Biopelículas y persistencia microbiana en la industria alimentaria
DOI:
https://doi.org/10.3989/arbor.2020.795n1002Palabras clave:
biofilms, persistencia, ecología microbiana, control, procesado de alimentosResumen
Este artículo de revisión examina la importancia que tienen las comunidades microbianas que colonizan los ambientes y equipos de procesado de alimentos formando biopelículas o biofilms en la persistencia microbiana en la industria alimentaria y consecuentemente, en la seguridad y la calidad de los alimentos. La atención se centra especialmente en biopelículas formadas por microorganismos no deseados, es decir, microorganismos alterantes y patógenos. Se presenta información sobre la variabilidad intraespecífica en la formación, la ecología y la arquitectura de las biopelículas, y los factores que influyen en su formación. Asimismo, se resume la información disponible sobre nuevos agentes o estrategias para el control de la formación o eliminación de biopelículas.
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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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