Prevention of Staphylococcus aureus biofilm formation by antibiotics in 96-Microtiter Well Plates and Drip Flow Reactors: Critical factors influencing outcomes

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Manner, Suvi ^a   Goeres, Darla M ^b   Skogman, Malena ^c   Vuorela, Pia ^c   Fallarero, Adyary ^c  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b MONTANA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; DOXYCYCLINE; OXACILLIN; RIFAMPICIN;

BIOFILM; DEVICES; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; DOXYCYCLINE; HUMANS; MICROBIAL SENSITIVITY TESTS; OXACILLIN; RIFAMPIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 85014466690     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep43854     Document Type: Article

References (53)

1. Donlan, R. M., Costerton, J. W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167-193 (2002).
2. Percival, S. L., Suleman, L., Vuotto, C., Donelli, G. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. J. Med. Microbiol. 64, 323-334, doi: 10. 1099/jmm. 0. 000032 (2015).
3. Worthington, R. J., Richards, J. J., Melander, C. Small molecule control of bacterial biofilms. Org. Biomol. Chem. 10, 7457-7474, doi: 10. 1039/c2ob25835h (2012).
4. Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., Ciofu, O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35, 322-332, doi: 10. 1016/j. ijantimicag. 2009. 12. 011 (2010).
5. Bjarnsholt, T., Ciofu, O., Molin, S., Givskov, M., Høiby, N. Applying insights from biofilm biology to drug development-can a new approach be developed Nat. Rev. Drug Discov. 12, 791-808, doi: 10. 1038/nrd4000 (2013).
6. Toté, K., et al. Inhibitory efficacy of various antibiotics on matrix and viable mass of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Int. J. Antimicrob. Agents 33, 525-531, doi: 10. 1016/j. iantimicag. 2008. 11. 004 (2009).
7. Lebeaux, D., Chauhan, A., Rendueles, O., Beloin, C. From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens 2, 288-356, doi: 10. 3390/pathogens2020288 (2013).
8. Coenye, T., Nelis, H. J. In vitro and in vivo model systems to study microbial biofilm formation. J. Microbiol. Methods 83, 89-105, doi: 10. 1016/j. mimet. 2010. 08. 018 (2010).
9. Gomes, I. B., Simões, M., Simões, L. C. An overview on the reactors to study drinking water biofilms. Water Res. 62, 63-87, doi:rfsti 1016/j. watres.2014. 05. 039 (2014)
10. Goeres, D. M., et al. A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nat. Protoc. 4, 783-788, doi: 10. 1038/nprot. 2009. 59 (2009).
11. Adams, H., et al. Development of a laboratory model to assess the removal of biofilm from interproximal spaces by powered tooth brushing. Am. J. Dent. 15, 12B-17B (2002).
12. Woods, J., et al. Development and application of a polymicrobial, in vitro, wound biofilm model. J. Appl. Microbiol. 112, 998-1006, doi: 10. 1111/j. 1365-2672. 2012. 05264. x (2012).
13. Fu, W., et al. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob. Agents Chemother. 54, 397-404, doi: 10. 1128/AAC. 00669-09 (2010).
14. Agostinho, A. M., et al. An in vitro model for the growth and analysis of chronic wound MRSA biofilms. J. Appl. Microbiol. 111, 1275-1282, doi: 10. 1111/j. 1365-2672. 2011. 05138. x (2011).
15. Manner, S., Skogman, M., Goeres, D., Vuorela, P., Fallarero, A. Systematic exploration of natural and synthetic flavonoids for the inhibition of Staphylococcus aureus biofilms. Int. J. Mol. Sci. 14, 19434-19451, doi: 10. 3390/ijms141019434 (2013).
16. Pitts, B., Hamilton, M. A., Zelver, N., Stewart, P. S. A microtiter-plate screening method for biofilm disinfection and removal. J. Microbiol. Methods 54, 269-276 (2003).
17. Amorena, B., et al. Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J. Antimicrob. Chemother. 44, 43-55 (1999).
18. Simões, M., Pereira, M. O., Vieira, M. J. Effect of different concentrations of ortho-phthalaldehyde on biofilms formed by Pseudomonas fluorescens under different flow conditions. Biofouling 19, 287-295, doi: 10. 1080/0892701031000153398 (2003).
19. Simões, M., Pereira, M. O., Vieira, M. J. Monitoring the effects of biocide treatment of Pseudomonas fluorescens biofilms formed under different flow regimes. Water Sci. Technol. 47, 217-223 (2003).
20. Simões, M., Pereira, M. O., Vieira, M. J. Action of a cationic surfactant on the activity and removal of bacterial biofilms formed under different flow regimes. Water Res. 39, 478-486, doi: 10. 1016/j. watres. 2004. 09. 018 (2005).
21. Buckingham-Meyer, K., Goeres, D. M., Hamilton, M. A. Comparative evaluation of biofilm disinfectant efficacy tests. J. Microbiol. Methods 70, 236-244, doi:10. 1016/j. mimet. 2007. 04. 010 (2007).
22. Treangen, T. J., et al. Complete Genome Sequence of the Quality Control Strain Staphylococcus aureus subsp. aureus ATCC 25923. Genome Announc 2, doi: 10. 1128/genomeA. 01110-14 (2014).
23. Gupta, A. Biofilm quantification and comparative analysis of MIC (Minimum Inhibitory Concentration) & MBIC (Minimum Biofilm Inhibitory Concentration) value for different antibiotics against E. coli. Int. J. Curr. Microbiol. App. Sci. 4, 198-224 (2015).
24. Stewart, P. S. Antimicrobial tolerance in biofilms. Microbiol. Spectr. 3, doi: 10. 1128/microbiolspec. MB-0010-2014 (2015).
25. Høiby, N., et al. The clinical impact of bacterial biofilms. Int. J. Oral Sci. 3, 55-65, doi:10. 4248/IJOS11026 (2011).
26. Wu, H., Moser, C., Wang, H. Z., Høiby, N., Song, Z. J. Strategies for combating bacterial biofilm infections. Int. J. Oral Sci. 7, 1-7, doi: 10. 1038/ijos. 2014. 65 (2015).
27. Høiby, N. Recent advances in the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. BMC Med. 9, 32, doi:10.1186/1741-7015-9-32 (2011).
28. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114-122, doi: 10. 1038/nrd1008 (2003).
29. Kiedrowski, M. R., Horswill, A. R. New approaches for treating staphylococcal biofilm infections. Ann. N. Y. Acad. Sci. 1241, 104-121, doi: 10. 1111/j. 1749-6632. 2011. 06281. x (2011).
30. Raad, I., et al. Comparative activities of daptomycin, linezolid, and tigecycline against catheter-related methicillin-resistant Staphylococcus bacteremic isolates embedded in biofilm. Antimicrob. Agents Chemother. 51, 1656-1660, doi: 10. 1128/AAC. 00350-06 (2007).
31. Rose, W. E., Otto, D. P., Aucamp, M. E., Miller, Z., de Villiers, M. M. Prevention of biofilm formation by methacrylate-based copolymer films loaded with rifampin, clarithromycin, doxycycline alone or in combination. Pharm. Res. 32, 61-73, doi: 10. 1007/s11095-014-1444-x (2015).
32. Raad, I., et al. In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob. Agents Chemother. 47, 3580-3585 (2003).
33. Wu, S., et al. Beta-lactam antibiotics stimulate biofilm formation in non-typeable Haemophilus influenzae by up-regulating carbohydrate metabolism. PLoS One 9, e99204, doi: 10. 1371/journal. pone. 0099204 (2014).
34. Seoane, L., et al. A thermodynamic study of the aggregation process of oxacillin sodium salt in aqueous solution. Colloid. Polym. Sci. 280, 624-629 (2002).
35. Stoodley, P., Dodds, I., Boyle, J. D., Lappin-Scott, H. M. Influence of hydrodynamics and nutrients on biofilm structure. J. Appl. Microbiol. 85 Suppl 1, 19S-28S, doi:10. 1111/j. 1365-2672. 1998. tb05279. x (1998).
36. Bird, R. B., Stewart, W. E., Lightfoot, E. N. Flow of a falling film in Transport Phenomena 2nd edition (ed. Kulek, P. ) 42-47 (John Wiley & Sons, Inc, 2002).
37. Salek, M. M., Sattari, P., Martinuzzi, R. J. Analysis of fluid flow and wall shear stress patterns inside partially filled agitated culture well plates. Ann. Biomed. Eng. 40, 707-728, doi: 10. 1007/s10439-011-0444-9 (2012).
38. Merritt, J. H., Kadouri, D. E., O'Toole, G. A. Growing and analyzing static biofilms. Curr. Protoc. Microbiol. 0 1, Unit-1B. 1., doi:10.1002/9780471729259. mc01b01s00 (2005).
39. O'Toole, G. A. Microtiter dish biofilm formation assay. J. Vis. Exp. 47, 2437, doi: 10. 3791/2437 (2011).
40. Oniciuc, E. A., Cerca, N., Nicolau, A. I. Compositional analysis of biofilms formed by Staphylococcus aureus isolated from food sources. Front. Microbiol. 7, 390, doi: 10. 3389/fmicb. 2016. 00390 (2016).
41. Olwoch, I. P., Greeff, O. B., Jooné, G., Steenkamp, V. The effects of the natural enzyme, Pectinex Ultra SP-L, on human cell cultures and bacterial biofilms in vitro. BMC Microbiol. 14, 251, doi: 10. 1186/s12866-014-0251-1 (2014).
42. Claessens, J., et al. Inefficacy of vancomycin and teicoplanin in eradicating and killing Staphylococcus epidermidis biofilms in vitro. Int. J. Antimicrob. Agents 45, 368-375, doi: 10. 1016/j. ijantimicag. 2014. 11. 011 (2015).
43. Toté, K., Horemans, T., Vanden Berghe, D., Maes, L., Cos, P. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 76, 3135-3142, doi: 10. 1128/AEM. 02095-09 (2010).
44. Fujimura, S., et al. Antimicrobial efficacy of combined clarithromycin plus daptomycin against biofilms-formed methicillin-resistant Staphylococcus aureus on titanium medical devices. J. Infect. Chemother. 21, 756-759, doi: 10. 1016/j. jiac. 2015. 06. 001 (2015).
45. Roberts, A. E., Kragh, K. N., Bjarnsholt, T., Diggle, S. P. The limitations of in vitro experimentation in understanding biofilms and chronic infection. J. Mol. Biol. 427, 3646-3661, doi: 10. 1016/j. jmb. 2015. 09. 002 (2015).
46. Bjarnsholt, T., et al. The in vivo biofilm. Trends Microbiol. 21, 466-474, doi: 10. 1016/j. tim. 2013. 06. 002 (2013).
47. Gomes, L. C., et al. 96-well microtiter plates for biofouling simulation in biomedical settings. Biofouling 30, 535-546, doi:10.1080/08927014. 2014. 890713 (2014).
48. Abbanat, D., et al. Evaluation of the in vitro activities of ceftobiprole and comparators in staphylococcal colony or microtitre plate biofilm assays. Int. J. Antimicrob. Agents 43, 32-39, doi: 10. 1016/j. ijantimicag. 2013. 09. 013 (2014).
49. Skogman, M. E., Vuorela, P. M., Fallarero, A. Combining biofilm matrix measurements with biomass and viability assays in susceptibility assessments of antimicrobials against Staphylococcus aureus biofilms. J. Antibiot. (Tokyo) 65, 453-459, doi: 10. 1038/ja. 2012. 49 (2012).
50. Sandberg, M., Maättänen, A., Peltonen, J., Vuorela, P. M., Fallarero, A. Automating a 96-well microtitre plate model for Staphylococcus aureus biofilms: an approach to screening of natural antimicrobial compounds. Int. J. Antimicrob. Agents 32, 233-240, doi: 10. 1016/j. ijantimicag. 2008. 04. 022 (2008).
51. Sandberg, M. E., et al. Pros and cons of using resazurin staining for quantification of viable Staphylococcus aureus biofilms in a screening assay. J. Microbiol. Methods 78, 104-106, doi: 10. 1016/j. mimet. 2009. 04. 014 (2009).
52. Fallarero, A., et al. Dehydroabietic acid, an abietane-type diterpene, inhibits Staphylococcus aureus biofilms in vitro. Int. J. Mol. Sci. 14, 12054-12072, doi: 10. 3390/ijms140612054 (2013).
53. Pitts, B., et al. A repeatable laboratory method for testing the efficacy of biocides against toilet bowl biofilms. J. Appl. Microbiol. 91, 110-117 (2001).