In vitro evaluation of antimicrobial and anti-biofilm properties of antiseptics against multidrug resistant clinical Escherichia coli strains, isolated from combat wounds
DOI:
https://doi.org/10.15574/PS.2023.80.8Keywords:
Escherichia coli, antiseptics, biofilms, infection, combat wounds, susceptibility to antiseptics, anti-biofilm-forming activityAbstract
The necessity for the investigation of novel approaches and strategies for the treatment of multidrug-resistant E. coli related infections becomes more and more essential.
Purpose - to investigate and compare the level of antimicrobial and anti-biofilm activity of antiseptic preparations against MDR clinical isolates of E. coli.
Materials and methods. In vitro effectiveness of modern antiseptics; octenidine 0.1% (OCT), polyhexanide 0.1% (PHMB), chlorhexidine 0.5% (CHG), miramistin 0.01% (MRM), decamethoxine 0.1% 0.02% (DCM), povidone-iodine 10% (PVP-I), was determined against forty-six polyresistant clinical strains of E. coli. MIC, MBC were found by standard methods, the value of which was interpreted as a bacteriostatic and bactericidal index of antiseptic activity (BS IAA and BC IAA). The effect of antiseptics on the immature biofilm was modelled using the Christensen test.
Results. MIC and MBC values were the lowest in DCM and OCT. The highest values of the antiseptic activity index (IAA>4) were determined for the antiseptics PHMB 0.1%, OCT 0.1% and DCM 0.1%. It was found that the feasibility of using MRM at a concentration of 0.01% is questionable as the BS IAA is above the threshold value, while the BC IAA is not. The effectiveness of PVP-I 1% against MDR E. coli was found insufficient. Sub-bacteriostatic concentrations of DCM, CHG, and PHMB reliably inhibited the formation of E. coli biofilms within 24 hours. MRM and PVP-I in sub-bacteriostatic concentrations stimulated biofilm formation.
Conclusions. Based on the analysis of all conducted studies, 0.1% and 0.02% DCM, 0.05% CHG, 0.1% OCT, 0.1% PHMB, 10% and 2% PVP-I are the most active against MDR clinical isolates of E. coli.
The research was carried out in accordance with the principles of the Helsinki Declaration. The study protocol was approved by the Local Ethics Committee of the participating institution. The informed consent of the patient was obtained for conducting the studies.
No conflict of interests was declared by the authors.
References
Alvarez-Marin R, Aires-de-Sousa M, Nordmann P, Kieffer N, Poirel L. (2017). Antimicrobial activity of octenidine against multidrug-resistant Gram-negative pathogens. European journal of clinical microbiology & infectious diseases: official publication of the European Society of Clinical Microbiology. 36 (12): 2379-2383. https://doi.org/10.1007/s10096-017-3070-0; PMid:28825186
Alves PJ, Barreto RT, Barrois BM, Gryson LG, Meaume S, Monstrey SJ. (2021). Update on the role of antiseptics in the management of chronic wounds with critical colonisation and/or biofilm. International wound journal. 18 (3): 342-358. https://doi.org/10.1111/iwj.13537; PMid:33314723 PMCid:PMC8244012
Andreeva SV, Bakhareva LI, Nokhrin DYu, Titova MV, Khaidarshina NE, Burmistrova AL. (2018). Susceptibility to antiseptic preparations in biofilm-forming Staphylococcus aureus and Pseudomonas aeruginosa isolated from burn wounds. Clinical Microbiology and Antimicrobial Chemotherapy. 20 (3): 249-256. https://doi.org/10.36488/cmac.2018.3.249-256
Assadian O. (2016). Octenidine dihydrochloride: chemical characteristics and antimicrobial properties. J. Wound Care. 25; 3: S3-S6. https://doi.org/10.12968/jowc.2016.25.Sup3.S3; PMid:26949863
Atkin L, Bućko Z, Conde Montero E, Cutting K, Moffatt C, Probst A et al. (2019). Implementing TIMERS: the race against hard-to-heal wounds. Journal of wound care. 23 (3a): S1-S50. https://doi.org/10.12968/jowc.2019.28.Sup3a.S1; PMid:30835604
Barreto R, Barrois B, Lambert J, Malhotra-Kumar S, Santos-Fernandes V, Monstrey S. (2020). Addressing the challenges in antisepsis: focus on povidone iodine. International journal of antimicrobial agents. 56 (3): 106064. https://doi.org/10.1016/j.ijantimicag.2020.106064; PMid:32599228
Bock LJ, Wand ME, Sutton JM. (2016). Varying activity of chlorhexidine-based disinfectants against Klebsiella pneumoniae clinical isolates and adapted strains. The Journal of hospital infection. 93 (1): 42-48. https://doi.org/10.1016/j.jhin.2015.12.019; PMid:26899354
Braz VS, Melchior K, Moreira CG. (2020). Escherichia coli as a Multifaceted Pathogenic and Versatile Bacterium. Frontiers in cellular and infection microbiology. 10: 548492. https://doi.org/10.3389/fcimb.2020.548492; PMid:33409157 PMCid:PMC7779793
Christensen GD, Simpson WA, Younger JJ et al. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. Journal of Clinical Microbiology. 22; 6: 996-1006. https://doi.org/10.1128/jcm.22.6.996-1006.1985; PMid:3905855 PMCid:PMC271866
Clinical and Laboratory Standards Institute (CLSI). (2014). Performance standards for antimicrobial susceptibility testing; twenty forth informational supplement M100-S24. Wayne, PA, USA. 34: 1.
Denysko TV, Nazarchuk OA, Gruzevskyi O, Bahniuk NÀ, Dmytriiev DV, Chornopyschuk RM, Bebyk VV. (2022). In vitro evaluation of the antimicrobial activity of antiseptics against clinical Acinetobacter baumannii strains isolated from combat wounds. Front. Microbiol. 13: 932467. https://doi.org/10.3389/fmicb.2022.932467; PMid:36267170 PMCid:PMC9577188
Di Domenico EG, Farulla I, Prignano G et al. (2017). Biofilm is a Major Virulence Determinant in Bacterial Colonization of Chronic Skin Ulcers Independently from the Multidrug Resistant Phenotype. Int J Mol Sci. 18 (5): 1077. Published 2017 May 17. https://doi.org/10.3390/ijms18051077; PMid:28513576 PMCid:PMC5454986
Diriba K, Kassa T, Alemu Y, Bekele S. (2020, Mar 18). In Vitro Biofilm Formation and Antibiotic Susceptibility Patterns of Bacteria from Suspected External Eye Infected Patients Attending Ophthalmology Clinic, Southwest Ethiopia. Int J Microbiol: 8472395. https://doi.org/10.1155/2020/8472395; PMid:32318110 PMCid:PMC7155758
Dydak K, Junka A, Dydak A, Brożyna M, Paleczny J, Fijalkowski K et al. (2021). In Vitro Efficacy of Bacterial Cellulose Dressings Chemisorbed with Antiseptics against Biofilm Formed by Pathogens Isolated from Chronic Wounds. International journal of molecular sciences. 22 (8): 3996. https://doi.org/10.3390/ijms22083996; PMid:33924416 PMCid:PMC8069587
European committee on antimicrobial susceptibility testing (EUCAST). (2015). EUCAST disk diffusion test methodology. URL: https://www.eucast.org/ast_of_bacteria/disk_diffusion_methodology/. updated 26 January. Accessed 12 Aug 2015.
Gregorchuk B, Reimer SL, Slipski CJ, Milner KA, Hiebert SL, Beniac DR et al. (2022). Applying fluorescent dye assays to discriminate Escherichia coli chlorhexidine resistance phenotypes from porin and mlaA deletions and efflux pumps. Scientific reports. 12 (1): 12149. https://doi.org/10.1038/s41598-022-15775-6; PMid:35840757 PMCid:PMC9287405
Günther F, Blessing B, Dapunt U, Mischnik A, Mutters NT. (2021). Ability of chlorhexidine, octenidine, polyhexanide and chloroxylenol to inhibit metabolism of biofilm-forming clinical multidrug-resistant organisms. Journal of infection prevention. 22 (1): 12-18. https://doi.org/10.1177/1757177420963829; PMid:33841557 PMCid:PMC7841706
Hall CW, Mah TF. (2017, May 1). Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 41 (3): 276-301. https://doi.org/10.1093/femsre/fux010; PMid:28369412
Hardy K et al. (2018). Increased Usage of antiseptics is associated with reduced susceptibility in clinical isolates of Staphylococcus aureus. MBio. 9: pii: e00894-18. https://doi.org/10.1128/mBio.00894-18; PMid:29844113 PMCid:PMC5974466
Kampf G (ed.). (2018). Chlorhexidine digluconate. In: Antiseptic Stewardship: Biocide Resistance and Clinical Implications. Springer International Publishing: 429-534. https://doi.org/10.1007/978-3-319-98785-9_13
Kane SP. (2023). ClinCalc.com: Chlorhexidine drug usage statistics, United States, 2008-2009. ClinCalc.com: 1.
Katouli M. (2010). Population structure of gut Escherichia coli and its role in development of extra-intestinal infections. Iranian journal of microbiology. 2 (2): 59-72.
Khan HA, Baig FK, Mehboob R. (2017). Nosocomial infections: Epidemiology, prevention, control and surveillance. Asian Pac. J. Trop. Biomed. 7 (5): 478-482. https://doi.org/10.1016/j.apjtb.2017.01.019
Kovalchuk VP, Nazarchuk OA, Burkot VM, Fomina NS, Prokopchuk ZM, Dobrovanov O. (2021). Biofilm forming activity of non-fermenting gram-negative bacteria. Wiadomosci lekarskie (Warsaw, Poland : 1960). 74 (2): 252-256. https://doi.org/10.36740/WLek202102114; PMid:33813481
Kramer A, Dissemond J, Kim S, Willy C, Mayer D, Papke R et al. (2018). Consensus on Wound Antisepsis: Update 2018. Skin pharmacology and physiology. 31 (1): 28-58. https://doi.org/10.1159/000481545; PMid:29262416
Krasilnikov AP. (1995). Guide on antiseptics. Minsk: Vyshjejshaja shkola: 368.
Krasowski G, Junka A, Paleczny J, Czajkowska J, Makomaska-Szaroszyk E, Chodaczek G et al. (2021). In Vitro Evaluation of Polihexanide, Octenidine and NaClO/HClO-Based Antiseptics against Biofilm Formed by Wound Pathogens. Membranes. 11 (1): 62. https://doi.org/10.3390/membranes11010062; PMid:33477349 PMCid:PMC7830887
Leimbach A, Hacker J, Dobrindt U. (2013). E. coli as an all-rounder: the thin line between commensalism and pathogenicity. Current topics in microbiology and immunology. 358: 3-32. https://doi.org/10.1007/82_2012_303; PMid:23340801
Ljungquist O, Nazarchuk O, Kahlmeter G, Andrews V, Koithan T, Wasserstrom L et al. (2023). Highly multidrug-resistant Gram-negative bacterial infections in war victims in Ukraine, 2022. The Lancet. Infectious diseases: 23. https://doi.org/10.1016/S1473-3099(23)00291-8; PMid:37236220
Loose M, Naber KG, Purcell L, Wirth MP, Wagenlehner F. (2021). Anti-Biofilm Effect of Octenidine and Polyhexanide on Uropathogenic Biofilm-Producing Bacteria. Urologia internationalis. 105 (3-4): 278-284. https://doi.org/10.1159/000512370; PMid:33401282 PMCid:PMC8006580
López-Rojas R et al. (2017). In vitro activity of a polyhexanide-betaine solution against high-risk clones of multidrug-resistant nosocomial pathogens. Enfermedades infecciosas y microbiologia clinica. 35; 1: 12-19. https://doi.org/10.1016/j.eimc.2016.02.008; PMid:27004429
Mahoney AR, Safaee MM, Wuest WM, Furst AL. (2021). The silent pandemic: Emergent antibiotic resistances following the global response to SARS-CoV-2. iScience. 24 (4): 102304. https://doi.org/10.1016/j.isci.2021.102304; PMid:33748695 PMCid:PMC7955580
Maillard JY, Kampf G, Cooper R. (2021). Antimicrobial stewardship of antiseptics that are pertinent to wounds: the need for a united approach. JAC-antimicrobial resistance. 3 (1): dlab027. https://doi.org/10.1093/jacamr/dlab027; PMid:34223101 PMCid:PMC8209993
Ministry of Health of Ukraine. (2007). About the statement of methodical instructions "Determination of sensitivity of microorganisms to antibacterial drugs". The order of the Ministry of Health of Ukraine No. 167.
Murray CK, Hinkle MK, Yun HC. (2008). History of infections associated with combat-related injuries. J Trauma Acute Care Surg. 64 (3): 221-231. https://doi.org/10.1097/TA.0b013e318163c40b; PMid:18316966
Murray CK, Yun HC, Griffith ME, Thompson B. (2009). Recovery of multidrug-resistant bacteria from combat personnel evacuated from Iraq and Afghanistan at a single military treatment facility. Mil Med. 174 (6): 598-604. https://doi.org/10.7205/MILMED-D-03-8008; PMid:19585772
Pallavali RR, Degati VL, Lomada D, Reddy MC, Durbaka V. (2017). Isolation and in vitro evaluation of bacteriophages against MDR-bacterial isolates from septic wound infections. PloS one. 12 (7): e0179245. https://doi.org/10.1371/journal.pone.0179245; PMid:28719657 PMCid:PMC5515400
Percival SL, Finnegan S, Donelli G, Vuotto C, Rimmer S, Lipsky BA. (2016). Antiseptics for treating infected wounds: Efficacy on biofilms and effect of pH. Critical reviews in microbiology. 42 (2): 293-309. https://doi.org/10.3109/1040841X.2014.940495; PMid:25159044
Puca V, Marulli RZ, Grande R, Vitale I, Niro A, Molinaro G et al. (2021). Microbial Species Isolated from Infected Wounds and Antimicrobial Resistance Analysis: Data Emerging from a Three-Years Retrospective Study. Antibiotics (Basel, Switzerland). 10 (10): 1162. https://doi.org/10.3390/antibiotics10101162; PMid:34680743 PMCid:PMC8532735
Roy S et al. (2017, Dec 7). Evaluation of antibiotic susceptibility in wound infections: A pilot study from Bangladesh. F1000Research. 6: 2103. https://doi.org/10.12688/f1000research.12887.1; PMid:29527295 PMCid:PMC5820593
Royer G, Ortiz de la Rosa JM, Vuillemin X, Lacombe B, Chau F, Clermont O et al. (2022). Reduced Chlorhexidine Susceptibility Is Associated with Tetracycline Resistance tet Genes in Clinical Isolates of Escherichia coli. Antimicrobial agents and chemotherapy. 66 (3): e0197221. https://doi.org/10.1128/aac.01972-21; PMid:35225650 PMCid:PMC8923171
Tian X, Sun S, Jia X, Zou H, Li S, Zhang L. (2018). Epidemiology of and risk factors for infection with extended-spectrum β-lactamase-producing carbapenem-resistant Enterobacteriaceae: results of a double case-control study. Infection and drug resistance. 11: 1339-1346. https://doi.org/10.2147/IDR.S173456; PMid:30214254 PMCid:PMC6120570
Urase T, Okazaki M, Tsutsui H. (2020). Prevalence of ESBL-producing Escherichia coli and carbapenem-resistant Enterobacteriaceae in treated wastewater: a comparison with nosocomial infection surveillance. Journal of water and health. 18 (6): 899-910. https://doi.org/10.2166/wh.2020.014; PMid:33328362
Valentine KP, Viacheslav KM. (2017). Bacterial flora of combat wounds from eastern Ukraine and time-specified changes of bacterial recovery during treatment in Ukrainian military hospital. BMC Res Notes. 10: 152. https://doi.org/10.1186/s13104-017-2481-4; PMid:28388920 PMCid:PMC5384141
Wand ME, Bock LJ, Bonney LC, Sutton JM. (2016). Mechanisms of Increased Resistance to Chlorhexidine and Cross-Resistance to Colistin following Exposure of Klebsiella pneumoniae Clinical Isolates to Chlorhexidine. Antimicrobial agents and chemotherapy. 61 (1): e01162-16. https://doi.org/10.1128/AAC.01162-16; PMid:27799211 PMCid:PMC5192135
Wand ME, Jamshidi S, Bock LJ, Rahman KM, Sutton JM. (2019). SmvA is an important efflux pump for cationic biocides in Klebsiella pneumoniae and other Enterobacteriaceae. Scientific reports. 9 (1): 1344. https://doi.org/10.1038/s41598-018-37730-0; PMid:30718598 PMCid:PMC6362122
Weintrob AC, Murray CK, Xu J, Krauss M, Bradley W, Warkentien TE et al. (2018). Early Infections Complicating the Care of Combat Casualties from Iraq and Afghanistan. Surgical infections. 19 (3): 286-297. https://doi.org/10.1089/sur.2017.240; PMid:29863446 PMCid:PMC5867509
Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM et al. (2013). The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. The Lancet. Infectious diseases. 13 (2): 155-165. https://doi.org/10.1016/S1473-3099(12)70317-1; PMid:23347633
Wilcox MH, Dryden M. (2021). Update on the epidemiology of healthcare-acquired bacterial infections: focus on complicated skin and skin structure infections. The Journal of antimicrobial chemotherapy. 76 (4): IV2-IV8. https://doi.org/10.1093/jac/dkab350; PMid:34849996 PMCid:PMC8632754
Williamson A et al. (2017). Current and Emerging Topical Antibacterials and Antiseptics: Agents, Action, and Resistance Patterns. Clinical microbiology reviews. 30; 3: 827-860. https://doi.org/10.1128/CMR.00112-16; PMid:28592405 PMCid:PMC5475228
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Paediatric Surgery (Ukraine)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The policy of the Journal “PAEDIATRIC SURGERY. UKRAINE” is compatible with the vast majority of funders' of open access and self-archiving policies. The journal provides immediate open access route being convinced that everyone – not only scientists - can benefit from research results, and publishes articles exclusively under open access distribution, with a Creative Commons Attribution-Noncommercial 4.0 international license(СС BY-NC).
Authors transfer the copyright to the Journal “PAEDIATRIC SURGERY.UKRAINE” when the manuscript is accepted for publication. Authors declare that this manuscript has not been published nor is under simultaneous consideration for publication elsewhere. After publication, the articles become freely available on-line to the public.
Readers have the right to use, distribute, and reproduce articles in any medium, provided the articles and the journal are properly cited.
The use of published materials for commercial purposes is strongly prohibited.
