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Prevalence of resistance genes to biocides in antibiotic-resistant Pseudomonas aeruginosa clinical isolates

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Abstract

Background

Biocides are frequently used as preservative, disinfectant and sterilizer against many microorganisms in hospitals, industry and home. However, the reduced susceptibility rate of Pseudomonas aeruginosa (P. aeruginosa) strains to biocides is increasing. The aim of this study was to evaluate the antimicrobial activity of four frequently used biocides against P. aeruginosa and to determine the prevalence of genes involved in biocide resistance.

Methods

A total of 76 clinical isolates of P. aeruginosa strains were used in the present study. The minimum inhibitory concentrations (MICs) of four biocides, i.e. chlorhexidine digluconate, benzalkonium chloride, triclosan and formaldehyde, against P. aeruginosa strains were determined using agar dilution method. In addition, the prevalence of biocide resistance genes was determined using the polymerase chain reaction (PCR) method.

Results

In the present study, the highest MIC90 and MIC95 (epidemiological cut-off) values were observed for benzalkonium chloride (1024 μg/mL), followed by formaldehyde (512 μg/mL), triclosan (512 μg/mL) and chlorhexidine digluconate (64 μg/mL). Furthermore, the prevalence of qacEΔ1, qacE, qacG, fabV, cepA and fabI genes were 73.7% (n = 56), 26.3% (n = 20), 11.8% (n = 9), 84.2% (n = 64), 81.5% (n = 62) and 0% (n = 0), respectively. A significant association was observed between the presence of biocide resistance genes and MICs (p < 0.05). Furthermore, there was no significant association between the presence of biocide resistance genes and antibiotic resistance (p > 0.05), except for levofloxacin and norfloxacin antibiotics and qacE and qacG genes (p < 0.05).

Conclusion

Our results revealed that chlorhexidine digluconate is the most effective biocide against P. aeruginosa isolates in Ardabil hospitals. However, we recommend continuous monitoring of the antimicrobial activity of biocides and the prevalence of biocide-associated resistance genes for a better prevention of microorganism dissemination and infection control in hospitals.

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Data availability

The data that support the findings of this study are available from the corresponding author on reasonable request.

Abbreviations

MIC:

Minimum inhibitory concentration

PCR:

Polymerase chain reaction

P. aeruginosa :

Pseudomonas aeruginosa

ICU:

Intensive care unit

MDR:

Multi-drug resistant

CLSI:

Clinical and Laboratory Standards Institute

ECOFF:

Epidemiological cut-off value

ENR:

Enoyl-acyl-carrier protein reductase

References

  1. Driscoll JA, Brody SL, Kollef MH (2007) The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67(3):351–368

    Article  CAS  Google Scholar 

  2. Vaez H, Salehi-Abargouei A, Khademi F (2017) Systematic review and meta-analysis of imipenem-resistant Pseudomonas aeruginosa prevalence in Iran. Germs 7(2):86–97

    Article  CAS  Google Scholar 

  3. Moradali MF, Ghods S, Rehm BH (2017) Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 7:39

    Article  Google Scholar 

  4. Ignak S, Nakipoglu Y, Gurler B (2017) Frequency of antiseptic resistance genes in clinical staphycocci and enterococci isolates in Turkey. Antimicrob Resist Infect Control 6(1):1–7

    Article  Google Scholar 

  5. Vásquez-Giraldo DF, Libreros-Zúñiga GA, Crespo-Ortiz MD (2017) Effects of biocide exposure on P. aeruginosa, E. coli and A. baumannii complex isolates from hospital and household environments. Infection 21(4):243–50

    Google Scholar 

  6. Babenko D, Turmuhambetova A, Sandle T, Pestrea SA, Moraru D, CHEŞCĂ A (2017) In silico comparison of different types of MLVA with PFGE based on Pseudomonas aeruginosa genomes. Acta Medica 33:347–352

    Google Scholar 

  7. Wesgate R, Grasha P, Maillard J-Y (2016) Use of a predictive protocol to measure the antimicrobial resistance risks associated with biocidal product usage. Am J Infect Control 44(4):458–464

    Article  CAS  Google Scholar 

  8. Ortega-Morente E, Fernández-Fuentes MA, Grande-Burgos MJ, Abriouel H, Pérez-Pulido R, Gálvez A (2013) Biocide tolerance in bacteria. Int J Food Microbiol 162(1):13–25

    Article  Google Scholar 

  9. Murray PR, Rosenthal KS, Pfaller MA (2015) Medical microbiology, 8th edn. Elsevier Health Sciences, UK, pp 272–277

    Google Scholar 

  10. Bridier A, Dubois-Brissonnet F, Greub G, Thomas V, Briandet R (2011) Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55(6):2648–2654

    Article  CAS  Google Scholar 

  11. Mima T, Joshi S, Gomez-Escalada M, Schweizer HP (2007) Identification and characterization of TriABC-OpmH, a triclosan efflux pump of Pseudomonas aeruginosa requiring two membrane fusion proteins. J Bacteriol 189(21):7600–7609

    Article  CAS  Google Scholar 

  12. Vikram A, Bomberger JM, Bibby KJ (2015) Efflux as a glutaraldehyde resistance mechanism in Pseudomonas fluorescens and Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 59(6):3433–3440

    Article  CAS  Google Scholar 

  13. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP (2001) Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 45(2):428–432

    Article  CAS  Google Scholar 

  14. Subedi D, Vijay AK, Willcox M (2018) Study of disinfectant resistance genes in ocular isolates of Pseudomonas aeruginosa. Antibiotics 7(4):88

    Article  CAS  Google Scholar 

  15. CLSI, 2018. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Eighth Informational Supplement. CLSI Document M100. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA.

  16. Bazghandi SA, Safarirad S, Arzanlou M, Peeri-Dogaheh H, AliMohammadi H, Khademi F (2021) Prevalence of multidrug-resistant Pseudomonas aeruginosa strains in Ardabil. J Ardabil Univ Med Sci 20(2):280–286

    Article  Google Scholar 

  17. Khademi F, Ashrafi SS, Neyestani Z, Vaez H, Sahebkar A (2021) Prevalence of class I, II and III integrons in multidrug-resistant and carbapenem-resistant Pseudomonas aeruginosa clinical isolates. Gene Rep 25:101407

    Article  Google Scholar 

  18. Delarampour A, Ghalehnoo ZR, Khademi F, Delarampour M, Vaez H (2019) Molecular detection of carbapenem-resistant genes in clinical isolates of Klebsiella pneumoniae. Ann Ig 31(4):349–355

    CAS  PubMed  Google Scholar 

  19. Rizzotti L, Rossi F, Torriani S (2016) Biocide and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from the swine meat chain. Food Microbiol 60:160–164

    Article  CAS  Google Scholar 

  20. Chapman JS (2003) Biocide resistance mechanisms. Int Biodeterior. Biodegradation 51(2):133–138

    Article  CAS  Google Scholar 

  21. Romão C, Miranda CA, Silva J, Clementino MM, de Filippis I, Asensi M (2011) Presence of qacEΔ1 gene and susceptibility to a hospital biocide in clinical isolates of Pseudomonas aeruginosa resistant to antibiotics. Curr Microbiol 63(1):16–21

    Article  Google Scholar 

  22. Zhu L, Lin J, Ma J, Cronan JE, Wang H (2010) Triclosan resistance of Pseudomonas aeruginosa PAO1 is due to FabV, a triclosan-resistant enoyl-acyl carrier protein reductase. Antimicrob Agents Chemother 54(2):689–698

    Article  CAS  Google Scholar 

  23. Heath RJ, Rock CO (2000) A triclosan-resistant bacterial enzyme. Nature 406(6792):145–146

    Article  CAS  Google Scholar 

  24. Huang YH, Lin JS, Ma JC, Wang HH (2016) Functional characterization of triclosan-resistant enoyl-acyl-carrier protein reductase (FabV) in Pseudomonas aeruginosa. Front Microbiol 7:1903

    PubMed  PubMed Central  Google Scholar 

  25. Thomas L, Maillard JY, Lambert RJ, Russell AD (2000) Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a “residual” concentration. J Hosp Infect 46(4):297–303

    Article  CAS  Google Scholar 

  26. Hassan KA, Liu Q, Henderson PJ, Paulsen IT (2015) Homologs of the Acinetobacter baumannii AceI transporter represent a new family of bacterial multidrug efflux systems. MBio 6(1):e01982-e2014

    Article  CAS  Google Scholar 

  27. Mendes ET, Ranzani OT, Marchi AP, da Silva MT, Amigo Filho JU, Alves T, Guimarães T, Levin AS, Costa SF (2016) Chlorhexidine bathing for the prevention of colonization and infection with multidrug-resistant microorganisms in a hematopoietic stem cell transplantation unit over a 9-year period: Impact on chlorhexidine susceptibility. Medicine 95(46):1–8

    Article  Google Scholar 

  28. Vijayakumar R, Sandle T, Al-Aboody MS, Alfonaisan MK, Alturaiki W, Mickymaray S, Premanathan M, Alsagaby SA (2018) Distribution of biocide resistant genes and biocides susceptibility in multidrug-resistant Klebsiella pneumoniae, Pseudomonas aeruginosa and Acinetobacter baumannii—A first report from the Kingdom of Saudi Arabia. J Infect Public Health 11(6):812–816

    Article  Google Scholar 

  29. Kücken D, Feucht HH, Kaulfers PM (2000) Association of qacE and qacEΔ1 with multiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria. FEMS Microbiol Lett 183(1):95–98

    Article  Google Scholar 

  30. Helal ZH, Khan MI (2015) QacE and QacEΔ1 Genes and Their Correlation to Antibiotics and Biocides Resistance Pseudomonas aeruginosa. Am J Biomed Sci 7(2):52–62

    Article  CAS  Google Scholar 

  31. Mahzounieh M, Khoshnood S, Ebrahimi A, Habibian S, Yaghoubian M (2014) Detection of antiseptic-resistance genes in Pseudomonas and Acinetobacter spp. isolated from burn patients. Jundishapur J Nat Pharm Prod 9(2):e15402

    Article  Google Scholar 

  32. McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12(1):147–179

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the Vice Chancellor for Research and Technology, Ardabil University of Medical Sciences, Ardabil, Iran, due to financial support.

Funding

This research was supported by Ardabil University of Medical Sciences, Iran (Grant Number: 1005761).

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran

    Malek Namaki, Mohsen Arzanlou, Somayeh Safarirad, Seyed Ali Bazghandi & Farzad Khademi

  2. Department of Infectious Diseases, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran

    Shahram Habibzadeh

  3. Department of Microbiology, School of Medicine, Zabol University of Medical Sciences, Zabol, Iran

    Hamid Vaez

  4. Applied Biomedical Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Amirhossein Sahebkar

  5. Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

    Amirhossein Sahebkar

  6. School of Medicine, The University of Western Australia, Perth, Australia

    Amirhossein Sahebkar

  7. School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

    Amirhossein Sahebkar

Authors
  1. Malek Namaki
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  2. Shahram Habibzadeh
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  3. Hamid Vaez
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  4. Mohsen Arzanlou
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  5. Somayeh Safarirad
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  6. Seyed Ali Bazghandi
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  7. Amirhossein Sahebkar
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  8. Farzad Khademi
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Contributions

MN, SS and SAB collected the data. FK and HV analyzed the data and led the writing of the manuscript. SH, MA and AS revised the manuscript.

Corresponding author

Correspondence to Farzad Khademi.

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The authors declare that there is no conflict of interest.

Ethical approval

This research was approved by the Research Ethics Committee of Ardabil University of Medical Sciences.

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Informed written consent was given to subjects from whom the samples were obtained for this study.

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Namaki, M., Habibzadeh, S., Vaez, H. et al. Prevalence of resistance genes to biocides in antibiotic-resistant Pseudomonas aeruginosa clinical isolates. Mol Biol Rep 49, 2149–2155 (2022). https://doi.org/10.1007/s11033-021-07032-2

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  • DOI: https://doi.org/10.1007/s11033-021-07032-2

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