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An investigation of the impact of triclosan adaptation on Proteus mirabilis clinical isolates from an Egyptian university hospital

  • Fungal and Bacterial Physiology - Research Paper
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Abstract

Antibiotic resistance is a main threat to the public health. It is established that the overuse and misuse of antibiotics are highly contributing to antibiotic resistance. However, the impact of nonantibiotic antimicrobial agents like biocides on antibiotic resistance is currently investigated and studied. Triclosan (TCS) is a broad-spectrum antibacterial agent widely used as antiseptic and disinfectant. In this study, we aimed to evaluate the effect of exposure of Proteus mirabilis clinical isolates to sublethal concentrations of TCS on their antibiotic susceptibility, membrane characteristics, efflux activity, morphology, and lipid profile. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of TCS were determined for 31 P. mirabilis clinical isolates. The tested isolates were adapted to increasing sublethal concentrations of TCS. The MICs of 16 antibiotics were determined before and after adaptation. Membrane characteristics, efflux activity, ultrastructure, and lipid profile of the tested isolates were examined before and after adaptation. Most adapted P. mirabilis isolates showed increased antibiotic resistance, lower membrane integrity, lower outer and inner membrane permeability, and higher membrane depolarization. Nonsignificant change in membrane potential and lipid profile was found in adapted cells. Various morphological changes and enhanced efflux activity was noticed after adaptation. The findings of the current study suggest that the extensive usage of TCS at sublethal concentrations could contribute to the emergence of antibiotic resistance in P. mirabilis clinical isolates. TCS could induce changes in the bacterial membrane properties and increase the efflux activity and in turn decrease its susceptibility to antibiotics which would represent a public health risk.

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References

  1. Abdelaziz A, Sonbol F, Elbanna T, Elekhnawy E (2019) Exposure to sublethal concentrations of benzalkonium chloride induces antimicrobial resistance and cellular changes in Klebsiellae pneumoniae clinical isolates. Microb Drug Resist 25:631–638

    Article  CAS  PubMed  Google Scholar 

  2. Braoudaki M, Hilton AC (2004) Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J Clin Microbiol 42:73–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Capita R, Riesco-Peláez F, Alonso-Hernando A, Alonso-Calleja C (2014) Exposure of Escherichia coli ATCC 12806 to sub lethal concentrations of food-grade biocides influences its ability to form biofilm, resistance to antimicrobials, and ultrastructure. Appl Environ Microbiol 80:1268–1280

    Article  PubMed  PubMed Central  Google Scholar 

  4. Carey DE, McNamara PJ (2015) The impact of triclosan on the spread of antibiotic resistance in the environment. Front Microbiol 5:17

    Article  Google Scholar 

  5. Chen CZ, Cooper SL (2002) Interactions between dendrimer biocides and bacterial membranes. Biomaterials 23:3359–3368

    Article  CAS  PubMed  Google Scholar 

  6. Clinical and Laboratory Standards Institute (CLSI) (2017) Performance standards for antimicrobial susceptibility testing. Wayne, Pennsylvania

    Google Scholar 

  7. Condell O, Iversen C, Cooney S, Power KA, Walsh C, Burgess C, Fanning S (2012) Efficacy of biocides used in the modern food industry to control Salmonella enterica, and links between biocide tolerance and resistance to clinically relevant antimicrobial compounds. Appl Environ Microbiol 78:3087–3097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Curiao T, Marchi E, Viti C, Oggioni M, Baquero F, Martinez J et al (2015) Polymorphic variation in susceptibility and metabolism of triclosan-resistant mutants of Escherichia coli and Klebsiella pneumoniae clinical strains obtained after exposure to biocides and antibiotics. Antimicrob Agents Chemother 59:3413–3423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Davin-Regli A, Pages JM (2012) Cross-resistance between biocides and antimicrobials: an emerging question. Rev Sci Tech 31:89–104

    CAS  PubMed  Google Scholar 

  10. Elbanna T, Abdelaziz A, Sonbol F, Elekhnawy E (2019) Adaptation of Pseudomonas aeruginosa clinical isolates to benzalkonium chloride retards its growth and enhances biofilm production. Mol Biol Rep 46:3437–3443

    Article  CAS  Google Scholar 

  11. El-Gamasy MA (2017) Prevalence of infective organisms of infections of urinary tract in a sample of Arab infants and children. Int Neph Andro 4:136–140

    Article  Google Scholar 

  12. Fernández-Cuenca F, Tomás M, Caballero-Moyano M, Bou G, Martínez L, Vila J et al (2015) Reduced susceptibility to biocides in Acinetobacter baumannii: association with resistance to antimicrobials, epidemiological behaviour, biological cost and effect on the expression of genes encoding porins and efflux pumps. J Antimicrob Chemother 70:3222–3229

    Article  PubMed  Google Scholar 

  13. Gidden J, Denson J, Liyanage R, Ivey DM, Lay J Jr (2009) Lipid compositions in Escherichia coli and Bacillus subtilis during growth as determined by MALDI-TOF and TOF/TOF mass spectrometry. Int J Mass Spectrom 283:178–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Girlich D, Bonnin RA, Dortet L, Naas T (2020) Genetics of acquired antibiotic resistance genes in Proteus spp. Front Microbiol 11:25

    Article  Google Scholar 

  15. Halder S, Yadav K, Sarkar R, Mukherjee S, Saha P, Karmakar S et al (2015) Alteration of zeta potential and membrane permeability in bacteria: a study with cationic agents. Springerplus 4:1–14

    Article  CAS  Google Scholar 

  16. Helmy M, Wasfi R (2014) Phenotypic and molecular characterization of plasmid mediate AmpC 훽-lactamases among Escherichia coli, Klebsiella spp., and Proteus mirabilis isolated from urinary tract infections in Egyptian hospitals. J Biomed Biotechnol 4:12–20

    Google Scholar 

  17. Huguet A, Pensec J, Soumet C (2013) Resistance in Escherichia coli: variable contribution of efflux pumps with respect to different fluoroquinolones. J Appl Microbiol 114:1294–1299

    Article  CAS  PubMed  Google Scholar 

  18. Kümmerer K (2004) Resistance in the environment. J Antimicrob Chemother 54:311–320

    Article  PubMed  Google Scholar 

  19. Liu H, Du Y, Wang X, Sun L (2004) Chitosan kills bacteria through cell membrane damage. Int J Food Microbiol 95:147–155

    Article  CAS  Google Scholar 

  20. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  21. MacFaddin JF (1976) Biochemical tests for identification of medical bacteria. Williams & Wilkins Co., Baltimore

    Google Scholar 

  22. Martins M, McCusker MP, Viveiros M, Couto I, Fanning S, Pagès J et al (2013) A simple method for assessment of MDR bacteria for over-expressed efflux pumps. Open Microbiol J 7:72–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Maseda H, Hashida Y, Konaka R, Shirai A, Kourai H (2009) Mutational upregulation of a resistance-nodulation-cell division-type multidrug efflux pump, SdeAB, upon exposure to a biocide, cetylpyridinium chloride, and antibiotic resistance in Serratia marcescens. Antimicrob Agents Chemother 53:5230–5235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. McDowell EM, Trump BF (1976) Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100:405–414

    CAS  PubMed  Google Scholar 

  25. Minarovičová J, Véghová A, Mikulášová M, Chovanová R, Šoltýs KH et al (2018) Benzalkonium chloride tolerance of Listeria monocytogenes strains isolated from a meat processing facility is related to presence of plasmid-borne bcrABC cassette. Antonie Van Leeuwenhoek 6:1–11

    Google Scholar 

  26. Nhung NT, Thuy CT, Trung NV, Campbell J, Baker S, Thwaites G, Hoa N, Carrique-Mas J (2015) Induction of antimicrobial resistance in Escherichia coli and non-typhoidal Salmonella strains after adaptation to disinfectant commonly used on farms in Vietnam. Antibiotics 4:480–494

    Article  PubMed  PubMed Central  Google Scholar 

  27. Poger D, Mark AE (2019) Effect of triclosan and chloroxylenol on bacterial membranes. J Phys Chem 123:5291–5301

    Article  CAS  Google Scholar 

  28. Romanova N, Wolffs P, Brovko L, Griffiths M (2006) Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl Environ Microbiol 72:3498–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Russell AD (2000) Do biocides select for antibiotic resistance? J Pharm Pharmacol 52:227–233

    Article  CAS  PubMed  Google Scholar 

  30. Saleh S, Haddadin RNS, Baillie S, Collier PJ (2011) Triclosan—an update. Lett Appl Microbiol 52:87–95

    Article  CAS  PubMed  Google Scholar 

  31. Schaffer JN, Pearson MM (2015) Proteus mirabilis and urinary tract infections. Microbiol Spectr 3:10

    Article  PubMed Central  Google Scholar 

  32. Seong M, Lee D (2017) Silver nanoparticles against Salmonella enterica serotype typhimurium: role of inner membrane dysfunction. Curr Microbol 74:1–10

    Article  Google Scholar 

  33. Sonbol F, Elbanna T, Abdelaziz A, Elekhnawy E (2018) Impact of triclosan adaptation on membrane properties, efflux and antimicrobial resistance of Escherichia coli clinical isolates. J Appl Microbiol 126:730–739

    Article  Google Scholar 

  34. Soumet C, Meheust D, Pissavin M, Le Grandois P, Fremaux B, Feurer M et al (2016) Reduced susceptibilities to biocides and resistance to antibiotics in food-associated bacteria following exposure to quaternary ammonium compounds. Microbiol 121:1275–1281

    CAS  Google Scholar 

  35. Suresh M, Nithy N, Jayasree P, Kumar P (2016) Detection and prevalence of efflux pump-mediated drug resistance in clinical isolates of multidrug resistant Gram negative bacteria from north Kerala, India. Asian J Pharm Clin Res 9:324–327

    CAS  Google Scholar 

  36. To M, Favrin S, Romanova N, Griffiths M (2002) Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol 68:5258–5264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Venkatesan AK, Halden RU (2014) Wastewater treatment plants as chemical observatories to forecast ecological and human health risks of manmade chemicals. Sci Rep 4:1–11

    Google Scholar 

  38. Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. PT 40:277–283

    Google Scholar 

  39. Young KD (2007) Bacterial morphology: why have different shapes? Curr Opin Microbiol 10:596–600

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Department of Pharmaceutical Microbiology, Faculty of Pharmacy, Tanta University, Egypt.

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EE, FS, AA, and TE conceived the experiments and analyzed the results. EE conducted the experiments. All authors wrote and reviewed the manuscript.

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Correspondence to Engy Elekhnawy.

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Elekhnawy, E., Sonbol, F., Abdelaziz, A. et al. An investigation of the impact of triclosan adaptation on Proteus mirabilis clinical isolates from an Egyptian university hospital. Braz J Microbiol 52, 927–937 (2021). https://doi.org/10.1007/s42770-021-00485-4

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