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Use of used vs. fresh cheese brines and the effect of pH and salt concentration on the survival of Listeria monocytogenes

Published online by Cambridge University Press:  16 January 2014

Bjørn C T Schirmer
Affiliation:
Nofima – Norwegian Institute of Food, Fisheries and Aquaculture Research, PO box 210, N-1431 ÅS, Norway
Even Heir
Affiliation:
Nofima – Norwegian Institute of Food, Fisheries and Aquaculture Research, PO box 210, N-1431 ÅS, Norway
Bjørn-Arne Lindstedt
Affiliation:
Norwegian Institute of Public Health, PO box 4404, Nydalen, N-0403 OH, Norway
Trond Møretrø
Affiliation:
Nofima – Norwegian Institute of Food, Fisheries and Aquaculture Research, PO box 210, N-1431 ÅS, Norway
Solveig Langsrud*
Affiliation:
Nofima – Norwegian Institute of Food, Fisheries and Aquaculture Research, PO box 210, N-1431 ÅS, Norway
*
*For correspondence; e-mail: Solveig.Langsrud@nofima.no ealth

Abstract

The aim of the study was to investigate how the use of fresh cheese brines compared with used brines and various combinations of pH and NaCl concentrations affected the survival of Listeria monocytogenes. Cheese brines from five Norwegian small scale cheese producers were analysed and showed great variations in pH (4·54–6·01) and NaCl concentrations (14·1–26·9 %). The survival of five strains of List. monocytogenes (two clinical isolates, two food isolates and one animal isolate) in four different cheese brines (three used and one fresh) was investigated. Results showed significant differences in survival both depending on the strains and the brines. Strains of human outbreak listeriosis cases showed greater ability to survive in the brines compared with food isolates and a List. monocytogenes reference strain (1–2 log10 difference after 200 d). All strains showed highest survival in the freshly prepared brine compared with the used brines. Molecular typing by multiple locus variable number tandem repeats analysis (MLVA) showed that there were no detectable alterations in the examined variable number tandem repeats of the genome in five strains after 200 d storage in any of the salt brines. Combined effects of pH (4·5, 5·25 and 6·0) and NaCl (15, 20 and 25 %) in fresh, filter sterilised brines on the survival of List. monocytogenes were examined and results showed that pathogen populations decreased over time in all brines. Death rates at any given NaCl concentration were highest at low pH (4·5) and death rates at any given pH were highest at low NaCl concentrations (15 %). In conclusion, the use of used brines reduced the survival of List. monocytogenes and a combination of low pH (4·5) and low salt concentrations (15 %) decreased the risk of List. monocytogenes survival compared with higher pH (5·25 or 6·0) and higher NaCl concentrations (20 or 25 %).

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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References

Barancelli, GV, Camargo, TM, Reis, CMF, Porto, E, Hofer, E & Oliveira, CAF 2011 Incidence of Listeria monocytogenes in cheese manufacturing plants from the northeast region of Sao Paulo, Brazil. Journal of Food Protection 74 816819 Google Scholar
Barat, JM, Grau, R, Ibanez, JB & Fito, P 2005 Post-salting studies in Spanish cured ham manufacturing. Time reduction by using brine thawing-salting. Meat Science 69 201208 Google Scholar
Bille, J, Blanc, DS, Schmid, H, Boubaker, K, Baumgartner, A, Siegrist, HH, Tritten, ML, Lienhard, R, Berner, D, Andreau, R, Treboux, M, Ducommun, JM, Malinverni, R, Genné, D, Erard, PH & Waespi, U 2006 Outbreak of human listeriosis associated with Tomme cheese in northwest Switzerland, 2005. Eurosurveillance 11 9193 CrossRefGoogle ScholarPubMed
Blom, H 2010 [Fermenting and fermented fish] In: Everything about Smoked, Fermented, Dried and Cured Foods, pp. 5677 2nd ed. (Ed. Hagen, H). Oslo, Norway: Tun Forlag AS Google Scholar
Bohaychuk, VM & Greer, GG 2003 Bacteriology and storage life of moisture-enhanced pork. Journal of Food Protection 66 293299 Google Scholar
Boyer, RR, Matak, K, Sumner, SS, Meadows, B, Williams, RC, Eifert, JD & Birbari, W 2009 Survival of Listeria monocytogenes, Listeria innocua, and lactic acid bacteria in chill brines. Journal of Food Science 74 M219M223 Google Scholar
Buncic, S, Avery, SM, Rocourt, J & Dimitrijevic, M 2001 Can food-related environmental factors induce different behaviour in two key serovars, 4b and 1/2a, of Listeria monocytogenes? International Journal of Food Microbiology 65 201212 Google Scholar
Bylund, G 1995 Dairy Processing Handbook. Lund, Sweden: Tetra Pak Processing Systems AB Google Scholar
Cooley, MB, Carychao, D, Nguyen, K, Whitehand, L & Mandrell, R 2010 Effects of environmental stress on stability of tandem repeats in Escherichia coli O157:H7. Applied and Environmental Microbiology 76 33983400 Google Scholar
De Jesus, AJ & Whiting, RC 2003 Thermal inactivation, growth, and survival studies of Listeria monocytogenes strains belonging to three distinct genotypic lineages. Journal of Food Protection 66 16111617 Google Scholar
Deleon, SP, Inoue, N & Shinano, H 1994 Shelf-life of sardine and bacterial-flora in brine containing acetic-acid during immersed storage. Fisheries Science 60 429433 Google Scholar
Di Bonaventura, G, Piccolomini, R, Paludi, D, D'Orio, V, Vergara, A, Conter, M & Ianieri, A 2008 Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. Journal of Applied Microbiology 104 15521561 CrossRefGoogle ScholarPubMed
Dogruer, Y, Guner, A & Gurbuz, U 2007 Effects of curing techniques and compositions on chemical, microbiological and sensory qualities of turkey pastirma. Archiv für Lebensmittelhygiene 58 6469 Google Scholar
Drevets, DA & Bronze, MS 2008 Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunology and Medical Microbiology 53 151165 Google Scholar
Duodu, S, Holst-Jensen, A, Skjerdal, T, Cappelier, JM, Pilet, MF & Loncarevic, S 2010 Influence of storage temperature on gene expression and virulence potential of Listeria monocytogenes strains grown in a salmon matrix. Food Microbiology 27 795801 Google Scholar
Durmaz, H, Aygun, O & Ardic, M 2009 The effect of cheese brine concentrations on survival of Listeria monocytogenes . Journal of Food Agriculture & Environment 7 1113 Google Scholar
Erdenlig, S, Ainsworth, AJ & Austin, FW 2000 Pathogenicity and production of virulence factors by Listeria monocytogenes isolates from channel catfish. Journal of Food Protection 63 613619 Google Scholar
Ermolaeva, S, Belyi, Y & Tartakovskii, I 1999 Characteristics of induction of virulence factor expression by activated charcoal in Listeria monocytogenes . FEMS Microbiology Letters 174 137141 Google Scholar
Fretz, R, Pichler, J, Sagel, U, Much, P, Ruppitsch, W, Pietzka, AT, Stoger, A, Huhulescu, S, Heuberger, S, Appl, G, Werber, D, Stark, K, Prager, R, Flieger, A, Karpiskova, R, Pfaff, G & Allerberger, F 2010 Update: Multinational listeriosis outbreak due to ‘Quargel’, a sour milk curd cheese, caused by two different List. monocytogenes serotype 1/2a strains, 2009–2010. Eurosurveillancs 15 23 Google Scholar
Gallart-Jornet, L, Barat, JM, Rustad, T, Erikson, U, Escriche, I & Fito, P 2007 Influence of brine concentration on Atlantic salmon fillet salting. Journal of Food Engineering 80 267275 Google Scholar
Gaulin, C, Ramsay, D & Bekal, S 2012 Widespread listeriosis outbreak attributable to pasteurized cheese, which lead to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. Journal of Food Protection 75 7178 Google Scholar
Gorski, L, Flaherty, D & Mandrell, RE 2006 Competitive fitness of Listeria monocytogenes serotype 1/2a and 4b strains in mixed cultures with and without food in the US Food and Drug Administration enrichment protocol. Applied and Environmental Microbiology 72 776783 CrossRefGoogle ScholarPubMed
Gottlieb, SL, Newbern, EC, Griffin, PM, Graves, LM, Hoekstra, RM, Baker, NL, Hunter, SB, Holt, KG, Ramsey, F, Head, M, Levine, P, Johnson, G, Schoonmaker-Bopp, D, Reddy, V, Kornstein, L, Gerwel, M, Nsubuga, J, Edwards, L, Stonecipher, S, Hurd, S, Austin, D, Jefferson, MA, Young, SD, Hise, K, Chernak, ED, Sobel, J & Grp, LOW 2006 Multistate outbreak of listeriosis linked to Turkey deli meat and subsequent changes in US regulatory policy. Clinical Infectious Diseases 42 2936 Google Scholar
Grinstead, DA & Cutter, CN 2007 Controlling Listeria monocytogenes in a retail setting. Food Protection Trends 27 2228 Google Scholar
Guinee, TP 2004 Salting and the role of salt in cheese. International Journal of Dairy Technology 57 99109 Google Scholar
Huss, HH, BenEmbarek, PK & Jeppesen, VF 1995 Control of biological hazards in cold smoked salmon production. Food Control 6 335340 Google Scholar
Ivanek, R, Grohn, YT & Wiedmann, M 2004 The cost and benefit of Listeria monocytogenes food safety measures. Critical Reviews in Food Science and Nutrition 44 513523 Google Scholar
Johnsen, BO, Lingaas, E, Torfoss, D, Strom, EH & Nordoy, I 2010 A large outbreak of Listeria monocytogenes infection with short incubation period in a tertiary care hospital. Journal of Infection 61 465470 Google Scholar
Lado, BH & Yousef, AE 2007 Characteristics of Listeria monocytogenes important to food processes. In: Listeria, Listeriosis and Food Safety, pp. 157213 (Eds Ryser, ET, Marth, EM). Boca-Raton, Florida, USA: CRC Press Google Scholar
Larson, AE, Johnson, EA & Nelson, JH 1999 Survival of Listeria monocytogenes in commercial cheese brines. Journal of Dairy Science 82 18601868 CrossRefGoogle ScholarPubMed
Lianou, A, Stopforth, JD, Yoon, Y, Wiedmann, M & Sofos, JN 2006 Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and origins. Journal of Food Protection 69 26402647 Google Scholar
Lindstedt, BA, Tham, W, Danielsson-Tham, ML, Vardund, T, Helmersson, S & Kapperud, G 2008 Multiple-locus variable-number tandem-repeats analysis of Listeria monocytogenes using multicolour capillary electrophoresis and comparison with pulsed-field gel electrophoresis typing. Journal of Microbiolical Methods 72 141148 CrossRefGoogle ScholarPubMed
Liu, DY, Lawrence, ML, Ainsworth, AJ & Austin, FW 2005 Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains. FEMS Microbiology Letters 243 373378 Google Scholar
Loncarevic, S, Bannerman, E, Bille, J, Danielsson-Tham, ML & Tham, W 1998 Characterization of Listeria strains isolated from soft and semi-soft cheeses. Food Microbiology 15 521525 Google Scholar
Makino, SI, Kawamoto, K, Takeshi, K, Okada, Y, Yamasaki, A, Yamamoto, S & Igimi, S 2005 An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. International Journal of Food Microbiology 104 189196 Google Scholar
Malorny, B, Junker, E & Helmuth, R 2008 Multi-locus variable-number tandem repeat analysis for outbreak studies of Salmonella enterica serotype Enteritidis. BMC Microbiology 8 84 Google Scholar
McCollum, JT, Cronquist, AB, Silk, BJ, Jackson, KA, O'Connor, KA, Cosgrove, S, Gossack, JP, Parachini, SS, Jain, NS, Ettestad, P, Ibraheem, M, Cantu, V, Joshi, M, DuVernoy, T, Fogg, NW, Gorny, JR, Mogen, KM, Spires, C, Teitell, P, Joseph, LA, Tarr, CL, Imanishi, M, Neil, KP, Tauxe, RV & Mahon, BE 2013 Multistate outbreak of Listeriosis associated with cantaloupe. New England Journal of Medicine 369 944953 Google Scholar
Miya, S, Kimura, B, Sato, M, Takahashi, H, Ishikawa, T, Suda, T, Takakura, C, Fujii, T & Wiedmann, M 2008 Development of a multilocus variable-number of tandem repeat typing method for Listeria monocytogenes serotype 4b strains. International Journal of Food Microbiology 124 239249 Google Scholar
Murray, EGD, Webb, RE & Swann, MBR 1926 A disease of rabbits characterized by a large mononuclear leucocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes (n. sp.). Journal of Pathology & Bacteriology 29 407439 Google Scholar
NMKL, Nordic committee on Food Analysis 2007 No 136 4. ed. – Listeria monocytogenes. Detection and ennumeration in foods and feeding stuffs Oslo, NorwayGoogle Scholar
Nygaard, K, Vold, L, Heier, BT, Bruun, T & Kapperud, G 2010 Norway – Trends and Sources of Zoonoses and Zoonotic Agents in Humans, Food Stuffs, Animals and Feedingstuffs, p. 35. Oslo: Norwegian Institute of Public Health Google Scholar
Palmai, M & Buchanan, RL 2002 The effect of Lactococcus lactis on the growth of Listeria monocytogenes in alfalfa sprout broth. Acta Alimentaria 31 379392 Google Scholar
Pintado, CMBS, Oliveira, A, Pampulha, ME & Ferreira, MASS 2005 Prevalence and characterization of Listeria monocytogenes isolated from soft cheese. Food Microbiology 22 7985 Google Scholar
Romanova, N, Favrin, S & Griffiths, MW 2002 Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Applied and Environmental Microbiology 68 64056409 Google Scholar
Sallam, KI 2008 Effect of marinating process on the microbiological quality of Pacific saury (Cololabis saira) during vacuum-packaged storage at 4 °C. International Journal of Food Science and Technology 43 220228 CrossRefGoogle Scholar
Schirmer, BCT, Heir, E, Møretrø, T, Skaar, I & Langsrud, S 2013 Microbial background flora in small-scale cheese production facilities does not inhibit growth and surface attachment of Listeria monocytogenes . Journal of Dairy Science 96 61616171 Google Scholar
Shabala, L, Lee, SH, Cannesson, P & Ross, T 2008 Acid and NaCl limits to growth of Listeria monocytogenes and influence of sequence of inimical acid and NaCl levels on inactivation kinetics. Journal of Food Protection 71 11691177 Google Scholar
Swaminathan, B & Gerner-Smidt, P 2007 The epidemiology of human listeriosis. Microbes and Infection 9 12361243 Google Scholar
Tham, W, Ericsson, H, Loncarevic, S, Unnerstad, H & Danielsson-Tham, ML 2000 Lessons from an outbreak of listeriosis related to vacuum-packed gravad and cold-smoked fish. International Journal of Food Microbiology 62 173175 Google Scholar
Uyttendaele, M, De Troy, P & Debevere, J 1999 Incidence of Listeria monocytogenes in different types of meat products on the Belgian retail market. International Journal of Food Microbiology 53 7580 Google Scholar
van der Veen, S, Moezelaar, R, Abee, T & Wells-Bennik, MHJ 2008 The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traits. Journal of Applied Microbiology 105 12461258 Google Scholar
Warriner, K & Namvar, A 2009 What is the hysteria with Listeria? Trends in Food Science and Technology 20 245254 Google Scholar
Wen, J, Anantheswaran, RC & Knabel, SJ 2009 Changes in Barotolerance, Thermotolerance, and Cellular Morphology throughout the Life Cycle of Listeria monocytogenes . Applied and Environmental Microbiology 75 15811588 Google Scholar
Werbrouck, H, Vermeulen, A, Van Coillie, E, Messens, W, Herman, L, Devlieghere, F & Uyttendaele, M 2009 Influence of acid stress on survival, expression of virulence genes and invasion capacity into Caco-2 cells of Listeria monocytogenes strains of different origins. International Journal of Food Microbiology 134 140146 Google Scholar