<?xml version="1.0" encoding="UTF-8"?>
<!DOCTYPE article PUBLIC "-//NLM//DTD JATS (Z39.96) Journal Publishing DTD v1.3 20210610//EN" "JATS-journalpublishing1-3.dtd">
<article article-type="research-article" dtd-version="1.3" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xml:lang="en"><front><journal-meta><journal-id journal-id-type="publisher-id">meat</journal-id><journal-title-group><journal-title xml:lang="en">Theory and practice of meat processing</journal-title><trans-title-group xml:lang="ru"><trans-title>Теория и практика переработки мяса</trans-title></trans-title-group></journal-title-group><issn pub-type="ppub">2414-438X</issn><issn pub-type="epub">2414-441X</issn><publisher><publisher-name>ФГБНУ «Федеральный научный центр пищевых систем им. В.М. Горбатова» РАН</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.21323/2414-438X-2023-8-4-273-281</article-id><article-id custom-type="elpub" pub-id-type="custom">meat-295</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="ru"><subject>Статьи</subject></subj-group></article-categories><title-group><article-title>Evaluation of approaches to increase the effectiveness of various disinfectants against biofilm communities of different ages</article-title><trans-title-group xml:lang="ru"><trans-title>Evaluation of approaches to increase the effectiveness of various disinfectants against biofilm communities of different ages</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0001-9265-5511</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Yushina</surname><given-names>Yu. K.</given-names></name><name name-style="western" xml:lang="en"><surname>Yushina</surname><given-names>Yu. K.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Yuliya K. Yushina, Doctor of Technical Sciences, Head of the Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–495–676–95–11 (402)</p></bio><bio xml:lang="en"><p>Yuliya K. Yushina, Doctor of Technical Sciences, Head of the Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–495–676–95–11 (402)</p></bio><email xlink:type="simple">yu.yushina@fncps.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0001-8545-6266</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Nasyrov</surname><given-names>N. A.</given-names></name><name name-style="western" xml:lang="en"><surname>Nasyrov</surname><given-names>N. A.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Nazarbay A. Nasyrov, Researcher, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–906–830–17–77</p></bio><bio xml:lang="en"><p>Nazarbay A. Nasyrov, Researcher, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–906–830–17–77</p></bio><email xlink:type="simple">n.nasyrov@fncps.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0009-0002-1236-0882</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Demkina</surname><given-names>E. V.</given-names></name><name name-style="western" xml:lang="en"><surname>Demkina</surname><given-names>E. V.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Elena V. Demkina, Candidate of Biological Sciences, Researcher, Laboratory of Microbial Survival</p><p>14, Leninsky Prospect, 119991, Moscow</p><p>Tel.: +7–499–135–12–29</p></bio><bio xml:lang="en"><p>Elena V. Demkina, Candidate of Biological Sciences, Researcher, Laboratory of Microbial Survival</p><p>14, Leninsky Prospect, 119991, Moscow</p><p>Tel.: +7–499–135–12–29</p></bio><email xlink:type="simple">elenademkina@mail.ru</email><xref ref-type="aff" rid="aff-2"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-5048-9321</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Zaiko</surname><given-names>E. V.</given-names></name><name name-style="western" xml:lang="en"><surname>Zaiko</surname><given-names>E. V.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Elena. V. Zaiko, Candidate of Technical Sciences, Junior Research Assistant, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–495–676–95–11 (407)</p></bio><bio xml:lang="en"><p>Elena. V. Zaiko, Candidate of Technical Sciences, Junior Research Assistant, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–495–676–95–11 (407)</p></bio><email xlink:type="simple">e.zaiko@fncps.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-1344-823X</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Reshchikov</surname><given-names>M. D.</given-names></name><name name-style="western" xml:lang="en"><surname>Reshchikov</surname><given-names>M. D.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Maksim D. Reshchikov, Senior Laboratory Assistant, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–962–959–32–22</p></bio><bio xml:lang="en"><p>Maksim D. Reshchikov, Senior Laboratory Assistant, Laboratory of Hygiene of Production and Microbiology</p><p>26, Talalikhina str., 109316, Moscow</p><p>Tel.: +7–962–959–32–22</p></bio><email xlink:type="simple">reshchikov@fncps.ru</email><xref ref-type="aff" rid="aff-1"/></contrib></contrib-group><aff-alternatives id="aff-1"><aff xml:lang="ru"><institution>V. M. Gorbatov Federal Research Center for Food Systems</institution><country>Россия</country></aff><aff xml:lang="en"><institution>V. M. Gorbatov Federal Research Center for Food Systems</institution><country>Russian Federation</country></aff></aff-alternatives><aff-alternatives id="aff-2"><aff xml:lang="ru"><institution>Research Center “Fundamentals of Biotechnology” of RAS</institution><country>Россия</country></aff><aff xml:lang="en"><institution>Research Center “Fundamentals of Biotechnology” of RAS</institution><country>Russian Federation</country></aff></aff-alternatives><pub-date pub-type="collection"><year>2023</year></pub-date><pub-date pub-type="epub"><day>10</day><month>01</month><year>2024</year></pub-date><volume>8</volume><issue>4</issue><fpage>273</fpage><lpage>281</lpage><permissions><copyright-statement>Copyright &amp;#x00A9; Yushina Y.K., Nasyrov N.A., Demkina E.V., Zaiko E.V., Reshchikov M.D., 2024</copyright-statement><copyright-year>2024</copyright-year><copyright-holder xml:lang="ru">Yushina Y.K., Nasyrov N.A., Demkina E.V., Zaiko E.V., Reshchikov M.D.</copyright-holder><copyright-holder xml:lang="en">Yushina Y.K., Nasyrov N.A., Demkina E.V., Zaiko E.V., Reshchikov M.D.</copyright-holder><license xml:lang="ru" license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>Данная работа распространяется под лицензией Creative Commons Attribution 4.0.</license-p></license><license xml:lang="en" license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>This work is licensed under a Creative Commons Attribution 4.0 License.</license-p></license></permissions><self-uri xlink:href="https://www.meatjournal.ru/jour/article/view/295">https://www.meatjournal.ru/jour/article/view/295</self-uri><abstract><p>Disinfectants are used as the main agents against microorganisms circulating on the surfaces of food enterprises. However, the adaptive ability of microorganisms to form biofilms complicates the process of surface cleaning and reduces the effectiveness of disinfectants. Modern disinfectants act against freely circulating microflora, but it is known that they are not always effective against biofilms. The purpose of this study was to investigate effective disinfectant compositions with bactericidal effect on binary bacterial biofilms of different ages. The article describes the effects of disinfectants based on chlorine, peracetic acid and quaternary ammonium compounds with enzymes in concentrations recommended by the manufacturer and increased several times on Salmonella 38, Brochothrix thermosphacta 2726 and Staphylococcus equorum 2736 planktonic cultures and binary biofilms. Binary biofilms of different ages (2 and 9 days old) were exposed to disinfectants with various active ingredients in combination with adjuvants, i. e. hydrogen peroxide 6% and various concentrations of isopropyl alcohol (30%). All products in concentrations recommended by the manufacturer did not have a disinfectant effect against the studied biofilm cultures. As a result of the work, it was found that the most effective disinfectants against multispecies biofilms were quaternary ammonium compounds in combination with enzymes and chlorine in combination with isopropyl alcohol (30%). The results obtained allow to expand knowledge about effective methods for controlling biofilms.</p></abstract><trans-abstract xml:lang="ru"><p>Disinfectants are used as the main agents against microorganisms circulating on the surfaces of food enterprises. However, the adaptive ability of microorganisms to form biofilms complicates the process of surface cleaning and reduces the effectiveness of disinfectants. Modern disinfectants act against freely circulating microflora, but it is known that they are not always effective against biofilms. The purpose of this study was to investigate effective disinfectant compositions with bactericidal effect on binary bacterial biofilms of different ages. The article describes the effects of disinfectants based on chlorine, peracetic acid and quaternary ammonium compounds with enzymes in concentrations recommended by the manufacturer and increased several times on Salmonella 38, Brochothrix thermosphacta 2726 and Staphylococcus equorum 2736 planktonic cultures and binary biofilms. Binary biofilms of different ages (2 and 9 days old) were exposed to disinfectants with various active ingredients in combination with adjuvants, i. e. hydrogen peroxide 6% and various concentrations of isopropyl alcohol (30%). All products in concentrations recommended by the manufacturer did not have a disinfectant effect against the studied biofilm cultures. As a result of the work, it was found that the most effective disinfectants against multispecies biofilms were quaternary ammonium compounds in combination with enzymes and chlorine in combination with isopropyl alcohol (30%). The results obtained allow to expand knowledge about effective methods for controlling biofilms.</p></trans-abstract><kwd-group xml:lang="ru"><kwd>multispecies biofilms</kwd><kwd>microorganisms</kwd><kwd>disinfection</kwd><kwd>resistance</kwd><kwd>meat industry</kwd><kwd>sanitation</kwd></kwd-group><kwd-group xml:lang="en"><kwd>multispecies biofilms</kwd><kwd>microorganisms</kwd><kwd>disinfection</kwd><kwd>resistance</kwd><kwd>meat industry</kwd><kwd>sanitation</kwd></kwd-group><funding-group><funding-statement xml:lang="ru">The article was published as part of the research topic No. FNEN2019–0007 of the state assignment of the V. M. Gorbatov Federal Research Center for Food Systems of RAS.</funding-statement><funding-statement xml:lang="en">The article was published as part of the research topic No. FNEN2019–0007 of the state assignment of the V. M. Gorbatov Federal Research Center for Food Systems of RAS.</funding-statement></funding-group></article-meta></front><back><ref-list><title>References</title><ref id="cit1"><label>1</label><citation-alternatives><mixed-citation xml:lang="ru">Corcoran, M., Morris, D., De Lappe, N., O’Connor, J., Lalor, P., Dockery, P. et al. (2014). Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Applied and Environmental Microbiology, 80(4), 1507–1514. https://doi.org/10.1128/AEM.03109-13</mixed-citation><mixed-citation xml:lang="en">Corcoran, M., Morris, D., De Lappe, N., O’Connor, J., Lalor, P., Dockery, P. et al. (2014). Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Applied and Environmental Microbiology, 80(4), 1507–1514. https://doi.org/10.1128/AEM.03109-13</mixed-citation></citation-alternatives></ref><ref id="cit2"><label>2</label><citation-alternatives><mixed-citation xml:lang="ru">Martínez-Suárez, J.V., Ortiz, S., López-Alonso, V. (2016). Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments. Frontiers in Microbiology, 7, Article 638. https://doi.org/10.3389/fmicb.2016.00638</mixed-citation><mixed-citation xml:lang="en">Martínez-Suárez, J.V., Ortiz, S., López-Alonso, V. (2016). Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments. Frontiers in Microbiology, 7, Article 638. https://doi.org/10.3389/fmicb.2016.00638</mixed-citation></citation-alternatives></ref><ref id="cit3"><label>3</label><citation-alternatives><mixed-citation xml:lang="ru">Gosling, R.J., Mawhinney, I., Vaughan, K., Davies, R.H., Smith, R.P. (2017). Efficacy of disinfectants and detergents intended for a pig farm environment where Salmonella is present. Veterinary Microbiology, 204, 46–53. https://doi.org/10.1016/j.vetmic.2017.04.004</mixed-citation><mixed-citation xml:lang="en">Gosling, R.J., Mawhinney, I., Vaughan, K., Davies, R.H., Smith, R.P. (2017). Efficacy of disinfectants and detergents intended for a pig farm environment where Salmonella is present. Veterinary Microbiology, 204, 46–53. https://doi.org/10.1016/j.vetmic.2017.04.004</mixed-citation></citation-alternatives></ref><ref id="cit4"><label>4</label><citation-alternatives><mixed-citation xml:lang="ru">Giaouris, E., Heir, E., Hébraud, M., Chorianopoulos, N., Langsrud, S., Møretrø, T. et al. (2013). Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Science, 97(3), 298–309. https://doi.org/10.1016/j.meatsci.2013.05.023</mixed-citation><mixed-citation xml:lang="en">Giaouris, E., Heir, E., Hébraud, M., Chorianopoulos, N., Langsrud, S., Møretrø, T. et al. (2013). Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Science, 97(3), 298–309. https://doi.org/10.1016/j.meatsci.2013.05.023</mixed-citation></citation-alternatives></ref><ref id="cit5"><label>5</label><citation-alternatives><mixed-citation xml:lang="ru">Chmielewski, R.A.N., Frank, J.-F. (2003). Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2(1), 22–32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x</mixed-citation><mixed-citation xml:lang="en">Chmielewski, R.A.N., Frank, J.-F. (2003). Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2(1), 22–32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x</mixed-citation></citation-alternatives></ref><ref id="cit6"><label>6</label><citation-alternatives><mixed-citation xml:lang="ru">Zhao, X., Zhao, F., Wang, J., Zhong, N. (2017). Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Advances, 7, 36670–36683. https://doi.org/10.1039/c7ra02497e</mixed-citation><mixed-citation xml:lang="en">Zhao, X., Zhao, F., Wang, J., Zhong, N. (2017). Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Advances, 7, 36670–36683. https://doi.org/10.1039/c7ra02497e</mixed-citation></citation-alternatives></ref><ref id="cit7"><label>7</label><citation-alternatives><mixed-citation xml:lang="ru">Bremer, P.J., Monk. I., Osborne, C.M. (2001). Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. Journal of Food Protection, 64(9), 1369–1376. https://doi.org/10.4315/0362-028X-64.9.1369</mixed-citation><mixed-citation xml:lang="en">Bremer, P.J., Monk. I., Osborne, C.M. (2001). Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. Journal of Food Protection, 64(9), 1369–1376. https://doi.org/10.4315/0362-028X-64.9.1369</mixed-citation></citation-alternatives></ref><ref id="cit8"><label>8</label><citation-alternatives><mixed-citation xml:lang="ru">Bridier, A., del Pilar Sanchez-Vizuete, M., Le Coq, D., Aymerich, S., Meylheuc, T., Maillard, J.-Y. et al. (2012). Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS One, 7(9), Article e44506. https://doi.org/10.1371/journal.pone.0044506</mixed-citation><mixed-citation xml:lang="en">Bridier, A., del Pilar Sanchez-Vizuete, M., Le Coq, D., Aymerich, S., Meylheuc, T., Maillard, J.-Y. et al. (2012). Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS One, 7(9), Article e44506. https://doi.org/10.1371/journal.pone.0044506</mixed-citation></citation-alternatives></ref><ref id="cit9"><label>9</label><citation-alternatives><mixed-citation xml:lang="ru">Burmølle, M., Webb, J.S., Rao, D., Hansen, L.H., Sørensen, S.J., Kjelleberg, S. (2006). Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Applied and Environmental Microbiology, 72(6), 3916–3923. https://doi.org/10.1128/AEM.03022-05</mixed-citation><mixed-citation xml:lang="en">Burmølle, M., Webb, J.S., Rao, D., Hansen, L.H., Sørensen, S.J., Kjelleberg, S. (2006). Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Applied and Environmental Microbiology, 72(6), 3916–3923. https://doi.org/10.1128/AEM.03022-05</mixed-citation></citation-alternatives></ref><ref id="cit10"><label>10</label><citation-alternatives><mixed-citation xml:lang="ru">Lee, K.W.K., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S., Rice, S.A. (2014). Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. The ISME Journal, 8(4), 894–907. https://doi.org/10.1038/ismej.2013.194</mixed-citation><mixed-citation xml:lang="en">Lee, K.W.K., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S., Rice, S.A. (2014). Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. The ISME Journal, 8(4), 894–907. https://doi.org/10.1038/ismej.2013.194</mixed-citation></citation-alternatives></ref><ref id="cit11"><label>11</label><citation-alternatives><mixed-citation xml:lang="ru">Uhlich, G.A., Rogers, D.P., Mosier, D.A. (2010). Escherichia coli serotype O157: H7 retention on solid surfaces and peroxide resistance is enhanced by dual-strain biofilm formation. Foodborne Pathogens and Disease, 7(8), 935–943. https://doi.org/10.1089/fpd.2009.0503</mixed-citation><mixed-citation xml:lang="en">Uhlich, G.A., Rogers, D.P., Mosier, D.A. (2010). Escherichia coli serotype O157: H7 retention on solid surfaces and peroxide resistance is enhanced by dual-strain biofilm formation. Foodborne Pathogens and Disease, 7(8), 935–943. https://doi.org/10.1089/fpd.2009.0503</mixed-citation></citation-alternatives></ref><ref id="cit12"><label>12</label><citation-alternatives><mixed-citation xml:lang="ru">van der Veen, S., Abee, T. (2011). Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. International Journal of Food Microbiology, 144(3), 421–431. https://doi.org/10.1016/j.ijfoodmicro.2010.10.029</mixed-citation><mixed-citation xml:lang="en">van der Veen, S., Abee, T. (2011). Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. International Journal of Food Microbiology, 144(3), 421–431. https://doi.org/10.1016/j.ijfoodmicro.2010.10.029</mixed-citation></citation-alternatives></ref><ref id="cit13"><label>13</label><citation-alternatives><mixed-citation xml:lang="ru">Wang, R. (2019). Biofilms and meat safety: A minireview. Journal of Food Protection, 82(1), 120–127. https://doi.org/10.4315/0362-028X.JFP-18-311</mixed-citation><mixed-citation xml:lang="en">Wang, R. (2019). Biofilms and meat safety: A minireview. Journal of Food Protection, 82(1), 120–127. https://doi.org/10.4315/0362-028X.JFP-18-311</mixed-citation></citation-alternatives></ref><ref id="cit14"><label>14</label><citation-alternatives><mixed-citation xml:lang="ru">Wang, R., Kalchayanand, N., Schmidt, J.W., 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), 1513–1522. https://doi.org/10.4315/0362-028X.JFP-13-077</mixed-citation><mixed-citation xml:lang="en">Wang, R., Kalchayanand, N., Schmidt, J.W., 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), 1513–1522. https://doi.org/10.4315/0362-028X.JFP-13-077</mixed-citation></citation-alternatives></ref><ref id="cit15"><label>15</label><citation-alternatives><mixed-citation xml:lang="ru">Marouani-Gadri, N., Augier, G., Carpentier, B. (2009). Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection-influence of isolated strains on biofilm formation by Sakaï and EDL 933 E. coli O157: H7. International Journal of Food Microbiology, 133(1–2), 62–67. https://doi.org/10.1016/j.ijfoodmicro.2009.04.028</mixed-citation><mixed-citation xml:lang="en">Marouani-Gadri, N., Augier, G., Carpentier, B. (2009). Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection-influence of isolated strains on biofilm formation by Sakaï and EDL 933 E. coli O157: H7. International Journal of Food Microbiology, 133(1–2), 62–67. https://doi.org/10.1016/j.ijfoodmicro.2009.04.028</mixed-citation></citation-alternatives></ref><ref id="cit16"><label>16</label><citation-alternatives><mixed-citation xml:lang="ru">Rivera-Betancourt, M., Shackelford, S.D., Arthur, T.M., Westmoreland, K.E., Bellinger, G., Rossman, M. et al. (2004). Prevalence of Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella in two geographically distant commercial beef processing plants in the United States. Journal of Food Protection, 67(2), 295–302. https://doi.org/10.4315/0362-028x-67.2.295</mixed-citation><mixed-citation xml:lang="en">Rivera-Betancourt, M., Shackelford, S.D., Arthur, T.M., Westmoreland, K.E., Bellinger, G., Rossman, M. et al. (2004). Prevalence of Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella in two geographically distant commercial beef processing plants in the United States. Journal of Food Protection, 67(2), 295–302. https://doi.org/10.4315/0362-028x-67.2.295</mixed-citation></citation-alternatives></ref><ref id="cit17"><label>17</label><citation-alternatives><mixed-citation xml:lang="ru">González-Rivas, F., Ripolles-Avila, C., Fontecha-Umaña, F., Ríos-Castillo, A.G., Rodríguez-Jerez, J.J. (2018). Biofilms in the spotlight: Detection, quantification, and removal methods. Comprehensive Reviews in Food Science and Food Safety, 17(5), 1261–1276. https://doi.org/10.1111/1541-4337.12378</mixed-citation><mixed-citation xml:lang="en">González-Rivas, F., Ripolles-Avila, C., Fontecha-Umaña, F., Ríos-Castillo, A.G., Rodríguez-Jerez, J.J. (2018). Biofilms in the spotlight: Detection, quantification, and removal methods. Comprehensive Reviews in Food Science and Food Safety, 17(5), 1261–1276. https://doi.org/10.1111/1541-4337.12378</mixed-citation></citation-alternatives></ref><ref id="cit18"><label>18</label><citation-alternatives><mixed-citation xml:lang="ru">Ripolles-Avila, C., Hascoët, A.S., Guerrero-Navarro, A.E., Rodríguez-Jerez, J.J. (2018). Establishment of incubation conditions to optimize the in vitro formation of mature Listeria monocytogenes biofilms on food-contact surfaces. Food Control, 92, 240–248. https://doi.org/10.1016/j.foodcont.2018.04.054</mixed-citation><mixed-citation xml:lang="en">Ripolles-Avila, C., Hascoët, A.S., Guerrero-Navarro, A.E., Rodríguez-Jerez, J.J. (2018). Establishment of incubation conditions to optimize the in vitro formation of mature Listeria monocytogenes biofilms on food-contact surfaces. Food Control, 92, 240–248. https://doi.org/10.1016/j.foodcont.2018.04.054</mixed-citation></citation-alternatives></ref><ref id="cit19"><label>19</label><citation-alternatives><mixed-citation xml:lang="ru">Wang, R., Kalchayanand, N., King, D.A., Luedtke, B.E., Bosilevac, J.M., Arthur, T.M. (2014). Biofilm formation and sanitizer resistance of Escherichia coli O157: H7 strains isolated from “high event period” meat contamination. Journal of Food Protection, 77(11), 1982–1987. https://doi.org/10.4315/0362-028X.JFP-14-253</mixed-citation><mixed-citation xml:lang="en">Wang, R., Kalchayanand, N., King, D.A., Luedtke, B.E., Bosilevac, J.M., Arthur, T.M. (2014). Biofilm formation and sanitizer resistance of Escherichia coli O157: H7 strains isolated from “high event period” meat contamination. Journal of Food Protection, 77(11), 1982–1987. https://doi.org/10.4315/0362-028X.JFP-14-253</mixed-citation></citation-alternatives></ref><ref id="cit20"><label>20</label><citation-alternatives><mixed-citation xml:lang="ru">Wang, R., Zhou, Y., Kalchayanand, N., Harhay, D.M., Wheeler, T.L. (2020). Effectiveness and functional mechanism of a multicomponent sanitizer against biofilms formed by Escherichia coli O157: H7 and five salmonella serotypes prevalent in the meat industry. Journal of Food Protection, 83(4), 568–575. https://doi.org/10.4315/0362-028X.JFP-19-393</mixed-citation><mixed-citation xml:lang="en">Wang, R., Zhou, Y., Kalchayanand, N., Harhay, D.M., Wheeler, T.L. (2020). Effectiveness and functional mechanism of a multicomponent sanitizer against biofilms formed by Escherichia coli O157: H7 and five salmonella serotypes prevalent in the meat industry. Journal of Food Protection, 83(4), 568–575. https://doi.org/10.4315/0362-028X.JFP-19-393</mixed-citation></citation-alternatives></ref><ref id="cit21"><label>21</label><citation-alternatives><mixed-citation xml:lang="ru">Vázquez-Sánchez, D., Cabo, M.L., Ibusquiza, P.S., Rodríguez-Herrera, J.J. (2014). Biofilm-forming ability and resistance to industrial disinfectants of Staphylococcus aureus isolated from fishery products. Food Control, 39, 8–16. https://doi.org/10.1016/j.foodcont.2013.09.029</mixed-citation><mixed-citation xml:lang="en">Vázquez-Sánchez, D., Cabo, M.L., Ibusquiza, P.S., Rodríguez-Herrera, J.J. (2014). Biofilm-forming ability and resistance to industrial disinfectants of Staphylococcus aureus isolated from fishery products. Food Control, 39, 8–16. https://doi.org/10.1016/j.foodcont.2013.09.029</mixed-citation></citation-alternatives></ref><ref id="cit22"><label>22</label><citation-alternatives><mixed-citation xml:lang="ru">Mah, T.F., O’Toole, G.A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9(1), 34–39. https://doi.org/10.1016/s0966-842x(00)01913-2</mixed-citation><mixed-citation xml:lang="en">Mah, T.F., O’Toole, G.A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9(1), 34–39. https://doi.org/10.1016/s0966-842x(00)01913-2</mixed-citation></citation-alternatives></ref><ref id="cit23"><label>23</label><citation-alternatives><mixed-citation xml:lang="ru">Marić, S., Vraneš, J. (2007). Characteristics and significance of microbial biofilm formation. Periodicum Biologorum, 109(2), 115–121.</mixed-citation><mixed-citation xml:lang="en">Marić, S., Vraneš, J. (2007). Characteristics and significance of microbial biofilm formation. Periodicum Biologorum, 109(2), 115–121.</mixed-citation></citation-alternatives></ref><ref id="cit24"><label>24</label><citation-alternatives><mixed-citation xml:lang="ru">Beveridge, T.J., Makin, S.A., Kadurugamuwa, J.L., Li, Z. (1997). Interactions between biofilms and the environment. FEMS Microbiology Reviews, 20(3–4), 291–303. https://doi.org/10.1111/j.1574-6976.1997.tb00315.x</mixed-citation><mixed-citation xml:lang="en">Beveridge, T.J., Makin, S.A., Kadurugamuwa, J.L., Li, Z. (1997). Interactions between biofilms and the environment. FEMS Microbiology Reviews, 20(3–4), 291–303. https://doi.org/10.1111/j.1574-6976.1997.tb00315.x</mixed-citation></citation-alternatives></ref><ref id="cit25"><label>25</label><citation-alternatives><mixed-citation xml:lang="ru">Flemming, H.-C. (1993). Biofilms and environmental protection. Water Science and Technology, 27(7–8), 1–10. https://doi.org/10.2166/wst.1993.0528</mixed-citation><mixed-citation xml:lang="en">Flemming, H.-C. (1993). Biofilms and environmental protection. Water Science and Technology, 27(7–8), 1–10. https://doi.org/10.2166/wst.1993.0528</mixed-citation></citation-alternatives></ref><ref id="cit26"><label>26</label><citation-alternatives><mixed-citation xml:lang="ru">Ban, G.-H. Kang, D.-H. (2016). Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiology, 55, 47–54. https://doi.org/10.1016/j.fm.2015.11.003</mixed-citation><mixed-citation xml:lang="en">Ban, G.-H. Kang, D.-H. (2016). Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiology, 55, 47–54. https://doi.org/10.1016/j.fm.2015.11.003</mixed-citation></citation-alternatives></ref><ref id="cit27"><label>27</label><citation-alternatives><mixed-citation xml:lang="ru">Shi, X., Zhu, X. (2009). Biofilm formation and food safety in food industries. Trends in Food Science and Technology, 20(9), 407–413. https://doi.org/10.1016/j.tifs.2009.01.054</mixed-citation><mixed-citation xml:lang="en">Shi, X., Zhu, X. (2009). Biofilm formation and food safety in food industries. Trends in Food Science and Technology, 20(9), 407–413. https://doi.org/10.1016/j.tifs.2009.01.054</mixed-citation></citation-alternatives></ref><ref id="cit28"><label>28</label><citation-alternatives><mixed-citation xml:lang="ru">Doerscher, D.R., Lutz, T.L., Whisenant, S.J., Smith, K.R., Morris, C.A., Schroeder, C.M. (2015). Microbiological testing results of boneless and ground beef purchased for the national school lunch program, 2011 to 2014. Journal of Food Protection, 78(9), 1656–1663. https://doi.org/10.4315/0362-028X.JFP-15-101</mixed-citation><mixed-citation xml:lang="en">Doerscher, D.R., Lutz, T.L., Whisenant, S.J., Smith, K.R., Morris, C.A., Schroeder, C.M. (2015). Microbiological testing results of boneless and ground beef purchased for the national school lunch program, 2011 to 2014. Journal of Food Protection, 78(9), 1656–1663. https://doi.org/10.4315/0362-028X.JFP-15-101</mixed-citation></citation-alternatives></ref><ref id="cit29"><label>29</label><citation-alternatives><mixed-citation xml:lang="ru">Plakunov, V.K., Mart’yanov, S.V., Teteneva, N.A., Zhurina, M.V. (2016). A universal method for quantitative characterization of growth and metabolic activity of microbial biofilms in static models. Microbiology, 85(4), 509–513. https://doi.org/10.1134/S0026261716040147</mixed-citation><mixed-citation xml:lang="en">Plakunov, V.K., Mart’yanov, S.V., Teteneva, N.A., Zhurina, M.V. (2016). A universal method for quantitative characterization of growth and metabolic activity of microbial biofilms in static models. Microbiology, 85(4), 509–513. https://doi.org/10.1134/S0026261716040147</mixed-citation></citation-alternatives></ref><ref id="cit30"><label>30</label><citation-alternatives><mixed-citation xml:lang="ru">Nikolaev, Y.A., Tutel’yan, A.V., Loiko, N.G., Buck, J., Sidorenko, S.V., Lazareva, I. et al. (2020). The use of 4-Hexylresorcinol as antibiotic adjuvant. PLoS One, 15(9), Article e0239147. https://doi.org/10.1371/journal.pone.023914</mixed-citation><mixed-citation xml:lang="en">Nikolaev, Y.A., Tutel’yan, A.V., Loiko, N.G., Buck, J., Sidorenko, S.V., Lazareva, I. et al. (2020). The use of 4-Hexylresorcinol as antibiotic adjuvant. PLoS One, 15(9), Article e0239147. https://doi.org/10.1371/journal.pone.023914</mixed-citation></citation-alternatives></ref><ref id="cit31"><label>31</label><citation-alternatives><mixed-citation xml:lang="ru">Shemyakin I. G., Manzenyuk, O. Yu., El-Registan, G.I., Firstova, V.V., Kombarova, T.I., Gneusheva, T. Yu. et al. (2021). Effect of 4-Hexylresorcinol on the efficiency of antibiotic treatment of experimental sepsis caused by antibiotic-resistant Klebsiella Pneumoniae strain in mice. Bulletin of Experimental Biology and Medicine, 171(4), 458–460. https://doi.org/10.1007/s10517-021-05249-6</mixed-citation><mixed-citation xml:lang="en">Shemyakin I. G., Manzenyuk, O. Yu., El-Registan, G.I., Firstova, V.V., Kombarova, T.I., Gneusheva, T. Yu. et al. (2021). Effect of 4-Hexylresorcinol on the efficiency of antibiotic treatment of experimental sepsis caused by antibiotic-resistant Klebsiella Pneumoniae strain in mice. Bulletin of Experimental Biology and Medicine, 171(4), 458–460. https://doi.org/10.1007/s10517-021-05249-6</mixed-citation></citation-alternatives></ref><ref id="cit32"><label>32</label><citation-alternatives><mixed-citation xml:lang="ru">Roy, R., Tiwari, M., Donelli, G., Tiwari, V. (2018). Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence, 9(1), 522–554. https://doi.org/10.1080%2F21505594.2017.1313372</mixed-citation><mixed-citation xml:lang="en">Roy, R., Tiwari, M., Donelli, G., Tiwari, V. (2018). Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence, 9(1), 522–554. https://doi.org/10.1080%2F21505594.2017.1313372</mixed-citation></citation-alternatives></ref><ref id="cit33"><label>33</label><citation-alternatives><mixed-citation xml:lang="ru">Verderosa, A.D., Totsika, M, Fairfull-Smith, K.E. (2019). Bacterial biofilm eradication agents: A current review. Frontiers in Chemistry, 28(7), 824. https://doi.org/10.3389/fchem.2019.00824</mixed-citation><mixed-citation xml:lang="en">Verderosa, A.D., Totsika, M, Fairfull-Smith, K.E. (2019). Bacterial biofilm eradication agents: A current review. Frontiers in Chemistry, 28(7), 824. https://doi.org/10.3389/fchem.2019.00824</mixed-citation></citation-alternatives></ref><ref id="cit34"><label>34</label><citation-alternatives><mixed-citation xml:lang="ru">Denyer, S.P., Hugo, W.B., Harding, V.D. (1985). Synergy in preservative combinations. International Journal of Pharmaceutics, 25(3), 245–253. https://doi.org/10.1016/0378-5173(85)90166-8</mixed-citation><mixed-citation xml:lang="en">Denyer, S.P., Hugo, W.B., Harding, V.D. (1985). Synergy in preservative combinations. International Journal of Pharmaceutics, 25(3), 245–253. https://doi.org/10.1016/0378-5173(85)90166-8</mixed-citation></citation-alternatives></ref><ref id="cit35"><label>35</label><citation-alternatives><mixed-citation xml:lang="ru">Lambert, R.J.W., Johnston, M.D., Hanlon, G.W., Denyer, S.P. (2003). Theory of antimicrobial combinations: biocide mixtures — synergy or addition? Journal of Applied Microbiology, 94(4), 747–759. https://doi.org/10.1046/j.1365-2672.2003.01908.x</mixed-citation><mixed-citation xml:lang="en">Lambert, R.J.W., Johnston, M.D., Hanlon, G.W., Denyer, S.P. (2003). Theory of antimicrobial combinations: biocide mixtures — synergy or addition? Journal of Applied Microbiology, 94(4), 747–759. https://doi.org/10.1046/j.1365-2672.2003.01908.x</mixed-citation></citation-alternatives></ref><ref id="cit36"><label>36</label><citation-alternatives><mixed-citation xml:lang="ru">McDonnell, G., Russell, A.D. (1999). Antiseptics and disinfectants: activity, action, and resistance. Clinical Microbiology Reviews, 12(1), 47–79. https://doi.org/10.1128/CMR.12.1.147</mixed-citation><mixed-citation xml:lang="en">McDonnell, G., Russell, A.D. (1999). Antiseptics and disinfectants: activity, action, and resistance. Clinical Microbiology Reviews, 12(1), 47–79. https://doi.org/10.1128/CMR.12.1.147</mixed-citation></citation-alternatives></ref><ref id="cit37"><label>37</label><citation-alternatives><mixed-citation xml:lang="ru">Fan, L., Muhammad, A.I., Ismail, B.B., Liu, D. (2021). Sonodynamic antimicrobial chemotherapy: An emerging alternative strategy for microbial inactivation. Ultrasonics Sonochemistry, 75, Article 105591. https://doi.org/10.1016/j.ultsonch.2021.105591</mixed-citation><mixed-citation xml:lang="en">Fan, L., Muhammad, A.I., Ismail, B.B., Liu, D. (2021). Sonodynamic antimicrobial chemotherapy: An emerging alternative strategy for microbial inactivation. Ultrasonics Sonochemistry, 75, Article 105591. https://doi.org/10.1016/j.ultsonch.2021.105591</mixed-citation></citation-alternatives></ref><ref id="cit38"><label>38</label><citation-alternatives><mixed-citation xml:lang="ru">Ciecholewska-Juśko, D., Żywicka, A., Junka, A., Woroszyło, M., Wardach, M., Chodaczek, G. et al. (2022). The effects of rotating magnetic field and antiseptic on in vitro pathogenic biofilm and its milieu. Scientific Reports, 12(1), Article 8836. https://doi.org/10.1038/s41598-022-12840-y</mixed-citation><mixed-citation xml:lang="en">Ciecholewska-Juśko, D., Żywicka, A., Junka, A., Woroszyło, M., Wardach, M., Chodaczek, G. et al. (2022). The effects of rotating magnetic field and antiseptic on in vitro pathogenic biofilm and its milieu. Scientific Reports, 12(1), Article 8836. https://doi.org/10.1038/s41598-022-12840-y</mixed-citation></citation-alternatives></ref><ref id="cit39"><label>39</label><citation-alternatives><mixed-citation xml:lang="ru">Orazi, G., Ruoff, K.L., O’Toole, G.A. (2019). Pseudomonas aeruginosa increases the sensitivity of biofilm-grown Staphylococcus aureus to membrane-targeting antiseptics and antibiotics. mBio, 10(4), Article e01501–19. https://doi.org/10.1128/mBio.01501-19</mixed-citation><mixed-citation xml:lang="en">Orazi, G., Ruoff, K.L., O’Toole, G.A. (2019). Pseudomonas aeruginosa increases the sensitivity of biofilm-grown Staphylococcus aureus to membrane-targeting antiseptics and antibiotics. mBio, 10(4), Article e01501–19. https://doi.org/10.1128/mBio.01501-19</mixed-citation></citation-alternatives></ref><ref id="cit40"><label>40</label><citation-alternatives><mixed-citation xml:lang="ru">Mehta, K.C., Dargad, R.R., Borade, D.M., Swami, O.C. (2014). Burden of antibiotic resistance in common infectious diseases: role of antibiotic combination therapy. Journal of Clinical and Diagnostic Research, 8(6), ME05–ME08. https://doi.org/10.7860/JCDR/2014/8778.4489</mixed-citation><mixed-citation xml:lang="en">Mehta, K.C., Dargad, R.R., Borade, D.M., Swami, O.C. (2014). Burden of antibiotic resistance in common infectious diseases: role of antibiotic combination therapy. Journal of Clinical and Diagnostic Research, 8(6), ME05–ME08. https://doi.org/10.7860/JCDR/2014/8778.4489</mixed-citation></citation-alternatives></ref><ref id="cit41"><label>41</label><citation-alternatives><mixed-citation xml:lang="ru">Alpatova, N.A., Avdeeva, Z.I., Lysikova, S.L., Golovinskaya, O.V., Gayderova, L.A. (2020). General characteristics of adjuvants and their mechanism of action (Part 1). BIOpreparations, Prevention, Diagnostics, Treatment, 20(4), 245–256. https://doi.org/10.30895/2221-996X-2020-20-4-245-256 (In Russian)</mixed-citation><mixed-citation xml:lang="en">Alpatova, N.A., Avdeeva, Z.I., Lysikova, S.L., Golovinskaya, O.V., Gayderova, L.A. (2020). General characteristics of adjuvants and their mechanism of action (Part 1). BIOpreparations, Prevention, Diagnostics, Treatment, 20(4), 245–256. https://doi.org/10.30895/2221-996X-2020-20-4-245-256 (In Russian)</mixed-citation></citation-alternatives></ref><ref id="cit42"><label>42</label><citation-alternatives><mixed-citation xml:lang="ru">Demkina, E.V., Ilicheva, E.A., El-Registan, G.I., Pankratov, T.A., Yushina, Y.K., Semenova, A.A. et al. (2023). New approach to improving the efficiency of disinfectants against biofilms. Coatings, 13(3), Article 582. https://doi.org/10.3390/coatings13030582</mixed-citation><mixed-citation xml:lang="en">Demkina, E.V., Ilicheva, E.A., El-Registan, G.I., Pankratov, T.A., Yushina, Y.K., Semenova, A.A. et al. (2023). New approach to improving the efficiency of disinfectants against biofilms. Coatings, 13(3), Article 582. https://doi.org/10.3390/coatings13030582</mixed-citation></citation-alternatives></ref><ref id="cit43"><label>43</label><citation-alternatives><mixed-citation xml:lang="ru">Li, Q., Liu, L., Guo, A., Zhang, X., Liu, W., Ruan, Y. (2021). Formation of multispecies biofilms and their resistance to disinfectants in food processing environments: A review. Journal of Food Protection, 84(12), 2071–2083. https://doi.org/10.4315/JFP-21-071</mixed-citation><mixed-citation xml:lang="en">Li, Q., Liu, L., Guo, A., Zhang, X., Liu, W., Ruan, Y. (2021). Formation of multispecies biofilms and their resistance to disinfectants in food processing environments: A review. Journal of Food Protection, 84(12), 2071–2083. https://doi.org/10.4315/JFP-21-071</mixed-citation></citation-alternatives></ref></ref-list><fn-group><fn fn-type="conflict"><p>The authors declare that there are no conflicts of interest present.</p></fn></fn-group></back></article>
