Inactivation of Pseudomonas aeruginosa biofilms formed under high shear stress on various hydrophilic and hydrophobic surfaces by a continuous flow of ozonated water

References

• Anicetti V, Mittelman M, Adley C, Amin P, Arigo J, Baseman H, Bevel JP, Clontz L, Deutschmann S, Devine RA et al. 2015. Bioburden and biofilm management in pharmaceutical manufacturing operations: Technical report no. 69. Bethesda (MD): Parenteral Drug Association, Inc; p. 1–67.
   Google Scholar
• Anselme K, Davidson P, Popa AM, Giazzon M, Liley M, Ploux L. 2010. The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater. 6:3824–3846. doi:10.1016/j.actbio.2010.04.001
   PubMed Web of Science ®Google Scholar
• Azeredo J, Azevedo NF, Briandet R, Cerca N, Coenye T, Costa AR, Desvaux M, Di Bonaventura G, Hebraud M, Jaglic Z, et al. 2017. Critical review on biofilm methods. Crit Rev Microbiol. 43:313–351. doi:10.1080/1040841X.2016.1208146
   PubMed Web of Science ®Google Scholar
• Brion J, Chakir A, Daumont D, Malicet J, Parisse C. 1993. High-resolution laboratory absorption cross-section of O3 - temperature effect. Chem Phys Lett. 213:610–612. doi:10.1016/0009-2614(93)89169-I
   Web of Science ®Google Scholar
• Buckingham-Meyer K, Goeres D, Hamilton MA. 2007. Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods. 70:236–244. doi:10.1016/j.mimet.2007.04.010
   PubMed Web of Science ®Google Scholar
• Coenye T, Nelis HJ. 2010. In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Methods. 83:89–105. doi:10.1016/j.mimet.2010.08.018
   PubMed Web of Science ®Google Scholar
• Costerton JW. 2004. A short history of the development of the biofilm concept. In: Ghannoum MA, O’Toole G, editors. Microbial Biofilms. Washington, DC: ASM Press; p. 4–19.
   Google Scholar
• Crawford RJ, Webb HK, Truong VK, Hasan J, Ivanova EP. 2012. Surface topographical factors influencing bacterial attachment. Adv Colloid Interface Sci. 179:142–149.
   PubMed Web of Science ®Google Scholar
• Daeschel MA, McGuire J. 1998. Interrelationships between protein surface adsorption and bacterial adhesion. Biotechnol Genet Eng Rev. 15:413–438. doi:10.1080/02648725.1998.10647964
   PubMed Web of Science ®Google Scholar
• Darouiche RO. 2001. Device-associated infections: a macroproblem that starts with microadherence. Clin Infect Dis. 33:1567–1572. doi:10.1086/323130
   PubMed Web of Science ®Google Scholar
• Domb WC. 2014. Ozone therapy in dentistry. A brief review for physicians. Interv Neuroradiol. 20:632–636. doi:10.15274/INR-2014-10083
   PubMed Web of Science ®Google Scholar
• Donlan RM, Costerton JW. 2002. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 15:167. doi:10.1128/CMR.15.2.167-193.2002
   PubMed Web of Science ®Google Scholar
• Donlan RM, Piede JA, Heyes CD, Sanii L, Murga R, Edmonds P, El-Sayed I, El-Sayed MA. 2004. Model system for growing and quantifying Streptococcus pneumoniae biofilms in situ and in real time. Appl Environ Microbiol. 70:4980–4988. doi:10.1128/AEM.70.8.4980-4988.2004
   PubMed Web of Science ®Google Scholar
• Dosti B, Guzel-Seydim Z, Greene AK. 2005. Effectiveness of ozone, heat and chloride for destroying common food spoilage bacteria in synthetic media and biofilms. Int J Dairy Technol. 58:19–24. doi:10.1111/j.1471-0307.2005.00176.x
   Web of Science ®Google Scholar
• Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8:623–633. doi:10.1038/nrmicro2415
   PubMed Web of Science ®Google Scholar
• Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life [Review]. Nat Rev Microbiol. 14:563–575. doi:10.1038/nrmicro.2016.94
   PubMed Web of Science ®Google Scholar
• Goeres D, Loetterie LR, Hamilton MA, Murga R, Kirby DW, Donlan RM. 2005. Statistical assessment of a laboratory method for growing biofilms. Microbiology. 151:757–762. doi:10.1099/mic.0.27709-0
   PubMed Web of Science ®Google Scholar
• Gomez-Suarez C, Busscher HJ, Van Der Mei HC. 2001. Analysis of bacterial detachment from substratum surfaces by the passage of air-liquid interfaces. Appl Environ Microbiol. 67:2531–2537. doi:10.1128/AEM.67.6.2531-2537.2001
   PubMed Web of Science ®Google Scholar
• Guo SS, Zhu XY, Loh XJ. 2017. Controlling cell adhesion using layer-by-layer approaches for biomedical applications. Mater Sci Eng C Mater Biol Appl. 70:1163–1175. doi:10.1016/j.msec.2016.03.074
   PubMed Web of Science ®Google Scholar
• Hadi R, Vickery K, Deva A, Charlton T. 2010. Biofilm removal by medical device cleaners: comparison of two bioreactor detection assays. J Hosp Infect. 74:160–167. doi:10.1016/j.jhin.2009.10.023
   PubMed Web of Science ®Google Scholar
• Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2:95–108. doi:10.1038/nrmicro821
   PubMed Web of Science ®Google Scholar
• Hems RS, Gulabivala K, Ng Y-L, Ready D, Spratt DA. 2005. An in vitro evaluation of the ability of ozone to kill a strain of Enterococcus faecalis. Int Endod J. 38:22–29. doi:10.1111/j.1365-2591.2004.00891.x
   PubMed Web of Science ®Google Scholar
• Herigstad B, Hamilton M, Heersink J. 2001. How to optimize the drop plate method for enumerating bacteria. J Microbiol Methods. 44:121–129. doi:10.1016/S0167-7012(00)00241-4
   PubMed Web of Science ®Google Scholar
• Hori K, Matsumoto S. 2010. Bacterial adhesion: From mechanism to control. Biochem Eng J. 48:424–434. doi:10.1016/j.bej.2009.11.014
   Web of Science ®Google Scholar
• Hsu LC, Fang J, Borca-Tasciuc DA, Worobo RW, Moraru CI. 2013. Effect of micro- and nanoscale topography on the adhesion of bacterial cells to solid surfaces. Appl Environ Microbiol. 79:2703–2712. doi:10.1128/AEM.03436-12
   PubMed Web of Science ®Google Scholar
• Huth KC, Quirling M, Maier S, Kamereck K, AlKhayer M, Paschos E, Welsch U, Miethke T, Brand K, Hickel R. 2009. Effectiveness of ozone against endodontopathogenic microorganisms in a root canal biofilm model. Int Endod J. 42:3–13. doi:10.1111/j.1365-2591.2008.01460.x
   PubMed Web of Science ®Google Scholar
• Ivankovic T, Goic-Barisic I, Hrenovic J. 2017. Reduced susceptibility to disinfectants of Acinetobacter baumanii biofilms on glass and ceramic. Arh Hig Rada Toksikol. 68:99–108. doi:10.1515/aiht-2017-68-2869
   PubMed Web of Science ®Google Scholar
• Khadre MA, Yousef AE, Kim JG. 2001. Microbiological aspects of ozone applications in food: a review. J Food Sci. 66:1242–1252. doi:10.1111/j.1365-2621.2001.tb15196.x
   Web of Science ®Google Scholar
• Knight GM, McIntyre JM, Craig GG, Mulyani, Zilm PS. 2008. The inability of Streptococcus mutans and Lactobacillus acidophilus to form a biofilm in vitro on dentine pretreated with ozone. Aust Dent J. 53:349–353. doi:10.1111/j.1834-7819.2008.00077.x
   PubMed Web of Science ®Google Scholar
• Masurovsky EB, Jordan WK. 1958. Studies on the relative bacterial cleanability of milk-contact surfaces. J Dairy Sci. 41:1342–1358. doi:10.3168/jds.S0022-0302(58)91098-1
   Web of Science ®Google Scholar
• Meas Y, Godinez LA, Bustos E. 2011. Ozone generation using boron-doped diamond electrodes. In: Brillas E, Martinez-Huitle CA, editors. Synthetic diamond films: preparation, electrochemistry, characterization, and application. Hoboken (NJ): John Willey & Sons; p. 311–331.
   Google Scholar
• Miller AZ, Sanmartin P, Pereira-Pardo L, Dionisio A, Saiz-Jimenez C, Macedo MF, Prieto B. 2012. Bioreceptivity of building stones: a review. Sci Total Environ. 426:1–12. doi:10.1016/j.scitotenv.2012.03.026
   PubMed Web of Science ®Google Scholar
• Nikkhah M, Edalat F, Manoucheri S, Khademhosseini A. 2012. Engineering microscale topographies to control the cell-substrate interface. Biomater. 33:5230–5246. doi:10.1016/j.biomaterials.2012.03.079
   PubMed Web of Science ®Google Scholar
• Parisse C, Brion J, Malicet J. 1996. UV absorption spectrum of ozone: structure analysis and study of the isotope effect in the Harley system. Chem Phys Lett. 248:31–36. doi:10.1016/0009-2614(95)01259-1
   Web of Science ®Google Scholar
• Pedersen K. 1990. Biofilm development on stainless steel and PVC surfaces in drinking water. Water Res. 24:239–243. doi:10.1016/0043-1354(90)90109-J
   Web of Science ®Google Scholar
• Pinheiro J, Bates D. 2000. Mixed effects models in S and S-PLUS. New York: Springler-Verlag.
   Google Scholar
• Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC. 2017. Package nlme: linear and nonlinear mixed effects models. R package version 31-131.
   Google Scholar
• R Core Team. 2017. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/
   Google Scholar
• Rezaee A, Ghanizadeh G, Yazdanbakhsh AR, Behzadiannejad G, Ghaneian MT, Siyadat SD, Hajizadeh E. 2008. Removal of endotoxin in water using ozonation process. Aust J Basic Appl Sci. 2:495–499.
   Google Scholar
• Robbins JB, Fisher CW, Moltz AG, Martin SE. 2005. Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. J Food Prot. 68:494–498. doi:10.4315/0362-028X-68.3.494
   PubMed Web of Science ®Google Scholar
• Santoro C, Guilizzoni M, Baena JPC, Pasaogullari U, Casalegno A, Li B, Babanova S, Artyushkova K, Atanassov P. 2014. The effects of carbon electrode surface properties on bacteria attachment and start up time of microbial fuel cells. Carbon. 67:128–139. doi:10.1016/j.carbon.2013.09.071
   Web of Science ®Google Scholar
• Simoes M, Simoes LC, Vieira MJ. 2010. A review of current and emergent biofilm control strategies. LWT Food Sci Technol. 43:573–583. doi:10.1016/j.lwt.2009.12.008
   Web of Science ®Google Scholar
• Singh A, Nocerino J. 2002. Robust estimation of mean and variance using environmental data sets with below detection limit observations. Chemometr Intell Lab Syst. 60:69–86. doi:10.1016/S0169-7439(01)00186-1
   Web of Science ®Google Scholar
• Skoog SA, Kumar G, Narayan RJ, Goering PL. 2018. Biological responses to immobilized microscale and nanoscale surface topographies. Pharmacol Ther. 182:33–55. doi:10.1016/j.pharmthera.2017.07.009
   PubMed Web of Science ®Google Scholar
• Stoodley P, Sauer K, Davies DG, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu Rev Microbiol. 56:187–209. doi:10.1146/annurev.micro.56.012302.160705
   PubMed Web of Science ®Google Scholar
• Taube H. 1956. Photochemical reactions of ozone in solution. Phys Chem Chem Phys. 53:656–665.
   Google Scholar
• Tilt N, Hamilton MA. 1999. Repeatability and reproducibility of germicide tests: a literature review. J AOAC Int. 82:384–389.
   PubMed Web of Science ®Google Scholar
• Varga L, Szigeti J. 2016. Use of ozone in the dairy industry: a review. Int J Dairy Technol. 69:157–168.
   Web of Science ®Google Scholar
• Vazquez-Nion D, Silva B, Prieto B. 2018. Influence of the properties of granitic rocks on their bioreceptivity to subaerial phototrophic biofilms. Sci Total Environ. 610:44–54.
   PubMed Web of Science ®Google Scholar
• Verran J, Packer A, Kelly PJ, Whitehead KA. 2010. Use of the atomic force microscope to determine the strength of bacterial attachment to grooved surface features. J Adhes Sci Technol. 24:2271–2285.
   Web of Science ®Google Scholar
• Verran J, Rowe DL, Boyd RD. 2001. The effect of nanometer dimension topographical features on the hygienic status of stainless steel. J Food Prot. 64:1183–1187.
   PubMed Web of Science ®Google Scholar
• Whitehead KA, Rogers D, Colligon J, Wright C, Verran J. 2006. Use of the atomic force microscope to determine the effect of substratum surface topography on the ease of bacterial removal. Colloids Surf B Biointerfaces. 51:44–53.
   PubMed Web of Science ®Google Scholar
• Williams DL, Bloebaum RD. 2009. Observing the biofilm matrix of Staphylococcus epidermidis ATCC 35984 grown using the CDC biofilm reactor. Microsc Microanal. 15:824–825.
   Web of Science ®Google Scholar