{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,26]],"date-time":"2026-03-26T18:42:45Z","timestamp":1774550565363,"version":"3.50.1"},"reference-count":87,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2024,2,10]],"date-time":"2024-02-10T00:00:00Z","timestamp":1707523200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Portuguese Foundation for Science and Technology (FCT)\/MCTES","award":["UIDP\/50017\/2020+UIDB\/50017\/2020+LA\/P\/0094\/2020"],"award-info":[{"award-number":["UIDP\/50017\/2020+UIDB\/50017\/2020+LA\/P\/0094\/2020"]}]},{"name":"Portuguese Foundation for Science and Technology (FCT)\/MCTES","award":["2020.06571.BD"],"award-info":[{"award-number":["2020.06571.BD"]}]},{"name":"Portuguese Foundation for Science and Technology (FCT)\/MCTES","award":["2021.05519.BD"],"award-info":[{"award-number":["2021.05519.BD"]}]},{"name":"FCT","award":["UIDP\/50017\/2020+UIDB\/50017\/2020+LA\/P\/0094\/2020"],"award-info":[{"award-number":["UIDP\/50017\/2020+UIDB\/50017\/2020+LA\/P\/0094\/2020"]}]},{"name":"FCT","award":["2020.06571.BD"],"award-info":[{"award-number":["2020.06571.BD"]}]},{"name":"FCT","award":["2021.05519.BD"],"award-info":[{"award-number":["2021.05519.BD"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The bacterial adhesion to food processing surfaces is a threat to human health, as these surfaces can serve as reservoirs of pathogenic bacteria. Escherichia coli is an easily biofilm-forming bacterium involved in surface contamination that can lead to the cross-contamination of food. Despite the application of disinfection protocols, contamination through food processing surfaces continues to occur. Hence, new, effective, and sustainable alternative approaches are needed. Bacteriophages (or simply phages), viruses that only infect bacteria, have proven to be effective in reducing biofilms. Here, phage phT4A was applied to prevent and reduce E. coli biofilm on plastic and stainless steel surfaces at 25 \u00b0C. The biofilm formation capacity of phage-resistant and sensitive bacteria, after treatment, was also evaluated. The inactivation effectiveness of phage phT4A was surface-dependent, showing higher inactivation on plastic surfaces. Maximum reductions in E. coli biofilm of 5.5 and 4.0 log colony-forming units (CFU)\/cm2 after 6 h of incubation on plastic and stainless steel, respectively, were observed. In the prevention assays, phage prevented biofilm formation in 3.2 log CFU\/cm2 after 12 h. Although the emergence of phage-resistant bacteria has been observed during phage treatment, phage-resistant bacteria had a lower biofilm formation capacity compared to phage-sensitive bacteria. Overall, the results suggest that phages may have applicability as surface disinfectants against pathogenic bacteria, but further studies are needed to validate these findings using phT4A under different environmental conditions and on different materials.<\/jats:p>","DOI":"10.3390\/microorganisms12020366","type":"journal-article","created":{"date-parts":[[2024,2,12]],"date-time":"2024-02-12T04:47:45Z","timestamp":1707713265000},"page":"366","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Effect of Bacteriophages against Biofilms of Escherichia coli on Food Processing Surfaces"],"prefix":"10.3390","volume":"12","author":[{"given":"Ana","family":"Br\u00e1s","sequence":"first","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2510-612X","authenticated-orcid":false,"given":"M\u00e1rcia","family":"Braz","sequence":"additional","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"given":"In\u00eas","family":"Martinho","sequence":"additional","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"given":"Jo\u00e3o","family":"Duarte","sequence":"additional","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9209-7687","authenticated-orcid":false,"given":"Carla","family":"Pereira","sequence":"additional","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8422-8664","authenticated-orcid":false,"given":"Adelaide","family":"Almeida","sequence":"additional","affiliation":[{"name":"Department of Biology, CESAM, Campus Universit\u00e1rio de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2024,2,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Moye, Z.D., Woolston, J., and Sulakvelidze, A. (2018). Bacteriophage applications for food production and processing. Viruses, 10.","DOI":"10.3390\/v10040205"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Garvey, M. (2022). Bacteriophages and food production: Biocontrol and bio-preservation options for food safety. Antibiotics, 11.","DOI":"10.3390\/antibiotics11101324"},{"key":"ref_3","unstructured":"WHO (2015). WHO Estimates of the Global Burden of Foodborne Diseases: Foodborne Diseases Burden Epidemiology Reference Group 2007\u20132015, WHO."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Ramos, S., Silva, V., de Lurdes Enes Dapkevicius, M., Cani\u00e7a, M., Tejedor-Junco, M.T., Igrejas, G., and Poeta, P. (2020). Escherichia coli as commensal and pathogenic bacteria among food-producing animals: Health implications of extended spectrum \u03b2-lactamase (ESBL) production. Animals, 10.","DOI":"10.3390\/ani10122239"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"EFSA (2023). The European Union one health 2022 zoonoses report. EFSA J., 21, e8442.","DOI":"10.2903\/j.efsa.2023.p211202"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/microbiolspec.ARBA-0026-2017","article-title":"Antimicrobial resistance in Escherichia coli","volume":"6","author":"Poirel","year":"2018","journal-title":"Microbiol. Spectr."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3593","DOI":"10.1128\/JB.182.12.3593-3596.2000","article-title":"Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture","volume":"182","author":"Danese","year":"2000","journal-title":"J. Bacteriol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1128\/MMBR.64.4.847-867.2000","article-title":"Microbial biofilms: From ecology to molecular genetics","volume":"64","author":"Davey","year":"2000","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4674235","DOI":"10.1155\/2020\/4674235","article-title":"Review on major food-borne zoonotic bacterial pathogens","volume":"2020","author":"Abebe","year":"2020","journal-title":"J. Trop. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1007\/s00203-017-1393-y","article-title":"Current pathogenic Escherichia coli foodborne outbreak cases and therapy development","volume":"199","author":"Yang","year":"2017","journal-title":"Arch. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zhou, F., Wang, D., Hu, J., Zhang, Y., Tan, B.K., and Lin, S. (2022). Control measurements of Escherichia coli biofilm: A review. Foods, 11.","DOI":"10.3390\/foods11162469"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Guti\u00e9rrez, D., Rodr\u00edguez-Rubio, L., Mart\u00ednez, B., Rodr\u00edguez, A., and Garc\u00eda, P. (2016). Bacteriophages as weapons against bacterial biofilms in the food industry. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00825"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2210","DOI":"10.1111\/jam.15766","article-title":"Biofilms as a microbial hazard in the food industry: A scoping review","volume":"133","author":"Sharan","year":"2022","journal-title":"J. Appl. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"7945","DOI":"10.1128\/JB.00858-07","article-title":"The EPS matrix: The \u201chouse of biofilm cells\u201d","volume":"189","author":"Flemming","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.tim.2004.11.006","article-title":"Biofilms: The matrix revisited","volume":"13","author":"Branda","year":"2005","journal-title":"Trends Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijnonlinmec.2018.10.012","article-title":"Biofilms as poroelastic materials","volume":"109","author":"Carpio","year":"2019","journal-title":"Int. J. Non Linear Mech."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1418","DOI":"10.4315\/0362-028X.JFP-11-427","article-title":"Biofilm formation by Shiga toxin\u2013producing Escherichia coli O157:H7 and non-O157 strains and their tolerance to sanitizers commonly used in the food processing environment","volume":"75","author":"Wang","year":"2012","journal-title":"J. Food Prot."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1111\/1750-3841.12123","article-title":"Biofilm formation of O157 and non-O157 Shiga toxin-producing Escherichia coli and multidrug-resistant and susceptible Salmonella Typhimurium and newport and their inactivation by sanitizers","volume":"78","author":"Fouladkhah","year":"2013","journal-title":"J. Food Sci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Bumunang, E.W., Zaheer, R., Niu, D., Narvaez-Bravo, C., Alexander, T., McAllister, T.A., and Stanford, K. (2023). Bacteriophages for the targeted control of foodborne pathogens. Foods, 12.","DOI":"10.3390\/foods12142734"},{"key":"ref_20","first-page":"267","article-title":"Phage biocontrol applications in food production and processing","volume":"40","author":"Vikram","year":"2020","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1111\/jam.13078","article-title":"Escherichia coli biofilm: Development and therapeutic strategies","volume":"121","author":"Sharma","year":"2016","journal-title":"J. Appl. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1128\/AEM.02283-13","article-title":"Exposure of Escherichia coli ATCC 12806 to sublethal concentrations of food-grade biocides influences its ability to form biofilm, resistance to antimicrobials, and ultrastructure","volume":"80","author":"Capita","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"55","DOI":"10.5897\/SRE2017.6546","article-title":"Bacteriophages and phage products: Applications in medicine and biotechnological industries, and general concerns","volume":"13","author":"Belay","year":"2018","journal-title":"Sci. Res. Essays"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.micres.2018.04.007","article-title":"Biotechnological applications of bacteriophages: State of the art","volume":"212\u2013213","author":"Harada","year":"2018","journal-title":"Microbiol. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"33","DOI":"10.3354\/dao053033","article-title":"Bacteriophage control of Pseudomonas plecoglossicida infection in ayu","volume":"53","author":"Park","year":"2003","journal-title":"Dis. Aquat. Organ."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.vetmic.2010.05.014","article-title":"Topical treatment of Pseudomonas aeruginosa otitis of dogs with a bacteriophage mixture: A before\/after clinical trial","volume":"146","author":"Hawkins","year":"2010","journal-title":"Vet. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1146\/annurev-food-030713-092415","article-title":"Phage therapy in the food industry","volume":"5","author":"Endersen","year":"2014","journal-title":"Annu. Rev. Food Sci. Technol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e00066-18","DOI":"10.1128\/CMR.00066-18","article-title":"Phage therapy in the postantibiotic era","volume":"32","author":"Altamirano","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.mib.2017.09.004","article-title":"Phage therapy as an alternative or complementary strategy to prevent and control biofilm-related infections","volume":"39","author":"Pires","year":"2017","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Ball\u00e9n, V., Cepas, V., Ratia, C., Gabasa, Y., and Soto, S.M. (2022). Clinical Escherichia coli: From biofilm formation to new antibiofilm strategies. Microorganisms, 10.","DOI":"10.3390\/microorganisms10061103"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1177\/1535370218755658","article-title":"Phage therapy in allergic disorders?","volume":"243","author":"Miedzybrodzki","year":"2018","journal-title":"Exp. Biol. Med."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Domingo-Calap, P., and Delgado-Mart\u00ednez, J. (2018). Bacteriophages: Protagonists of a post-antibiotic era. Antibiotics, 7.","DOI":"10.3390\/antibiotics7030066"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s00425-020-03549-1","article-title":"Kiwifruit bacterial canker: An integrative view focused on biocontrol strategies","volume":"253","author":"Pereira","year":"2021","journal-title":"Planta"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1089\/fpd.2012.1473","article-title":"Phage inhibition of Escherichia coli in ultrahigh-temperature-treated and raw milk","volume":"10","author":"McLean","year":"2013","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/lam.12074","article-title":"Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli during milk fermentation","volume":"57","author":"Tomat","year":"2013","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3417","DOI":"10.1128\/AEM.70.6.3417-3424.2004","article-title":"Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7","volume":"70","author":"Ross","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1177\/1082013213513031","article-title":"Effect of phage and host concentration on the inactivation of Escherichia coli O157:H7 on cooked and raw beef","volume":"21","author":"Hudson","year":"2013","journal-title":"Food Sci. Technol. Int."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"6230","DOI":"10.1128\/AEM.01465-08","article-title":"Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7","volume":"74","author":"Abuladze","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"178","DOI":"10.4161\/bact.22825","article-title":"Bacteriophage cocktail significantly reduces Escherichia coli O157: H7 contamination of lettuce and beef, but does not protect against recontamination","volume":"2","author":"Carter","year":"2012","journal-title":"Bacteriophage"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e24323","DOI":"10.4161\/bact.24323","article-title":"Lytic bacteriophages reduce Escherichia coli O157","volume":"3","author":"Ferguson","year":"2013","journal-title":"Bacteriophage"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.4315\/0362-028X-72.7.1481","article-title":"Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettucet","volume":"72","author":"Sharma","year":"2009","journal-title":"J. Food Prot."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1051\/animres:2003009","article-title":"Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep","volume":"52","author":"Bach","year":"2003","journal-title":"Anim. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.fm.2016.09.003","article-title":"Application of phage therapy during bivalve depuration improves Escherichia coli decontamination","volume":"61","author":"Pereira","year":"2017","journal-title":"Food Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.foodres.2016.10.031","article-title":"Application of bacteriophages during depuration reduces the load of Salmonella Typhimurium in cockles","volume":"90","author":"Pereira","year":"2016","journal-title":"Food Res. Int."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.ijfoodmicro.2010.11.021","article-title":"Reduction of Escherichia coli O157:H7 viability on hard surfaces by treatment with a bacteriophage mixture","volume":"145","author":"Viazis","year":"2011","journal-title":"Int. J. Food Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1089\/fpd.2010.0734","article-title":"Inactivation of Escherichia coli O157:H7 attached to spinach harvester blade using bacteriophage","volume":"8","author":"Patel","year":"2011","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Jaroni, D., Litt, P.K., Bule, P., and Rumbaugh, K. (2023). Effectiveness of bacteriophages against biofilm-forming Shiga-toxigenic Escherichia coli in vitro and on food-contact surfaces. Foods, 12.","DOI":"10.20944\/preprints202306.1904.v1"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Gonz\u00e1lez-G\u00f3mez, J.P., Gonz\u00e1lez-Torres, B., Guerrero-Medina, P.J., L\u00f3pez-Cuevas, O., Chaidez, C., Avila-Novoa, M.G., and Guti\u00e9rrez-Lomel\u00ed, M. (2021). Efficacy of novel bacteriophages against Escherichia coli biofilms on stainless steel. Antibiotics, 10.","DOI":"10.3390\/antibiotics10101150"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2","DOI":"10.2174\/138920110790725311","article-title":"Phage choice, isolation, and preparation for phage therapy","volume":"11","author":"Gill","year":"2010","journal-title":"Curr. Pharm. Biotechnol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.diagmicrobio.2012.11.019","article-title":"Comparison of three methods to study biofilm formation by clinical strains of Escherichia coli","volume":"75","author":"Corvec","year":"2013","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1111\/j.1365-2672.2008.03791.x","article-title":"Measurement of biofilm formation by clinical isolates of Escherichia coli is method-dependent","volume":"105","author":"Naves","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.virusres.2016.09.019","article-title":"Characterization and in vitro evaluation of new bacteriophages for the biocontrol of Escherichia coli","volume":"227","author":"Pereira","year":"2016","journal-title":"Virus Res."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Costa, P., Pereira, C., Gomes, A., and Almeida, A. (2019). Efficiency of single phage suspensions and phage cocktail in the inactivation of Escherichia coli and Salmonella Typhimurium: An in vitro preliminary study. Microorganisms, 7.","DOI":"10.3390\/microorganisms7040094"},{"key":"ref_54","unstructured":"Adams, M.H. (1959). Bacteriophages, John Wiley and Sons Inc."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1111\/1750-3841.13729","article-title":"Do Reduction of Escherichia coli O157:H7 in biofilms using bacteriophage BPECO 19","volume":"82","author":"Sadekuzzaman","year":"2017","journal-title":"J. Food Sci."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Mukane, L., Racenis, K., Rezevska, D., Petersons, A., and Kroica, J. (2022). Anti-biofilm effect of bacteriophages and antibiotics against uropathogenic Escherichia coli. Antibiotics, 11.","DOI":"10.3390\/antibiotics11121706"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Park, D.W., and Park, J.H. (2021). Characterization and food application of the novel lytic phage becp10: Specifically recognizes the o-polysaccharide of Escherichia coli O157:H7. Viruses, 13.","DOI":"10.3390\/v13081469"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Mangieri, N., Foschino, R., and Picozzi, C. (2021). Application of bacteriophages on Shiga toxin-producing Escherichia coli (STEC) biofilm. Antibiotics, 10.","DOI":"10.3390\/antibiotics10111423"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Filloux, A., and Ramos, J. (2014). Pseudomonas Methods and Protocols. Methods in Molecular Biology, Humana Press.","DOI":"10.1007\/978-1-4939-0473-0"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Zhu, W., Ding, Y., Huang, C., Wang, J., Wang, J., and Wang, X. (2022). Genomic characterization of a novel bacteriophage STP55 revealed its prominent capacity in disrupting the dual-species biofilm formed by Salmonella Typhimurium and Escherichia coli O157:H7 strains. Arch. Microbiol., 204.","DOI":"10.1007\/s00203-022-03208-x"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1007\/s12275-021-1413-0","article-title":"Characterization of a novel phage depolymerase specific to Escherichia coli O157:H7 and biofilm control on abiotic surfaces","volume":"59","author":"Park","year":"2021","journal-title":"J. Microbiol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Filippov, A., Sergueev, K.V., He, Y., Huang, X.Z., Gnade, B.T., Mueller, A.J., Fernandez-Prada, C., and Nikolich, M.P. (2011). Bacteriophage-resistant mutants in Yersinia pestis: Identification of phage receptors and attenuation for mice. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0025486"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"205","DOI":"10.2147\/IDR.S290093","article-title":"Bacteriophage\u2014A promising alternative measure for bacterial biofilm control","volume":"14","author":"Tian","year":"2021","journal-title":"Infect. Drug Resist."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Buck, L.D., Paladino, M.M., Nagashima, K., Brezel, E.R., Holtzman, J.S., Urso, S.J., and Ryno, L.M. (2021). Temperature-dependent influence of FliA overexpression on PHL628 E. coli biofilm growth and composition. Front. Cell. Infect. Microbiol., 11.","DOI":"10.3389\/fcimb.2021.775270"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1111\/1574-6968.12439","article-title":"Growth media and temperature effects on biofilm formation by serotype O157: H7 and non-O157 Shiga toxin-producing Escherichia coli","volume":"354","author":"Uhlich","year":"2014","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1842","DOI":"10.1128\/aem.60.6.1842-1851.1994","article-title":"Influence of plumbing materials on biofilm formation and growth of Legionella pneumophila in potable water systems","volume":"60","author":"Rogers","year":"1994","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Ruhal, R., and Kataria, R. (2021). Biofilm patterns in gram-positive and gram-negative bacteria. Microbiol. Res., 251.","DOI":"10.1016\/j.micres.2021.126829"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1139\/w02-063","article-title":"Adhesion of Bacillus spores and Escherichia coli cells to inert surfaces: Role of surface hydrophobicity","volume":"48","author":"Faille","year":"2002","journal-title":"Can. J. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1584","DOI":"10.4315\/JFP-22-112","article-title":"Influence of different stainless steel finishes on biofilm formation by Listeria monocytogenes","volume":"85","author":"Pathirajah","year":"2022","journal-title":"J. Food Prot."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2581","DOI":"10.1007\/s13197-023-05778-0","article-title":"Microbial investigation of cleanability of different plastic and metal surfaces used by the food industry","volume":"60","author":"Waldhans","year":"2023","journal-title":"J. Food Sci. Technol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1007\/s10856-019-6281-3","article-title":"Effect of biomaterials hydrophobicity and roughness on biofilm development","volume":"30","author":"Cobos","year":"2019","journal-title":"J. Mater. Sci. Mater. Med."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Wang, C., Hang, H., Zhou, S., Niu, Y.D., Du, H., Stanford, K., and McAllister, T.A. (2020). Bacteriophage biocontrol of Shiga toxigenic Escherichia coli (STEC) O145 biofilms on stainless steel reduces the contamination of beef. Food Microbiol., 92.","DOI":"10.1016\/j.fm.2020.103572"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"17904","DOI":"10.1038\/s41598-018-36229-y","article-title":"Complete genome analysis of a Siphoviridae phage TSK1 showing biofilm removal potential against Klebsiella pneumoniae","volume":"8","author":"Tabassum","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Kozelskaya, A.I., Verzunova, K.N., Akimchenko, I.O., Frueh, J., Petrov, V.I., Slepchenko, G.B., Bakina, O.V., Lerner, M.I., Brizhan, L.K., and Davydov, D.V. (2023). Antibacterial calcium phosphate coatings for biomedical applications fabricated via micro-arc oxidation. Biomimetics, 8.","DOI":"10.3390\/biomimetics8050444"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Montso, P.K., Mlambo, V., and Ateba, C.N. (2021). Efficacy of novel phages for control of multi-drug resistant Escherichia coli O177 on artificially contaminated beef and their potential to disrupt biofilm formation. Food Microbiol., 94.","DOI":"10.1016\/j.fm.2020.103647"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Chen, L., Yuan, S., Liu, Q., Mai, G., Yang, J., Deng, D., Zhang, B., Liu, C., and Ma, Y. (2018). In Vitro design and evaluation of phage cocktails against Aeromonas salmonicida. Front. Microbiol., 9.","DOI":"10.3389\/fmicb.2018.01476"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1111\/1574-6976.12072","article-title":"Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities","volume":"38","author":"Koskella","year":"2014","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Duarte, J., Pereira, C., Costa, P., and Almeida, A. (2021). Bacteriophages with potential to inactivate Aeromonas hydrophila in cockles: In Vitro and in vivo preliminary studies. Antibiotics, 10.","DOI":"10.3390\/antibiotics10060710"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1086\/648478","article-title":"Bacteriophage therapy of Salmonella enterica: A fresh appraisal of bacteriophage therapy","volume":"201","author":"Capparelli","year":"2010","journal-title":"J. Infect. Dis."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Capparelli, R., Nocerino, N., Lanzetta, R., Silipo, A., Amoresano, A., Giangrande, C., Becker, K., Blaiotta, G., Evidente, A., and Cimmino, A. (2010). Bacteriophage-resistant Staphylococcus aureus mutant confers broad immunity against staphylococcal infection in mice. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0011720"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Le\u00f3n, M., Kokkari, C., Garc\u00eda, K., Castillo, D., Katharios, P., and Bast\u00edas, R. (2019). Diversification of Vibrio anguillarum driven by the bacteriophage CHOED. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.01396"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"292","DOI":"10.2307\/2640942","article-title":"Epistatic interactions can lower the cost of resistance to multiple consumers","volume":"53","author":"Bohannan","year":"1999","journal-title":"Evolution"},{"key":"ref_83","first-page":"1385","article-title":"The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa","volume":"272","author":"Brockhurst","year":"2005","journal-title":"Proc. Biol. Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1038\/ismej.2007.37","article-title":"Is there a cost of virus resistance in marine cyanobacteria?","volume":"1","author":"Lennon","year":"2007","journal-title":"ISME J."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1406","DOI":"10.1111\/j.1558-5646.2009.00654.x","article-title":"Effects of temperature on the fitness cost of resistance to bacteriophage T4 in Escherichia coli","volume":"63","author":"Quance","year":"2009","journal-title":"Evolution"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Harper, D., Abedon, S., Burrowes, B., and McConville, M. (2021). Bacteriophages, Springer.","DOI":"10.1007\/978-3-319-41986-2"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Costa, M.J., Pastrana, L.M., Teixeira, J.A., Sillankorva, S.M., and Cerqueira, M.A. (2023). Bacteriophage delivery systems for food applications: Opportunities and perspectives. 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