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Absence of growth of Listeria monocytogenes in naturally contaminated Cheddar cheese

Published online by Cambridge University Press:  17 December 2013

Marion Dalmasso
Affiliation:
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland
Kieran Jordan*
Affiliation:
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland
*
*For correspondence; e-mail: kieran.jordan@teagasc.ie

Abstract

Each cheese producer is responsible by the legislation for the number of Listeria monocytogenes in cheese and is required to prove that numbers will not exceed 100 cfu/g throughout the shelf-life of the cheese. Even in the case of hard-cheese such as Cheddar cheese, the absence of growth of List. monocytogenes during ripening has to be demonstrated to comply with EU legislation. Studies dedicated to assessing List. monocytogenes growth throughout cheese shelf-life are generally based on artificially contaminated cheeses. Contrary to the majority of works, the current study focused on the growth of List. monocytogenes in naturally contaminated raw milk farmhouse Cheddar cheeses during a five-month ripening period. List. monocytogenes growth was assessed by direct count and its presence was detected by enrichment in two naturally contaminated cheese batches. In order to track routes of contamination, 199 processing environment samples from inside and outside the processing facility were taken, and their analysis for the presence of List. monocytogenes was performed on four occasions over a 9-month period. List. monocytogenes isolates were differentiated using PFGE and serotyping. List. monocytogenes never exceeded 20 cfu/g in the cheeses and could not be detected after five months of ripening. Eleven pulsotypes were identified. One pulsotype was found in the yard outside the processing facility, in a vat, on the processing area floor and in a cheese. This indicated that the outside environment constitutes a potential source of contamination of the processing environment and of the cheese. These results demonstrate that this farmhouse Cheddar cheese does not support List. monocytogenes growth and suggests that the efforts to reduce processing environment contamination are worthwhile.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2013 

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References

Alessandria, V, Rantsiou, K, Dolci, P & Cocolin, L 2010 Molecular methods to assess Listeria monocytogenes route of contamination in a dairy processing plant. International Journal of Food Microbiology 141 S156S162 CrossRefGoogle Scholar
Angelidis, AS, Boutsiouki, P & Papageorgiou, DK 2010 Loss of viability of Listeria monocytogenes in contaminated processed cheese during storage at 4, 12 and 22 °C. Food Microbiology 27 809818 CrossRefGoogle Scholar
AOAC 1990 Salt in cheese. Official method of analysis, 15th ed., vol. 2 (Ed. Helrich, K, section 971·19). Washington, DC, USA: Association of Official Analytical Chemists Google Scholar
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 CrossRefGoogle ScholarPubMed
Baranyi, J & Tamplin, ML 2004 ComBase: a common database on microbial responses to food environments. Journal of Food Protection 67 19671971 Google Scholar
Bille, J, Blanc, DS, Schmid, H, Boubaker, K, Baumgartner, A, Siegrist, HH, Tritten, ML, Lienhard, R, Berner, D, Anderau, R, Treboux, M, Ducommun, JM, Malinverni, R, Genne, D, Erard, PH & Waespi, U 2006 Outbreak of human listeriosis associated with tomme cheese in northwest Switzerland, 2005. Eurosurveillance 11 9193 CrossRefGoogle ScholarPubMed
Bishop, JR & Smukowski, M 2006 Storage temperatures necessary to maintain cheese safety. Food Protection Trends 26 714724 Google Scholar
Brooks, JC, Martinez, B, Stratton, J, Bianchini, A, Krokstrom, R & Hutkins, R 2012 Survey of raw milk cheeses for microbiological quality and prevalence of foodborne pathogens. Food Microbiology 31 154158 Google Scholar
Buyong, N, Kok, J & Luchansky, JB 1998 Use of a genetically enhanced, pediocin-producing starter culture, Lactococcus lactis subsp. lactis MM217, to control Listeria monocytogenes in Cheddar cheese. Applied and Environmental Microbiology 64 48424845 Google Scholar
Carrasco, E, Valero, A, Pérez-Rodríguez, F, García-Gimeno, RM & Zurera, G 2007 Management of microbiological safety of ready-to-eat meat products by mathematical modelling: Listeria monocytogenes as an example. International Journal of Food Microbiology 114 221226 Google Scholar
Chen, B-Y, Pyla, R, Kim, T-J, Silva, JL & Jung, Y-S 2010 Incidence and persistence of Listeria monocytogenes in the catfish processing environment and fresh fillets. Journal of Food Protection 73 16411650 Google Scholar
Cocolin, L, Nucera, D, Alessandria, V, Rantsiou, K, Dolci, P, Grassi, MA, Lomonaco, S & Civera, T 2009 Microbial ecology of Gorgonzola rinds and occurrence of different biotypes of Listeria monocytogenes . International Journal of Food Microbiology 133 200205 Google Scholar
De Buyser, M-L, Dufour, B, Maire, M & Lafarge, V 2001 Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. International Journal of Food Microbiology 67 117 Google Scholar
Doumith, M, Buchrieser, C, Glaser, P, Jacquet, C & Martin, P 2004 Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. Journal of Clinical Microbiology 42 38193822 Google Scholar
European Commission 2005 Commission regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. European Commission. Official Journal of the EU L.338 126 Google Scholar
Finazzi, G, Daminelli, P, Serraino, A, Pizzamiglio, V, Riu, R, Giacometti, F, Bertasi, B, Losio, MN & Boni, P 2011 Behaviour of Listeria monocytogenes in packaged water buffalo mozzarella cheese. Letters in Applied Microbiology 53 364370 Google Scholar
Fox, EM, O'Mahony, T, Clancy, M, Dempsey, R, O'Brien, M & Jordan, K 2009 Listeria monocytogenes in the Irish dairy farm environment. Journal of Food Protection 72 14501456 Google Scholar
Fox, EM, Hunt, K, O'Brien, M & Jordan, K 2011 Listeria monocytogenes in Irish farmhouse cheese processing environments. International Journal of Food Microbiology 145 S39S45 Google Scholar
Fox, EM, deLappe, N, Garvey, P, McKeown, P, Cormican, M, Leonard, N & Jordan, K 2012 PFGE analysis of Listeria monocytogenes isolates of clinical, animal, food and environmental origin from Ireland. Journal of Medical Microbiology 61 540547 CrossRefGoogle ScholarPubMed
Gaulin, C, Ramsay, D & Bekal, S 2012 Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. Journal of Food Protection 75 7178 Google Scholar
Gudmundsdottir, S, Gudbjornsdottir, B, Einarsson, H, Kristinsson, KG & Kristjansson, M 2006 Contamination of cooked peeled shrimp (Pandalus borealis) by Listeria monocytogenes during processing at two processing plants. Journal of Food Protection 69 13041311 CrossRefGoogle ScholarPubMed
Ho, AJ, Lappi, VR & Wiedmann, M 2007 Longitudinal monitoring of Listeria monocytogenes contamination patterns in a farmstead dairy processing facility. Journal of Dairy Science 90 25172524 CrossRefGoogle Scholar
Hunt, K, Drummond, N, Murphy, M, Butler, F, Buckley, J & Jordan, K 2012 A case of bovine raw milk contamination with Listeria monocytogenes . Irish Veterinary Journal 65 13 Google Scholar
International Standarisation Organisation 2004a ISO 11290-1: 1997; Amd 1:2004. Microbiology of food and animal feeding stuffs – Horizontal method for the detection and enumeration of Listeria monocytogenes. Part 1: Detection method. International Organization for Standardization (ISO) Google Scholar
International Standarisation Organisation 2004b ISO 11290-2: 1998; Amd 1:2004. Microbiology of food and animal feeding stuffs – Horizontal method for the detection and enumeration of Listeria monocytogenes – Part 2: Enumeration method. International Organization for Standardization (ISO) Google Scholar
International Standarisation Organisation 2004c ISO 5534:2004 (IDF 4: 2004) – Cheese and processed cheese – Determination of the total solids content (Reference method). International Organization for Standardization (ISO) Google Scholar
Jackson, KA, Biggerstaff, M, Tobin-D'Angelo, M, Sweat, D, Klos, R, Nosari, J, Garrison, O, Boothe, E, Saathoff-Huber, L, Hainstock, L & Fagan, RP 2011 Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant, Hispanic women. Journal of Food Protection 74 949953 CrossRefGoogle ScholarPubMed
Keto-Timonen, R, Tolvanen, R, Lundén, J & Korkeala, H 2007 An 8-year surveillance of the diversity and persistence of Listeria monocytogenes in a chilled food processing plant analyzed by Amplified Fragment Length Polymorphism. Journal of Food Protection 70 18661873 CrossRefGoogle Scholar
Khelef, N, Lecuit, M, Buchrieser, C, Cabanes, D, Dussurget, O & Cossart, P 2006 Listeria monocytogenes and the genus Listeria . In The Prokaryotes, Vol. 4, pp. 404476 (Eds Dworkin, M, Falkow, S, Rosenberg, E, Schleifer, K-H, Stackebrandt, E). Springer Google Scholar
Lianou, A & Sofos, JN 2007 A Review of the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments. Journal of Food Protection 70 21722198 Google Scholar
Lomonaco, S, Decastelli, L, Nucera, D, Gallina, S, Manila Bianchi, D & Civera, T 2009 Listeria monocytogenes in Gorgonzola: subtypes, diversity and persistence over time. International Journal of Food Microbiology 128 516520 Google Scholar
Lorber, B 1997 Listeriosis. Clinical Infectious Diseases 24 19 CrossRefGoogle ScholarPubMed
Makino, SI, Kawamoto, K, Takeshi, K, Okada, Y, Yamasaki, M, 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 CrossRefGoogle ScholarPubMed
McLauchlin, J, Mitchell, RT, Smerdon, WJ & Jewell, K 2004 Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. International Journal of Food Microbiology 92 1533 CrossRefGoogle ScholarPubMed
Mejlholm, O, Kjeldgaard, J, Modberg, A, Vest, MB, Bøknæs, N, Koort, J, Björkroth, J & Dalgaard, P 2008 Microbial changes and growth of Listeria monocytogenes during chilled storage of brined shrimp (Pandalus borealis). International Journal of Food Microbiology 124 250259 CrossRefGoogle ScholarPubMed
MMWR 2011 Outbreak of invasive listeriosis associated with the consumption of hog head cheese - Louisiana, 2010. MMWR Morbidity and Mortality Weekly Report 60 401405 Google Scholar
O'Brien, M, Hunt, K, McSweeney, S & Jordan, K 2009 Occurrence of foodborne pathogens in Irish farmhouse cheese. Food Microbiology 26 910914 CrossRefGoogle ScholarPubMed
Pearson, LJ & Marth, EH 1990 Listeria monocytogenes – Threat to a safe food supply: a review. Journal of Dairy Science 73 912928 Google Scholar
Peccio, A, Autio, T, Korkeala, H, Rosmini, R & Trevisani, M 2003 Listeria monocytogenes occurrence and characterization in meat-producing plants. Letters in Applied Microbiology 37 234238 Google Scholar
Pontello, M, Guaita, A, Sala, G, Cipolla, M, Gattuso, A, Sonnessa, M & Gianfranceschi, MV 2012 Listeria monocytogenes serotypes in human infections (Italy, 2000–2010). Annali Dell Istituto Superiore Di Sanità 48 146150 Google Scholar
PulseNet USA 2009 One-day (24–28 h) standardized laboratory protocol for molecular subtyping of Listeria monocytogenes by Pulsed Field Gel Electrophoresis (PFGE). Available at: http://www.cdc.gov/pulsenet/pathogens/listeria.html. Accessed July 12th 2013 Google Scholar
Reij, MW, Den Aantrekker, ED & ILSI Europe Risk Analysis in Microbiology Task Force 2004 Recontamination as a source of pathogens in processed foods. International Journal of Food Microbiology 91 111 Google Scholar
Rodríguez-Lázaro, D, Hernández, M, Scortti, M, Esteve, T, Vázquez-Boland, JA & Pla, M 2004 Quantitative detection of Listeria monocytogenes and Listeria innocua by Real-Time PCR: assessment of hly, iap, and lin02483 targets and AmpliFluor technology. Applied and Environmental Microbiology 70 13661377 CrossRefGoogle ScholarPubMed
Rosshaug, PS, Detmer, A, Ingmer, H & Larsen, MH 2012 Modelling the growth of Listeria monocytogenes in soft blue white cheese. Applied and Environmental Microbiology 78 85088514 Google Scholar
Schoder, D, Melzner, D, Schmalwieser, A, Zangana, A, Winter, P & Wagner, M 2011 Important vectors for Listeria monocytogenes transmission at farm dairies manufacturing fresh sheep and goat cheese from raw milk. Journal of Food Protection 74 919924 Google Scholar
Schoder, D, Rossmanith, P, Glaser, K & Wagner, M 2012 Fluctuation in contamination dynamics of List. monocytogenes in quargel (acid curd cheese) lots recalled during the multinational listeriosis outbreak 2009/2010. International Journal of Food Microbiology 157 326331 CrossRefGoogle Scholar
Schvartzman, MS, Belessi, C, Butler, F, Skandamis, PN & Jordan, K 2011a Effect of pH and water activity on the growth limits of Listeria monocytogenes in a cheese matrix at two contamination levels. Journal of Food Protection 74 18051813 CrossRefGoogle Scholar
Schvartzman, MS, Maffre, A, Tenenhaus-Aziza, F, Sanaa, M, Butler, F & Jordan, K 2011b Modelling the fate of Listeria monocytogenes during manufacture and ripening of smeared cheese made with pasteurised or raw milk. International Journal of Food Microbiology 145 S31S38 CrossRefGoogle ScholarPubMed
Shrestha, S, Grieder, JA, McMahon, DJ & Nummer, BA 2011 Survival of Listeria monocytogenes introduced as a post-aging contaminant during storage of low-salt Cheddar cheese at 4, 10, and 21 °C. Journal of Dairy Science 94 43294335 Google Scholar
Skalina, L & Nikolajeva, V 2010 Growth potential of Listeria monocytogenes strains in mixed ready-to-eat salads. International Journal of Food Microbiology 144 317321 Google Scholar
Sleator, RD, Watson, D, Hill, C & Gahan, CGM 2009 The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155 24632475 Google Scholar
Tompkin, RB 2002 Control of Listeria monocytogenes in the food-processing environment. Journal of Food Protection 65 709725 Google Scholar
Torres-Vitela, MR, Mendoza-Bernardo, M, Castro-Rosas, J, Gomez-Aldapa, CA, Garay-Martinez, LE, Navarro-Hidalgo, V & Villarruel-Lopez, A 2012 Incidence of Salmonella, Listeria monocytogenes, Escherichia coli O157:H7, and staphylococcal enterotoxin in two types of Mexican fresh cheeses. Journal of Food Protection 75 7984 CrossRefGoogle ScholarPubMed
Uyttendaele, M, Busschaert, P, Valero, A, Geeraerd, AH, Vermeulen, A, Jacxsens, L, Goh, KK, De Loy, A, Van Impe, JF & Devlieghere, F 2009 Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and retailed mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007. International Journal of Food Microbiology 133 94104 Google Scholar
Vermeulen, A, Devlieghere, F, De Loy-Hendrickx, A & Uyttendaele, M 2011 Critical evaluation of the EU-technical guidance on shelf-life studies for List. monocytogenes on RTE-foods: a case study for smoked salmon. International Journal of Food Microbiology 145 176185 Google Scholar
Wagner, M, Eliskases-Lechner, F, Rieck, P, Hein, I & Allerberger, F 2006 Characterization of Listeria monocytogenes isolates from 50 small-scale Austrian cheese factories. Journal of Food Protection 69 12971303 CrossRefGoogle ScholarPubMed