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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 37, 2021 - Issue 1
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Research Article

Anti-biofilm activity of dodecyltrimethylammonium chloride microcapsules against Salmonella enterica serovar Enteritidis and Staphylococcus aureus

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Pages 49-60 | Received 21 Aug 2020, Accepted 04 Jan 2021, Published online: 31 Jan 2021

References

  • Abdallah M, Chataigne G, Ferreira-Theret P, Benoliel C, Drider D, Dhulster P, Chihib N-E. 2014. Effect of growth temperature, surface type and incubation time on the resistance of Staphylococcus aureus biofilms to disinfectants. Appl Microbiol Biotechnol. 98:2597–2607. doi:10.1007/s00253-013-5479-4
  • Abdallah M, Khelissa O, Ibrahim A, Benoliel C, Heliot L, Dhulster P, Chihib N-E. 2015. Impact of growth temperature and surface type on the resistance of Pseudomonas aeruginosa and Staphylococcus aureus biofilms to disinfectants. Int J Food Microbiol. 214:38–47. doi:10.1016/j.ijfoodmicro.2015.07.022
  • Abrahão FR, Rocha LCR, Santos TA, Carmo E. d, Pereira LAS, Borges SV, Pereira RGFA, Botrel DA. 2019. Microencapsulation of bioactive compounds from espresso spent coffee by spray drying. LWT. 103:116–124. doi:10.1016/j.lwt.2018.12.061
  • Ben Amara C, Eghbal N, Degraeve P, Gharsallaoui A. 2016. Using complex coacervation for lysozyme encapsulation by spray-drying. J Food Eng. 183:50–57. doi:10.1016/j.jfoodeng.2016.03.016
  • Ben Amara C, Kim L, Oulahal N, Degraeve P, Gharsallaoui A. 2017. Using complexation for the microencapsulation of nisin in biopolymer matrices by spray-drying. Food Chem. 236:32–40. doi:10.1016/j.foodchem.2017.04.168
  • Carneiro HCF, Tonon RV, Grosso CRF, Hubinger MD. 2013. Encapsulation efficiency and oxidative stability of flaxseed oil microencapsulated by spray drying using different combinations of wall materials. J Food Eng. 115:443–451. doi:10.1016/j.jfoodeng.2012.03.033
  • Debbasch C, Brignole F, Pisella PJ, Warnet JM, Rat P, Baudouin C. 2001. Quaternary ammoniums and other preservatives’ contribution in oxidative stress and apoptosis on Chang conjunctival cells. Invest Ophthalmol Vis Sci. 42:642–652.
  • Delvigne F, Brognaux A, Francis F, Twizere J-C, Gorret N, Sorensen SJ, Thonart P. 2011. Green fluorescent protein (GFP) leakage from microbial biosensors provides useful information for the evaluation of the scale-down effect. Biotechnol J. 6:968–978. doi:10.1002/biot.201000410
  • Dynes JJ, Lawrence JR, Korber DR, Swerhone GDW, Leppard GG, Hitchcock AP. 2009. Morphological and biochemical changes in Pseudomonas fluorescens biofilms induced by sub-inhibitory exposure to antimicrobial agents. Can J Microbiol. 55:163–178. doi:10.1139/w08-109
  • Elersek T, Zenko M, Filipic M. 2018. Ecotoxicity of disinfectant benzalkonium chloride and its mixture with antineoplastic drug 5-fluorouracil towards alga Pseudokirchneriella subcapitata. PeerJ. 6:e4986. doi:10.7717/peerj.4986
  • Elsayed MM, Elgohary FA, Zakaria AI, Elkenany RM, EL-Khateeb AY. 2020. Novel eradication methods for Staphylococcus aureus biofilm in poultry farms and abattoirs using disinfectants loaded onto silver and copper nanoparticles. Environ Sci Pollut Res Int. 27:30716–30728. doi:10.1007/s11356-020-09340-9
  • Ferk F, Misik M, Hoelzl C, Uhl M, Fuerhacker M, Grillitsch B, Parzefall W, Nersesyan A, Micieta K, Grummt T, et al. 2007. Benzalkonium chloride (BAC) and dimethyldioctadecyl-ammonium bromide (DDAB), two common quaternary ammonium compounds, cause genotoxic effects in mammalian and plant cells at environmentally relevant concentrations. Mutagenesis. 22:363–370. doi:10.1093/mutage/gem027
  • Ferreira C, Rosmaninho R, Simões M, Pereira MC, Bastos MMSM, Nunes OC, Coelho M, Melo LF. 2010. Biofouling control using microparticles carrying a biocide. Biofouling. 26:205–212. doi:10.1080/08927010903419630
  • Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F. 2018. Biofilms in the food industry: health aspects and control methods. Front Microbiol. 9:898–898. doi:10.3389/fmicb.2018.00898
  • Gerba CP. 2015. Quaternary ammonium biocides: efficacy in application. Müller V. editor. Appl Environ Microbiol. 81:464–469. doi:10.1128/AEM.02633-14
  • Gravel J, Paradis-Bleau C, Schmitzer AR. 2017. Adaptation of a bacterial membrane permeabilization assay for quantitative evaluation of benzalkonium chloride as a membrane-disrupting agent. Medchemcomm. 8:1408–1413. doi:10.1039/c7md00113d
  • Health Council of the Netherlands. 2016. Resistance due to disinfectants - Background report to the advisory report careful use of disinfectants. p. 88.
  • Hora PI, Pati SG, McNamara PJ, Arnold WA. 2020. Increased use of quaternary ammonium compounds during the SARS-CoV-2 pandemic and beyond: consideration of environmental implications. Environ Sci Technol Lett. 7:622–631. doi:10.1021/acs.estlett.0c00437
  • Hugo WB. 1995. A brief history of heat, chemical and radiation preservation and disinfection. Int Biodeterior Biodegradation. 36:197–217. doi:10.1016/0964-8305(95)00055-0
  • I Ré M. 1998. Microencapsulation by spray drying. Dry Technol. 16:1195–1236. doi:10.1080/07373939808917460
  • Inácio ÂS, Costa GN, Domingues NS, Santos MS, Moreno AJM, Vaz WLC, Vieira OV. 2013. Mitochondrial dysfunction is the focus of quaternary ammonium surfactant toxicity to mammalian epithelial cells. Antimicrob Agents Chemother. 57:2631–2639. doi:10.1128/AAC.02437-12
  • Iñiguez-Moreno M, Gutiérrez-Lomelí M, Guerrero-Medina PJ, Avila-Novoa MG. 2018. Biofilm formation by Staphylococcus aureus and Salmonella spp. under mono and dual-species conditions and their sensitivity to cetrimonium bromide, peracetic acid and sodium hypochlorite. Braz J Microbiol. 49:310–319. doi:10.1016/j.bjm.2017.08.002
  • Ioannou CJ, Hanlon GW, Denyer SP. 2007. Action of disinfectant quaternary ammonium compounds against Staphylococcus aureus. AAC. 51:296–306. doi:10.1128/AAC.00375-06
  • Jing G, Zhou Z, Zhuo J. 2012. Quantitative structure-activity relationship (QSAR) study of toxicity of quaternary ammonium compounds on Chlorella pyrenoidosa and Scenedesmus quadricauda. Chemosphere. 86:76–82. doi:10.1016/j.chemosphere.2011.09.021
  • Kautz MJM, Dvorzhinskiy A, Frye JG, Stevenson N, Herson DS. 2013. Pathogenicity of dodecyltrimethylammonium chloride-resistant Salmonella enterica. Appl Environ Microbiol. 79:2371–2376. doi:10.1128/AEM.03228-12
  • Khelissa SO, Abdallah M, Jama C, Chihib N-E. 2019. Actively detached Pseudomonas aeruginosa biofilm cell susceptibility to benzalkonium chloride and associated resistance mechanism. Arch Microbiol. 201:747–755. doi:10.1007/s00203-019-01643-x
  • Khelissa SO, Abdallah M, Jama C, Faille C, Chihib NE. 2017. Bacterial contamination and biofilm formation on abiotic surfaces and strategies to overcome their persistence. J Mater Environ Sci. 8:3326–3346.
  • Khelissa SO, Abdallah M, Jama C, Gharsallaoui A, Chihib N-E. 2019a. Comparative study of growth temperature impact on the susceptibility of biofilm-detached and planktonic Staphylococcus aureus cells to benzalkonium chloride. Ann Microbiol. 69:291–298. doi:10.1007/s13213-018-1419-y
  • Levine SL, Han Z, Liu J, Farmer DR, Papadopoulos V. 2007. Disrupting mitochondrial function with surfactants inhibits MA-10 Leydig cell steroidogenesis. Cell Biol Toxicol. 23:385–400. doi:10.1007/s10565-007-9001-6
  • Lopes NA, Pinilla CMB, Brandelli A. 2017. Pectin and polygalacturonic acid-coated liposomes as novel delivery system for nisin: preparation, characterization and release behavior. Food Hydrocoll. 70:1–7. doi:10.1016/j.foodhyd.2017.03.016
  • Ma Z, Bumunang EW, Stanford K, Bie X, Niu YD, McAllister TA. 2019. Biofilm formation by shiga toxin-producing Escherichia coli on stainless steel coupons as affected by temperature and incubation time. Microorganisms. 7:95. doi:10.3390/microorganisms7040095
  • Martínez-Suárez JV, Ortiz S, López-Alonso V. 2016. Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments. Front Microbiol. 7:638. doi:10.3389/fmicb.2016.00638
  • Medoš Ž, Plechkova NV, Friesen S, Buchner R, Bešter-Rogač M. 2019. Insight into the hydration of cationic surfactants: a thermodynamic and dielectric study of functionalized quaternary ammonium chlorides. Langmuir. 35:3759–3772. doi:10.1021/acs.langmuir.8b03993
  • Merchel Piovesan Pereira B, Tagkopoulos I. 2019. Benzalkonium chlorides: uses, regulatory status, and microbial resistance. Appl Environ Microbiol. 85:e00377-19. doi:10.1128/AEM.00377-19
  • Mulder I, Siemens J, Sentek V, Amelung W, Smalla K, Jechalke S. 2018. Quaternary ammonium compounds in soil: implications for antibiotic resistance development. Rev Environ Sci Biotechnol. 17:159–185. doi:10.1007/s11157-017-9457-7
  • Muñoz-Bonilla A, Echeverria C, Sonseca Á, Arrieta MP, Fernández-García M. 2019. Bio-based polymers with antimicrobial properties towards sustainable development. Materials. 12:641. doi:10.3390/ma12040641
  • Paniel N, Noguer T. 2019. Detection of Salmonella in food matrices, from conventional methods to recent aptamer-sensing technologies. Foods. 8:371.
  • Perani A, Gérardin C, Stacey G, Infante MR, Vinardell P, Rodehüser L, Selve C, Maugras M. 2001. Interactions of surfactants with living cells. Induction of apoptosis by detergents containing a beta-lactam moiety. Amino Acids. 21:185–194. doi:10.1007/s007260170025
  • Rogers KS, Higgins ES. 1973. Lipophilic interactions of organic cations with mitochondrial inner membranes during respiratory control. J Biol Chem. 248:7142–7148.
  • Saccucci M, Bruni E, Uccelletti D, Bregnocchi A, Sarto MS, Bossù M, Di Carlo G, Polimeni A. 2018. Surface disinfections: present and future. J Nanomater. 2018:1–9. doi:10.1155/2018/8950143
  • Sansone F, Mencherini T, Picerno P, d’Amore M, Aquino RP, Lauro MR. 2011. Maltodextrin/pectin microparticles by spray drying as carrier for nutraceutical extracts. J Food Eng. 105:468–476. doi:10.1016/j.jfoodeng.2011.03.004
  • Šarac B, Bešter-Rogač M. 2009. Temperature and salt-induced micellization of dodecyltrimethylammonium chloride in aqueous solution: a thermodynamic study. J Colloid Interface Sci. 338:216–221. doi:10.1016/j.jcis.2009.06.027
  • Song Z, Wang H, Wu Y, Gu J, Li S, Han H. 2018. Fabrication of bis-quaternary ammonium salt as an efficient bactericidal weapon against Escherichia coli and Staphylococcus aureus. ACS Omega. 3:14517–14525. doi:10.1021/acsomega.8b01265
  • Soriano JM, Blesa J, Rico H, Molto JC, Manes J. 2002. Incidence of Staphylococcus aureus in meals from cafeterias. J Food Safety. 22:135–140. doi:10.1111/j.1745-4565.2002.tb00336.x
  • Teixeira MI, Andrade LR, Farina M, Rocha-Leão MHM. 2004. Characterization of short chain fatty acid microcapsules produced by spray drying. Mater Sci Eng C. 24:653–658. doi:10.1016/j.msec.2004.08.008
  • Tezel U, Pavlostathis SG. 2015. Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr Opin Biotechnol. 33:296–304. doi:10.1016/j.copbio.2015.03.018
  • Wickham G. 2017. An investigation into the relative resistances of common bacterial pathogens to quaternary ammonium cation disinfectants. Bioscience Horizons: Int J Stud Res. [Internet]. [accessed 2020 Mar 29] 10:(hzx008. doi:10.1093/biohorizons/hzx008
  • Xiang L, Wang X-K, Li Y-W, Huang X-P, Wu X-L, Zhao H-M, Li H, Cai Q-Y, Mo C-H. 2015. Analysis of trace quaternary ammonium compounds (QACs) in vegetables using ultrasonic-assisted extraction and gas Chromatography-Mass Spectrometry. J Agric Food Chem. 63:6689–6697. doi:10.1021/acs.jafc.5b01828
  • Yuan L, Sadiq FA, Wang N, Yang Z, He G. 2020a. Recent advances in understanding the control of disinfectant-resistant biofilms by hurdle technology in the food industry. Crit. Rev. Food Sci. Nutr. 25:1–16.
  • Yuan L, Wang N, Sadiq FA, He G. 2020b. Interspecies interactions in dual-species biofilms formed by psychrotrophic bacteria and the tolerance of sessile communities to disinfectants. J Food Prot. 83:951–958. doi:10.4315/0362-028X.JFP-19-396

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