[en] Listeria monocytogenes can proliferate at the beginning of cheesemaking as the conditions favor growth. The objective of this study was to establish the growth limits of L. monocytogenes in a cheese matrix, in case of potential contamination of the milk prior to cheese manufacture. A semisoft laboratory scale model cheese system was made at different initial pH and water activity (a(w)) levels with a mix of two strains of L. monocytogenes. A factorial design of five pH values (5.6 to 6.5), four a(w) values (0.938 to 0.96), and two L. monocytogenes inoculation levels (1 to 20 CFU/ml and 500 to 1,000 CFU/ml) was carried out. Each combination was evaluated in six independent replicates. In order to determine if there was a dominant strain, isolated colonies from the cheeses were analyzed by pulsed-field gel electrophoresis. The data relating to growth initiation were fitted to a logistic regression model. The a(w) of milk influenced the probability of growth initiation of L. monocytogenes at both low and high contamination levels. The pH, at the concentrations tested, had a lower effect on the probability of growth initiation. At pH 6.5 and a(w) of 0.99 for low contamination levels and pH 6.5 and a(w) of 0.97 for high contamination levels, increases in population of up to 4 and 2 log were observed at low and high contamination levels, respectively. This shows that if conditions are favorable for growth initiation at the early stages of the cheesemaking process, contamination of milk, even with low numbers, could lead to L. monocytogenes populations that exceed the European Union's microbiological limit of 100 CFU/g of cheese.
Disciplines :
Food science
Author, co-author :
Schvartzman Echenique, Maria Sol ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Belessi, C.
Butler, F.
Skandamis, P. N.
Jordan, K. N.
Language :
English
Title :
Effect of pH and water activity on the growth limits of Listeria monocytogenes in a cheese matrix at two contamination levels.
Publication date :
2011
Journal title :
Journal of Food Protection
ISSN :
0362-028X
eISSN :
1944-9097
Publisher :
International Association for Food Protection, United States - Iowa
Adda, J., Gripon, J.C., Vassal, L., The chemistry of flavour and texture generation in cheese (1982) Food Chem., 9, pp. 115-129
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 raw milk (1998) Preventive Veterinary Medicine, 37 (1-4), pp. 129-145. , PII S0167587798001123
Bolton, L.F., Frank, J.F., Defining the growth/no-growth interface for listeria monocytogenes in mexican-style cheese based on salt, ph, and moisture content (1999) Journal of Food Protection, 62 (6), pp. 601-609
Boziaris, I.S., Skandamis, P.N., Anastasiadi, M., Nychas, G.J., Effect of NaCl and KCl on fate and growth/no growth interfaces of Listeria monocytogenes Scott A at different pH and nisin concentrations (2007) J. Appl. Microbiol., 102, pp. 796-805
(2007), www.ComBase.cc, Accessed May 2011
Dalton, C.B., Austin, C.C., Sobel, J., Hayes, P.S., Bibb, W.F., Graves, L.M., Swaminathan, B., Griffin, P.M., An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk (1997) New England Journal of Medicine, 336 (2), pp. 100-105. , DOI 10.1056/NEJM199701093360204
Dawson, S.J., Evans, M.R., Willby, D., Bardwell, J., Chamberlain, N., Lewis, D.A., Listeria outbreak associated with sandwich consumption from a hospital retail shop, United Kingdom (2006) Euro Surveill., 11, pp. 89-91
De Buyser, M.-L., Dufour, B., Maire, M., Lafarge, V., Implication of milk and milk products in food-borne diseases in France and in different industrialised countries (2001) International Journal of Food Microbiology, 67 (1-2), pp. 1-17. , DOI 10.1016/S0168-1605(01)00443-3, PII S0168160501004433
Dillon, R., Occurrence of Listeria in hot and cold smoked seafood products (1994) International Journal of Food Microbiology, 22 (1), pp. 73-77. , DOI 10.1016/0168-1605(94)90009-4
Dmitrovskii, A.A., Chemistry of processed cheese (1951) Uchenye Zapiski. Vtoroi Moskovskii Ordena Lenina Gosudarstvennyi Meditsinskii Institut im N. I. Pirogova., 1, pp. 248-253
Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs (2005) Off. J. Eur. Union L, 338, pp. 1-26. , European Commission
Commission Regulation (EC) No 1441/2007 on microbiological criteria for foodstuffs (2007) Off. J. Eur. Union L, 322, pp. 12-29. , European Commission
Gaya, P., Saralegui, C., Medina, M., Nunez, M., Occurrence of Listeria monocytogenes and Other Listeria spp. in Raw Caprine Milk (1996) Journal of Dairy Science, 79 (11), pp. 1936-1941
Gibson, A.M., Predicting fungal growth: The effect of water activity on Aspergillus flavus and related species (1994) International Journal of Food Microbiology, 23 (3-4), pp. 419-431. , DOI 10.1016/0168-1605(94)90167-8
Graves, L.M., Swaminathan, B., PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis (2001) International Journal of Food Microbiology, 65 (1-2), pp. 55-62. , DOI 10.1016/S0168-1605(00)00501-8, PII S0168160500005018
Guerra, M.M., McLauchlin, J., Bernardo, F.A., Listeria in ready-to-eat and unprocessed foods produced in portugal (2001) Food Microbiology, 18 (4), pp. 423-429. , DOI 10.1006/fmic.2001.0421
Harvey, J., Gilmour, A., Occurrence of Listeria species in raw milk and dairy products produced in Northern Ireland (1992) J. Appl. Bacteriol., 72, pp. 119-125
Holah, J.T., Taylor, J.H., Dawson, D.J., Hall, K.E., Biocide use in the food industry and the disinfectant resistance of persistent strains of Listeria monocytogenes and Escherichia coli (2002) Journal of Applied Microbiology Symposium Supplement, 92 (1), pp. 111S-120S
Hwang, C.-A., The probability of growth of Listeria monocytogenes in cooked salmon and tryptic soy broth as affected by salt, smoke compound, and storage temperature (2009) Food Microbiol., 26, pp. 253-258
(1982) Cheese & Processed Cheese. Determination of the Total Solid content., , International Dairy Federation, Standard 4A. International Dairy Federation, Brussels
Milk and milk products (1985) Guidance on sampling., , International Dairy Federation, Standard 50B. International Dairy Federation, Brussels
(1987) Milk, Cream & Evaporated Milk. Determination of Total Solids content., , International Dairy Federation, Standard 21B. International Dairy Federation, Brussels
(1992) Milk and Milk Products: Preparation of Samples and Dilutions for Microbiological Examination., , International Dairy Federation, Standard 122B. International Dairy Federation, Brussels
Koutsoumanis, K.P., Kendall, P.A., Sofos, J.N., A comparative study on growth limits of Listeria monocytogenes as affected by temperature, pH and a w when grown in suspension or on a solid surface (2004) Food Microbiology, 21 (4), pp. 415-422. , DOI 10.1016/j.fm.2003.11.003
Koutsoumanis, K.P., Sofos, J.N., Effect of inoculum size on the combined temperature, pH and a w limits for growth of Listeria monocytogenes (2005) International Journal of Food Microbiology, 104 (1), pp. 83-91. , DOI 10.1016/j.ijfoodmicro.2005.01.010, PII S0168160505002400
Lianou, A., Sofos, J.N., A review of the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments (2007) Journal of Food Protection, 70 (9), pp. 2172-2198
Little, C.L., Rhoades, J.R., Sagoo, S.K., Harris, J., Greenwood, M., Mithani, V., Grant, K., McLauchlin, J., Microbiological quality of retail cheeses made from raw, thermized or pasteurized milk in the UK (2008) Food Microbiol., 25, pp. 304-312
Little, C.L., Taylor, F.C., Sagoo, S.K., Gillespie, I.A., Grant, K., McLauchlin, J., Prevalence and level of Listeria monocytogenes and other Listeria species in retail pre-packaged mixed vegetable salads in the UK (2007) Food Microbiology, 24 (7-8), pp. 711-717. , DOI 10.1016/j.fm.2007.03.009, PII S0740002007000524
Loncarevic, S., Danielsson-Tham, M.L., Tham, W., Occurrence of Listeria monocytogenes in soft and semi-soft cheeses in retail outlets in Sweden (1995) Int. J. Food Microbiol., 26, pp. 245-250
Lund, B.M., Baird-Parker, T.C., Gould, G.W., (2000) The Microbiological Safety and Quality of Food, 1, p. 164. , Aspen Publishers Inc., Gaithersburg, MD
Makino, S.-I., Kawamoto, K., Takeshi, K., Okada, Y., Yamasaki, M., Yamamoto, S., Igimi, S., An outbreak of food-borne listeriosis due to cheese in Japan, during 2001 (2005) International Journal of Food Microbiology, 104 (2), pp. 189-196. , DOI 10.1016/j.ijfoodmicro.2005.02.009, PII S0168160505002497
McKellar, R.C., Lu, X., (2004) Modelling Microbial Responses in Foods, , ed., CRC Press, Washington, DC
McMeekin, T.A., Presser, K., Ratkowsky, D., Ross, T., Salter, M., Tienungoon, S., Quantifying the hurdle concept by modelling the bacterial growth/no growth interface (2000) International Journal of Food Microbiology, 55 (1-3), pp. 93-98. , DOI 10.1016/S0168-1605(00)00182-3, PII S0168160500001823
Medrala, D., Dabrowski, W., Czekajlo-Kolodziej, U., Daczkowska-Kozon, E., Koronkiewicz, A., Augustynowicz, E., Manzano, M., Persistence of Listeria monocytogenes strains isolated from products in a Polish fish-processing plant over a 1-year period (2003) Food Microbiology, 20 (6), pp. 715-724. , DOI 10.1016/S0740-0020(02)00173-9
Miettinen, H., Wirtanen, G., Prevalence and location of Listeria monocytogenes in farmed rainbow trout (2005) International Journal of Food Microbiology, 104 (2), pp. 135-143. , DOI 10.1016/j.ijfoodmicro.2005.01.013, PII S0168160505002436
Nolan, D.A., Chamblim, D.C., Troller, J.A.J., Minimal a w for growth of Listeria monocytogenes as affected by solute and temperature (1991) Int. J. Food Microbiol., 14, pp. 333-337
Presser, K.A., Ross, T., Ratkowsky, D.A., Modelling the growth limits (growth/no growth interface) of Escherichia coli as a function of temperature, pH, lactic acid concentration, and water activity (1998) Applied and Environmental Microbiology, 64 (5), pp. 1773-1779
Ratkowsky, D.A., Ross, T., Modelling the bacterial growth/no growth interface (1995) Lett. Appl. Microbiol., 20, pp. 29-33
Ross, T., Dalgaard, P., Secondary models (2004) Modelling Microbial Responses in Foods, pp. 63-150. , R. C. McKellar and X. Lu ed., CRC Press, Washington, DC
Rudolf, M., Scherer, S., High incidence of Listeria monocytogenes in European red smear cheese (2001) International Journal of Food Microbiology, 63 (1-2), pp. 91-98. , DOI 10.1016/S0168-1605(00)00413-X, PII S016816050000413X
Samelis, J., Metaxopoulos, J., Incidence and principal sources of Listeria spp. and Listeria monocytogenes contamination in processed meats and a meat processing plant (1999) Food Microbiology, 16 (5), pp. 465-477. , DOI 10.1006/fmic.1998.0263
Skandamis, P.N., Stopforth, J.D., Kendall, P.A., Belk, K.E., Scanga, J.A., Smith, G.C., Sofos, J.N., Modeling the effect of inoculum size and acid adaptation on growth/no growth interface of Escherichia coli O157:H7 (2007) International Journal of Food Microbiology, 120 (3), pp. 237-249. , DOI 10.1016/j.ijfoodmicro.2007.08.028, PII S0168160507004618
Soultos, N., Koidis, P., Madden, R.H., Presence of Listeria and Salmonella spp. in retail chicken in Northern Ireland (2003) Letters in Applied Microbiology, 37 (5), pp. 421-423. , DOI 10.1046/j.1472-765X.2003.01423.x
(1976) Methods for Chemical Analysis of Cheese. Determination of PH value., , Standard BS 770-5:, British Standards Institute, London
Swaminathan, B., Gerner-Smidt, P., The epidemiology of human listeriosis (2007) Microbes and Infection, 9 (10), pp. 1236-1243. , DOI 10.1016/j.micinf.2007.05.011, PII S1286457907001876, Forum on Listeria From Genomics to Pathagonesis
Thevenot, D., Delignette-Muller, M.L., Christieans, S., Vernozy-Rozand, C., Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and their products (2005) International Journal of Food Microbiology, 102 (1), pp. 85-94. , DOI 10.1016/j.ijfoodmicro.2004.12.008, PII S0168160505000486
Tienungoon, S., Ratkowsky, D.A., McMeekin, T.A., Ross, T., Growth limits of Listeria monocytogenes as a function of temperature, pH, NaCl, and lactic acid (2000) Appl. Environ. Microbiol., 66, pp. 4979-4987
Valero, A., Carrasco, E., Perez-Rodriguez, F., Garcia-Gimeno, R.M., Zurera, G., Growth/no growth model of Listeria monocytogenes as a function of temperature, pH, citric acid and ascorbic acid (2006) European Food Research and Technology, 224 (1), pp. 91-100. , DOI 10.1007/s00217-006-0293-1
Vermeulen, A., Gysemans, K.P., Bernaerts, K., Geeraerd, A.H., Van Impe, J.F., Debevere, J., Devlieghere, F., Influence of pH, aw and acetic acid concentration on Listeria monocytogenes at 7 degrees C: Data collection for the development of a growth/no growth model (2007) Int. J. Food Microbiol., 114, pp. 332-341
Zuliani, V., Lebert, I., Augustin, J.-C., Garry, P., Vendeuvre, J.-L., Lebert, A., Modelling the behaviour of Listeria monocytogenes in ground pork as a function of pH, water activity, nature and concentration of organic acid salts (2007) Journal of Applied Microbiology, 103 (3), pp. 536-550. , DOI 10.1111/j.1365-2672.2007.03283.x