Control of Listeria monocytogenes in milk by using phage cocktail
DOI:
https://doi.org/10.17268/sci.agropecu.2022.001Palavras-chave:
biocontrol, foodborne pathogens, Listex P100, predictive microbiology, Weibull modelResumo
Biocontrol applications such as using phages against the contamination of Listeria monocytogenes are promising trends in terms of reducing the use of chemical additives in food industry. The aim of this study was to determine the effectiveness of Listex P100 phage (phage P100) on different Listeria monocytogenes strains (PL2, PL3, PL9 and PL10) in pasteurized milk and broth. Survival data of L. monocytogenes were successfully described by Weibull model. Time parameter of the Weibull model was used to evaluate the phage-resistances of L. monocytogenes strains. The reduction of L. monocytogenes was greater in broth than in milk regardless of the temperature level and it was significantly higher at 30 °C than at 4 °C in both media. The reductions of L. monocytogenes strains by the phage treatment were between 2.7 to 3.4 log10 units at 30 °C and 1.4 to 2.1 log10 units at 4 °C after 4 days of incubation in broth whereas 1.9 to 2.9 log10 units and 1.0 to1.6 log10 units were observed after 4 days of incubation in milk at 30 °C and 4 °C, respectively. It was found that L. monocytogenes PL2 is the most phage-resistant strain in broth at 30 °C and at 4 °C, and in milk at 30 °C, while L. monocytogenes PL9 is the most phage-resistant L. monocytogenes strain in milk at 4 °C. This study demonstrated P100 phage could be used to control L. monocytogenes counts in milk.
Referências
Akhtar, M., Viazis, S., & Diaz–Gonzalez, F. (2014). Isolation, identification and characterization of lytic, wide host range bacteriophages from waste effluents against Salmonella enterica. Food Control, 38, 67–74.
Akhtar, M., Viazis, S., Christensen, K., Kraemer, P., & Diez–Gonzalez, F. (2017). Isolation, characterization and evaluation of virulent bacteriophages against Listeria monocytogenes. Food Control, 75, 108–115.
Arachchi, G.J.G., Mutukumira, A.N., Dias–Waigasekera, B.M., Cruz, C.D., Mclyntyre, L., Young, J., Flint, S.H., Hudson, A., & Billington, C. (2013). Characterization of three listeriophages isolated from New Zealand seafood environments. Journal of Applied Microbiology, 115, 1427–1438.
Bigot, B., Lee, W.–J., Mclntyre, L., Wilson, T., Hudson, J. A., Billington, C., & Heinemann, J.A. (2011). Control of Listeria monocytogenes growth in a ready–to–eat poultry using a bacteriophage. Food Microbiology, 28, 1448–1452.
Buzrul, S. (2007). On the use of Weibull model for isothermal and nonisothermal heat treatments. Molecular Nutrition and Food Research, 51, 374-375.
Carlton, R. M., Noordman, W. H., Biswas, B., de Meester, E. D., & Loessner, M. J. (2005). Bacteriophage P100 for control of Listeria monocytogenes in foods: Genome sequence, bioinformatic analyses, oral toxicity study, and application. Regulatory Toxicology and Pharmacology, 43, 301–312.
Criscuolo, E., Spadini, S., Lamanna, J., Ferro, M., & Burioni, R. (2017). Bacteriophages and Their Immunological Applications against Infectious Threats. Hindawi Journal of Immunology Research, Article ID 3780697.
Galarce, N., Escobar, B., Rojas, V., Navarro, C., Turra, G., Robenson, J., & Borie, C. (2016). Application of a virulent bacteriophage cocktail leads to reduction of Salmonella enterica serovar Enteritidis counts in processed meat products. Biocontrol Science and Technology, 26(4), 462–475.
Goodridge, L. D., & Bisha, B. (2011). Phage–based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage, 1(3), 130–137.
Granato, D., de Araújo Calado, V. M., & Jarvis, B. (2014). Observations on the use of statistical methods in Food Science and Technology. Food Research International, 55, 137-149.
Guenther, S., & Loessner, M. J. (2011). Bacteriophage Biocontrol of Listeria monocytogenes on soft ripened white mold and red–smear cheeses. Bacteriophage, 1(2), 94–100.
Guenther, S., Huwyler, D., Richard, S., & Loessner, M. J. (2009). Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready–to–eat foods. Applied and Environmental Microbiology, 75(1), 93–100.
Gutierrez, D., Rodriguez–Rubio, L., Fernandez, L., Martinez, B., Rodriguez, A., & Garcia, P. (2017). Applicability of commercial phage–based products against Listeria monocytogenes for improvement of food safety in Spanish dry–cured ham and food contact surfaces, Food Control, 73, 1474–1482.
Holck, A., & Berg, J. (2009). Inhibition of Listeria monocytogenes in Cooked Ham by Virulent Bacteriophages and Protective Cultures. Applied and Environmental Microbiology, 75(21), 6944–6946.
Jadhav, S., Bhave, M., & Palombo, E.A. (2012). Methods used for the detection and subtyping of Listeria monocytogenes. Journal of Microbiological Methods, 88(3), 327–341.
Klump, J., & Loessner, M. J. (2013). Listeria phages: Genomes, evolutions, and applications. Bacteriophages, 3, e26861–1.
Komora, N., Maciel, C., Pinto, C. A., Ferreira, V., Brandao, T. R. S., Saraiva, J. M. A., et al. (2020). Non-thermal approach to Listeria monocytogenes inactivation in milk: The combined effect of high pressure, pediocin PA-1 and bacteriophage P100. Food Microbiology, 86, 103315.
Korsak, D., & Szuplewska, M. (2016). Characterization of nonpathogenic Listeria species isolated from food and food processing environment. International Journal of Food Microbiology, 238, 274–280.
Korsak, D., Borek, A., Daniluk, S., Grabowska, A., & Papplbaum, K. (2012). Antimicrobial susceptibilities of Listeria monocyte-genes strains isolated from food and food processing environment in Poland. International Journal of Food Microbiology, 158(3), 203–208.
Lee, S., Kim, M. G., Lee, H. S., Heo, S., Kwon, M., & Kim, G. (2017). Isolation and characterization of Listeria phages for control of growth of Listeria monocytogenes in milk. Korean Journal for Food Science of Animal Resources, 37(2), 320–328.
Leverentz, B., Conway, W. S., Camp, M. J., Janisiewicz, W. J., Abuladze, T., Yang, M., et al. (2003). Biocontrol of Listeria monocytogenes on fresh–cut produce by treatment with lytic bacteriophages and a bacteriocin. Applied and Environmental Microbiology, 69(8), 4519–4526.
Leverentz, B., Conway, W. S., Janisiewicz, W., & Camp, M. J. (2004). Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. Journal of Food Protection, 67(8), 1682–1686.
Leverentz, B., Conway, W. S., Janisiewicz, W., Abadias, M., Kurtzman, C. P., & Camp, M. J. (2006). Biocontrol of the food–borne pathogens Listeria monocytogenes and Salmonella enterica Serovar Poona on fresh–cut apples with naturally occurring bacterial and yeast antagonists. Applied and Environmental Microbiology, 72(2), 1135–1140.
Leylak, C., Yurdakul, M., & Buzrul, S. (2020). Use of Excel in food science 1: Linear regression. Food and Health, 6(3), 186-198.
Leylak, C., & Buzrul, S. (2020). The combined effect of temperature, pH and lactose concentration on the growth probability of Listeria innocua. Journal of Microbiology, Biotechnology and Food Sciences, 10(3), 474-477.
Mafart, P., Couvert, O., Gaillard, S., & Leguerinel, I. (2002). On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. International Journal of Food Microbiology, 72, 107-113.
McLean, S. K., Dunn, L. A., & Palombo, E. A. (2013). Phage inhibition of Escherichia coli in Ultrahigh–Temperature–Treated and raw milk. Foodborne Pathogens and Disease, 10(11), 956–962.
Migueis, S., Saraiva, C., & Esteves, A. (2017). Efficacy of LISTEX P100 at different concentrations for reduction of Listeria monocytogenes inoculated in Sashimi. Journal of Food Protection, 80(12), 2094–2098.
NCBI-National Centers for Biotechnology Information. (2021). Taxonomy Browser Listeria. Available at: https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?id=1637
Öksüz, H., & Buzrul, S. (2020). Monte Carlo analysis for microbial growth curves. Journal of Microbiology, Biotechnology and Food Sciences, 10(3), 418-423.
Oliveira, M., Vińas, I., Colãs, P., Anguera, M., Usall, J., & Abadias, M. (2014). Effectiveness of a bacteriophage in reducing Listeria monocytogenes on fresh–cut fruits and fruit juices. Food Microbiology, 38, 137–142.
Peleg, M. (1999). On calculating sterility in thermal and non-thermal preservation methods. Food Research International, 32(4), 271-278.
Peleg, M., & Cole, M. B. (2000). Estimating the survival of Clostridium botulinum spores during heat treatments. Journal of Food Protection, 63(2), 190-195.
Perera, M. N., Abuladze, T., Li, M., Woolston, J., & Sulakvelidze, A. (2015). Bacteriophage cocktail significantly reduce or eliminates Listeria monocytogenes contamination on lettuce, cheese, smoked salmon and frozen foods. Food Microbiology, 52, 42–48.
Prabhu, G., Husak, R., Peterson, R., Hagens, S., Riemer, C. Y., & Engle, R. (2016). Validition of the Listex P100 bacteriophage on survival of Listeria monocytogenes. Meat and Muscle Biology, 1(2), 117–118.
Rahimi, E., Ameri, M., & Momtaz, H. (2010). Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran. Food Control, 21(11), 1448–1452.
Ratkowsky, D. A. (2004). Model fitting and uncertainty. In book: Modelling Microbial Responses in Food. Edited by Robin C. et al., Chapter 4, pp.151-196, CRC Press, 1st Edition.
Rossi, L. P. R., Almeida, R. C. C., Lopes, L. S., Figueiredo, A. C. L., Ramos, M. P. P., & Almeida, P.F. (2011). Occurrence of Listeria spp. in Brazilian fresh sausage and control of Listeria monocytogenes using bacteriophage P100. Food Control, 22, 954–958.
Safraz, M., Ashraf, Y., & Ashraf, S. A. (2017). Review: Prevalence and antimicrobial susceptibility profile of Listeria species in milk products. Matrix Science Medica, 1(1), 03–09.
Sarker, R., & Ahmed, S. (2015). Prevalence and Antimicrobial Susceptibility of Listeria spp. in Dairy Food Products and Water Samples in Dhaka, Bangladesh. Journal of Life Sciences, 9, 152–158.
Silva, E. N. G., Figueiredo, A. C. L., Miranda, F. A., & de Castro–Almeida, R. C. (2014). Control of Listeria monocytogenes growth in soft cheeses by bacteriophage P100. Brazilian Journal of Microbiology, 45(1), 11–16.
Soni, K. A., & Nannapaneni, R. (2010). Bacteriophage significantly reduced Listeria monocytogenes on raw salmon fillet tissue. Journal of Food Protection, 73(1), 32–38.
Soni, K. A., Desai, S. M., Oladunjoye, A., Skrobot, F., & Nannapaneni, R. (2012). Reduction of Listeria monocytogenes in queso fresco cheese by a combination of listericidal and listeriostatik GRAS antimicrobials. International Journal of Food Microbiology, 155, 82–88.
Soni, K. A., Nannapaneni, R., & Hagens, S. (2010). Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage Listex P100. Foodborne Pathogens and Disease, 7(4), 427–434.
Teng–Hern, L. T., Kok–Gan, C., & Han, L. L. (2014). Application of bacteriophage in biocontrol of major foodborne bacterial pathogens. Journal of Molecular Biology and Molecular Imaging, 1(1), 9.
Tolba, M. H., Meshref, A. M. S., & Zeinhom, M. M. A. (2014). Biocontrol of Escherichia coli 0126:H7 in skim milk using bacteriophages. American Journal of Animal and Veterinary Sciences, 9(4), 221–229.
Tomat, D., Mercanti, D., Balague, C., & Quiberoni, A. (2013). Phage biocontrol of enteropathogenic and Shiga toxin–producing Escherichia coli during milk fermentation. Letters in Applied Microbiology, 57, 3–10.
Valimaa, A. L., Tilsala–Timisjarvi, A., & Virtanen, E. (2015). Rapid detection and identification methods for Listeria monocytogenes in the food chain–A review. Food Control, 55, 103–114.
van Boekel, M. A. J. S. (2002). On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. International Journal of Food Microbiology, 74(1-2), 139-159.
Xanthiakos, K., Simos, D., Angelidis, A.S., Nychas, G. J.–E., & Koutsoumanis, K. (2006). Dynamic modeling of Listeria monocytogenes growth in pasteurized milk. Journal of Applied Microbiology, 100, 1289–1298.
Yang, S., Sadekuzzaman, M., & Ha, S. D. (2017). Reduction of Listeria monocytogenes on chicken breast by combined treatment with UV-C light and bacteriophage ListShield. LWT-Food Science and Technology, 86, 193–200.
Downloads
Publicado
Como Citar
Edição
Seção
Licença
Copyright (c) 2022 Scientia Agropecuaria
Este trabalho está licenciado sob uma licença Creative Commons Attribution-NonCommercial 4.0 International License.
Los autores que publican en esta revista aceptan los siguientes términos:
a. Los autores conservan los derechos de autor y conceden a la revista el derecho publicación, simultáneamente licenciada bajo una licencia de Creative Commons que permite a otros compartir el trabajo, pero citando la publicación inicial en esta revista.
b. Los autores pueden celebrar acuerdos contractuales adicionales separados para la distribución no exclusiva de la versión publicada de la obra de la revista (por ejemplo, publicarla en un repositorio institucional o publicarla en un libro), pero citando la publicación inicial en esta revista.
c. Se permite y anima a los autores a publicar su trabajo en línea (por ejemplo, en repositorios institucionales o en su sitio web) antes y durante el proceso de presentación, ya que puede conducir a intercambios productivos, así como una mayor citación del trabajo publicado (ver efecto del acceso abierto).
