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Disinfection efficacy of ozone on ESKAPE bacteria biofilms: Potential use in difficult-to-access medical devices

Published:April 25, 2022DOI:https://doi.org/10.1016/j.ajic.2022.03.037

      Highlight

      • ESKAPE bacteria with biofilm-forming capacity.
      • Ozone showed bactericidal activity on bacteria ESKAPE.
      • Ozone as a disinfectant alternative.

      Abstract

      Background

      Medical devices can be reservoirs of multidrug-resistant bacteria that may be involved in the acquisition of infections since bacteria with the ability to form biofilms that are difficult to eradicate, mainly in mechanical ventilators. The aim of this work was to evaluate the efficacy of O3 against biofilms of bacteria ESKAPE group through disinfection studies.

      Methods

      The formation of biofilms of ESKAPE group bacteria was induced in vitro. O3 was injected at different exposure times at a constant dose of 600 mg/h. The recovery of surviving bacteria after O3 treatment was assessed by bacterial counts and biofilm disruption was analyzed. Finally, the viability and integrity of biofilms after O3 treatment was determined by confocal laser scanning microscopy (CLSM).

      Results

      O3 showed bactericidal activity on biofilms from 12 min/7.68 ppm for A. baumannii and C. freundii. P. aeruginosa, K. pneumoniae and S. aureus were killed after 15 min/9.60 ppm. Correlation analyses showed inversely proportional relationships between the variables "disruption versus O3". CLSM revealed that death was time-dependent of biofilms upon O3 exposure. Orthogonal plane analysis showed that bacteria located in the outer region of the biofilms were the ones that initially suffered damage from O3 exposure.

      Conclusions

      Our findings suggest that this method could be an alternative for the disinfection in mechanical ventilators colonized by bacteria biofilm forming.

      Keywords

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      References

        • Sosa-Hernández O
        • Matías-Téllez B
        • Estrada-Hernández A
        • et al.
        Incidence and costs of ventilator-associated pneumonia in the adult intensive care unit of a tertiary referral hospital in Mexico.
        Am j Infect Control. 2019; 47: e21-e25
        • Ibn Saied W
        • Mourvillier B
        • Cohen Y
        • et al.
        A Comparison of the mortality risk associated with ventilator-acquired bacterial pneumonia and nonventilator ICU-acquired bacterial pneumonia.
        Crit Care Med. 2019; 47: 345-352
        • Durán-Manuel EM
        • Cruz-Cruz C
        • Ibáñez-Cervantes G
        • et al.
        Clonal dispersion of Acinetobacter baumannii in an intensive care unit designed to patients COVID-19.
        J Infect Dev Ctries. 2021; 15: 58-68
        • Santajit S
        • Indrawattana N.
        Mechanisms of antimicrobial resistance in ESKAPE pathogens.
        Biomed Res Int. 2016; : 2475067
        • Cureño-Díaz MA
        • Durán-Manuel EM
        • Cruz-Cruz C
        • et al.
        Impact of the modification of a cleaning and disinfection method of mechanical ventilators of COVID-19 patients and ventilator-associated pneumonia: One year of experience.
        Am J Infect Control. 2021; 202149: 1474-1480
        • Josephs-Spaulding J
        • Singh OV.
        Medical device sterilization and reprocessing in the era of Multidrug-Resistant (MDR) bacteria: issues and regulatory concepts.
        Front Med Technol. 2021; 2587352
        • Ibáñez-Cervantes G
        • Lugo-Zamudio GE
        • Cruz-Cruz C
        • et al.
        Ozone as an alternative decontamination process for N95 facemask and biosafety gowns.
        Mater Let. 2022; : 131554
        • Oliver JC
        • Bredarioli P
        • Leandro FD
        • et al.
        Ozone against Pseudomonas aeruginosa biofilms in contact lenses storage cases.
        Rev Inst Med Trop Sao Paulo. 2019; 61: e23
        • Tachikawa M
        • Yamanaka K
        • Nakamuro K.
        Studies on the disinfection and removal of biofilms by ozone water using an artificial microbial biofilm system.
        Ozone: Sci Engineer. 2009; 31: 3-9
      1. de la Salud P Regulation of the general health law on research for health. 1987. Accessed January 2, 2022. http://www.salud.gob.mx/unidades/cdi/nom/compi/rlgsmis.html.

        • Qi L
        • Li H
        • Zhang C
        • et al.
        Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii.
        Front Microbiol. 2016; 7: 483
        • Rodríguez-Baño J
        • Martí S
        • Soto S
        • et al.
        Biofilm formation in Acinetobacter baumannii: Associated features and clinical implications.
        Clin Microbiol Infect. 2008; 14: 276-278
        • Bello-López JM
        • López-Ornelas A
        • Vilchis-Rangel RE
        • et al.
        In vitro bactericidal activity of a carbohydrate polymer with zinc oxide for the treatment of chronic wounds.
        J Med Microbiol. 2020; 69: 874-880
        • Bialoszewski D
        • Pietruczuk-Padzik A
        • Kalicinska A.
        Activity of ozonated water and ozone against Staphylococcus aureus and Pseudomonas aeruginosa biofilms.
        Med Sci Monit. 2011; 17: BR339-BR344
        • Saha R
        • Saha N
        • Atwain A
        • et al.
        Evaluation of disinfection efficacy of ozone and chlorinated disinfectant against the biofilm of Klebsiella michiganensis and Pseudomonas aeruginosa.
        Ann Microbiol. 2014; 64: 1607-1613
        • Rangel K
        • Cabral FO
        • Lechuga GC
        • et al.
        Detrimental Effect of Ozone on Pathogenic Bacteria. Microorganisms. 2021; 10: 1-17
        • Sauer K
        • Camper AK
        • Ehrlich GD
        • et al.
        Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm.
        J Bacteriol. 2002; 184: 1140-1154
        • Leighton TL
        • Buensuceso RN
        • Howell PL
        • et al.
        Biogenesis of Pseudomonas aeruginosa type IV pili and regulation of their function.
        Environ Microbiol. 2015; 17: 4148-4163
        • Hynen AL
        • Lazenby JJ
        • Savva GM
        • et al.
        Multiple holins contribute to extracellular DNA release in Pseudomonas aeruginosa biofilms.
        Microbiology (Reading). 2021; 167000990
        • Colvin KM
        • Irie Y
        • Tart CS
        • et al.
        The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix.
        Environ Microbiol. 2012; 14: 1913-1928
        • Tomaras AP
        • Flagler MJ
        • Dorsey CW
        • et al.
        Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology.
        Microbiology. 2008; 154: 3398-3409
        • Lee HW
        • Koh Y
        • Kim J
        • et al.
        Capacity of multidrug-resistant clinical isolates of Acinetobacter baumannii to form biofilm and adhere to epithelial cell surfaces.
        Clin Microbiol Infec. 2008; 14: 49-54
        • Gaddy JA
        • Tomaras AP
        • Actis LA.
        The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells.
        Infect Immun. 2009; 77: 3150-3160
        • Murphy CN
        • Clegg S.
        Klebsiella pneumoniae and type 3 fimbriae: nosocomial infection, regulation and biofilm formation.
        Future Microbiol. 2012; 7: 991-1002
        • Morales-León F
        • Opazo-Capurro A
        • Caro C
        • et al.
        Hypervirulent and hypermucoviscous extended-spectrum β-lactamase-producing Klebsiella pneumoniae and Klebsiella variicola in Chile.
        Virulence. 2021; 12: 35-44
        • Pereira AL
        • Silva TN
        • Gomes AC
        • et al.
        Diarrhea-associated biofilm formed by enteroaggregative Escherichia coli and aggregative Citrobacter freundii: a consortium mediated by putative F pili.
        BMC microbiology. 2010; 23: 10-57
        • Lee JS
        • Bae YM
        • Lee SY
        • et al.
        Biofilm formation of Staphylococcus aureus on various surfaces and their resistance to chlorine sanitizer.
        J Food Sci. 2015; 80: M2279-M2286
        • Parastan R
        • Kargar M
        • Solhjoo K
        • et al.
        Staphylococcus aureus biofilms: structures, antibiotic resistance, inhibition, and vaccines.
        Gene Reports. 2020; 20100739
        • Cue D
        • Lei MG
        • Lee CY.
        Genetic regulation of the intercellular adhesion locus in staphylococci.
        Front Cell Infect Microbiol. 2012; 26: 38
        • Tachikawa M
        • Yamanaka K.
        Synergistic disinfection and removal of biofilms by a sequential two-step treatment with ozone followed by hydrogen peroxide.
        Water Res. 2014; 64: 94-101
        • Ibáñez-Cervantes G
        • Bravata-Alcántara JC
        • Nájera-Cortés AS
        • et al.
        Disinfection of N95 masks artificially contaminated with SARS-CoV-2 and ESKAPE bacteria using hydrogen peroxide plasma: Impact on the reutilization of disposable devices.
        Am J Infect Control. 2020; 48: 1037-1041
        • Tajeddin E
        • Rashidan M
        • Razaghi M
        • et al.
        The role of the intensive care unit environment and health-care workers in the transmission of bacteria associated with hospital acquired infections.
        J Infect Public Health. 2016; 9: 13-23
        • Von Eiff C
        • Jansen B
        • Kohnen W
        • et al.
        Infections associated with medical devices.
        Drugs. 2005; 65: 179-214
        • Guillon A
        • Fouquenet D
        • Morello E
        • et al.
        Treatment of pseudomonas aeruginosa biofilm present in endotracheal tubes by poly-l-lysine.
        Antimicrobial agents chemother. 2018; 62 (e00564-18)
        • Li X
        • Sun L
        • Zhang P
        • et al.
        Novel approaches to combat medical device-associated BioFilms.
        Coatings. 2021; 11: 3-294