Research Article
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Year 2019, Volume: 32 Issue: 3, 137 - 143, 31.10.2019

Didem Kart

https://doi.org/10.5472/marumj.637153

Abstract

References

  • [1] Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002;15:167-93. doi: 10.1128/Cmr.15.2.167.193.2002
  • [2] Peeters E, Nelis HJ, Coenye T. Evaluation of the efficacy of disinfection procedures against Burkholderia cenocepacia biofilms. J Hosp Infect 2008;70:361-8. doi: 10.1016/j. jhin.2008.08.015.
  • [3] Harriott MM, Noverr MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 2009;53:3914-22. doi: 10.1128/Aac.00657-09.
  • [4] Armbruster CE, Mobley HLT. Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Micro 2012;10:743-54. doi: 10.1038/nrmicro2890.
  • [5] Armbruster CE, Smith SN, Johnson AO, et al. The pathogenic potential of proteus mirabilis is enhanced by other uropathogens during polymicrobial urinary tract ınfection. Infect Immun 2017;85:e00808-16. doi:10.1128/IAI.00808-16.
  • [6] Armbruster CE, Forsyth-DeOrnellas V, Johnson AO, et al. Genome-wide transposon mutagenesis of Proteus mirabilis: Essential genes, fitness factors for catheter-associated urinary tract infection, and the impact of polymicrobial infection on fitness requirements. PLoS Pathog 2017;13: e1006434. doi: 10.1371/journal.ppat.1006434.
  • [7] Hidron AI, Edwards JR, Patel J, et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcareassociated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007 Infect Control Hosp Epidemiol 2008;29:996-1011. doi: 10.1086/591861.
  • [8] Paganelli FL, Willems RJ and Leavis HL. Optimizing future treatment of enterococcal infections: attacking the biofilm? Trends Microbiol 2012;20:1. doi: 10.1016/j.tim.2011.11.001.
  • [9] Kolenbrander PE, Palmer RJ, Periasamy S, et al. Oral multispecies biofilm development and the key role of cellcell distance. Nat Rev Microbiol 2010;8:471-80. doi: 10.1038/ nrmicro2381.
  • [10] Burmolle M, Webb JS, Rao D, et al. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 2016;72:3916- 23. doi: 10.1128/Aem.03022-05.
  • [11] Schwering M, Song J, Louie M, et al. Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling 2013;29:917-28. doi: 10.1080/08927.014.2013.816298.
  • [12] Galván EM, Mateyca C, Ielpi L. Role of interspecies interactions in dual-species biofilms developed in vitro by uropathogens isolated from polymicrobial urinary catheterassociated bacteriuria. Biofouling 2016;32:1067-77. doi: 10.1080/08927.014.2016.1231300.
  • [13] Peters BM, Ward RM, Rane HS, et al. Efficacy of ethanol against Candida albicans and Staphylococcus aureus polymicrobial biofilms. Antimicrob Agents Chemother 2013;57:74-82. doi: 10.1128/Aac.01599-12.
  • [14] Kart D, Tavernier S, Van Acker H, et al. Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling 2014;30: 377-83. doi:10.1080/08927.014.2013.878 333.
  • [15] ASTM Standard E2647, 2008. Test method for quantification of Pseudomonas aeruginosa biofilm grown using drip flow biofilm reactor with low shear and continuous flow. ASTM International. doi:10.1520/e2647-13.
  • [16] Goeres D, Hamilton M, Beck N, et al. A method for growing a biofilm under low shear at the air–liquid interface using the drip flow biofilm reactor. Nat Protoc 2009;4:783-8. doi: 10.1038/nprot.2009.59.
  • [17] Goeres DM, Loetterle LR, Hamilton MA, et al. Statistical assessment of a laboratory method for growing biofilms. Microbiology 2005;151:757-62. doi: 10.1099/mic.0.27709-0.
  • [18] Wang L, Dong M, Zheng J, et al. Relationship of biofilm formation and gelE gene expression in Enterococcus faecalis recovered from root canals in patients requiring endodontic retreatment. J Endod 2011;37:631-6. doi:10.1016/j. joen.2011.02.006.
  • [19] Simoes LC, Simoes M, Vieira MJ. Influence of the diversity of bacterial isolates from drinking water on resistance of biofilms to disinfection. Appl Environ Microbiol 2010;76:6673-9. doi: 10.1128/Aem.00872-10.
  • [20] Luciano CC, Olson N, Tipple AFV, et al. Evaluation of the ability of different detergents and disinfectants to remove and kill organisms in traditional biofilm. Am J Infect Control 2016;44: e243-e249. doi: 10.1016/j.ajic.2016.03.040.
  • [21] Perumal PK, Wand ME, Sutton JM, et al. Evaluation of the effectiveness of hydrogen-peroxide-based disinfectants on biofilms formed by Gram-negative pathogens. J Hosp Infect. 2014;87: 227e233. doi: 10.1016/j.jhin.2014.05.004.
  • [22] Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001;45:999-1007. doi: 10.1128/Aac.45.4.999- 1007.2001.
  • [23] Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. antimicrob Agents Chemother 2000;44:1818-24. doi: 10.1128/Aac.44.7.1818- 1824.2000.
  • [24] Kumon H, Tomochika K, Matunaga T, et al. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol Immunol 1994;38:615-9.
  • [25] Jensen ET, Kharazmi A, Lam K et al. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 1990;58:2383-5.
  • [26] Thieme L, Klinger-Strobel M, Hartung A, et al. In vitro synergism and anti-biofilm activity of ampicillin, gentamicin, ceftaroline and ceftriaxone against Enterococcus faecalis. J Antimicrob Chemother 2018;73:1553-61. doi: 10.1093/jac/ dky051.
  • [27] Li X, Lu N, Brady HR. Biomineralization strongly modulates the formation of Proteus mirabilis and Pseudomonas aeruginosa dual-species biofilms. FEMS Microbiol Ecol 2016;92:fiw189. doi: 10.1093/femsec/fiw189.
  • [28] Wasfi R, Abd El-Rahman OA, Mansour LE, et al. Antimicrobial activities against biofilm formed by Proteus mirabilis isolates from wound and urinary tract infections. Indian J Med Microbiol 2012;30:76-80. doi: 10.4103/0255-0857.93044.
  • [29] KwieciNska-Pirog J, Skowron K, Zniszczol K, et al. The assessment of Proteus mirabilis susceptibility to ceftazidime and ciprofloxacin and the impact of these antibiotics at subinhibitory concentrations on Proteus mirabilis biofilms. BioMed Res Int 2013;2013; 930876. doi: 10.1155/2013/930876.
  • [30] Rybalchenko OV, Bondarenko VM, Orlova OG, et al. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation, Arch Microbiol 2015;197:1027- 32. doi: 10.1007/s00203.015.1140-1.
  • [31] Schwendicke F, Korte F, Drfer CE, et al. Inhibition of Streptococcus mutans Growth and Biofilm Formation by Probiotics in vitro. Caries Res 2017;51:87-95. doi: 10.1159/000452960.

The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor

Year 2019, Volume: 32 Issue: 3, 137 - 143, 31.10.2019

Didem Kart

https://doi.org/10.5472/marumj.637153

Abstract

Objectives: Interspecies interactions in poly-species biofilm are substantial. Our aim is to set up dynamic biofilm models of
Enterococcus faecalis and Proteus mirabilis using Drip Flow Biofilm Reactor (DFR) and to evaluate the effect of these dual population
on anti-biofilms of some antimicrobials.
Materials and Methods: E.faecalis and P.mirabilis biofilms were formed in a DFR. Influences of the dual interactions on their
susceptibilities to antimicrobial agents (disinfectants, antibiotics and probiotic strains) were determined.
Results: Gluteraldehyde and quaternary ammonium compounds (QAC) effectively killed the cells in both biofilms of E.faecalis and
P.mirabilis. However, the efficacy of hydrogen peroxide (H2O2) was dependant on the microbial species present. P. mirabilis was less
susceptible to the ampicillin and ciprofloxacin in co-culture compared to when cultured alone. Here, the influence of the presence
of E.faecalis on P.mirabilis susceptibility was determined. For high concentrations of ciprofloxacin (1024 and 512 μg/ml), the log
reduction in P.mirabilis cells was determined as approximately 4.5 and 3.5 in mono and dual-species biofilms respectively. Compared
to B.lactis, L.acidophilus was found to be more effective both on single and dual species.
Conclusion: The effect of antimicrobial agents on microbial cells in a polymicrobial biofilm may depend on the composition of the
biofilm.

Keywords

Polymicrobial biofilm E. faecalis P. mirabilis Antimicrobial Drip flow reactor Probiotic strains

References

  • [1] Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002;15:167-93. doi: 10.1128/Cmr.15.2.167.193.2002
  • [2] Peeters E, Nelis HJ, Coenye T. Evaluation of the efficacy of disinfection procedures against Burkholderia cenocepacia biofilms. J Hosp Infect 2008;70:361-8. doi: 10.1016/j. jhin.2008.08.015.
  • [3] Harriott MM, Noverr MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 2009;53:3914-22. doi: 10.1128/Aac.00657-09.
  • [4] Armbruster CE, Mobley HLT. Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Micro 2012;10:743-54. doi: 10.1038/nrmicro2890.
  • [5] Armbruster CE, Smith SN, Johnson AO, et al. The pathogenic potential of proteus mirabilis is enhanced by other uropathogens during polymicrobial urinary tract ınfection. Infect Immun 2017;85:e00808-16. doi:10.1128/IAI.00808-16.
  • [6] Armbruster CE, Forsyth-DeOrnellas V, Johnson AO, et al. Genome-wide transposon mutagenesis of Proteus mirabilis: Essential genes, fitness factors for catheter-associated urinary tract infection, and the impact of polymicrobial infection on fitness requirements. PLoS Pathog 2017;13: e1006434. doi: 10.1371/journal.ppat.1006434.
  • [7] Hidron AI, Edwards JR, Patel J, et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcareassociated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007 Infect Control Hosp Epidemiol 2008;29:996-1011. doi: 10.1086/591861.
  • [8] Paganelli FL, Willems RJ and Leavis HL. Optimizing future treatment of enterococcal infections: attacking the biofilm? Trends Microbiol 2012;20:1. doi: 10.1016/j.tim.2011.11.001.
  • [9] Kolenbrander PE, Palmer RJ, Periasamy S, et al. Oral multispecies biofilm development and the key role of cellcell distance. Nat Rev Microbiol 2010;8:471-80. doi: 10.1038/ nrmicro2381.
  • [10] Burmolle M, Webb JS, Rao D, et al. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 2016;72:3916- 23. doi: 10.1128/Aem.03022-05.
  • [11] Schwering M, Song J, Louie M, et al. Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling 2013;29:917-28. doi: 10.1080/08927.014.2013.816298.
  • [12] Galván EM, Mateyca C, Ielpi L. Role of interspecies interactions in dual-species biofilms developed in vitro by uropathogens isolated from polymicrobial urinary catheterassociated bacteriuria. Biofouling 2016;32:1067-77. doi: 10.1080/08927.014.2016.1231300.
  • [13] Peters BM, Ward RM, Rane HS, et al. Efficacy of ethanol against Candida albicans and Staphylococcus aureus polymicrobial biofilms. Antimicrob Agents Chemother 2013;57:74-82. doi: 10.1128/Aac.01599-12.
  • [14] Kart D, Tavernier S, Van Acker H, et al. Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling 2014;30: 377-83. doi:10.1080/08927.014.2013.878 333.
  • [15] ASTM Standard E2647, 2008. Test method for quantification of Pseudomonas aeruginosa biofilm grown using drip flow biofilm reactor with low shear and continuous flow. ASTM International. doi:10.1520/e2647-13.
  • [16] Goeres D, Hamilton M, Beck N, et al. A method for growing a biofilm under low shear at the air–liquid interface using the drip flow biofilm reactor. Nat Protoc 2009;4:783-8. doi: 10.1038/nprot.2009.59.
  • [17] Goeres DM, Loetterle LR, Hamilton MA, et al. Statistical assessment of a laboratory method for growing biofilms. Microbiology 2005;151:757-62. doi: 10.1099/mic.0.27709-0.
  • [18] Wang L, Dong M, Zheng J, et al. Relationship of biofilm formation and gelE gene expression in Enterococcus faecalis recovered from root canals in patients requiring endodontic retreatment. J Endod 2011;37:631-6. doi:10.1016/j. joen.2011.02.006.
  • [19] Simoes LC, Simoes M, Vieira MJ. Influence of the diversity of bacterial isolates from drinking water on resistance of biofilms to disinfection. Appl Environ Microbiol 2010;76:6673-9. doi: 10.1128/Aem.00872-10.
  • [20] Luciano CC, Olson N, Tipple AFV, et al. Evaluation of the ability of different detergents and disinfectants to remove and kill organisms in traditional biofilm. Am J Infect Control 2016;44: e243-e249. doi: 10.1016/j.ajic.2016.03.040.
  • [21] Perumal PK, Wand ME, Sutton JM, et al. Evaluation of the effectiveness of hydrogen-peroxide-based disinfectants on biofilms formed by Gram-negative pathogens. J Hosp Infect. 2014;87: 227e233. doi: 10.1016/j.jhin.2014.05.004.
  • [22] Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001;45:999-1007. doi: 10.1128/Aac.45.4.999- 1007.2001.
  • [23] Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. antimicrob Agents Chemother 2000;44:1818-24. doi: 10.1128/Aac.44.7.1818- 1824.2000.
  • [24] Kumon H, Tomochika K, Matunaga T, et al. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol Immunol 1994;38:615-9.
  • [25] Jensen ET, Kharazmi A, Lam K et al. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 1990;58:2383-5.
  • [26] Thieme L, Klinger-Strobel M, Hartung A, et al. In vitro synergism and anti-biofilm activity of ampicillin, gentamicin, ceftaroline and ceftriaxone against Enterococcus faecalis. J Antimicrob Chemother 2018;73:1553-61. doi: 10.1093/jac/ dky051.
  • [27] Li X, Lu N, Brady HR. Biomineralization strongly modulates the formation of Proteus mirabilis and Pseudomonas aeruginosa dual-species biofilms. FEMS Microbiol Ecol 2016;92:fiw189. doi: 10.1093/femsec/fiw189.
  • [28] Wasfi R, Abd El-Rahman OA, Mansour LE, et al. Antimicrobial activities against biofilm formed by Proteus mirabilis isolates from wound and urinary tract infections. Indian J Med Microbiol 2012;30:76-80. doi: 10.4103/0255-0857.93044.
  • [29] KwieciNska-Pirog J, Skowron K, Zniszczol K, et al. The assessment of Proteus mirabilis susceptibility to ceftazidime and ciprofloxacin and the impact of these antibiotics at subinhibitory concentrations on Proteus mirabilis biofilms. BioMed Res Int 2013;2013; 930876. doi: 10.1155/2013/930876.
  • [30] Rybalchenko OV, Bondarenko VM, Orlova OG, et al. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation, Arch Microbiol 2015;197:1027- 32. doi: 10.1007/s00203.015.1140-1.
  • [31] Schwendicke F, Korte F, Drfer CE, et al. Inhibition of Streptococcus mutans Growth and Biofilm Formation by Probiotics in vitro. Caries Res 2017;51:87-95. doi: 10.1159/000452960.
There are 31 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Original Research
Authors

Didem Kart 0000-0001-7119-5763

Publication Date October 31, 2019
Published in Issue Year 2019 Volume: 32 Issue: 3

Cite

APA Kart, D. (2019). The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor. Marmara Medical Journal, 32(3), 137-143. https://doi.org/10.5472/marumj.637153
AMA Kart D. The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor. Marmara Med J. October 2019;32(3):137-143. doi:10.5472/marumj.637153
Chicago Kart, Didem. “The Susceptibility of Proteus Mirabilis and Enterococcus Faecalis to Various Antimicrobial Agents in Polymicrobial Biofilms Formed Using a Drip Flow Reactor”. Marmara Medical Journal 32, no. 3 (October 2019): 137-43. https://doi.org/10.5472/marumj.637153.
EndNote Kart D (October 1, 2019) The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor. Marmara Medical Journal 32 3 137–143.
IEEE D. Kart, “The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor”, Marmara Med J, vol. 32, no. 3, pp. 137–143, 2019, doi: 10.5472/marumj.637153.
ISNAD Kart, Didem. “The Susceptibility of Proteus Mirabilis and Enterococcus Faecalis to Various Antimicrobial Agents in Polymicrobial Biofilms Formed Using a Drip Flow Reactor”. Marmara Medical Journal 32/3 (October 2019), 137-143. https://doi.org/10.5472/marumj.637153.
JAMA Kart D. The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor. Marmara Med J. 2019;32:137–143.
MLA Kart, Didem. “The Susceptibility of Proteus Mirabilis and Enterococcus Faecalis to Various Antimicrobial Agents in Polymicrobial Biofilms Formed Using a Drip Flow Reactor”. Marmara Medical Journal, vol. 32, no. 3, 2019, pp. 137-43, doi:10.5472/marumj.637153.
Vancouver Kart D. The susceptibility of Proteus mirabilis and Enterococcus faecalis to various antimicrobial agents in polymicrobial biofilms formed using a drip flow reactor. Marmara Med J. 2019;32(3):137-43.