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

  • Eri Yoshida
  • Murray Lawn
  • Takeshi Nagayasu
  • Kai Kamada
Research Paper

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.

Keywords

Titanate nanosheets Quaternary ammonium compounds Enterobacter cloacae Antibacterial Bactericidal Colloids 

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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
  15. 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
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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):127–135Google Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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
  27. 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

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Eri Yoshida
    • 1
  • Murray Lawn
    • 2
  • Takeshi Nagayasu
    • 1
  • Kai Kamada
    • 2
  1. 1.Graduate School of Biomedical SciencesNagasaki UniversityNagasakiJapan
  2. 2.Graduate School of Engineering, Department of Chemistry and Materials EngineeringNagasaki UniversityNagasakiJapan

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