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Enhancement of antibacterial effect of quaternary ammonium with inorganic nanosheets against Enterobacter cloacae

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Abstract

To suppress nosocomial infections, numerous studies of quaternary ammonium cations (R4N+) to improve the antibiotic properties have been investigated. However, most of them reported developments of novel organic or polymeric materials with R4N+. To pioneer antibacterial inorganic materials hybridized with R4N+, a colloidal solution of metal oxide nanosheets, which have a small particle size (typically less than 10 nm), is considered to be a suitable option because oxide nanosheets with a negative surface charge strongly interact R4N+. Herein, we demonstrate for the first time that the high antibacterial/bactericidal effects of titanate nanosheets (TNS) adsorbing tetramethylammonium (TMA-TNS) or tetrabultylammonium ions (TBA-TNS). Their antibacterial effects against Enterobacter cloacae were evaluated using a colony forming unit (CFU) counting method. The results showed that the synthesized TNS composites had superior antibacterial and bactericidal effects to those of free R4N+ and TBA-TNS exhibited the strongest effect (69% CFU reduction compared with that of free TBA+ and 98% CFU reduction compared with the control) among the samples examined. Dark incubation was employed to ensure that photocatalytic reaction of semiconducting TNS did not contribute to the process. Compared with TiO2 spherical particles, such high bactericidal effect would be induced by a synergistic function of TBA+ and TNS, which physically damages bacteria due to long hydrophobic alkyl chains and an anisotropic nanocrystalline structure with sharp edges, respectively.

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References

  • Chanawanno K, Chantrapromma S, Anantapong T, Kanjana-Opas A, Fun H (2010) Synthesis, structure and in vitro antibacterial activities of new hybrid disinfectants quaternary ammonium compounds: Pyridinium and quinolinium stilbene benzenesulfonates. Eur J Med Chem 45:4199–4208. https://doi.org/10.1016/j.ejmech.2010.06.014

    Article  Google Scholar 

  • Chen M, Hu M, Wang D, Wang G, Zhu X, Yan D, Sun J (2012) Multifunctional Hyperbranched Glycoconjugated polymers based on natural aminoglycosides. Bioconjug Chem 23:1189–1199. https://doi.org/10.1021/bc300016b

    Article  Google Scholar 

  • Chen M, Zhu X, Yan D (2014) A controlled release system for simultaneous promotion of gene transfection and antitumor effects. RSC Adv 4:64596–64600. https://doi.org/10.1039/c4ra10447a

    Article  Google Scholar 

  • Davin-Regli A, Pagès J (2015) Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00392

  • Deal EN, Micek ST, Ritchie DJ, Reichley RM, Dunne WM, Kollef MH (2007) Predictors of in-hospital mortality for bloodstream infections caused by Enterobacter species or Citrobacter freundii. Pharmacotherapy 27:191–199. https://doi.org/10.1592/phco.27.2.191

    Article  Google Scholar 

  • Farah S, Aviv O, Laout N, Ratner S, Beyth N, Domb AJ (2015) Quaternary ammonium poly(diethylaminoethyl methacrylate) possessing antimicrobial activity. Colloids Surf B 128:608–613. https://doi.org/10.1016/j.colsurfb.2015.01.051

    Article  Google Scholar 

  • Inada M, Kamada K, Enomoto N, Hojo J (2006) Microwave effect for synthesis of TiO2 particles by self-hydrolysis of TiOCl2. J Ceram Soc Jpn 114:814–818. https://doi.org/10.2109/jcersj.114.814

    Article  Google Scholar 

  • Ivanova EP, Hasan J, Webb HK, Gervinskas G, Juodkazis S, Truong VK, Wu AHF, Lamb RN, Baulin VA, Watson GS, Watson JA, Mainwaring DE, Crawford RJ (2013) Bactericidal activity of black silicon. Nat Commun 4:2838. https://doi.org/10.1038/ncomms3838

    Article  Google Scholar 

  • Jiao Y, Niu L, Ma S, Li J, Tay FR, Chen J (2017) Quaternary ammonium-based biomedical materials: state-of-the-art, toxicological aspects and antimicrobial resistance. Prog Polym Sci 71:53–90. https://doi.org/10.1016/j.progpolymsci.2017.03.001

    Article  Google Scholar 

  • Kamada K, Soh N (2014) Temperature-controlled reversible exfoliation-stacking of Titanate Nanosheets in an aqueous solution containing Tetraalkylammonium ions. RSC Adv 4. https://doi.org/10.1039/C3RA47233G

  • Kikuchi Y, Sunada K, Iyoda T, Hashimoto K, Akira Fujishima A (1997) Photocatalytic bactericidal effect of TiO2 thin films: dynamic view of the active oxygen species responsible for the effect. J Photochem Photobiol A 106:51–56. https://doi.org/10.1016/s1010-6030(97)00038-5

    Article  Google Scholar 

  • Kim CH, Choi JW, Chun HJ, Choi KS (1997) Synthesis of chitosan derivatives with quaternary ammonium salt and their antibacterial activity. Polym Bull 38:387–393. https://doi.org/10.1007/s002890050064

    Article  Google Scholar 

  • Kourai H, Yabuhara T, Shirai A, Maeda T, Nagamune H (2006) Syntheses and antimicrobial activities of a series of new bis-quaternary ammonium compounds. Eur J Med Chem 41:437–444. https://doi.org/10.1016/j.ejmech.2005.10.021

    Article  Google Scholar 

  • Kubacka A, Diez MS, Rojo D, Bargiela R, Ciordia S, Zapico I, Albar JP, Barbas C, Martins Dos Santos VAP, Fernández-García M, Ferrer M (2014) Understanding the antimicrobial mechanism of TiO2-based nanocomposite films in a pathogenic bacterium. Sci Rep 4. https://doi.org/10.1038/srep04134

  • Maeda T, Manabe Y, Yamamoto M, Yoshida M, Okazaki K, Nagamune H, Kourai H (1999) Synthesis and antimicrobial characteristics of novel biocides, 4,4-(1,6-Hexamethylenedioxydicarbonyl)bis(1-alkylpyridinium iodide)s. Chem Pharm Bull. https://doi.org/10.1248/cpb.47.1020

  • Muramatsu M, Akatsuka K, Ebina Y, Wang K, Sasaki T, Ishida T, Miyake K, Haga M (2005) Fabrication of densely packed Titania Nanosheet films on solid surface by use of Langmuir−Blodgett deposition method without amphiphilic additives. Langmuir 21:6590–6595. https://doi.org/10.1021/la050293f

    Article  Google Scholar 

  • Ohya T, Nakayama A, Ban T, Ohya Y, Takahashi Y (2002) Synthesis and characterization of halogen-free, transparent, aqueous colloidal Titanate solutions from titanium Alkoxide. Chem Mater 14:3082–3089. https://doi.org/10.1021/cm0200588

    Article  Google Scholar 

  • Pfaller MA, Bassetti M, Duncan LR, Castanheira M (2017) Ceftolozane/tazobactam activity against drug-resistant Enterobacteriaceae and Pseudomonas aeruginosa causing urinary tract and intraabdominal infections in Europe: report from an antimicrobial surveillance programme (2012–15). J Antimicrob Chemother 72:1386–1395. https://doi.org/10.1093/jac/dkx009

    Article  Google Scholar 

  • Pfaller MA, Shortridge D, Sader HS, Castanheira M, Flamm RK (2018) Ceftolozane/tazobactam activity against drug-resistant Enterobacteriaceae and Pseudomonas aeruginosa causing healthcare-associated infections in the Asia-Pacific region (minus China, Australia and New Zealand): report from an antimicrobial surveillance Programme (2013–2015). Int J Antimicrob Agents 51:181–189. https://doi.org/10.1016/j.ijantimicag.2017.09.016

    Article  Google Scholar 

  • Poorabbas B, Mardaneh J, Rezaei Z, Kalani M, Pouladfar G, Alami MH, Soltani J, Shamsi-Zadeh A, Abdoli-Oskooi S, Saffar MJ, Alborzi A (2015) Nosocomial infections: multicenter surveillance of antimicrobial resistance profile of Staphylococcus aureus and gram negative rods isolated from blood and other sterile body fluids in Iran. Iran J Microbiol 7(3):127–135

    Google Scholar 

  • Shtyrlin NV, Sapozhnikov SV, Galiullina AS, Kayumov AR, Bondar OV, Mirchink EP, Isakova EB, Firsov AA, Balakin KV, Shtyrlin YG (2016) Synthesis and antibacterial activity of quaternary ammonium 4-Deoxypyridoxine derivatives. Biomed Res Int 2016:1–8. https://doi.org/10.1155/2016/3864193

    Article  Google Scholar 

  • Souza AOD, Galetti FCS, Silva CL, Bicalho B, Parma MM, Fonseca SF, Marsaioli AJ, Trindade ACLB, Gil RPF, Bezerra FS, Andrade-Neto M, Oliveira MCF (2007) Antimycobacterial and cytotoxicity activity of synthetic and natural compounds. Quim Nova 30. https://doi.org/10.1590/s0100-40422007000700012

  • Tanaka T, Fukuda K, Ebina Y, Takada K, Sasaki T (2004) Highly organized self-assembled monolayer and multilayer films of Titania Nanosheets. Adv Mater 16:872–875. https://doi.org/10.1002/adma.200306470

    Article  Google Scholar 

  • Ye Y, Li JB, Ye DQ, Jiang ZJ (2006) Enterobacter bacteremia: clinical features, risk factors for multiresistance and mortality in a Chinese University hospital. Infection 34:252–257. https://doi.org/10.1007/s15010-006-5038-3

    Article  Google Scholar 

  • Zalacain M, Biedenbach DJ, Badal RE, Young K, Motyl M, Sahm DF (2016) Pathogen prevalence and antimicrobial susceptibility among Enterobacteriaceae causing hospital-associated intra-abdominal infections in adults in the United States (2012–2013). Clin Ther 38:1510–1521. https://doi.org/10.1016/j.clinthera.2016.04.035

    Article  Google Scholar 

  • Zaltsman N, Kesler-Shvero D, Weiss EI, Beyth N (2016) Synthesis variants of quaternary ammonium polyethyleneimine nanoparticles and their antibacterial efficacy in dental materials. J Appl Biomater Funct Mater 14:0. https://doi.org/10.5301/jabfm.5000269

    Google Scholar 

  • Zhang Y, Zhou Z, Chen M (2018) The length of hydrophobic chain in amphiphilic polypeptides regulates the efficiency of gene delivery. Polymer 10. https://doi.org/10.3390/polym10040379

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Acknowledgements

The authors would like to thank Yuki Nakatsu (Faculty of Engineering, Nagasaki University) for his technical assistance.

Funding

The present work was partly supported by Research Fellow of Japan Society for the Promotion of Science (JSPS), KAKENHI Grant No. 26410244 and 16J10617.

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Authors and Affiliations

  1. Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, 852-8521, Japan

    Eri Yoshida & Takeshi Nagayasu

  2. Graduate School of Engineering, Department of Chemistry and Materials Engineering, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki, 852-8521, Japan

    Murray Lawn & Kai Kamada

Authors
  1. Eri Yoshida
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  2. Murray Lawn
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  3. Takeshi Nagayasu
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  4. Kai Kamada
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Correspondence to Kai Kamada.

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Yoshida, E., Lawn, M., Nagayasu, T. et al. Enhancement of antibacterial effect of quaternary ammonium with inorganic nanosheets against Enterobacter cloacae. J Nanopart Res 20, 199 (2018). https://doi.org/10.1007/s11051-018-4303-6

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