Effect of different conditions on Listeria monocytogenes biofilm formation and removal

https://doi.org/10.17221/199/2017-CJFSCitation:Russo P., Hadjilouka A., Beneduce L., Capozzi V., Paramithiotis S., Drosinos E.H., Spano G. (2018): Effect of different conditions on Listeria monocytogenes biofilm formation and removal. Czech J. Food Sci., 36: 208-214.
download PDF

Listeria monocytogenes poses a major risk for the safety of food products due to the ability to persist in food products and process line surfaces as biofilm. In this work, we investigated the L. monocytogenes biofilms in relation to development factors and possible control under different conditions. In particular, the ability of six strains of L. monocytogenes from vegetable and animal sources to form biofilms was evaluated on glass or polystyrene substrates under different temperatures (15, 30 and 37°C) and availability of nutrients, by using rich (BHI) or poor (HTM) growth media. Moreover, the effectiveness of three commonly used sanitizers (benzalkonium chloride, sodium hypochlorite and hydrogen peroxide) was compared to eradicate established biofilms. Our results showed that starved conditions, hydrophilic surfaces, and high temperatures increased the L. monocytogenes ability to produce biofilms. In general, benzalkonium chloride was the most effective chemical to remove established biofilms.

References:
Ban Ga-Hee, Kang Dong-Hyun (2016): Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiology, 55, 47-54 https://doi.org/10.1016/j.fm.2015.11.003
 
Belessi Charalambia-Eirini A., Gounadaki Antonia S., Psomas Antonios N., Skandamis Panagiotis N. (2011): Efficiency of different sanitation methods on Listeria monocytogenes biofilms formed under various environmental conditions. International Journal of Food Microbiology, 145, S46-S52 https://doi.org/10.1016/j.ijfoodmicro.2010.10.020
 
Bonsaglia E.C.R., Silva N.C.C., Fernades Júnior A., Araújo Júnior J.P., Tsunemi M.H., Rall V.L.M. (2014): Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control, 35, 386-391 https://doi.org/10.1016/j.foodcont.2013.07.023
 
Carpentier Brigitte, Cerf Olivier (2011): Review — Persistence of Listeria monocytogenes in food industry equipment and premises. International Journal of Food Microbiology, 145, 1-8 https://doi.org/10.1016/j.ijfoodmicro.2011.01.005
 
CDC (2011): Multistate outbreak of listeriosis associated with Jensen Farms cantaloupe – United States, August –September 2011. Morbidity and Mortality Weekly Report, 60: 1357–1358.
 
Chavant P., Martinie B., Meylheuc T., Bellon-Fontaine M.-N., Hebraud M. (2002): Listeria monocytogenes LO28: Surface Physicochemical Properties and Ability To Form Biofilms at Different Temperatures and Growth Phases. Applied and Environmental Microbiology, 68, 728-737 https://doi.org/10.1128/AEM.68.2.728-737.2002
 
Choi Na-Young, Kim Bo-Ram, Bae Young-Min, Lee Sun-Young (2013): Biofilm formation, attachment, and cell hydrophobicity of foodborne pathogens under varied environmental conditions. Journal of the Korean Society for Applied Biological Chemistry, 56, 207-220 https://doi.org/10.1007/s13765-012-3253-4
 
Combrouse T., Sadovskaya I., Faille C., Kol O., Guérardel Y., Midelet-Bourdin G. (2013): Quantification of the extracellular matrix of the Listeria monocytogenes biofilms of different phylogenic lineages with optimization of culture conditions. Journal of Applied Microbiology, 114, 1120-1131 https://doi.org/10.1111/jam.12127
 
da Silva Eliane Pereira, De Martinis Elaine Cristina Pereira (2013): Current knowledge and perspectives on biofilm formation: the case of Listeria monocytogenes. Applied Microbiology and Biotechnology, 97, 957-968 https://doi.org/10.1007/s00253-012-4611-1
 
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, 1552-1561 https://doi.org/10.1111/j.1365-2672.2007.03688.x
 
Djordjevic D., Wiedmann M., McLandsborough L. A. (2002): Microtiter Plate Assay for Assessment of Listeria monocytogenes Biofilm Formation. Applied and Environmental Microbiology, 68, 2950-2958 https://doi.org/10.1128/AEM.68.6.2950-2958.2002
 
Doijad Swapnil P., Barbuddhe Sukhadeo B., Garg Sandeep, Poharkar Krupali V., Kalorey Dewanand R., Kurkure Nitin V., Rawool Deepak B., Chakraborty Trinad, Ahmed Niyaz (2015): Biofilm-Forming Abilities of Listeria monocytogenes Serotypes Isolated from Different Sources. PLOS ONE, 10, e0137046- https://doi.org/10.1371/journal.pone.0137046
 
Dutta Vikrant, Elhanafi Driss, Kathariou Sophia (2013): Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes. Applied and Environmental Microbiology, 79, 6067-6074 https://doi.org/10.1128/AEM.01751-13
 
FERREIRA V., WIEDMANN M., TEIXEIRA P., STASIEWICZ M. J. (2014): Listeria monocytogenes Persistence in Food-Associated Environments: Epidemiology, Strain Characteristics, and Implications for Public Health. Journal of Food Protection, 77, 150-170 https://doi.org/10.4315/0362-028X.JFP-13-150
 
FOLSOM JAMES P., SIRAGUSA GREGORY R., FRANK JOSEPH F. (2006): Formation of Biofilm at Different Nutrient Levels by Various Genotypes of Listeria monocytogenes. Journal of Food Protection, 69, 826-834 https://doi.org/10.4315/0362-028X-69.4.826
 
Gandhi Megha, Chikindas Michael L. (2007): Listeria: A foodborne pathogen that knows how to survive. International Journal of Food Microbiology, 113, 1-15 https://doi.org/10.1016/j.ijfoodmicro.2006.07.008
 
Guilbaud Morgan, Piveteau Pascal, Desvaux Mickaël, Brisse Sylvain, Briandet Romain, Liu S.-J. (2015): Exploring the Diversity of Listeria monocytogenes Biofilm Architecture by High-Throughput Confocal Laser Scanning Microscopy and the Predominance of the Honeycomb-Like Morphotype. Applied and Environmental Microbiology, 81, 1813-1819 https://doi.org/10.1128/AEM.03173-14
 
Henriques A.R., Fraqueza M.J. (2017): Biofilm-forming ability and biocide susceptibility of Listeria monocytogenes strains isolated from the ready-to-eat meat-based food products food chain. LWT - Food Science and Technology, 81, 180-187 https://doi.org/10.1016/j.lwt.2017.03.045
 
Ibusquiza P. Saá, Herrera J.J.R., Cabo M.L. (2011): Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiology, 28, 418-425 https://doi.org/10.1016/j.fm.2010.09.014
 
Kadam Sachin R., den Besten Heidy M.W., van der Veen Stijn, Zwietering Marcel H., Moezelaar Roy, Abee Tjakko (2013): Diversity assessment of Listeria monocytogenes biofilm formation: Impact of growth condition, serotype and strain origin. International Journal of Food Microbiology, 165, 259-264 https://doi.org/10.1016/j.ijfoodmicro.2013.05.025
 
Liu S., Graham J. E., Bigelow L., Morse P. D., Wilkinson B. J. (2002): Identification of Listeria monocytogenes Genes Expressed in Response to Growth at Low Temperature. Applied and Environmental Microbiology, 68, 1697-1705 https://doi.org/10.1128/AEM.68.4.1697-1705.2002
 
Mai Tam L., Conner Donald E. (2007): Effect of temperature and growth media on the attachment of Listeria monocytogenes to stainless steel. International Journal of Food Microbiology, 120, 282-286 https://doi.org/10.1016/j.ijfoodmicro.2007.09.006
 
MOLTZ ANDREW G., MARTIN SCOTT E. (2005): Formation of Biofilms by Listeria monocytogenes under Various Growth Conditions. Journal of Food Protection, 68, 92-97 https://doi.org/10.4315/0362-028X-68.1.92
 
Møretrø T., Langsrud S. (1999): Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms, 1, 107-121 https://doi.org/10.1017/S1479050504001322
 
Mosquera-Fernández M., Sanchez-Vizuete P., Briandet R., Cabo M.L., Balsa-Canto E. (2016): Quantitative image analysis to characterize the dynamics of Listeria monocytogenes biofilms. International Journal of Food Microbiology, 236, 130-137 https://doi.org/10.1016/j.ijfoodmicro.2016.07.015
 
Nilsson Rolf E., Ross Tom, Bowman John P. (2011): Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. International Journal of Food Microbiology, 150, 14-24 https://doi.org/10.1016/j.ijfoodmicro.2011.07.012
 
Norwood D. E., Gilmour A. (1999): Adherence of Listeria monocytogenes strains to stainless steel coupons. Journal of Applied Microbiology, 86, 576-582 https://doi.org/10.1046/j.1365-2672.1999.00694.x
 
Norwood D.E., Gilmour A. (2001): The differential adherence capabilities of two Listeria monocytogenes strains in monoculture and multispecies biofilms as a function of temperature. Letters in Applied Microbiology, 33, 320-324 https://doi.org/10.1046/j.1472-765X.2001.01004.x
 
Nowak Jessika, Cruz Cristina D., Palmer Jon, Fletcher Graham C., Flint Steve (2015): Biofilm formation of the L. monocytogenes strain 15G01 is influenced by changes in environmental conditions. Journal of Microbiological Methods, 119, 189-195 https://doi.org/10.1016/j.mimet.2015.10.022
 
Ortiz Sagrario, López Victoria, Martínez-Suárez Joaquín V. (2014): The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by Listeria monocytogenes. International Journal of Food Microbiology, 189, 106-112 https://doi.org/10.1016/j.ijfoodmicro.2014.08.007
 
Purkrtová S., Turoňová H., Pilchová T., Demnerová K., Pazlarová J. (2010): Resistance of Listeria monocytogenes biofilms to disinfectants 326. Czech Journal of Food Sciences, 28, 326-332 https://doi.org/10.17221/153/2010-CJFS
 
Russo P., Botticella G., Capozzi V., Massa S., Spano G., Beneduce L. (2014): A fast, reliable, and sensitive method for detection and quantification of Listeria monocytogenes and Escherichia coli O157:H7 in ready-to-eat fresh-cut products by MPN-qPCR. BioMed Research International, Article ID 608296. doi 10.1155/2014/608296
 
Shi Xianming, Zhu Xinna (2009): Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20, 407-413 https://doi.org/10.1016/j.tifs.2009.01.054
 
Simões Manuel, Simões Lúcia C., Vieira Maria J. (2010): A review of current and emergent biofilm control strategies. LWT - Food Science and Technology, 43, 573-583 https://doi.org/10.1016/j.lwt.2009.12.008
 
Srey Sokunrotanak, Jahid Iqbal Kabir, Ha Sang-Do (2013): Biofilm formation in food industries: A food safety concern. Food Control, 31, 572-585 https://doi.org/10.1016/j.foodcont.2012.12.001
 
STEPANOVIĆ SRDJAN, VUKOVIĆ DRAGANA, HOLA VERONIKA, BONAVENTURA GIOVANNI DI, DJUKIĆ SLOBODANKA, ĆIRKOVIĆ IVANA, RUZICKA FILIP (2007): Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS, 115, 891-899 https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
 
Takahashi H., Suda T., Tanaka Y., Kimura B. (2010): Cellular hydrophobicity of Listeria monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl chloride. Letters in Applied Microbiology, 50, 618-625 https://doi.org/10.1111/j.1472-765X.2010.02842.x
 
Torlak E., Sert D. (2013): Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Letters in Applied Microbiology, 57, 220-226 https://doi.org/10.1111/lam.12100
 
Tsai H.-N., Hodgson D. A. (2003): Development of a Synthetic Minimal Medium for Listeria monocytogenes. Applied and Environmental Microbiology, 69, 6943-6945 https://doi.org/10.1128/AEM.69.11.6943-6945.2003
 
Vaid Richa, Linton Richard H., Morgan Mark T. (2010): Comparison of inactivation of Listeria monocytogenes within a biofilm matrix using chlorine dioxide gas, aqueous chlorine dioxide and sodium hypochlorite treatments. Food Microbiology, 27, 979-984 https://doi.org/10.1016/j.fm.2010.05.024
 
Van Houdt R., Michiels C.W. (2010): Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology, 109, 1117-1131 https://doi.org/10.1111/j.1365-2672.2010.04756.x
 
Zhou Qingchun, Feng Xiaoqin, Zhang Qiang, Feng Feifei, Yin Xiaojiao, Shang Junli, Qu Huiping, Luo Qin (2012): Carbon Catabolite Control is Important for Listeria monocytogenes Biofilm Formation in Response to Nutrient Availability. Current Microbiology, 65, 35-43 https://doi.org/10.1007/s00284-012-0125-4
 
download PDF

© 2019 Czech Academy of Agricultural Sciences