Skip to main content
PMC home page
Antimicrobial Agents and Chemotherapy logoLink to Antimicrobial Agents and Chemotherapy
. 1997 Jun;41(6):1352–1358. doi: 10.1128/aac.41.6.1352

Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa bofilms displaying rapid-transport characteristics.

J D Vrany 1, P S Stewart 1, P A Suci 1
PMCID: PMC163914  PMID: 9174198

Abstract

Attenuated total reflection Fourier transform infrared spectroscopy was used to measure transport of the fluoroquinolones (FQs) ciprofloxacin and levofloxacin into Pseudomonas aeruginosa biofilms. Biofilms were exposed to each FQ at dose levels of 100, 250, and 500 microg/ml for 30 min. A mathematical transport model was used to extract the diffusion coefficient, binding site density, and adsorption and desorption rates for each experiment. Recalcitrance of the biofilms toward each FQ was evaluated by comparison of efficacies with planktonic bacteria. By this criterion, biofilms were found to exhibit more recalcitrance toward levofloxacin than ciprofloxacin under the experimental conditions. These results cannot be explained by the more hindered transport of levofloxacin, implicating the domination of physiological factors.

Full Text

The Full Text of this article is available as a PDF (392.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anwar H., Costerton J. W. Enhanced activity of combination of tobramycin and piperacillin for eradication of sessile biofilm cells of Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1990 Sep;34(9):1666–1671. doi: 10.1128/aac.34.9.1666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anwar H., Strap J. L., Costerton J. W. Kinetic interaction of biofilm cells of Staphylococcus aureus with cephalexin and tobramycin in a chemostat system. Antimicrob Agents Chemother. 1992 Apr;36(4):890–893. doi: 10.1128/aac.36.4.890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anwar H., van Biesen T., Dasgupta M., Lam K., Costerton J. W. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system. Antimicrob Agents Chemother. 1989 Oct;33(10):1824–1826. doi: 10.1128/aac.33.10.1824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bedard J., Chamberland S., Wong S., Schollaardt T., Bryan L. E. Contribution of permeability and sensitivity to inhibition of DNA synthesis in determining susceptibilities of Escherichia coli, Pseudomonas aeruginosa, and Alcaligenes faecalis to ciprofloxacin. Antimicrob Agents Chemother. 1989 Sep;33(9):1457–1464. doi: 10.1128/aac.33.9.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blaser J., Vergères P., Widmer A. F., Zimmerli W. In vivo verification of in vitro model of antibiotic treatment of device-related infection. Antimicrob Agents Chemother. 1995 May;39(5):1134–1139. doi: 10.1128/aac.39.5.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown M. L., Aldrich H. C., Gauthier J. J. Relationship between glycocalyx and povidone-iodine resistance in Pseudomonas aeruginosa (ATCC 27853) biofilms. Appl Environ Microbiol. 1995 Jan;61(1):187–193. doi: 10.1128/aem.61.1.187-193.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chapman J. S., Georgopapadakou N. H. Routes of quinolone permeation in Escherichia coli. Antimicrob Agents Chemother. 1988 Apr;32(4):438–442. doi: 10.1128/aac.32.4.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chu D. T., Fernandes P. B. Structure-activity relationships of the fluoroquinolones. Antimicrob Agents Chemother. 1989 Feb;33(2):131–135. doi: 10.1128/aac.33.2.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crumplin G. C., Smith J. T. Nalidixic acid: an antibacterial paradox. Antimicrob Agents Chemother. 1975 Sep;8(3):251–261. doi: 10.1128/aac.8.3.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deretic V., Schurr M. J., Boucher J. C., Martin D. W. Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors. J Bacteriol. 1994 May;176(10):2773–2780. doi: 10.1128/jb.176.10.2773-2780.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Domagala J. M., Heifetz C. L., Hutt M. P., Mich T. F., Nichols J. B., Solomon M., Worth D. F. 1-Substituted 7-[3-[(ethylamino)methyl]-1-pyrrolidinyl]-6,8- difluoro-1,4-dihydro-4-oxo-3-quinolinecarboxylic acids. New quantitative structure-activity relationships at N1 for the quinolone antibacterials. J Med Chem. 1988 May;31(5):991–1001. doi: 10.1021/jm00400a017. [DOI] [PubMed] [Google Scholar]
  12. Evans D. J., Allison D. G., Brown M. R., Gilbert P. Susceptibility of Pseudomonas aeruginosa and Escherichia coli biofilms towards ciprofloxacin: effect of specific growth rate. J Antimicrob Chemother. 1991 Feb;27(2):177–184. doi: 10.1093/jac/27.2.177. [DOI] [PubMed] [Google Scholar]
  13. Evans R. C., Holmes C. J. Effect of vancomycin hydrochloride on Staphylococcus epidermidis biofilm associated with silicone elastomer. Antimicrob Agents Chemother. 1987 Jun;31(6):889–894. doi: 10.1128/aac.31.6.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Furet Y. X., Deshusses J., Pechère J. C. Transport of pefloxacin across the bacterial cytoplasmic membrane in quinolone-susceptible Staphylococcus aureus. Antimicrob Agents Chemother. 1992 Nov;36(11):2506–2511. doi: 10.1128/aac.36.11.2506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gilbert P., Collier P. J., Brown M. R. Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother. 1990 Oct;34(10):1865–1868. doi: 10.1128/aac.34.10.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gootz T. D., McGuirk P. R., Moynihan M. S., Haskell S. L. Placement of alkyl substituents on the C-7 piperazine ring of fluoroquinolones: dramatic differential effects on mammalian topoisomerase II and DNA gyrase. Antimicrob Agents Chemother. 1994 Jan;38(1):130–133. doi: 10.1128/aac.38.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gordon C. A., Hodges N. A., Marriott C. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J Antimicrob Chemother. 1988 Nov;22(5):667–674. doi: 10.1093/jac/22.5.667. [DOI] [PubMed] [Google Scholar]
  18. Gordon C. A., Hodges N. A., Marriott C. Use of slime dispersants to promote antibiotic penetration through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1991 Jun;35(6):1258–1260. doi: 10.1128/aac.35.6.1258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Green N. M. Avidin. Adv Protein Chem. 1975;29:85–133. doi: 10.1016/s0065-3233(08)60411-8. [DOI] [PubMed] [Google Scholar]
  20. Gristina A. G., Oga M., Webb L. X., Hobgood C. D. Adherent bacterial colonization in the pathogenesis of osteomyelitis. Science. 1985 May 24;228(4702):990–993. doi: 10.1126/science.4001933. [DOI] [PubMed] [Google Scholar]
  21. Hodges N. A., Gordon C. A. Protection of Pseudomonas aeruginosa against ciprofloxacin and beta-lactams by homologous alginate. Antimicrob Agents Chemother. 1991 Nov;35(11):2450–2452. doi: 10.1128/aac.35.11.2450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hoyle B. D., Alcantara J., Costerton J. W. Pseudomonas aeruginosa biofilm as a diffusion barrier to piperacillin. Antimicrob Agents Chemother. 1992 Sep;36(9):2054–2056. doi: 10.1128/aac.36.9.2054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kitamura A., Hoshino K., Kimura Y., Hayakawa I., Sato K. Contribution of the C-8 substituent of DU-6859a, a new potent fluoroquinolone, to its activity against DNA gyrase mutants of Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1995 Jul;39(7):1467–1471. doi: 10.1128/aac.39.7.1467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Klopman G., Li J. Y., Wang S., Pearson A. J., Chang K., Jacobs M. R., Bajaksouzian S., Ellner J. J. In vitro anti-Mycobacterium avium activities of quinolones: predicted active structures and mechanistic considerations. Antimicrob Agents Chemother. 1994 Aug;38(8):1794–1802. doi: 10.1128/aac.38.8.1794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Korber D. R., James G. A., Costerton J. W. Evaluation of Fleroxacin Activity against Established Pseudomonas fluorescens Biofilms. Appl Environ Microbiol. 1994 May;60(5):1663–1669. doi: 10.1128/aem.60.5.1663-1669.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. LeChevallier M. W., Cawthon C. D., Lee R. G. Inactivation of biofilm bacteria. Appl Environ Microbiol. 1988 Oct;54(10):2492–2499. doi: 10.1128/aem.54.10.2492-2499.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Marsh P. D., Bradshaw D. J. Microbiological effects of new agents in dentifrices for plaque control. Int Dent J. 1993 Aug;43(4 Suppl 1):399–406. [PubMed] [Google Scholar]
  28. McCaffrey C., Bertasso A., Pace J., Georgopapadakou N. H. Quinolone accumulation in Escherichia coli, Pseudomonas aeruginosa, and Staphylococcus aureus. Antimicrob Agents Chemother. 1992 Aug;36(8):1601–1605. doi: 10.1128/aac.36.8.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mortimer P. G., Piddock L. J. The accumulation of five antibacterial agents in porin-deficient mutants of Escherichia coli. J Antimicrob Chemother. 1993 Aug;32(2):195–213. doi: 10.1093/jac/32.2.195. [DOI] [PubMed] [Google Scholar]
  30. Nichols W. W., Dorrington S. M., Slack M. P., Walmsley H. L. Inhibition of tobramycin diffusion by binding to alginate. Antimicrob Agents Chemother. 1988 Apr;32(4):518–523. doi: 10.1128/aac.32.4.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nichols W. W., Evans M. J., Slack M. P., Walmsley H. L. The penetration of antibiotics into aggregates of mucoid and non-mucoid Pseudomonas aeruginosa. J Gen Microbiol. 1989 May;135(5):1291–1303. doi: 10.1099/00221287-135-5-1291. [DOI] [PubMed] [Google Scholar]
  32. Nickel J. C., Ruseska I., Wright J. B., Costerton J. W. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother. 1985 Apr;27(4):619–624. doi: 10.1128/aac.27.4.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nold S. C., Ward D. M. Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl Environ Microbiol. 1996 Dec;62(12):4598–4607. doi: 10.1128/aem.62.12.4598-4607.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pascual A., Ramirez de Arellano E., Martínez Martínez L., Perea E. J. Effect of polyurethane catheters and bacterial biofilms on the in-vitro activity of antimicrobials against Staphylococcus epidermidis. J Hosp Infect. 1993 Jul;24(3):211–218. doi: 10.1016/0195-6701(93)90050-a. [DOI] [PubMed] [Google Scholar]
  35. Stewart P. S. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother. 1996 Nov;40(11):2517–2522. doi: 10.1128/aac.40.11.2517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Suci P. A., Mittelman M. W., Yu F. P., Geesey G. G. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 1994 Sep;38(9):2125–2133. doi: 10.1128/aac.38.9.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sung J. Y., Leung J. W., Shaffer E. A., Lam K., Costerton J. W. Bacterial biofilm, brown pigment stone and blockage of biliary stents. J Gastroenterol Hepatol. 1993 Jan-Feb;8(1):28–34. doi: 10.1111/j.1440-1746.1993.tb01171.x. [DOI] [PubMed] [Google Scholar]
  38. Voss E. W., Jr, Eschenfeldt W., Root R. T. Fluorescein: a complete antigenic group. Immunochemistry. 1976 May;13(5):447–453. doi: 10.1016/0019-2791(76)90382-7. [DOI] [PubMed] [Google Scholar]
  39. Widmer A. F., Wiestner A., Frei R., Zimmerli W. Killing of nongrowing and adherent Escherichia coli determines drug efficacy in device-related infections. Antimicrob Agents Chemother. 1991 Apr;35(4):741–746. doi: 10.1128/aac.35.4.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Willmott C. J., Critchlow S. E., Eperon I. C., Maxwell A. The complex of DNA gyrase and quinolone drugs with DNA forms a barrier to transcription by RNA polymerase. J Mol Biol. 1994 Sep 30;242(4):351–363. doi: 10.1006/jmbi.1994.1586. [DOI] [PubMed] [Google Scholar]
  41. Wolfaardt G. M., Lawrence J. R., Robarts R. D., Caldwell S. J., Caldwell D. E. Multicellular organization in a degradative biofilm community. Appl Environ Microbiol. 1994 Feb;60(2):434–446. doi: 10.1128/aem.60.2.434-446.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Antimicrobial Agents and Chemotherapy are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES