Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Hurdle factors minimizing growth of Listeria monocytogenes while counteracting in situ antilisterial effects of a novel nisin A-producing Lactococcus lactis subsp. cremoris costarter in thermized cheese milks

Dairy Research Institute, General Directorate of Agricultural Research, Hellenic Agricultural Organization DEMETER, Katsikas, 45221 Ioannina, Greece

Topical Section: Lactic Acid Bacteria: Genetics, Metabolism and Applications

The capacity of growth, survival, and adaptive responses of an artificial contamination of a three-strain L. monocytogenes cocktail in factory-scale thermized (65 °C, 30 s) Graviera cheese milk (TGCM) was evaluated. Bulk TGCM samples for inoculation were sequentially taken from the cheese making vat before process initiation (CN-LM) and after addition of a commercial starter culture (CSC), the CSC plus the nisin A-producing (NisA+) costarter strain Lactococcus lactis subsp. cremoris M78 (CSC + M78), and all ingredients with the rennet last (CSC + M78-RT). Additional treatments included Listeria-inoculated TGCM samples coinoculated with the NisA+ costarter strain M78 in the absence of the CSC or with the CSC in previously sterilized TGCM to inactivate the background microbiota (CSC-SM). All cultures were incubated at 37 to 42 °C for 6 h, followed by additional 66 h at 22 °C, and 48 h at 12 °C after addition of 2% edible salt. L. monocytogenes failed to grow and declined in all CSC-inoculated treatments after 24 h. In contrast, the pathogen increased by 3.34 and 1.46 log units in the CN-LM and the CSC-SM treatments, respectively, indicating that the background microbiota or the CSC alone failed to suppress it, but they did so synergistically. Supplementation of the CSC with the NisA+ strain M78 did not deliver additional antilisterial effects, because the CSC Streptococcus thermophilus reduced the growth prevalence rates and counteracted the in situ NisA+ activity of the costarter. In the absence of the CSC, however, strain M78 predominated and caused the strongest in situ nisin-A mediated effects, which resulted in the highest listerial inactivation rates after 24 to 72 h at 22 °C. In all TGCM treatments, however, L. monocytogenes displayed a “tailing” survival (1.63 to 1.96 log CFU/mL), confirming that this pathogen is exceptionally tolerant to cheese-related stresses, and thus, can’t be easily eliminated.
  Figure/Table
  Supplementary
  Article Metrics

Keywords Listeria monocytogenes; Lactococcus lactis; nisin A; thermized cheese milk

Citation: John Samelis, Athanasia Kakouri. Hurdle factors minimizing growth of Listeria monocytogenes while counteracting in situ antilisterial effects of a novel nisin A-producing Lactococcus lactis subsp. cremoris costarter in thermized cheese milks. AIMS Microbiology, 2018, 4(1): 19-41. doi: 10.3934/microbiol.2018.1.19

References

  • 1. Lianou A, Sofos JN (2007) A review on the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments. J Food Protect 70: 2172–2198.    
  • 2. Kousta M, Mataragas M, Skandamis P, et al. (2010) Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food Control 21: 805–815.    
  • 3. Verraes C, Vlaemynck G, Van Weyenberg S, et al. (2015) A review of the microbiological hazards of dairy products made from raw milk. Int Dairy J 50: 32–44.    
  • 4. Silk BJ, Mahon BE, Griffin PM, et al. (2013) Vital signs: Listeria illnesses, deaths, and outbreaks-United States, 2009-2011. MMWR-Morbid Mortal W 62: 448–452.
  • 5. Gould LH, Mungai E, Behravesh CB (2014) Outbreaks attributed to cheese: Differences between outbreaks caused by unpasterurized and pasteurized dairy products, United States, 1998-2011. Foodborne Pathog Dis 11: 545–551.    
  • 6. Raheem D (2016) Outbreaks of listeriosis associated with deli meats and cheese: an overview. AIMS Microbiol 2: 230–250.    
  • 7. Angelidis AS, Govaris A (2012) The behavior of Listeria monocytogenes during the manufacture and storage of Greek Protected Designation of Origin (PDO) cheeses, In: Romano A, Giordano CF, Editors, Listeria Infections: Epidemiology, Pathogenesis and Treatment, Nova Science Publishers, 1–34.
  • 8. Álvarez-Ordóñez A, Leong D, Hickey B, et al. (2015) The challenge of challenge testing to monitor Listeria monocytogenes growth on ready-to-eat foods in Europe by following the European Commission (2014) Technical Guidance document. Food Res Int 75: 233–243.
  • 9. European Commission (2005) Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official J Eur Union L338: 1–26.
  • 10. European Commission (2007) Commission Regulation (EC) No 1441/2007 of 5 December 2007 amending Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. Official J Eur Union L322: 12–29.
  • 11. Giannou E, Kakouri A, Matijašic BB, et al. (2009) Fate of Listeria monocytogenes on fully ripened Greek Graviera cheese stored at 4, 12, or 25 °C in air or vacuum packages: in situ PCR detection of a cocktail of bacteriocins potentially contributing to pathogen inhibition. J Food Protect 72: 531–538.    
  • 12. Samelis J, Giannou E, Lianou A (2009) Assuring growth inhibition of listerial contamination during processing and storage of traditional Greek Graviera cheese: compliance with the new European Union regulatory criteria for Listeria monocytogenes. J Food Protect 72: 2264–2271.    
  • 13. Chatelard-Chauvin C, Pelissier F, Hulin S, et al. (2015) Behaviour of Listeria monocytogenes in raw milk Cantal type cheeses during cheese making, ripening and storage in different packaging conditions. Food Control 54: 53–65.    
  • 14. Wemmenhove E, Beumer RR, Van Hooijdonk ACM, et al. (2014) The fate of Listeria monocytogenes in brine and on Gouda cheese following artificial contamination during brining. Int Dairy J 39: 253–258.    
  • 15. Kapetanakou AE, Gkerekou MA, Vitzilaiou ES, et al. (2017) Assessing the capacity of growth, survival, and acid adaptive response of Listeria monocytogenes during storage of various cheeses and subsequent simulated gastric digestion. Int J Food Microbiol 246: 50–63.    
  • 16. Shrestha S, Grieder JA, McMahon DJ, et al. (2011) Survival of Listeria monocytogenes introduced as a post-aging contaminant during storage of low-salt Cheddar cheese at 4, 10, and 21 °C. J Dairy Sci 94: 4329–4335.    
  • 17. Dalmasso M, Jordan K (2014) Absence of growth of Listeria monocytogenes in naturally contaminated Cheddar cheese. J Dairy Res 81: 46–53.    
  • 18. Adrião A, Vieira M, Fernandes I, et al. (2008) Marked intra-strain variation in response of Listeria monocytogenes dairy isolates to acid or salt stress and the effect of acid or salt adaptation on adherence to abiotic surfaces. Int J Food Microbiol 123: 142–150.    
  • 19. Samelis J, Ikeda JS, Sofos JN (2003) Evaluation of the pH-dependent, stationary-phase acid tolerance in Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli O157:H7. J Appl Microbiol 95: 563–575.    
  • 20. Samelis J, Kakouri A, Pappa EC, et al. (2010) Microbial stability and safety of traditional Greek Graviera cheese: characterization of the lactic acid bacterial flora and culture-independent detection of bacteriocin genes in the ripened cheeses and their microbial consortia. J Food Protect 73: 1294–1303.    
  • 21. Wemmenhove E, Van Valenberg HJF, Zwietering MH, et al. (2016) Minimal inhibitory concentrations of undissociated lactic, acetic, citric and propionic acid for Listeria monocytogenes under conditions relevant to cheese. Food Microbiol 58: 63–67.    
  • 22. 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 Microbiol 27: 809–818.    
  • 23. Wemmenhove E, Stampelou I, van Hooijdonk ACM, et al. (2013) Fate of Listeria monocytogenes in Gouda microcheese: No growth, and substantial inactivation after extended ripening times. Int Dairy J 32: 192–198.    
  • 24. Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Tech 15: 67–78.    
  • 25. Gálvez A, Lopez RL, Abriouel H, et al. (2008) Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit Rev Biotechnol 28: 125–152.    
  • 26. Alvarez-Sieiro P, Montalban-Lopez M, Mu DD, et al. (2016) Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 100: 2939–2951.    
  • 27. Rodriguez E, Arques JL, Gaya P, et al. (2001) Control of Listeria monocytogenes by bacteriocins and monitoring of bacteriocin-producing lactic acid bacteria by colony hybridization in semi-hard raw milk cheese. J Dairy Res 68: 131–137.    
  • 28. Alegria A, Delgado S, Roces C, et al. (2010) Bacteriocins produced by wild Lactococcus lactis strains isolated from traditional, starter-free cheeses made of raw milk. Int J Food Microbiol 143: 61–66.    
  • 29. Dal Bello B, Cocolin L, Zeppa G, et al. (2012) Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in Cottage cheese. Int J Food Microbiol 153: 58–65.    
  • 30. Pisano MB, Fadda ME, Melis R, et al. (2015) Molecular identification of bacteriocins produced by Lactococcus lactis dairy strains and their technological and genotypic characterization. Food Control 51: 1–8.    
  • 31. Bouksaim M, Lacroix C, Audet P, et al. (2000) Effects of mixed starter composition on nisin Z production by Lactococcus lactis subsp. lactis biovar. diacetylactis UL 719 during production and ripening of Gouda cheese. Int J Food Microbiol 59: 141–156.
  • 32. O'Sullivan L, Ryan MP, Ross RP, et al. (2003) Generation of food-grade lactococcal starters which produce the lantibiotics lacticin 3147 and lacticin 481. Appl Environ Microbiol 69: 3681–3685.    
  • 33. Mills S, Griffin C, O'Connor PM, et al. (2017) A multibacteriocin cheese starter system, comprising nisin and lacticin 3147 in Lactococcus lactis, in combination with plantaricin from Lactobacillus plantarum. Appl Environ Microbiol 83: e00799-17.
  • 34. Chollet E, Sebti I, Martial-Gros A, et al. (2008) Nisin preliminary study as a potential preservative for sliced ripened cheese: NaCl, fat and enzymes influence on nisin concentration and its antimicrobial activity. Food Control 19: 982–989.    
  • 35. Benech RO, Kheadr EE, Lacroix C, et al. (2002)Antibacterial activities of nisin Z encapsulated in liposomes or produced in situ by mixed culture during Cheddar cheese ripening. Appl Environ Microbiol 68: 5607–5619.
  • 36. Benkerroum N, Sandine WE (1998) Inhibitory action of nisin against Listeria monocytogenes. J Dairy Sci 71: 3237–3245.
  • 37. Ferreira MASS, Lund BM (1996) The effect of nisin on Listeria monocytogenes in culture medium and long-life cottage cheese. Lett Appl Microbiol 22: 433–438.    
  • 38. Ryser ET (1999) Incidence and behavior of Listeria monocytogenes in cheese and other fermented dairy products, In: Ryser ET, Marth EH, Editors., Listeria, Listeriosis and Food Safety, New York: Marcel Dekker, 411–503.
  • 39. Collins B, Cotter PD, Hill C, et al. (2011) The impact of nisin on sensitive and resistant mutants of Listeria monocytogenes in cottage cheese. J Appl Microbiol 110: 1509–1514.    
  • 40. Al-Holy MA, Al-Nabulsi A, Osaili TM, et al. (2012) Inactivation of Listeria innocua in brined white cheese by a combination of nisin and heat. Food Control 23: 48–53.    
  • 41. Aly S, Floury J, Piot M, et al. (2012) The efficacy of nisin can drastically vary when produced in situ in model cheeses. Food Microbiol 32: 185–190.    
  • 42. Dal Bello B, Zeppa G, Bianchi DM, et al. (2013) Effect of nisin-producing Lactococcus lactis starter cultures on the inhibition of two pathogens in ripened cheeses. Int J Dairy Technol 66: 468–477.
  • 43. Sallami L, Kheadr EE, Fliss I, et al. (2004) Impact of autolytic, proteolytic, and nisin-producing adjunct cultures on biochemical and textural properties of cheddar cheese. J Dairy Sci 87: 1585–1594.    
  • 44. Samelis J, Lianou A, Kakouri A, et al. (2009) Changes in the microbial composition of raw milk induced by thermization treatments applied prior to traditional Greek hard cheese processing. J Food Protect 72: 783–790.    
  • 45. Parapouli M, Delbés-Paus C, Kakouri A, et al. (2013) Characterization of a wild, novel nisin A-producing Lactococcus strain with an L. lactis subsp. cremoris genotype and an L. lactis subsp. lactis phenotype isolated from Greek raw milk. Appl Environ Microbiol 79: 3476–3484.
  • 46. Samelis J, Giannou E, Pappa EC, et al. (2017) Behavior of artificial listerial contamination in model Greek Graviera cheeses manufactured with the indigenous nisin A-producing strain Lactococcus lactis subsp. cremoris M104 as costarter culture. J Food Safety 37: e12326.
  • 47. Trmčić A, Monnet C, Rogelj I, et al. (2010) Expression of nisin genes in cheese-A quantitative real-time polymerase chain reaction approach. J Dairy Sci 94: 77–85.
  • 48. Lianou A, Samelis J (2014) Addition to thermized milk of Lactococcus lactis subsp. cremoris M104, a wild, novel nisin A-producing strain, replaces the natural antilisterial activity of the autochthonous raw milk microbiota reduced by thermization. J Food Protect 77: 1289–1297.
  • 49. Lianou A, Kakouri A, Pappa EC, et al. (2017) Growth interactions and antilisterial effects of the bacteriocinogenic Lactococcus lactis subsp. cremoris M104 and Enterococcus faecium KE82 strains in thermized milk in the presence or absence of a commercial starter culture. Food Microbiol 64: 145–154.
  • 50. Noutsopoulos D, Kakouri A, Kartezini E, et al. (2017) Growth, nisA gene expression and in situ nisin A activity of novel Lactococcus lactis subsp. cremoris costarter culture in commercial hard cheese production. J Food Protect 80: 2137–2146.
  • 51. Vandera E, Lianou A, Kakouri A, et al. (2017) Enhanced control of Listeria monocytogenes by Enterococcus faecium KE82, a multiple enterocin-producing strain, in different milk environments. J Food Protect 80: 74–85.    
  • 52. Schaffner E, Muhlemann M, Spahr U, et al. (2003) Quantification of the probability of milk contamination by Listeria monocytogenes during manufacture of hard cheese. Rev Epidemiol Sante 51:493–503.
  • 53. Rogga KJ, Samelis J, Kakouri A, et al. (2005) Survival of Listeria monocytogenes in Galotyri, a traditional Greek soft acid-curd cheese, stored aerobically at 4 and 12 °C. Int Dairy J 15: 59–67.    
  • 54. Lortal S, Chapot-Chartier MP (2005) Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int Dairy J 15: 857–871.    
  • 55. Masoud W, Vogensen FK, Lillevang S, et al. (2012) The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR. Int J Food Microbiol 153: 192–202.    
  • 56. Wemmenhove E, van Valenberg HJF, van Hooijdonk, et al. (2018) Factors that inhibit growth of Listeria monocytogenes in nature-ripened Gouda cheese: A major role for undissociated lactic acid. Food Control 84: 413–418.    
  • 57. Samelis J, Lianou A, Pappa EC, et al. (2014) Behavior of Staphylococcus aureus in culture broth, in raw and thermized milk, and during processing and storage of traditional Greek Graviera cheese in the presence or absence of Lactococcus lactis subsp. cremoris M104, a wild, novel nisin A-producing raw milk isolate. J Food Protect 77: 1703–1714.
  • 58. Lekkas C, Kakouri A, Paleologos E, et al. (2006) Survival of Escherichia coli O157:H7 in Galotyri cheese stored at 4 and 12 °C. Food Microbiol 23: 268–276.    
  • 59. Callon C, Saubusse M, Didienne R, et al. (2011) Simplification of a complex microbial antilisterial consortium to evaluate the contribution of its flora in uncooked pressed cheese. Int J Food Microbiol 145: 379–389.    
  • 60. Peláez C, Requena T (2005) Exploiting the potential of bacteria in the cheese ecosystem. Int Dairy J 15: 831–844.    
  • 61. Montel MC, Buchin S, Mallet A, et al. (2014) Traditional cheeses: Rich and diverse microbiota with associated benefits. Int J Food Microbiol 177: 136–154.    
  • 62. Schvartzman MS, Belessi C, Butler F, et al. (2011) Effect of pH and water activity on the growth limits of Listeria monocytogenes in a cheese matrix at two contamination levels. J Food Protect 74: 1805–1813.    

 

Reader Comments

your name: *   your email: *  

© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved