy tank milk microbiota revealed by a polyphasic approach is independent from geographical origin. Int. J. Food Microbiol. 2011, 145:S24-S30.
13. Gaulin C., Ramsay D., Bekal S. Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. J. Food Prot. 2012, 75:71-78.
14. Gaulin C., Ramsay D., Ringuette L., Ismaïl J. First documented outbreak of Listeria monocytogenes in Quebec, 2002. Can. Commun. Dis. Rep. 2003, 29:181-186.
15. Glass N.L., Donaldson G.C. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 1995, 61:1323-1330.
16. Gudbjörnsdóttir B., Einarsson H., Thorkelsson G. Microbial adhesion to processing lines for fish fillets and cooked shrimp: Influence of stainless steel surface finish and presence of gram-negative bacteria on the attachment of Listeria monocytogenes. Food Technol. Biotechnol. 2005, 43:55-61.
17. Guillier L., Stahl V., Hezard B., Notz E., Briandet R. Modelling the competitive growth between Listeria monocytogenes and biofilm microflora of smear cheese wooden shelves. Int. J. Food Microbiol. 2008, 128:51-57.
18. Johnsen B.O., Lingaas E., Torfoss D., Strøm E.H., Nordøy I. A large outbreak of Listeria monocytogenes infection with short incubation period in a tertiary care hospital. J. Infect. 2010, 61:465-470.
19. Lado B.H., Yousef A.E. Characteristics of Listeria monocytogenes important to food processes. Listeria, Listeriosis, and Food Safety 2007, E. T. Ryser and E. H. Marth, ed. CRC Press, Pages 157-213.
20. Langsrud S., Møretrø T., Heir E. Bacteria in the food production environment. Food Sci. Technol. 2012, 26:26-30.
21. Larsen A.G., Knøchel S. Antimicrobial activity of food-related Penicillium sp. against pathogenic bacteria in laboratory media and a cheese model system. J. Appl. Microbiol. 1997, 83:111-119.
22. Larson A.E., Johnson E.A., Nelson J.H. Survival of Listeria monocytogenes in commercial cheese brines. J. Dairy Sci. 1999, 82:1860-1868.
23. Leriche V., Carpentier B. Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms. J. Appl. Microbiol. 2000, 88:594-605.
24. Leriche V., Chassaing D., Carpentier B. Behaviour of L. monocytogenes in an artificially made biofilm of a nisin-producing strain of Lactococcus lactis. Int. J. Food Microbiol. 1999, 51:169-182.
25. Licitra G., Ogier J.C., Parayre S., Pediliggieri C., Carnemolla T.M., Falentin H., Madec M.N., Carpino S., Lortal S. Variability of bacterial biofilms of the "Tina" wood vats used in the Ragusano cheese-making process. Appl. Environ. Microbiol. 2007, 73:6980-6987.
26. Lortal S., Di Blasi A., Madec M.N., Pediliggieri C., Tuminello L., Tanguy G., Fauquant J., Lecuona Y., Campo P., Carpino S., Licitra G. Tina wooden vat biofilm: A safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. Int. J. Food Microbiol. 2009, 132:1-8.
27. Makino S.I., Kawamoto K., Takeshi K., Okada Y., Yamasaki A., Yamamoto S., Igimi S. An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. Int. J. Food Microbiol. 2005, 104:189-196.
28. Mariani C., Briandet R., Chamba J.-F., Notz E., Carnet-Pantiez A., Eyoug R.N., Oulahal N. Biofilm ecology of wooden shelves used in ripening the French raw milk smear cheese Reblochon de Savoie. J. Dairy Sci. 2007, 90:1653-1661.
29. Mariani C., Oulahal N., Chamba J.-F., Dubois-Brissonnet F., Notz E., Briandet R. Inhibition of Listeria monocytogenes by resident biofilms present on wooden shelves used for cheese ripening. Food Contr. 2011, 22:1357-1362.
30. Murray M.G., Thompson W.F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980, 8:4321-4325.
31. Nadkarni M.A., Martin F.E., Jacques N.A., Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 2002, 148:257-266.
32. Nieto-Arribas P., Seseña S., Poveda J.M., Palop L., Cabezas L. Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol. 2010, 27:85-93.
33. Pitt J.I. The Genus Penicillium and its Teleomorphic States Eupenicillium and Talaromyces 1979, Academic Press, London, UK.
34. Pitt J.I. Fungi and food spoilage 1999, Aspen Publishers Inc., Frederick, MD. 2nd.
35. Ponder M.A., Thomashow M.F., Tiedje J.M. Metabolic activity of Siberian permafrost isolates, Psychrobacter arcticus and Exiguobacterium sibiricum, at low water activities. Extremophiles 2008, 12:481-490.
36. Quigley L., O'Sullivan O., Beresford T.P., Ross R.P., Fitzgerald G.F., Cotter P.D. Molecular approaches to analysing the microbial composition of raw milk and raw milk cheese. Int. J. Food Microbiol. 2011, 150:81-94.
37. Retureau É., Callon C., Didienne R., Montel M.-C. Is microbial diversity an asset for inhibiting Listeria monocytogenes in raw milk cheeses?. Dairy Sci. Technol. 2010, 90:375-398.
38. Rieu A., Lemaître J.-P., Guzzo J., Piveteau P. Interactions in dual species biofilms between Listeria monocytogenes EGD-e and several strains of Staphylococcus aureus. Int. J. Food Microbiol. 2008, 126:76-82.
39. Romanova N., Favrin S., Griffiths M.W. Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Appl. Environ. Microbiol. 2002, 68:6405-6409.
40. Saá Ibusquiza P., Herrera J.J.R., Vázquez-Sánchez D., Cabo M.L. Adherence kinetics, resistance to benzalkonium chloride and microscopic analysis of mixed biofilms formed by Listeria monocytogenes and Pseudomonas putida. Food Contr. 2012, 25:202-210.
41. Samson R.A., Frisvad J.C. Penicillium subgenus Penicillium: New taxonomic schemes and mycotoxins and other extrolites. Page 257 in Studies in Mycology 2004, Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands.
42. Samson R.A., Houbraken J., Thrane U., Frisvad J.C., Andersen B. Food and Indoor Fungi 2010, Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands.
43. Schvartzman M.S., Maffre A., Tenenhaus-Aziza F., Sanaa M., Butler F., Jordan K. Modelling the fate of Listeria monocytogenes during manufacture and ripening of smeared cheese made with pasteurised or raw milk. Int. J. Food Microbiol. 2011, 145(Suppl. 1):S31-S38.
44. Skånseng B., Kaldhusdal M., Rudi K. Comparison of chicken gut colonisation by the pathogens Campylobacter jejuni and Clostridium perfringens by real-time quantitative PCR. Mol. Cell. Probes 2006, 20:269-279.
45. Swaminathan B., Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect. 2007, 9:1236-1243.
46. Van Kessel J.A.S., Karns J.S., Lombard J.E., Kopral C.A. Prevalence of Salmonella enterica, Listeria monocytogenes, and Escherichia coli virulence factors in bulk tank milk and in-line filters from US dairies. J. Food Prot. 2011, 74:759-768.
47. Vít M., Olejník R., Dlhý J., Karpišková R., Částcová J., Príkazský V., Príkazská M., Beneš Č., Petráš P. Outbreak of listeriosis in the Czech Republic, late 2006-Preliminary report. Euro Surveill. 2007, 12. E070208.1.
48. White T.J., Burns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 1990, 315-322. Academic Press Inc., New York, NY. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).
49. Zameer F., Kreft J., Gopal S. Interaction of Listeria monocytogenes and Staphylococcus epidermidis in dual species biofilms. J. Food Saf. 2010, 30:954-968.
50. Zhao T., Doyle M.P., Zhao P. Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Appl. Environ. Microbiol. 2004, 70:3996-4003.