Biofilms and microbial persistence in the food industry

Authors

DOI:

https://doi.org/10.3989/arbor.2020.795n1002

Keywords:

biofilms, persistence, microbial ecology, control, food processing

Abstract


This review examines the importance that microbial communities colonizing food processing environments in the form of biofilms have on food safety and food quality. The focus is on biofilms of undesired microorganisms, i.e. pathogenic and spoilage microorganisms. Information is presented on intraspecies variability in biofilm formation, biofilm ecology and architecture and the factors influencing their formation. Finally, research on novel agents or strategies for the control of biofilm formation or its removal is summarized.

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References

Al-Seraih, A., Belguesmia, Y., Baah, J., Szunerits, S., Boukherroub, R. y Drider, D. (2017). Enterocin B3A-B3B produced by LAB collected from infant faeces: potential utilization in the food indus­try for Listeria monocytogenes biofilm management. Antonie van Leeuwen­hoek. International Journal of General and Molecular Microbiology, 110 (2), pp. 205-219. https://doi.org/10.1007/s10482-016-0791-5 PMid:27878401

Álvarez-Ordóñez, A., Alvseike, O., Omer, M. K ., Heir, E., Axelsson, L., Holck, A. y Prieto, M. (2013). Heterogeneity in resistance to food-related stresses and biofilm formation ability among verocytotoxigenic Escherichia coli strains. International Journal of Food Microbiology, 161 (3), pp. 220-230. https://doi.org/10.1016/j.ijfoodmicro.2012.12.008 PMid:23337122

Araújo, P. A., Machado, I., Meireles, A., Leiknes, T. O., Mergulhão, F., Melo, L. F. y Simões, M. (2017). Combination of se­lected enzymes with cetyltrimethylam­monium bromide in biofilm inactivation, removal and regrowth. Food Research International, 95, pp. 101-107. https://doi.org/10.1016/j.foodres.2017.02.016 PMid:28395817

Ashraf, M. A., Ullah, S., Ahmad, I., Qureshi, A. K., Balkhair, K. S. y Abdur Rehman, M. (2014). Green biocides, a promising technology: Current and future applica­tions to industry and industrial process­es. Journal of the Science of Food and Agriculture, 94 (3), pp. 388-403. https://doi.org/10.1002/jsfa.6371 PMid:23983055

Axelson, L., Holck, A., Rud, I., Samah, D., Tierce, P., Favre, M. y Kure, C. F. (2013). Cleaning of conveyor belt ma­terials using ultrasound in a thin layer of water. Journal of Food Protection, 76 (8), pp. 1401-1407. https://doi.org/10.4315/0362-028X.JFP-12-563 PMid:23905796

Bas, S., Kramer, M. y Stopar, D. (2017). Bio­film surface density determines biocide effectiveness. Frontiers in Microbiol­ogy, 8, 2443. https://doi.org/10.3389/fmicb.2017.02443 PMid:29276508 PMCid:PMC5727120

Bassi, D., Cappa, F., Gazzola, S., Orrù, L. y Cocconcelli, P. S. (2017). Biofilm forma­tion on stainless steel by Streptococcus thermophilus UC8547 in milk environ­ments is mediated by the proteinase PrtS. Applied and Environmental Micro­biology, 83 (8), e02840-16. https://doi.org/10.1128/AEM.02840-16 PMid:28159787 PMCid:PMC5377502

Benítez-Páez, A. y Sanz, Y. (2017). Multi-locus and long amplicon sequencing approach to study microbial diversity at species level using the MinIONTM por­table nanopore sequencer. GigaScience, 6 (7), pp. 1-12. https://doi.org/10.1093/gigascience/gix043 PMid:28605506 PMCid:PMC5534310

Berlanga, M. y Guerrero, R. (2016). Living together in biofilms: The microbial cell factory and its biotechnological implica­tions. Microbial Cell Factories, 15, 165. https://doi.org/10.1186/s12934-016-0569-5 PMid:27716327 PMCid:PMC5045575

Bolocan, A. S., Pennone, V., O'Connor, P. M., Coffey, A., Nicolau, A. I., McAuliffe, O. y Jordan, K. (2017). Inhibition of Listeria monocytogenes biofilms by bacterio­cin-producing bacteria isolated from mushroom substrate. Journal of Applied Microbiology, 122 (1), pp. 279-293. https://doi.org/10.1111/jam.13337 PMid:27797439

Bridier, A., Sanchez-Vizuete, P., Guilbaud, M., Piard, J. C., Naïtali, M. y Briandet, R. (2015). Biofilm-associated persistence of food-borne pathogens. Food Micro­biology, 45 (Pt B), pp. 167-178. https://doi.org/10.1016/j.fm.2014.04.015 PMid:25500382

Brown, H. L., Hanman, K., Reuter, M., Betts, R. P. y Vliet, A. H. M. van (2015). Campylobacter jejuni biofilms contain extracellular DNA and are sensitive to DNase I treatment. Frontiers in Microbi­ology, 6, 699. https://doi.org/10.3389/fmicb.2015.00699 PMid:26217328 PMCid:PMC4498105

Brown, H. L., Reuter, M., Salt, L. J., Cross, K. L., Betts, R. P. y Vliet, A. H. M. (2014). Chicken juice enhances surface attach­ment and biofilm formation of Campylo­bacter jejuni. Applied and Environmental Microbiology, 80 (22), pp. 7053-7060. https://doi.org/10.1128/AEM.02614-14 PMid:25192991 PMCid:PMC4249011

Buzón-Durán, L., Alonso-Calleja, C., Riesco- Peláez, F. y Capita, R. (2017). Effect of sub­inhibitory concentrations of biocides on the architecture and viability of MRSA bio­films. Food Microbiology, 65, pp. 294-301. https://doi.org/10.1016/j.fm.2017.01.003 PMid:28400016

Caballero Gómez, N., Abriouel, H., Gran­de, M. J., Pérez Pulido, R. y Gálvez, A. (2013). Combined treatments of en­terocin AS-48 with biocides to improve the inactivation of methicillin-sensitive and methicillin-resistant Staphylococ­cus aureus planktonic and sessile cells. International Journal of Food Microbiol­ogy, 163 (2-3), pp. 96-100. https://doi.org/10.1016/j.ijfoodmicro.2013.02.018 PMid:23558192

Capita, R., Buzón-Durán, L., Riesco-Peláez, F. y Alonso-Calleja, C. (2017). Effect of sub-lethal concentrations of biocides on the structural parameters and vi­ability of the biofilms formed by Salmo­nella Typhimurium. Foodborne Patho­gens and Disease, 14 (6), pp. 350-356. https://doi.org/10.1089/fpd.2016.2241 PMid:28605289

Chaitiemwong, N., Hazeleger, W. C. y Beum­er, R. R. (2014). Inactivation of Listeria monocytogenes by disinfectants and bac­teriophages in suspension and stainless steel carrier tests. Journal of Food Protec­tion, 77 (12), pp. 2012-2020. https://doi.org/10.4315/0362-028X.JFP-14-151 PMid:25474045

Chen, C. Y., Hofmann, C. S., Cottrell, B. J., Strobaugh, T. P., Paoli, G. C., Nguyen, L. H., Yan, X. y Uhlich, G. A. (2013). Phenotypic and genotypic characterization of biofilm forming capabilities in non-O157 Shiga toxin-producing Escherichia coli strains. PLoS ONE, 8 (12), e84863 https://doi.org/10.1371/journal.pone.0084863 PMid:24386426 PMCid:PMC3874044

Cherifi, T., Jacques, M., Quessy, S. y Fra­valo, P. (2017). Impact of nutrient re­striction on the structure of Listeria monocytogenes biofilm grown in a mi­crofluidic system. Frontiers in Microbi­ology 8, 864. https://doi.org/10.3389/fmicb.2017.00864 PMid:28567031 PMCid:PMC5434154

Chopra, L., Singh, G., Kumar Jena, K. y Sa­hoo, D. K. (2015). Sonorensin: A new bacteriocin with potential of an anti-biofilm agent and a food biopreser­vative. Scientific Reports, 5, 13412. https://doi.org/10.1038/srep13412 PMid:26292786 PMCid:PMC4544038

Chylkova, T., Cadena, M., Ferreiro, A. y Pi­tesky, M. (2017). Susceptibility of Sal­monella biofilm and planktonic bacteria to common disinfectant agents used in poultry processing. Journal of Food Pro­tection, 80 (7), pp. 1072-1079. https://doi.org/10.4315/0362-028X.JFP-16-393 PMid:28561639

Coronel-León, J., Marqués, A. M., Basti­da, J. y Manresa, A. (2016). Optimizing the production of the biosurfactant li­chenysin and its application in biofilm control. Journal of Applied Microbiol­ogy, 120 (1), pp. 99-111. https://doi.org/10.1111/jam.12992 PMid:26519210

Cossu, A., Si, Y., Sun, G. y Nitin, N. (2017). Antibiofilm effect of poly(vinyl alcohol-coethylene) halamine film against Listeria innocua and Escherichia coli O157:H7. Applied and Environmen­tal Microbiology, 83 (19), e00975-17. https://doi.org/10.1128/AEM.00975-17 PMid:28802271 PMCid:PMC5601348

Coughlan, L. M., Cotter, P. D., Hill, C. y Al­varez-Ordóñez, A. (2016). New weap­ons to fight old enemies: Novel strate­gies for the (bio)control of bacterial biofilms in the food industry. Frontiers in Microbiology, 7, 1641. https://doi.org/10.3389/fmicb.2016.01641 PMid:27803696 PMCid:PMC5067414

Daneshvar Alavi, H. E. y Truelstrup Hansen, L. (2013). Kinetics of biofilm forma­tion and desiccation survival of Listeria monocytogenes in single and dual spe­cies biofilms with Pseudomonas fluore­scens, Serratia proteamaculans or She­wanella baltica on food-grade stainless steel surfaces. Biofouling, 29 (10), pp. 1253-1268. https://doi.org/10.1080/08927014.2013.835805 PMid:24102145

Dhowlaghar, N., De Abrew Abeysundara, P., Nannapaneni, R., Schilling, M. W., Chang, S., Cheng, W. H. y Sharma, C. S. (2018). Biofilm formation by Salmo­nella spp. in catfish mucus extract un­der industrial conditions. Food Micro­biology, 70, pp. 172-180. https://doi.org/10.1016/j.fm.2017.09.016 PMid:29173625

Dimakopoulou-Papazoglou, D., Lianou, A. y Koutsoumanis, K. P. (2016). Model­ling biofilm formation of Salmonella enterica ser. Newport as a function of pH and water activity. Food Microbiol­ogy, 53 (Pt B), pp. 76-81. https://doi.org/10.1016/j.fm.2015.09.002 PMid:26678133

Duanis-Assaf, D., Steinberg, D., Chai, Y. y Shemesh, M. (2016). The LuxS based quorum sensing governs lactose in­duced biofilm formation by Bacillus subtilis. Frontiers in Microbiology, 6, 1517. https://doi.org/10.3389/fmicb.2015.01517 PMid:26779171 PMCid:PMC4705240

Endersen, L., Buttimer, C., Nevin, E., Coffey, A., Neve, H., Oliveira, H., Lavigne, R. y O'Mahony, J. (2017). Investigating the biocontrol and anti-biofilm potential of a three phage cocktail against Cronobacter sakazakii in different brands of infant formula. International Journal of Food Microbiology, 253, pp. 1-11. https://doi.org/10.1016/j.ijfoodmicro.2017.04.009 PMid:28460269

Fagerlund, A., Langsrud, S., Heir, E., Mik­kelsen, M. I. y Møretrø, T. (2016). Biofilm matrix composition affects the susceptibility of food associated staphylococci to cleaning and disin­fection agents. Frontiers in Microbiol­ogy, 7, 856. https://doi.org/10.3389/fmicb.2016.00856 PMid:27375578 PMCid:PMC4893552

Faille, C., Bénézech, T., Midelet-Bourdin, G., Lequette, Y., Clarisse, M., Ronse, G., Ronse, A. y Slomianny, C. (2014). Sporu­lation of Bacillus spp. within biofilms: A potential source of contamination in food processing environments. Food Microbiology, 40, pp. 64-74. https://doi.org/10.1016/j.fm.2013.12.004 PMid:24549199

Feng, G., Cheng, Y., Wang, S. Y., Hsu, L. C., Fe­liz, Y., Borca-Tasciuc, D. A., Worobo, R. W. y Moraru, C. I. (2014). Alumina surfaces with nanoscale topography reduce at­tachment and biofilm formation by Esch­erichia coli and Listeria spp. Biofouling, 30 (10), pp. 1253-1268. https://doi.org/10.1080/08927014.2014.976561 PMid:25427545

Fialho, J. F. Q., Naves, E. A. A., Bernar­des, P. C., Ferreira, D. C., Anjos, L. D. dos, Gelamo, R. V., Sá, J. P. N. de y Andrade, N. J. de (2018). Stainless steel and polyethylene surfaces func­tionalized with silver nanoparticles. Food Science and Technology Interna­tional, 24 (1), pp. 87-94. https://doi.org/10.1177/1082013217731414 PMid:28929793

Field, D., O'Connor, R., Cotter, P. D., Ross, R. P. y Hill, C. (2016). In vitro activities of nisin and nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Frontiers in Microbiology, 7, 508. https://doi.org/10.3389/fmicb.2016.00508 PMid:27148197 PMCid:PMC4834297

Flemming, H. C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S. A. y Kjelleberg, S. (2016). Biofilms: An emergent form of bacterial life. Nature Reviews Microbi­ology, 14 (9), pp. 563-575. https://doi.org/10.1038/nrmicro.2016.94 PMid:27510863

Gaglio, R., Cruciata, M., Gerlando, R. di, Scatassa, M. L., Cardamone, C., Man­cuso, I., Sardina, M. T., Moschetti, G., Portolano, B. y Settanni, L. (2016). Mi­crobial activation of wooden vats used for traditional cheese production and evolution of neoformed biofilms. Ap­plied and Environmental Microbiol­ogy, 82 (2), pp. 585-595. https://doi.org/10.1128/AEM.02868-15 PMid:26546430 PMCid:PMC4711119

Gião, M. S. y Keevil, C. W. (2014). Listeria monocytogenes can form biofilms in tap water and enter into the viable but non-cultivable state. Microbial Ecol­ogy, 67 (3), pp. 603-611. https://doi.org/10.1007/s00248-013-0364-3 PMid:24452996

Giaouris, E., Chorianopoulos, N., Doulgera­ki, A. y Nychas, G. J. (2013). Co-Culture with Listeria monocytogenes within a dual-species biofilm community strong­ly increases resistance of Pseudomo­nas putida to benzalkonium chloride. PLoS ONE, 8 (10), e77276. https://doi.org/10.1371/journal.pone.0077276 PMid:24130873 PMCid:PMC3795059

Giaouris, E., Heir, E., Desvaux, M., Hé­braud, M., Møretrø, T., Langsrud, S., Doulgeraki, A., Nychas, G. J., Kačániová, M., Czaczyk, K., Ölmez, H. y Simões, M. (2015). Intra- and inter-species interac­tions within biofilms of important food­borne bacterial pathogens. Frontiers in Microbiology, 6, 841. https://doi.org/10.3389/fmicb.2015.00841 PMid:26347727 PMCid:PMC4542319

Gingichashvili, S., Duanis-Assaf, D., Shem­esh, M., Featherstone, J. D. B., Feuer­stein, O. y Steinberg, D. (2017). Bacil­lus subtilis biofilm development - a computerized study of morphology and kinetics. Frontiers in Microbiolo­gy, 8, 2072. https://doi.org/10.3389/fmicb.2017.02072 PMid:29163384 PMCid:PMC5674941

Gkana, E. N., Doulgeraki, A. I., Chori­anopoulos, N. G. y Nychas, G. J. E. (2017). Anti-adhesion and anti-biofilm potential of organosilane nanoparticles against foodborne pathogens. Frontiers in Microbiology, 8, 1295. https://doi.org/10.3389/fmicb.2017.01295 PMid:28744277 PMCid:PMC5504163

Gomes, L. C., Deschamps, J., Briandet, R. y Mergulhão, F. J. (2018). Impact of modi­fied diamond-like carbon coatings on the spatial organization and disinfection of mixed-biofilms composed of Escherichia coli and Pantoea agglomerans industrial isolates. International Journal of Food Microbiology, 277, pp. 74-82. https://doi.org/10.1016/j.ijfoodmicro.2018.04.017 PMid:29689455

González, S., Fernández, L., Campelo, A. B., Gutiérrez, D., Martínez, B., Rodríguez, A. y García, P. (2017). The behavior of Staphylococcus aureus dual-species bio­films treated with bacteriophage phiIP­LA-RODI depends on the accompanying microorganism. Applied and Environ­mental Microbiology, 83 (3), e02821-16. https://doi.org/10.1128/AEM.02821-16 PMid:27836851 PMCid:PMC5244312

Gutiérrez, D., Rodríguez-Rubio, L., Martí­nez, B., Rodríguez, A. y García, P. (2016). Bacteriophages as weapons against bac­terial biofilms in the food industry. Fron­tiers in Microbiology, 7, 825. https://doi.org/10.3389/fmicb.2016.00825

Gutiérrez, D., Ruas-Madiedo, P., Martínez, B., Rodríguez, A. y García, P. (2014). Effective removal of Staphylococ­cal biofilms by the endolysin LysH5. PLoS ONE, 9 (9), e107307. https://doi.org/10.1371/journal.pone.0107307 PMid:25203125 PMCid:PMC4159335

Han, Q., Song, X., Zhang, Z., Fu, J., Wang, X., Malakar, P. K. Liu, H., Pan, Y. y Zhao, Y. (2017). Removal of foodborne patho­gen biofilms by acidic electrolyzed water. Frontiers in Microbiology, 8, 988. https://doi.org/10.3389/fmicb.2017.00988 PMid:28638370 PMCid:PMC5461821

Hayrapetyan, H., Muller, L., Tempelaars, M., Abee, T. y Nierop Groot, M. (2015). Comparative analysis of biofilm forma­tion by Bacillus cereus reference strains and undomesticated food isolates and the effect of free iron. International Journal of Food Microbiology, 200, pp. 72-79. https://doi.org/10.1016/j.ijfoodmicro.2015.02.005 PMid:25700364

Heir, E., Møretrø, T., Simensen, A. y Langs­rud, S. (2018). Listeria monocytogenes strains show large variations in com­petitive growth in mixed culture bio­films and suspensions with bacteria from food processing environments. International Journal of Food Micro­biology, 275, pp. 46-55. https://doi.org/10.1016/j.ijfoodmicro.2018.03.026 PMid:29631210

Herschend, J., Damholt, Z. B. V., Marquard, A. M., Svensson, B., Sørensen, S. J., Häg­glund, P. y Burmølle, M. (2017). A meta-proteomics approach to study the inter­species interactions affecting microbial biofilm development in a model com­munity. Scientific Reports, 7 (1), 16483. https://doi.org/10.1038/s41598-017-16633-6 PMid:29184101 PMCid:PMC5705676

Hsu, L. C., Fang, J., Borca-Tasciuc, D. A., Worobo, R. W. y Moraru, C. I. (2013). Effect of micro- and nanoscale topogra­phy on the adhesion of bacterial cells to solid surfaces. Applied and Environmen­tal Microbiology, 79 (8), pp. 2703-2712. https://doi.org/10.1128/AEM.03436-12 PMid:23416997 PMCid:PMC3623177

Huang, K., Chen, J., Nugen, S. R. y God­dard, J. M. (2016). Hybrid antifouling and antimicrobial coatings prepared by electroless co-deposition of fluo­ropolymer and cationic silica nanopar­ticles on stainless steel: efficacy against Listeria monocytogenes. ACS Applied Materials and Interfaces, 8 (25), pp. 15926-15936. https://doi.org/10.1021/acsami.6b04187 PMid:27268033

Hussain, M. S., Kwon, M., Tango, C. N. y Oh, D. H. (2018). Effect of electrolyzed water on the disinfection of Bacillus cereus biofilms: the mechanism of en­hanced resistance of sessile cells in the biofilm matrix. Journal of Food Protec­tion, 81 (5), pp. 860-869. https://doi.org/10.4315/0362-028X.JFP-17-450 PMid:29667430

Hüwe, C., Schmeichel, J., Brodkorb, F., Dohlen, S., Kalbfleisch, K., Kreyen­schmidt, M., Lorenz, R. y Kreyen­schmidt, J. (2018). Potential of antimi­crobial treatment of linear low-density polyethylene with poly((tert-butyl-amino)-methyl-styrene) to reduce bio­film formation in the food industry. Bio­fouling, 34 (4), pp. 378-387. https://doi.org/10.1080/08927014.2018.1453926 PMid:29663827

Iliadis, I., Daskalopoulou, A., Simões, M. y Giaouris, E. (2018). Integrated com­bined effects of temperature, pH and sodium chloride concentration on bio­film formation by Salmonella enterica ser. Enteritidis and Typhimurium under low nutrient food-related conditions. Food Research International, 107, pp. 10-18. https://doi.org/10.1016/j.foodres.2018.02.015 PMid:29580466

Jahid, I. K., Lee, N.-Y., Kim, A. y Ha, S.-D. (2013). Influence of glucose concen­trations on biofilm formation, motility, exoprotease production, and quorum sensing in Aeromonas hydrophila. Jour­nal of Food Protection, 76 (2), pp. 239- 247. https://doi.org/10.4315/0362-028X.JFP-12-321 PMid:23433371

Jeon, H. R., Kwon, M. J. y Yoon, K. S. (2018). Control of Listeria innocua biofilms on food contact surfaces with slightly acid­ic electrolyzed water and the risk of bio­film cells transfer to duck meat. Journal of Food Protection, 81 (4), pp. 582-592. https://doi.org/10.4315/0362-028X.JFP-17-373 PMid:29517351

Jindal, S., Anand, S., Metzger, L. y Amam­charla, J. (2018). Short communication: A comparison of biofilm development on stainless steel and modified-surface plate heat exchangers during a 17-h milk pasteurization run. Journal of Dairy Science, 101 (4), pp. 2921-2926. https://doi.org/10.3168/jds.2017-14028 PMid:29398018

Kadam, S. R., den Besten, H. M. W., van der Veen, S., Zwietering, M. H., Moezelaar, R. y Abee, T. (2013). Diversity assess­ment of Listeria monocytogenes biofilm formation: Impact of growth condition, serotype and strain origin. International Journal of Food Microbiology, 165 (3), pp. 259-264. https://doi.org/10.1016/j.ijfoodmicro.2013.05.025 PMid:23800738

Kim, S., Bang, J., Kim, H., Beuchat, L. R. y Ryu, J. H. (2013). Inactivation of Esch­erichia coli O157: H7 on stainless steel upon exposure to Paenibacillus poly­myxa biofilms. International Journal of Food Microbiology, 167 (3), pp. 328- 336. https://doi.org/10.1016/j.ijfoodmicro.2013.10.004 PMid:24184611

Kim, M. K., Zhao, A., Wang, A., Brown, Z. Z., Muir, T. W., Stone, H. A. y Bassler, B. L. (2017). Surface-attached molecules control Staphylococcus aureus quorum sensing and biofilm development. Na­ture Microbiology, 2 (8), 17080. https://doi.org/10.1038/nmicrobiol.2017.80 PMid:28530651 PMCid:PMC5526357

Kiran, G. S., Lipton, A. N., Kennedy, J., Dobson, A. D. W. y Selvin, J. (2014). A halotolerant thermostable lipase from the marine bac­terium Oceanobacillus sp. PUMB02 with an ability to disrupt bacterial biofilms. Bioengineered Bugs, 5 (5), pp. 305-318. https://doi.org/10.4161/bioe.29898 PMid:25482232 PMCid:PMC4156492

Larsen, M. H., Dalmasso, M., Ingmer, H., Langsrud, S., Malakauskas, M., Mader, A., Møretrø, T., Možina, S. S., Rychli, K., Wagner, R., Wallace, R. J., Zentek, J. y Jor­dan, K. (2014). Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control, 44, pp. 92-109. https://doi.org/10.1016/j.foodcont.2014.03.039

Li, J., Feng, J., Ma, L., Fuente Núñez, C. de la, Gölz, G. y Lu, X. (2017). Effects of meat juice on biofilm formation of Campylo­bacter and Salmonella. International Journal of Food Microbiology, 253, pp. 20-28. https://doi.org/10.1016/j.ijfoodmicro.2017.04.013 PMid:28463724

Liu, J., Prindle, A., Humphries, J., Gabalda- Sagarra, M., Asally, M., Lee, D. Y. D., Ly, S. y Süel, G. M. (2015). Metabolic co-de­pendence gives rise to collective oscilla­tions within biofilms. Nature, 523 (7562), pp. 550-554. https://doi.org/10.1038/nature14660 PMid:26200335 PMCid:PMC4862617

Mai-Prochnow, A., Clauson, M., Hong, J. y Murphy, A. B. (2016). Gram positive and Gram negative bacteria differ in their sensitivity to cold plasma. Scien­tific Reports, 6 (1), 38610. https://doi.org/10.1038/srep38610 PMid:27934958 PMCid:PMC5146927

Makovcova, J., Babak, V., Kulich, P., Masek, J., Slany, M. y Cincarova, L. (2017). Dynamics of mono- and dual-species biofilm formation and interactions between Staphylococcus aureus and Gram-negative bacteria. Microbial Bio­technology, 10 (4), pp. 819-832. https://doi.org/10.1111/1751-7915.12705 PMid:28401747 PMCid:PMC5481519

Mariani, C., Oulahal, N., Chamba, J. F., Du­bois-Brissonnet, F., Notz, E. y Briandet, R. (2011). Inhibition of Listeria mono­cytogenes by resident biofilms present on wooden shelves used for cheese ripening. Food Control, 22 (8), pp. 1357-1362. https://doi.org/10.1016/j.foodcont.2011.02.012

Marti, R., Schmid, M., Kulli, S., Schneeberg­er, K., Naskova, J., Knøchel, S. Ahrens, C. H. y Hummerjohann, J. (2017). Biofilm formation potential of heat-resistant Escherichia coli dairy isolates and the complete genome of multidrug-resis­tant, heat-resistant strain FAM21845. Applied and Environmental Microbio­logy, 83 (15), e00628-17. https://doi.org/10.1128/AEM.00628-17 PMid:28550056 PMCid:PMC5514686

Martin, J. G. P., Oliveira e Silva, G. de, Fon­seca, C. R. da, Morales, C. B., Souza Pamplona Silva, C., Miquelluti, D. L. y Porto, E. (2016). Efficiency of a cleaning protocol for the removal of enterotoxi­genic Staphylococcus aureus strains in dairy plants. International Journal of Food Microbiology, 238, pp. 295-301. https://doi.org/10.1016/j.ijfoodmicro.2016.09.018 PMid:27716472

McKenzie, K., Maclean, M., Timoshkin, I. V., Endarko, E., Macgregor, S. J. y Anderson, J. G. (2013). Photoinactivation of bacte­ria attached to glass and acrylic surfaces by 405 nm light: Potential application for biofilm decontamination. Photochem­istry and Photobiology, 89 (4), pp. 927- 935. https://doi.org/10.1111/php.12077 PMid:23550978

Montgomery, N. L. y Banerjee, P. (2015). Inactivation of Escherichia coli O157:H7 and Listeria monocytogenes in biofilms by pulsed ultraviolet light. BMC Re­search Notes, 8 (1), 235. https://doi.org/10.1186/s13104-015-1206-9 PMid:26054759 PMCid:PMC4467610

Moradi, M. y Tajik, H. (2017). Biofilm re­moval potential of neutral electrolysed water on pathogen and spoilage bac­teria in dairy model systems. Journal of Applied Microbiology, 123 (6), pp. 1429-1437. https://doi.org/10.1111/jam.13608 PMid:28994493

Nadell, C. D., Drescher, K. y Foster, K. R. (2016). Spatial structure, cooperation and competition in biofilms. Nature Reviews Microbiology, 14 (9), pp. 589- 600. https://doi.org/10.1038/nrmicro.2016.84 PMid:27452230

Nam, H., Seo, H. S., Bang, J., Kim, H., Beu­chat, L. R. y Ryu, J. H. (2014). Efficacy of gaseous chlorine dioxide in inacti­vating Bacillus cereus spores attached to and in a biofilm on stainless steel. International Journal of Food Microbi­ology, 188, pp. 122-127. https://doi.org/10.1016/j.ijfoodmicro.2014.07.009 PMid:25090607

Nguyen, U. T. y Burrows, L. L. (2014). DN­ase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing bio­films. International Journal of Food Mi­crobiology, 187, pp. 26-32. https://doi.org/10.1016/j.ijfoodmicro.2014.06.025 PMid:25043896

Nicholas, R., Dunton, P., Tatham, A. y Field­ing, L. (2013). The effect of ozone and open air factor on surface-attached and biofilm environmental Listeria monocy­togenes. Journal of Applied Microbiol­ogy, 15 (2), pp. 555-564. https://doi.org/10.1111/jam.12239 PMid:23621101

Niemira, B. A., Boyd, G. y Sites, J. (2014). Cold plasma rapid decontamination of food contact surfaces contaminated with Salmonella biofilms. Journal of Food Science, 79 (5), M917-M922. https://doi.org/10.1111/1750-3841.12379 PMid:24749764

Nowak, J., Cruz, C. D., Tempelaars, M., Abee, T., van Vliet, A. H. M., Fletcher, G. C., Hedderley, D., Palmer, J. y Flint, S. (2017). Persistent Listeria monocyto­genes strains isolated from mussel pro­duction facilities form more biofilm but are not linked to specific genetic mark­ers. International Journal of Food Mi­crobiology, 256, pp. 45-53. https://doi.org/10.1016/j.ijfoodmicro.2017.05.024 PMid:28599174

Ortiz, S., López, V. y Martínez-Suárez, J. V. (2014). The influence of subminimal inhibitory concentrations of benzalko­nium chloride on biofilm formation by Listeria monocytogenes. International Journal of Food Microbiology, 189, pp. 106-112. https://doi.org/10.1016/j.ijfoodmicro.2014.08.007 PMid:25136789

Overney, A., Jacques-André-Coquin, J., Ng, P., Carpentier, B., Guillier, L. y Firmesse, O. (2017). Impact of environmental fac­tors on the culturability and viability of Listeria monocytogenes under condi­tions encountered in food processing plants. International Journal of Food Mi­crobiology, 244, pp. 74-81. https://doi.org/10.1016/j.ijfoodmicro.2016.12.012 PMid:28073080

Papaioannou, E., Giaouris, E. D., Berillis, P. y Boziaris, I. S. (2018). Dynamics of biofilm formation by Listeria monocy­togenes on stainless steel under mono-species and mixed-culture simulated fish processing conditions and chemical disinfection challenges. International Journal of Food Microbiology, 267, pp. 9-19. https://doi.org/10.1016/j.ijfoodmicro.2017.12.020 PMid:29275280

Pasvolsky, R., Zakin, V., Ostrova, I. y Shem­esh, M. (2014). Butyric acid released during milk lipolysis triggers biofilm for­mation of Bacillus species. International Journal of Food Microbiology, 181, pp. 19-27. https://doi.org/10.1016/j.ijfoodmicro.2014.04.013 PMid:24801271

Puligundla, P. y Mok, C. (2017). Potential applications of nonthermal plasmas against biofilm-associated micro-organ­isms in vitro. Journal of Applied Microbi­ology, 122 (5), pp. 1134-1148. https://doi.org/10.1111/jam.13404 PMid:28106311

Røder, H. L., Raghupathi, P. K., Herschend, J., Brejnrod, A., Knøchel, S., Sørensen, S. J. y Burmølle, M. (2015). Interspe­cies interactions result in enhanced biofilm formation by co-cultures of bac­teria isolated from a food processing environment. Food Microbiology, 51, pp. 18-24. https://doi.org/10.1016/j.fm.2015.04.008 PMid:26187823

Rodríguez-López, P., Saá-Ibusquiza, P., Mos­quera-Fernández, M. y López-Cabo, M. (2015). Listeria monocytogenes-carry­ing consortia in food industry. Compo­sition, subtyping and numerical charac­terisation of mono-species biofilm dy­namics on stainless steel. International Journal of Food Microbiology, 206, pp. 84-95. https://doi.org/10.1016/j.ijfoodmicro.2015.05.003 PMid:26001376

Rosenberg, G., Steinberg, N., Oppenheimer- Shaanan, Y., Olender, T., Doron, S., Ben- Ari, J., Sirota-Madi, A, Bloom-Acker­mann, Z. y Kolodkin-Gal, I. (2016). Not so simple, not so subtle: The interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. NPJ Biofilms and Microbiomes, 2 (1), 15027. https://doi.org/10.1038/npjbiofilms.2015.27 PMid:28721238 PMCid:PMC5515258

Sadekuzzaman, M., Yang, S., Mizan, M. F. R. y Ha, S. D. (2017). Reduction of Escherichia coli O157:H7 in biofilms using bacterio­phage BPECO 19. Journal of Food Sci­ence, 82 (6), pp. 1433-1442. https://doi.org/10.1111/1750-3841.13729 PMid:28542913

Sepehr, S., Rahmani-Badi, A., Babaie-Naiej, H. y Soudi, M. R. (2014). Unsaturated fatty acid, cis-2-decenoic acid, in com­bination with disinfectants or antibiot­ics removes pre-established biofilms formed by food-related bacteria. PLoS ONE, 9 (7), e101677. https://doi.org/10.1371/journal.pone.0101677 PMid:25000301 PMCid:PMC4084997

Shafique, M., Alvi, I. A., Abbas, Z. y ur Re­hman, S. (2017). Assessment of bio­film removal capacity of a broad host range bacteriophage JHP against Pseu­domonas aeruginosa. APMIS, 125 (6), pp. 579-584. https://doi.org/10.1111/apm.12691 PMid:28418081

Silva Fernandes, M. da, Kabuki, D. Y. y Kua­ye, A. Y. (2015). Behavior of Listeria monocytogenes in a multi-species bio­film with Enterococcus faecalis and En­terococcus faecium and control through sanitation procedures. International Journal of Food Microbiology, 200, pp. 5-12. https://doi.org/10.1016/j.ijfoodmicro.2015.01.003 PMid:25655573

Skovager, A., Larsen, M. H., Castro-Mejia, J. L., Hecker, M., Albrecht, D., Gerth, U., Arneborg, N. y Ingmer, H. (2013). Initial adhesion of Listeria monocytogenes to fine polished stainless steel under flow conditions is determined by prior growth conditions. International Jour­nal of Food Microbiology, 165 (1), pp. 35-42. https://doi.org/10.1016/j.ijfoodmicro.2013.04.014 PMid:23685728

Slany, M., Oppelt, J. y Cincarova, L. (2017). Formation of Staphylococcus aureus biofilm in the presence of sublethal concentrations of disinfectants stud­ied via a transcriptomic analysis using transcriptome sequencing (RNA-seq). Applied and Environmental Microbiol­ogy, 83 (24), e01643-17. https://doi.org/10.1128/AEM.01643-17 PMid:29030437 PMCid:PMC5717214

Son, H., Park, S., Beuchat, L. R., Kim, H. y Ryu, J. H. (2016). Inhibition of Staphy­lococcus aureus by antimicrobial bio­films formed by competitive exclusion microorganisms on stainless steel. International Journal of Food Microbi­ology, 238, pp. 165-171. https://doi.org/10.1016/j.ijfoodmicro.2016.09.007 PMid:27648758

Stevens, M. R. E., Luo, T. L., Vornhagen, J., Jakubovics, N. S., Gilsdorf, J. R., Marrs, C. F., Møretrø, T. y Rickard, A. H. (2015). Coaggregation occurs between microor­ganisms isolated from different environ­ments. FEMS Microbiology Ecology, 91 (11), fiv123. https://doi.org/10.1093/femsec/fiv123 PMid:26475462

Tack, I. L. M. M., Nimmegeers, P., Akker­mans, S., Hashem, I. y van Impe, J. F. M. (2017). Simulation of Escherichia coli dynamics in biofilms and submerged colonies with an individual-based model including metabolic network information. Frontiers in Microbiol­ogy, 8, 2509. https://doi.org/10.3389/fmicb.2017.02509 PMid:29321772 PMCid:PMC5733555

Tarifa, M. C., Genovese, D., Lozano, J. E. y Brugnoni, L. I. (2018). In situ micro­structure and rheological behavior of yeast biofilms from the juicprocessing industries. Biofouling, 34 (1), pp. 74-85. https://doi.org/10.1080/08927014.2017.1407758 PMid:29228797

Techaruvichit, P., Takahashi, H., Kuda, T., Miya, S., Keeratipibul, S. y Kimura, B. (2016). Adaptation of Campylobacter jejuni to biocides used in the food in­dustry affects biofilm structure, adhe­sion strength, and cross-resistance to clinical antimicrobial compounds. Bio­fouling, 32 (7), pp. 827-839. https://doi.org/10.1080/08927014.2016.1198476 PMid:27353218

Turonova, H., Briandet, R., Rodrigues, R., Hernould, M., Hayek, N., Stintzi, A., Pazlarova, J. y Tresse, O. (2015). Bio­film spatial organization by the emerg­ing pathogen Campylobacter jejuni: Comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions. Frontiers in Microbiology, 6, 709. https://doi.org/10.3389/fmicb.2015.00709 PMid:26217332 PMCid:PMC4499754

Visvalingam, J., Ells, T. C. y Yang, X. (2017). Impact of persistent and nonpersistent generic Escherichia coli and Salmo­nella sp. recovered from a beef pack­ing plant on biofilm formation by E. coli O157. Journal of Applied Microbiology, 123 (6), pp. 1512-1521. https://doi.org/10.1111/jam.13591 PMid:28944561

Vogeleer, P., Tremblay, Y. D. N., Jubelin, G., Jacques, M. y Harel, J. (2016). Biofilm-forming abilities of Shiga toxin-produc­ing Escherichia coli isolates associated with human infections. Applied and Environmental Microbiology, 82 (5), pp. 1448-1458. https://doi.org/10.1128/AEM.02983-15 PMid:26712549 PMCid:PMC4771338

Wang, R., Kalchayanand, N., Schmidt, J. W. y Harhay, D. M. (2013). Mixed biofilm formation by Shiga Toxin-Producing Escherichia coli and Salmonella enterica Serovar Typhimurium enhanced bacte­rial resistance to sanitization due to ex­tracellular polymeric substances. Jour­nal of Food Protection, 76 (9), pp. 1513- 1522. https://doi.org/10.4315/0362-028X.JFP-13-077 PMid:23992495

Wang, J., Ray, A. J., Hammons, S. R. y Oliver, H. F. (2015). Persistent and transient Lis­teria monocytogenes strains from retail deli environments vary in their ability to adhere and form biofilms and rarely have inlA premature stop codons. Food­borne Pathogens and Disease, 12 (2), pp. 151-158. https://doi.org/10.1089/fpd.2014.1837 PMid:25569840

Xue, T., Chen, X. y Shang, F. (2014). Short communication: Effects of lactose and milk on the expression of biofilm-as­sociated genes in Staphylococcus au­reus strains isolated from a dairy cow with mastitis. Journal of Dairy Science, 97 (10), pp. 6129-6134. https://doi.org/10.3168/jds.2014-8344 PMid:25151886

Yu, S., Su, T., Wu, H., Liu, S., Wang, D., Zhao, T., Jin, Z., Du, W., Zhu, M.-J., Chua, S. L., Yang, L., Zhu, D., Gu, L. y Ma, L. Z. (2015). PslG, a self-produced glycosyl hydrolase, triggers biofilm disassembly by disrupting exopolysaccharide matrix. Cell Research, 25 (12), pp. 1352-1367. https://doi.org/10.1038/cr.2015.129 PMid:26611635 PMCid:PMC4670989

Zhao, T., Podtburg, T. C., Zhao, P., Chen, D., Baker, D. A., Cords, B. y Doyle, M. P. (2013). Reduction by competitive bacteria of Listeria monocytogenes in biofilms and Listeria bacteria in floor drains in a ready-to-eat poultry pro­cessing plant. Journal of Food Protec­tion, 76 (4), pp. 601-607. https://doi.org/10.4315/0362-028X.JFP-12-323 PMid:23575121

Ziuzina, D., Boehm, D., Patil, S., Cullen, P. J. y Bourke, P. (2015). Cold plasma inactiva­tion of bacterial biofilms and reduction of quorum sensing regulated virulence factors. PLoS ONE, 10 (9), e0138209. https://doi.org/10.1371/journal.pone.0138209 PMid:26390435 PMCid:PMC4577073

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2020-03-30

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Fernández-Gómez, P., Prieto, M., Fernández-Escámez, P. S., López, M., & Alvarez-Ordóñez, A. (2020). Biofilms and microbial persistence in the food industry. Arbor, 196(795), a538. https://doi.org/10.3989/arbor.2020.795n1002

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