Inhibitory Effect of Selenium Nanoparticles on the Biofilm Formation of Multidrug-Resistant Acinetobacter Baumannii

Keywords: Acinetobacter baumannii, Selenium nanoparticles, Biofilm

Abstract


Background/Aim: Treatment of infections caused by biofilm-producing multidrug-resistant (MDR) pathogens represents a huge global problem due to primary antimicrobial multi-resistance enhanced by reduced penetration of antibiotics in the biofilm-embedded bacteria. The aim of this study was to determine the capacity of biofilm production among MDR Acinetobacter baumannii (A baumannii) isolates obtained from different clinical specimens and to evaluate the inhibitory effect of selenium nanoparticles (SeNPs) coated with cationic polymer cetyltrimethylammonium bromide (CTAB) on the biofilm formation.

Methods: Antimicrobial effect of antibiotics (meropenem, imipenem, gentamicin, amikacin, ciprofloxacin, levofloxacin and trimethoprim-sulfamethoxazole) was determined by disk-diffusion assay, while sensitivity to colistin was determined with E test. All 60 isolates were tested on biofilm production in microtiter plates with crystal violet dye. Minimal biofilm inhibitory concentration (MBIC) of SeNPs was tested in order to prevent biofilm formation in microtiter plates.

Results: All tested clinical isolates were classified as MDR (n = 60) and extensively drug-resistant (XDR, n = 60). Out of the total 60 isolates, 55 isolates (92 %) showed the ability for biofilm formation, with the majority of them classified as strong (42 %) and moderate (42 %) biofilm producers. MBIC values of SeNPs for 55 biofilm-producing isolates ranged from 0.07 to 1.25 mg/mL. Strong biofilm producers had statistically higher MBIC (0.15 mg/mL) in correlation to other biofilm-producing isolates (0.07 mg/mL). There was no correlation between invasiveness of isolates with biofilm production and MBIC values.

Conclusion: Presented results are very promising and interesting especially in nanotechnology and medical fields, while SeNPs with the addition of cationic surfactant inhibit biofilm formation of MDR A baumannii clinical isolates.

 

References

Kyriakidis I, Vasileiou E, Pana ZD, Tragiannidis A. Acinetobacter baumannii antibiotic resistance mechanisms. Pathogens. 2021 Mar 19;10(3):373. doi: 10.3390/pathogens10030373.

Gajic I, Jovicevic M, Milic M, Kekic D, Opavski N, Zrnic Z, et al. Clinical and molecular characteristics of OXA-72-producing Acinetobacter baumannii ST636 outbreak at a neonatal intensive care unit in Serbia. J Hosp Infect. 2021 Jun;112:54-60. doi: 10.1016/j.jhin.2021.02.023

Lukovic B, Gajic I, Dimkic I, Kekic D, Zornic S, Pozder T, et al. The first nationwide multicenter study of Acinetobacter baumannii recovered in Serbia: emergence of OXA-72, OXA-23 and NDM-1-producing isolates. Antimicrob Resist Infect Control. 2020 Jul 6;9(1):101. doi: 10.1186/s13756-020-00769-8.

Sharifipour E, Shams S, Esmkhani M, Khodadadi J, Fotouhi-Ardakani R, Koohpaei A, et al. Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect Dis. 2020 Sep 1; 20:646. doi: 10.1186/s12879-020-05374-z.

Russo A, Gavaruzzi F, Ceccarelli G, Borrazzo C, Oliva A, Alessandri F, et al. Multidrug-resistant Acinetobacter baumannii infections in COVID-19 patients hospitalized in intensive care unit. Infection. 2020 Feb;50(1):83-92. doi: 10.1007/s15010-021-01643-4.

Bafghi MH, Darroudi M, Zargar M, Zarrinfar H, Nazari, R. Biosynthesis of Selenium nanoparticles by Aspergillus Flavus and Candida Albicans for antifungal applications. Micro Nano Lett. 2021;16:656–69. doi:10.1049/mna2.12096.

Johnson J, Shanmugam R, Lakshmi T. A review on plant-mediated selenium nanoparticles and its applications. J Popul Ther Clin Pharmacol. 2022 Jan 6;28(2):e29-e40. doi: 10.47750/jptcp.2022.870.

The European Committee on Antimicrobial Susceptibility Testing. [Internet]. Breakpoint tables for interpretation of MICs and zone diameters, Version 14.0. [Cited: 15-Jan-2024]. Available at: http://www.eucast.org.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012 Mar;18(3):268-81. doi: 10.1111/j.1469-0691.2011.03570.x.

Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007 Aug;115(8):891-9. doi: 10.1111/j.1600-0463.2007.apm_630.x.

Filipović N, Ušjak D, Milenković MT, Zheng K, Liverani L, Boccaccini AR, et al. Comparative study of the antimicrobial activity of selenium nanoparticles with different surface chemistry and structure. Front Bioeng Biotechnol. 2021 Jan 25;8:624621. doi: 10.3389/fbioe.2020.624621.

Ahmad W, Shams S, Ahmad A, Wei Y, Yuan Q, Ullah Khan A, et al. Synthesis of selenium–silver nanostructures with enhanced antibacterial, photocatalytic and antioxidant activities. Appl Nanosci. 2020;10(4):1191-204. doi: 10.1007/s13204-019-01213-z.

Bagheri-Josheghani S, Bakhshi B. Investigation of the antibacterial and antibiofilm activity of Selenium nanoparticles against Vibrio cholerae as a potent therapeutics. Can J Infect Dis Med Microbiol. 2022 Mar 23;2022:3432235. doi: 10.1155/2022/3432235.

Elkheloui R, Laktib A, Mimouni R, Aitalla A, Hassi M, Elboulani A, et al. Acinetobacter baumannii biofilm: intervening factors, persistence, drug resistance, and strategies of treatment. Mediterr J Infect Microb Antimicrob. 2020 Sep 10;9(7):1–12. doi: 10.4274/mjima.galenos.2020.2020.7.

Gedefie A, Demsis W, Ashagrie M, Kassa Y, Tesfaye M, Tilahun M, et al. Acinetobacter baumannii biofilm formation and its role in disease pathogenesis: a review. Infect Drug Resist. 2021 Sep 10;14:3711-3719. doi: 10.2147/IDR.S332051.

Zeighami H, Valadkhani F, Shapouri R, Samadi E, Haghi F. Virulence characteristics of multidrug resistant biofilm forming Acinetobacter baumannii isolated from intensive care unit patients. BMC Infect Dis. 2019 Jul 17;19(1):629. doi: 10.1186/s12879-019-4272-0.

Hu H, Lou Y, Feng H, Tao J, Shi W, Ni S, et al. Molecular characterization of carbapenem-resistant Acinetobacter baumannii isolates among intensive care unit patients and environment. Infect Drug Resist. 2022 Apr 13;15:1821-9. doi: 10.2147/IDR.S349895.

D'Onofrio V, Conzemius R, Varda-Brkić D, Bogdan M, Grisold A, Gyssens IC, et al. Epidemiology of colistin-resistant, carbapenemase-producing Enterobacteriaceae and Acinetobacter baumannii in Croatia. Infect Genet Evol. 2020 Jul;81:104263. doi: 10.1016/j.meegid.2020.104263.

Afhami S, Borumand MA, Bazzaz NE, Saffar H, Hadadi A, Nezhadet MJ, al. Antimicrobial resistance pattern of Acinetobacter; a multicenter study, comparing European Committee on Antimicrobial Susceptibility Testing (EUCAST) and the Clinical and Laboratory Standards Institute (CLSI); evaluation of susceptibility testing methods for polymyxin. Immunopath Persa. 2020;7(1):e04-e04. doi: 10.34172/ipp.2021.04.

Harding CM, Hennon SW, Feldman MF. Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol. 2018 Feb;16(2):91-102. doi: 10.1038/nrmicro.2017.148.

Jain A, Agarwal A. Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J Microbiol Methods. 2009 Jan;76(1):88-92. doi: 10.1016/j.mimet.2008.09.017.

Pompilio A, Scribano D, Sarshar M, Di Bonaventura G, Palamara AT, Ambrosi C. Gram-negative bacteria holding together in a biofilm: the Acinetobacter baumannii way. Microorganisms. 2021 Jun 22; 9(7):1353. doi: 10.3390/microorganisms9071353.

Smitran A, Lukovic B, Bozic L, Jelic D, Jovicevic M, Kabic J, et al. Carbapenem-resistant Acinetobacter baumannii: biofilm-associated genes, biofilm-eradication potential of disinfectants, and biofilm-inhibitory effects of Selenium nanoparticles. Microorganisms. 2023 Jan 10;11(1):171. doi: 10.3390/microorganisms11010171.

Tran PA, O'Brien-Simpson N, Palmer JA, Bock N, Reynolds EC, Webster TJ, et al. Selenium nanoparticles as anti-infective implant coatings for trauma orthopedics against methicillin-resistant Staphylococcus aureus and epidermidis: in vitro and in vivo assessment. Int J Nanomedicine. 2019 Jul 1;14:4613-24. doi: 10.2147/IJN.S197737.

Ramya S, Shanmugasundaram T, Balagurunathan R. Biomedical potential of Actinobacterially synthesized Selenium nanoparticles with special reference to anti- biofilm, anti-oxidant, wound healing, cytotoxic and anti-viral activities. J Trace Elem Med Biol. 2015 Oct;32:30–9. doi: 10.1016/j.jtemb.2015.05.005.

Hosseini Bafghi M, Zarrinfar H, Darroudi M, Zargar M, Nazari R. Green synthesis of selenium nanoparticles and evaluate their effect on the expression of ERG3, ERG11 and FKS1 antifungal resistance genes in Candida albicans and Candida glabrata. Lett Appl Microbiol. 2022 May;74(5):809-19. doi: 10.1111/lam.13667.

Ullah A, Mirani ZA, Binbin S, Wang F, Chan MWH, Aslam S, et al. An elucidative study of the anti-biofilm effect of selenium nanoparticles (SeNPs) on selected biofilm producing pathogenic bacteria: A disintegrating effect of SeNPs on bacteria. Process Biochem. 2023;126:98-107. doi:10.1016/j.procbio.2022.12.031.

Prateeksha, Singh BR, Shoeb M, Sharma S, Naqvi AH, Gupta VK, et al. Scaffold of Selenium nanovectors and honey phytochemicals for inhibition of Pseudomonas aeruginosa quorum sensing and biofilm formation. Front Cell Infect Microbiol. 2017 Mar 23;7:93. doi: 10.3389/fcimb.2017.00093.

Published
2024/06/28
Section
Original article