{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T22:42:31Z","timestamp":1791931351462,"version":"4.3.4"},"reference-count":95,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2025,1,3]],"date-time":"2025-01-03T00:00:00Z","timestamp":1735862400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Higher Education of the Russian Federation","award":["124020500028-4"],"award-info":[{"award-number":["124020500028-4"]}]},{"name":"Ministry of Science and Higher Education of the Russian Federation","award":["C-26\/542"],"award-info":[{"award-number":["C-26\/542"]}]},{"name":"Development of new detergent-disinfectant compositions\/solutions that are promising for use in a complex of sanitary and anti-epidemic measures in medical organizations","award":["124020500028-4"],"award-info":[{"award-number":["124020500028-4"]}]},{"name":"Development of new detergent-disinfectant compositions\/solutions that are promising for use in a complex of sanitary and anti-epidemic measures in medical organizations","award":["C-26\/542"],"award-info":[{"award-number":["C-26\/542"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The widespread use of disinfectants and antiseptics has led to the emergence of nosocomial pathogens that are less sensitive to these agents, which in combination with multidrug resistance (MDR) can pose a significant epidemiologic risk. We investigated the susceptibility of nosocomial Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus to a 0.05% chlorhexidine (CHX) solution and a biocidal S7 composite solution based on CHX (0.07%) and benzalkonium chloride (BAC, 0.055%). The prevalence of efflux pump genes associated with biocide resistance and their relationship to antibiotic resistance was also determined. Both biocides were more effective against Gram-positive S. aureus than Gram-negative bacteria. The most resistant strains were P. aeruginosa strains, which were mainly killed by 0.0016% CHX and by 0.0000084% (CHX)\/0.0000066% (BAC) S7. The S7 bactericidal effect was observed on P. aeruginosa and S. aureus after 10 min, while the bactericidal effect of CHX was only observed after 30 min. qacE\u03941 and qacE efflux pump genes were prevalent among E. coli and K. pneumoniae, while mexB was more often detected in P. aeruginosa. norA, norB, mepA, mdeA, and sepA were prevalent in S. aureus. The observed prevalence of efflux pump genes highlights the potential problem whereby the sensitivity of bacteria to biocides could decline rapidly in the future.<\/jats:p>","DOI":"10.3390\/ijms26010355","type":"journal-article","created":{"date-parts":[[2025,1,3]],"date-time":"2025-01-03T05:02:02Z","timestamp":1735880522000},"page":"355","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["Nosocomial Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus: Sensitivity to Chlorhexidine-Based Biocides and Prevalence of Efflux Pump Genes"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2448-4823","authenticated-orcid":false,"given":"Marina V.","family":"Kuznetsova","sequence":"first","affiliation":[{"name":"Laboratory of Molecular Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614081 Perm, Russia"},{"name":"Department of Microbiology and Virology, Perm State Medical University Named After Academician E. A. Wagner, 614000 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Larisa Y.","family":"Nesterova","sequence":"additional","affiliation":[{"name":"Laboratory of Microorganisms\u2019 Adaptation, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614081 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4264-8177","authenticated-orcid":false,"given":"Veronika S.","family":"Mihailovskaya","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614081 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-3718-8602","authenticated-orcid":false,"given":"Polina A.","family":"Selivanova","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614081 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darja A.","family":"Kochergina","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614081 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina O.","family":"Karipova","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Virology, Perm State Medical University Named After Academician E. A. Wagner, 614000 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Igor V.","family":"Valtsifer","sequence":"additional","affiliation":[{"name":"Department of Multiphase Dispersed System, Institute of Technical Chemistry Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614013 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anastasia S.","family":"Averkina","sequence":"additional","affiliation":[{"name":"Department of Multiphase Dispersed System, Institute of Technical Chemistry Ural Branch Russian Academy of Sciences, Perm Federal Research Centre of Ural Branch of RAS, 614013 Perm, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0200-573X","authenticated-orcid":false,"given":"Marjanca","family":"Star\u010di\u010d Erjavec","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia"},{"name":"Department of Biology, Faculty of Natural Sciences and Mathematics, University of Maribor, 2000 Maribor, Slovenia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,1,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Nowakiewicz, A., Zi\u0119ba, P., Gnat, S., and Matuszewski, \u0141. (2020). Last Call for Replacement of Antimicrobials in Animal Production: Modern Challenges, Opportunities, and Potential Solutions. Antibiotics, 9.","DOI":"10.3390\/antibiotics9120883"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Urban-Chmiel, R., Marek, A., St\u0119pie\u0144-Py\u015bniak, D., Wieczorek, K., Dec, M., Nowaczek, A., and Osek, J. (2022). Antibiotic Resistance in Bacteria-A Review. Antibiotics, 11.","DOI":"10.3390\/antibiotics11081079"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Salam, M.A., Al-Amin, M.Y., Salam, M.T., Pawar, J.S., Akhter, N., Rabaan, A.A., and Alqumber, M.A.A. (2023). Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Healthcare, 11.","DOI":"10.20944\/preprints202305.0555.v1"},{"key":"ref_4","unstructured":"World Health Organization (WHO) (2002). Prevention of Hospital-Acquired Infections. A Practical Guide, World Health Organization. [2nd ed.]."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/j.apjtb.2017.01.019","article-title":"Nosocomial infections. Epidemiology, prevention, control and surveillance","volume":"7","author":"Khan","year":"2017","journal-title":"Asian Pac. J. Trop. Biomed."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"361","DOI":"10.26444\/aaem\/122629","article-title":"Nosocomial infections as one of the most important problems of healthcare system","volume":"28","author":"Kiersnowska","year":"2021","journal-title":"Ann. Agric. Environ. Med."},{"key":"ref_7","unstructured":"(2024). WHO Bacterial Priority Pathogens List, 2024: Bacterial Pathogens of Public Health Importance to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance, World Health Organization."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.ajic.2012.12.004","article-title":"Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings","volume":"41","author":"Otter","year":"2013","journal-title":"Am. J. Infect. Control."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Robakowska, M., Bronk, M., Tyra\u0144ska-Fobke, A., \u015al\u0119zak, D., Kraszewski, J., and Balwicki, \u0141. (2021). Patient Safety Related to Microbiological Contamination of the Environment of a Multi-Profile Clinical Hospital. Int. J. Environ. Res. Public. Health., 18.","DOI":"10.3390\/ijerph18073844"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"629","DOI":"10.3390\/applmicrobiol3030044","article-title":"Biofilm Formation, and Related Impacts on Healthcare, Food Processing and Packaging, Industrial Manufacturing, Marine Industries, and Sanitation\u2013A Review","volume":"3","author":"Shineh","year":"2023","journal-title":"Appl. Microbiol."},{"key":"ref_11","unstructured":"World Health Organization (WHO) (2022, June 01). WHO Model List of Essential Medicine. Available online: https:\/\/www.who.int\/publications\/i\/item\/WHO-MHP-HPS-EML-2021.02."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1128\/CMR.12.1.147","article-title":"Antiseptics and disinfectants: Activity, action, and resistance","volume":"12","author":"McDonnell","year":"1999","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"117074","DOI":"10.1016\/j.envpol.2021.117074","article-title":"Biocide-tolerance and antibiotic-resistance in community environments and risk of direct transfers to humans: Unintended consequences of community-wide surface disinfecting during COVID-19?","volume":"283","author":"Chen","year":"2021","journal-title":"Environ. Pollut."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Huang, L., Wu, C., Gao, H., Xu, C., Dai, M., Huang, L., Hao, H., Wang, X., and Cheng, G. (2022). Bacterial Multidrug Efflux Pumps at the Frontline of Antimicrobial Resistance: An Overview. Antibiotics, 11.","DOI":"10.3390\/antibiotics11040520"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1080\/17425255.2017.1251581","article-title":"Multidrug efflux pumps and their role in antibiotic and antiseptic resistance: A pharmacodynamic perspective","volume":"13","author":"Alibert","year":"2017","journal-title":"Expert Opin. Drug Metab. Toxicol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"AAC0106921","DOI":"10.1128\/AAC.01069-21","article-title":"Characterization of proteobacterial plasmid integron-encoded qac efflux pump sequence diversity and quaternary ammonium compound antiseptic selection in E. coli grown planktonically and as biofilms","volume":"65","author":"Slipski","year":"2021","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Abbood, H.M., Hijazi, K., and Gould, I.M. (2023). Chlorhexidine Resistance or Cross-Resistance, That Is the Question. Antibiotics, 12.","DOI":"10.3390\/antibiotics12050798"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Hrovat, K., Zupan\u010di\u010d, J.\u010c., Seme, K., and Avgu\u0161tin, J.A. (2023). QAC Resistance Genes in ESBL-Producing E. coli Isolated from Patients with Lower Respiratory Tract Infections in the Central Slovenia Region\u2014A 21-Year Survey. Trop. Med. Infect. Dis., 8.","DOI":"10.3390\/tropicalmed8050273"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Rakshit, P., Singh, A., Singh, R., and Banerjee, T. (2024). An in-depth study on survival mechanism of bacterial isolates in disinfectants within the hospital environment. Front. Cell. Infect. Microbiol., 14.","DOI":"10.3389\/fcimb.2024.1442914"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"136","DOI":"10.3390\/hygiene3020012","article-title":"Bacterial Contamination of Antiseptics, Disinfectants and Hand Hygiene Products in Healthcare Facilities in High-Income Countries: A Scoping Review","volume":"3","author":"Lompo","year":"2023","journal-title":"Hygiene"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.drup.2016.06.007","article-title":"Multidrug efflux pumps as main players in intrinsic and acquired resistance to antimicrobials","volume":"28","author":"Blanco","year":"2016","journal-title":"Drug Resist. Updates"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Laborda, P., Molin, S., Johansen, H.K., Mart\u00ednez, J.L., and Hernando-Amado, S. (2024). Role of bacterial multidrug efflux pumps during infection. World J. Microbiol. Biotechnol., 40.","DOI":"10.1007\/s11274-024-04042-7"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Cheung, H.-Y., Wong, M.M.-K., Cheung, S.-H., Liang, L.Y., Lam, Y.-W., and Chiu, S.-K. (2012). Differential Actions of Chlorhexidine on the Cell Wall of Bacillus subtilis and Escherichia coli. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0036659"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Maillard, J. (2018). Resistance of Bacteria to Biocides. Microbiol. Spectr., 6.","DOI":"10.1128\/microbiolspec.ARBA-0006-2017"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Morrissey, I., Oggioni, M.R., Knight, D., Curiao, T., Coque, T., Kalkanci, A., Martinez, J.L., and the BIOHYPO Consortium (2014). Evaluation of Epidemiological Cut-Off Values Indicates that Biocide Resistant Subpopulations Are Uncommon in Natural Isolates of Clinically-Relevant Microorganisms. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0086669"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Allaion, J.R., Barrionuevo, K.G., Grande Burgos, M.J., G\u00e1lvez, A., and Franco, B. (2022). Staphylococcus aureus from Minas Artisanal Cheeses: Biocide Tolerance, Antibiotic Resistance and Enterotoxin Genes. Appl. Sci., 12.","DOI":"10.3390\/app12031019"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"99e108","DOI":"10.1016\/j.jhin.2024.06.010","article-title":"The effects of chlorhexidine, povidone-iodine and vancomycin on growth and biofilms of pathogens that cause prosthetic joint infections: An in-vitro model","volume":"151","author":"Coles","year":"2024","journal-title":"J. Hosp. Infect."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"S312","DOI":"10.1016\/j.arth.2019.02.002","article-title":"Efficacy of Intraoperative Antiseptic Techniques in the Prevention of Periprosthetic Joint Infection: Superiority of Betadine","volume":"34","author":"Cichos","year":"2019","journal-title":"J. Arthroplast."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.ejps.2014.08.013","article-title":"Synthesis, surface and antimicrobial properties of some quaternary ammonium homochiral camphor sulfonamides","volume":"65","year":"2014","journal-title":"Eur. J. Pharm. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e119","DOI":"10.1016\/j.ajic.2013.05.002","article-title":"Chlorhexidine activity against bacterial biofilms","volume":"41","author":"Bonez","year":"2013","journal-title":"Am. J. Infect. Control."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e14298","DOI":"10.17795\/jjnpp-14298","article-title":"Chlorhexidine Digluconate Effects on Planktonic Growth and Biofilm Formation in Some Field Isolates of Animal Bacterial Pathogens","volume":"9","author":"Ebrahimi","year":"2014","journal-title":"Jundishapur J. Nat. Pharm. Prod."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"20254","DOI":"10.1073\/pnas.1317052110","article-title":"Transcriptomic and biochemical analyses identify a family of chlorhexidine efflux proteins","volume":"110","author":"Hassan","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e30464","DOI":"10.1016\/j.heliyon.2024.e30464","article-title":"Assessment of antimicrobial resistance, biofilm formation, and surface modification potential in hospital strains of Pseudomonas aeruginosa and Klebsiella pneumoniae","volume":"10","author":"Lordelo","year":"2024","journal-title":"Heliyon"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Mohapatra, S. (2017). Sterilization and Disinfection. Essent. Neuroanesthesia, 929\u2013944.","DOI":"10.1016\/B978-0-12-805299-0.00059-2"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Fink, R. (2023). Terpenoids as Natural Agents against Food-Borne Bacteria\u2014Evaluation of Biofilm Biomass versus Viability Reduction. Processes, 11.","DOI":"10.3390\/pr11010148"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1016\/j.envpol.2018.01.107","article-title":"Investigating antibiotics, antibiotic resistance genes, and microbial contaminants in groundwater in relation to the proximity of urban areas","volume":"236","author":"Szekeres","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1111\/j.1365-2958.1989.tb00153.x","article-title":"A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: Integrons","volume":"3","author":"Stokes","year":"1989","journal-title":"Mol. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2024","DOI":"10.1128\/AAC.46.6.2024-2028.2002","article-title":"Cloning of a cation efflux pump gene associated with chlorhexidine resistance in Klebsiella pneumoniae","volume":"46","author":"Fang","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.jhin.2012.03.003","article-title":"Klebsiella pneumoniae susceptibility to biocides and its association with cepA, qac\u0394E and qacE efflux pump genes and antibiotic resistance","volume":"81","author":"Abuzaid","year":"2012","journal-title":"J. Hospital infection."},{"key":"ref_40","first-page":"535","article-title":"qacE\u03941 gene frequency and biocide resistance in extended-spectrum \u03b2-lactamase producing Enterobacteriaceae clinical isolates","volume":"64","author":"Barrios","year":"2013","journal-title":"Rev. Investig. Cl\u00ednica"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"49","DOI":"10.31631\/2073-3046-2020-19-5-49-60","article-title":"Prevalence of Carbapenemase Genes, qacE, qacE\u03941 and cepA in Multidrug-Resistant Gram-Negative Bacteria with Different Susceptibility to Chlorhexidine","volume":"19","author":"Kosyakova","year":"2020","journal-title":"Epidemiol. Vaccinal Prev."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S0378-1097(99)00636-9","article-title":"Association of qacE and qacE\u03941 with multiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria","volume":"183","author":"Kucken","year":"2000","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5275","DOI":"10.1007\/s11033-021-06533-4","article-title":"Susceptibility to biocides and the prevalence of biocides resistance genes in clinical multidrug-resistant P. aeruginosa isolates from Hamadan","volume":"48","author":"Goodarzi","year":"2021","journal-title":"Iran. Mol. Biol. Rep."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.jhin.2007.01.012","article-title":"Distribution of the antiseptic-resistance genes qacEDelta1 in 331 clinical isolates of P. aeruginosa in China","volume":"66","author":"Wang","year":"2007","journal-title":"J. Hospital Infect."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Radmehr, M., Majid, M., Ghasemzadeh-Moghaddam, H., Azimian, A., and van Belkum, A. (2023). High Prevalence of Antiseptic Resistance Encoding Genes and Reduced Phenotypic Antiseptic Susceptibility Among Antibiotic-Resistant Pseudomonas aeruginosa Isolates. Jundishapur J. Microbiol., 16.","DOI":"10.5812\/jjm-135911"},{"key":"ref_46","first-page":"173","article-title":"Distribution of the antiseptic-resistance genes qacE and qacE\u03941 in Gram-negative bacteria","volume":"159","author":"Kazama","year":"1998","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1093\/jac\/dks086","article-title":"Prevalence of the oqxAB gene complex in Klebsiella pneumoniae and Escherichia coli clinical isolates","volume":"67","author":"Yuan","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e107397","DOI":"10.5812\/iji.107397","article-title":"Detection of OqxAB and QepA efflux pumps and their association with antibiotic resistance in Klebsiella pneumoniae isolated from urinary tract infection","volume":"7","author":"Dehnamaki","year":"2020","journal-title":"Int. J. Infect."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Ni, L., Zhang, Z., Shen, R., Liu, X., Li, X., Chen, B., Wu, X., Li, H., Xie, X., and Huang, S. (2022). Disinfection Strategies for Carbapenem-Resistant Klebsiella pneumoniae in a Healthcare Facility. Antibiotics, 11.","DOI":"10.21203\/rs.3.rs-1220609\/v1"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"65S","DOI":"10.1046\/j.1365-2672.92.5s1.4.x","article-title":"Active efflux, a common mechanism for biocide and antibiotic resistance","volume":"92","author":"Levy","year":"2002","journal-title":"Appl. Microbiol."},{"key":"ref_51","first-page":"Doc15","article-title":"Contribution of AcrAB efflux pump to ciprofloxacin resistance in Klebsiella pneumoniae isolated from burn patients","volume":"8","author":"Pakzad","year":"2013","journal-title":"GMS Hyg. Infect. Control."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1089\/mdr.2018.0414","article-title":"Alliance of efflux pumps with \u03b2-lactamases in multidrug-resistant Klebsiella pneumoniae isolates","volume":"25","author":"Maurya","year":"2019","journal-title":"Microb. Drug Resist."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Smith, B.L., Fernando, S., and King, M.D. (2024). Escherichia coli resistance mechanism AcrAB-TolC efflux pump interactions with commonly used antibiotics: A molecular dynamics study. Sci. Rep., 14.","DOI":"10.1038\/s41598-024-52536-z"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"5416","DOI":"10.1128\/jb.170.12.5416-5422.1988","article-title":"The marA locus causes decreased expression of OmpF porin in multiple antibiotic resistant (Mar) mutants of Escherichia coli","volume":"170","author":"Cohen","year":"1988","journal-title":"J. Bacteriol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1179\/2047773215Y.0000000022","article-title":"Determining the resistance of carbapenem-resistant Klebsiella pneumoniae to common disinfectants and elucidating the underlying resistance mechanisms","volume":"109","author":"Guo","year":"2015","journal-title":"Pathog. Glob. Health"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1128\/AAC.00715-09","article-title":"Klebsiella pneumoniae AcrAB Efflux Pump Contributes to Antimicrobial Resistance and Virulence","volume":"54","author":"Padilla","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e0030323","DOI":"10.1128\/iai.00303-23","article-title":"Klebsiella pneumoniae TolC contributes to antimicrobial resistance, exopolysaccharide production, and virulence","volume":"91","author":"Bina","year":"2023","journal-title":"Infect. Immun."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Aparna, V., Dineshkumar, K., Mohanalakshmi, N., Velmurugan, D., and Hopper, W. (2014). Identification of natural compound inhibitors for multidrug efflux pumps of Escherichia coli and Pseudomonas aeruginosa using in silico high-throughput virtual screening and in vitro validation. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0101840"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1128\/AAC.42.1.65","article-title":"Expression of Pseudomonas aeruginosa multidrug efflux pumps MexA-MexB-OprM and MexC-MexD-OprJ in a multidrug-sensitive Escherichia coli strain","volume":"42","author":"Srikumar","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2547","DOI":"10.1093\/jac\/dks284","article-title":"Reduced susceptibility to chlorhexidine in staphylococci: Is it increasing and does it matter?","volume":"67","author":"Horner","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"LaBreck, P.T., Rice, G.K., Paskey, A.C., Elassal, E.M., Cer, R.Z., Law, N.N., Schlett, C.D., Bennett, J.W., Millar, E.V., and Ellis, M.W. (2018). Conjugative Transfer of a Novel Staphylococcal Plasmid Encoding the Biocide Resistance Gene, qacA. Front. Microbiol., 19.","DOI":"10.3389\/fmicb.2018.02664"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Damavandi, M.S., Maryam, S.D., Alireza, D., Fatemeh, H., Roohollah, T., and Abolfazl, G. (2016). Detection of Antiseptic Resistance Genes among Staphylococcus aureus Colonising Nurses and Coagulase-Negative Staphylococci Isolated from Clinical Specimens at Teaching Hospitals in Southwest of Iran. Jundishapur J. Microbiol., 10.","DOI":"10.5812\/jjm.39285"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"4404","DOI":"10.1128\/AAC.02419-14","article-title":"Prevalence of Chlorhexidine-Resistant Methicillin-Resistant Staphylococcus aureus following Prolonged Exposure","volume":"58","author":"Schlett","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1857","DOI":"10.1128\/JCM.02488-16","article-title":"Novel Multiplex PCR Assay for Detection of Chlorhexidine-Quaternary Ammonium, Mupirocin, and Methicillin Resistance Genes, with Simultaneous Discrimination of Staphylococcus aureus from Coagulase-Negative Staphylococci","volume":"55","author":"McClure","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"ref_65","first-page":"775","article-title":"High prevalence and expression of antiseptic resistance genes among infectious t037\/ST239 methicillin-resistant Staphylococcus aureus (MRSA) strains in North Khorasan Province, Iran","volume":"25","author":"Azimian","year":"2022","journal-title":"Iran. J. Basic Med. Sci."},{"key":"ref_66","first-page":"7","article-title":"Genetic basis of resistance waves among methicillin resistant Staphylococcus aureus isolates recovered from milk and meat products in Egypt","volume":"62","author":"Ammar","year":"2016","journal-title":"Cell. Mol. Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"59","DOI":"10.2174\/1874285801307010059","article-title":"Multidrug Efflux Pumps in Staphylococcus aureus: An Update","volume":"7","author":"Costa","year":"2013","journal-title":"Open Microbiol. J."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"103850","DOI":"10.1016\/j.micpath.2019.103850","article-title":"Epidemiology of efflux pumps genes mediating resistance among Staphylococcus aureus; A systematic review","volume":"139","author":"Hassanzadeh","year":"2020","journal-title":"Microb. Pathog."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1128\/AAC.49.1.161-169.2005","article-title":"Effect of promoter region mutations and mgrA overexpression on transcription of norA, which encodes a Staphylococcus aureus multidrug efflux transporter","volume":"49","author":"Kaatz","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2525","DOI":"10.1128\/JB.00018-10","article-title":"Phosphorylation of MgrA and its effect on expression of the NorA and NorB efflux pumps of Staphylococcus aureus","volume":"192","author":"Hooper","year":"2010","journal-title":"J Bacteriol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1128\/JB.06582-11","article-title":"Expression of multidrug resistance efflux pump gene norA is iron responsive in Staphylococcus aureus","volume":"194","author":"Deng","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_72","first-page":"33","article-title":"Detection the Prevalence of Some Chromosomal Efflux Pump Genes in Methicillin Resistant Staphylococcus aureus Isolated from Iraqi Patients","volume":"18","author":"Ghufran","year":"2019","journal-title":"Iraqi J. Biotechnol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1248\/bpb.25.1533","article-title":"Cloning and characterization of a novel chromosomal drug efflux gene in Staphylococcus aureus","volume":"25","author":"Narui","year":"2002","journal-title":"Biol. Pharm. Bull."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"132","DOI":"10.2174\/1874285801711010132","article-title":"Diversity of Multidrug Efflux Genes and Phenotypic Evaluation of the In vitro Resistance Dynamics of Clinical Staphylococcus Aureus Isolates Using Methicillin; a Model \u03b2-lactam","volume":"11","author":"Antiabong","year":"2017","journal-title":"Open Microbiol. J."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1412","DOI":"10.1093\/cid\/cix462","article-title":"The Role of Patient Care Items as a Fomite in Healthcare-Associated Outbreaks and Infection Prevention","volume":"65","author":"Kanamori","year":"2017","journal-title":"Clin. Infect. Dis."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"A96","DOI":"10.1016\/j.ajic.2019.01.014","article-title":"Best practices for disinfection of noncritical environmental surfaces and equipment in health care facilities: A bundle approach","volume":"47","author":"Rutala","year":"2019","journal-title":"Am. J. Infect. Control."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Amsalu, A., Sapula, S.A., De Barros Lopes, M., Hart, B.J., Nguyen, A.H., Drigo, B., Turnidge, J., Leong, L.E., and Venter, H. (2020). Efflux pump-driven antibiotic and biocide cross-resistance in Pseudomonas aeruginosa isolated from different ecological niches: A case study in the development of multidrug resistance in environmental hotspots. Microorganisms, 8.","DOI":"10.3390\/microorganisms8111647"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1080\/08927014.2011.626899","article-title":"Resistance of bacterial biofilms to disinfectants: A review","volume":"27","author":"Bridier","year":"2011","journal-title":"Biofouling"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1021\/acs.est.6b03132","article-title":"Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera","volume":"51","author":"Zhang","year":"2017","journal-title":"Environ. Sci. Technol."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Ghaly, T.M., Chow, L., Asher, A.J., Waldron, L.S., and Gillings, M.R. (2017). Evolution of class 1 integrons: Mobilization and dispersal via food-borne bacteria. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0179169"},{"key":"ref_81","first-page":"27","article-title":"The linkage between prevalence of integron I and reduced susceptibility to biocides in MDR Klebsiella pneumoniae isolated from neonates","volume":"15","author":"Samir","year":"2023","journal-title":"Iran. J. Microbiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"88","DOI":"10.5350\/BMB20170828103017","article-title":"Comparison Between Reduced Susceptibility to Disinfectants and Multidrug Resistance Among Hospital Isolates of Pseudomonas aeruginosa and Staphylococcus aureus in Bangladesh","volume":"2","author":"Islam","year":"2017","journal-title":"Bagcilar Med. Bull."},{"key":"ref_83","unstructured":"ATCC (2023, May 05). The Global Bioresource Center. Available online: https:\/\/www.lgcstandards-atcc.org."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Merritt, J.H., Kadouri, D.E., and O\u2019Toole, G.A. (2005). Growing and analyzing static biofilm. Curr. Protoc. Microbiol., 1.","DOI":"10.1002\/9780471729259.mc01b01s00"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1111\/j.1574-695X.2010.00703.x","article-title":"Microbial diversity in biofilm infections of the urinary tract with the use of sonication techniques","volume":"59","author":"Ruzicka","year":"2010","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_87","unstructured":"(2018). Disinfectants. Methods for Determining Efficiency Factor. Standard No. GOST R 58151.4-2018."},{"key":"ref_88","unstructured":"Shkarin, V.V., Kovalishena, O.V., Blagonravova, A.S., Vorob\u2019yeva, O.N., and Alekseyeva, I.G. (2010). Method for Determining the Sensitivity of Microorganisms to Disinfectants: Methodological Recommendations [Sposob Opredeleniya Chuvstvitel\u2019nosti Mikroorganizmov k Dezinfitsiruyushchim Sredstvam: Metodicheskiye Rekomendatsii], NGMA. (In Russian)."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Chen, Y., Liao, K., Huang, Y., Guo, P., Huang, H., Wu, Z., and Liu, M. (2020). Determining the susceptibility of carbapenem resistant Klebsiella pneumoniae and Escherichia coli strains against common disinfectants at a tertiary hospital in China. BMC Infect. Dis., 20.","DOI":"10.1186\/s12879-020-4813-6"},{"key":"ref_90","first-page":"820","article-title":"CRISPR-Cas system in multi drugs resistant Klebsiella pneumoniae from different clinical samples and its correlation with antibiotic-resistant genes in Mosul city","volume":"16","author":"Mohammad","year":"2024","journal-title":"Iraqi J. Appl. Nat. Sci."},{"key":"ref_91","first-page":"97","article-title":"Occurrence of MexAB-OprM efflux pump operon on septicemic Pseudomonas aeruginosa chromosome","volume":"2","author":"Kareem","year":"2012","journal-title":"Iraqi Postgrad. Med. J."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"2119","DOI":"10.1128\/JCM.02690-05","article-title":"Antimicrobial agent of susceptibilities and antiseptic resistance gene distribution among methicillin-resistant Staphylococcus aureus isolates from patients with impetigo and staphylococcal scalded skin syndrome","volume":"44","author":"Noguchi","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"5070","DOI":"10.1128\/AAC.01058-10","article-title":"Ethidium Bromide MIC Screening for Enhanced Efflux Pump Gene Expression or Efflux Activity in Staphylococcus aureus","volume":"54","author":"Patel","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1128\/AAC.48.3.909-917.2004","article-title":"Novel chromosomally encoded multidrug efflux transporter MdeA in Staphylococcus aureus","volume":"48","author":"Huang","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Suma, T.A., Alam, N., Raihan, S.Z., Zahid, M.A., Mandal, S.C., Suchana, F.J., Kundu, R., Hossain, A., and Muhit, M.A. (2023). Association of Antibacterial Susceptibility Profile with the Prevalence of Genes Encoding Efflux Proteins in the Bangladeshi Clinical Isolates of Staphylococcus aureus. Antibiotics, 12.","DOI":"10.3390\/antibiotics12020305"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/1\/355\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T10:22:19Z","timestamp":1759918939000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/1\/355"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,3]]},"references-count":95,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["ijms26010355"],"URL":"https:\/\/doi.org\/10.3390\/ijms26010355","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,3]]}}}