Macroscale versus microscale methods for physiological analysis of biofilms formed in 96-well microtiter plates

Journal of Microbiological Methods

Volumn 95, Issue 3, 2013, Pages 342-349

  Gomes, L C ^a   Moreira, J M R ^a   Miranda, J M ^a   Simoes M ^a   Melo, L F ^a   Mergulhao F J ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

Biofilm heterogeneity; Computational fluid dynamics; Crystal violet; Microtiter plate; Resazurin; Scanning electron microscopy

Indexed keywords

CRYSTAL VIOLET; RESAZURIN;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; CELL SIZE; COMPUTATIONAL FLUID DYNAMICS; CONTROLLED STUDY; ESCHERICHIA COLI; HYDRODYNAMICS; INTERMETHOD COMPARISON; MICROTITER PLATE ASSAY; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SHEAR STRESS; SIMULATION;

BIOFILM HETEROGENEITY; COMPUTATIONAL FLUID DYNAMICS; CRYSTAL VIOLET; MICROTITER PLATE; RESAZURIN; SCANNING ELECTRON MICROSCOPY;

BACTERIOLOGICAL TECHNIQUES; BIOFILMS; ESCHERICHIA COLI; GENTIAN VIOLET; HYDRODYNAMICS; MICROSCOPY, ELECTRON, SCANNING; OXAZINES; STAINING AND LABELING; XANTHENES;

EID: 84886809883     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2013.10.002     Document Type: Article

References (75)

1. Alhede M., Qvortrup K., Liebrechts R., Høiby N., Givskov M., Bjarnsholt T. Combination of microscopic techniques reveals a comprehensive visual impression of biofilm structure and composition. FEMS Immunol. Med. Microbiol. 2012, 65:335-342.
2. Alnnasouri M., Dagot C., Pons M.-N. Comparison of four methods to assess biofilm development. Water Sci. Technol. 2011, 63:432-439.
3. Azevedo N., Lopes S., Keevil C., Pereira M., Vieira M. Time to "go large" on biofilm research: advantages of an omics approach. Biotechnol. Lett. 2009, 31:477-485.
4. Bandara H.M.H.N., Yau J.Y.Y., Watt R.M., Jin L.J., Samaranayake L.P. Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation. J. Med. Microbiol. 2009, 58:1623-1631.
5. Berson R.E., Purcell M., Sharp M.K. Computationally determined shear on cells grown in orbiting culture dishes. Oxygen Transport to Tissue XXIX 2008, 189-198. Springer, US. K. Kang, D. Harrison, D. Bruley (Eds.).
6. Borges A., Simões L.C., Saavedra M.J., Simões M. The action of selected isothiocyanates on bacterial biofilm prevention and control. Int. Biodeterior. Biodegrad. 2013, (in press).
7. Brackbill J.U., Kothe D.B., Zemach C. A continuum method for modeling surface tension. J. Comput. Phys. 1992, 100:335-354.
8. Bridier A., Dubois-Brissonnet F., Boubetra A., Thomas V., Briandet R. The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J. Microbiol. Methods 2010, 82:64-70.
9. Bridier A., Meylheuc T., Briandet R. Realistic representation of Bacillus subtilis biofilms architecture using combined microscopy (CLSM, ESEM and FESEM). Micron 2013, 48:65-69.
10. Bryers J.D. Medical biofilms. Biotechnol. Bioeng. 2008, 100:1-18.
11. Busscher H.J., van der Mei H.C. Microbial adhesion in flow displacement systems. Clin. Microbiol. Rev. 2006, 19:127-141.
12. Cady N.C., McKean K.A., Behnke J., Kubec R., Mosier A.P., Kasper S.H., Burz D.S., Musah R.A. Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS ONE 2012, 7:e38492.
13. Coenye T., Nelis H.J. In vitro and in vivo model systems to study microbial biofilm formation. J. Microbiol. Methods 2010, 83:89-105.
14. Coraça-Hubér D.C., Fille M., Hausdorfer J., Pfaller K., Nogler M. Evaluation of MBEC™-HTP biofilm model for studies of implant associated infections. J. Orthop. Res. 2012, 30:1176-1180.
15. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
16. Dardik A., Chen L., Frattini J., Asada H., Aziz F., Kudo F.A., Sumpio B.E. Differential effects of orbital and laminar shear stress on endothelial cells. J. Vasc. Surg. 2005, 41:869-880.
17. Davey M.E., O'Toole G.A. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 2000, 64:847-867.
18. Duetz W.A. Microtiter plates as mini-bioreactors: miniaturization of fermentation methods. Trends Microbiol. 2007, 15:469-475.
19. Elkhatib W.F., Noreddin A.M. A new fluorogenic assay for monitoring and determining planktonic and biofilm forms of Pseudomonas aeruginosa viable count in vitro. J. Rapid Methods Autom. Microbiol. 2009, 17:304-314.
20. Fedel M., Caciagli P., Chistè V., Caola I., Tessarolo F. Microbial biofilm imaging ESEM vs HVSEM. Imaging Microsc. 2007, 9:44-47.
21. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis. Mon. 2003, 49:53-70.
22. Hancock V., Ferrières L., Klemm P. Biofilm formation by asymptomatic and virulent urinary tract infectious Escherichia coli strains. FEMS Microbiol. Lett. 2007, 267:30-37.
23. Hannig C., Follo M., Hellwig E., Al-Ahmad A. Visualization of adherent micro-organisms using different techniques. J. Med. Microbiol. 2010, 59:1-7.
24. Heydorn A., Nielsen A.T., Hentzer M., Sternberg C., Givskov M., Ersbøll B.K., Molin S. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 2000, 146:2395-2407.
25. Hilgenstock A., Ernst R. Analysis of installation effects by means of computational fluid dynamics - CFD vs experiments?. Flow Meas. lnstrum. 1996, 7:161-171.
26. Hirt C.W., Nichols B.D. Volume of fluid (VOF) method for the dynamics of free boundaries. J. Comput. Phys. 1981, 39:201-225.
27. Honraet K., Goetghebeur E., Nelis H.J. Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J. Microbiol. Methods 2005, 63:287-295.
28. Horath T., Neu T.R., Bachofen R. An endolithic microbial community in dolomite rock in central Switzerland: characterization by reflection spectroscopy, pigment analyses, scanning electron microscopy, and laser scanning microscopy. Microb. Ecol. 2006, 51:353-364.
29. Kostenko V., Salek M.M., Sattari P., Martinuzzi R.J. Staphylococcus aureus biofilm formation and tolerance to antibiotics in response to oscillatory shear stresses of physiological levels. FEMS Immunol. Med. Microbiol. 2010, 59:421-431.
30. Kwok W.K., Picioreanu C., Ong S.L., van Loosdrecht M.C.M., Ng W.J., Heijnen J.J. Influence of biomass production and detachment forces on biofilm structures in a biofilm airlift suspension reactor. Biotechnol. Bioeng. 1998, 58:400-407.
31. Lantz J., Renner J., Karlsson M. Wall shear stress in a subject specific human aorta - influence of fluid structure interaction. Int. J. Appl. Mech. 2011, 3:759-778.
32. Lee J.-H., Park J.-H., Kim J.-A., Neupane G.P., Cho M.H., Lee C.-S., Lee J. Low concentrations of honey reduce biofilm formation, quorum sensing, and virulence in Escherichia coli O157:H7. Biofouling 2011, 27:1095-1104.
33. Li X., Yan Z., Xu J. Quantitative variation of biofilms among strains in natural populations of Candida albicans. Microbiology 2003, 149:353-362.
34. Liu Y., Tay J.-H. The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res. 2002, 36:1653-1665.
35. Manuel C. Biofilm Dynamics and Drinking Water Stability: Effects of Hydrodynamics and Surface Materials 2007, Department of Chemical Engineering, PhD, University of Porto, Faculty of Engineering.
36. Martinez L.R., Mihu M.R., Han G., Frases S., Cordero R.J.B., Casadevall A., Friedman A.J., Friedman J.M., Nosanchuk J.D. The use of chitosan to damage Cryptococcus neoformans biofilms. Biomaterials 2010, 31:669-679.
37. Melo L., Flemming H.-C. Mechanistic aspects of heat exchanger and membrane biofouling and prevention. The Science and Technology of Industrial Water Treatment 2010, 365-380. Taylor & Francis, Boca Raton (USA). Z. Amjad (Ed.).
38. Melo A.S., Bizerra F.C., Freymüller E., Arthington-Skaggs B.A., Colombo A.L. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med. Mycol. 2011, 49:253-262.
39. Moreira J.M.R., Gomes L.C., Araújo J.D.P., Miranda J.M., Simões M., Melo L.F., Mergulhão F.J. The effect of glucose concentration and shaking conditions on Escherichia coli biofilm formation in microtiter plates. Chem. Eng. Sci. 2013, 94:192-199.
40. Moreira J.M.R., Teodósio J.S., Silva F.C., Simões M., Melo L.F., Mergulhão F.J. Influence of flow rate variation on the development of Escherichia coli biofilms. Bioprocess Biosyst. Eng. 2013, 36:1787-1796.
41. Norton T.A., Thompson R.C., Pope J., Veltkamp C.J., Banks B., Howard C.V., Hawkins S.J. Using confocal laser scanning microscopy, scanning electron microscopy and phase contrast light microscopy to examine marine biofilms. Aquat. Microb. Ecol. 1998, 16:199-204.
42. Palmer R.J., Sternberg C. Modern microscopy in biofilm research: confocal microscopy and other approaches. Curr. Opin. Biotechnol. 1999, 10:263-268.
43. Palmer R.J., Haagensen J.J., Neu T., Sternberg C. Confocal microscopy of biofilms - spatiotemporal approaches. Handbook of Biological Confocal Microscopy 2006, 870-888. Springer, US. J.B. Pawley (Ed.).
44. Paris T., Skali-Lami S., Block J.-C. Effect of wall shear rate on biofilm deposition and grazing in drinking water flow chambers. Biotechnol. Bioeng. 2007, 97:1550-1561.
45. Peeters E., Nelis H.J., Coenye T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods 2008, 72:157-165.
46. Pettit R., Weber C., Pettit G. Application of a high throughput Alamar blue biofilm susceptibility assay to Staphylococcus aureus biofilms. Ann. Clin. Microbiol. Antimicrob. 2009, 8:28.
47. Pitts B., Hamilton M.A., Zelver N., Stewart P.S. A microtiter-plate screening method for biofilm disinfection and removal. J. Microbiol. Methods 2003, 54:269-276.
48. Potter C.M.F., Schobesberger S., Lundberg M.H., Weinberg P.D., Mitchell J.A., Gorelik J. Shape and compliance of endothelial cells after shear stress in vitro or from different aortic regions: scanning ion conductance microscopy study. PLoS ONE 2012, 7:e31228.
49. Quave C.L., Plano L.R.W., Pantuso T., Bennett B.C. Effects of extracts from Italian medicinal plants on planktonic growth, biofilm formation and adherence of methicillin-resistant Staphylococcus aureus. J. Ethnopharmacol. 2008, 118:418-428.
50. Rochex A., Godon J.-J., Bernet N., Escudié R. Role of shear stress on composition, diversity and dynamics of biofilm bacterial communities. Water Res. 2008, 42:4915-4922.
51. Salek M., Sattari P., Martinuzzi R. Analysis of fluid flow and wall shear stress patterns inside partially filled agitated culture well plates. Ann. Biomed. Eng. 2012, 40:707-728.
52. Sanchez C., Mende K., Beckius M., Akers K., Romano D., Wenke J., Murray C. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect. Dis. 2013, 13:47.
53. Serra D.O., Richter A.M., Klauck G., Mika F., Hengge R. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. Ambio 2013, 4:e100103-e100113.
54. Shakeri S., Kermanshahi R.K., Moghaddam M.M., Emtiazi G. Assessment of biofilm cell removal and killing and biocide efficacy using the microtiter plate test. Biofouling 2007, 23:79-86.
55. Shields R.C., Mokhtar N., Ford M., Hall M.J., Burgess J.G., ElBadawey M.R., Jakubovics N.S. Efficacy of a marine bacterial nuclease against biofilm forming microorganisms isolated from chronic rhinosinusitis. PLoS ONE 2013, 8:e55339.
56. Shunmugaperumal T. Introduction and overview of biofilm, Biofilm Eradication and Prevention 2010, 36-72. John Wiley & Sons, Inc., Hoboken (USA).
57. Simões M., Pereira M.O., Sillankorva S., Azeredo J., Vieira M.J. The effect of hydrodynamic conditions on the phenotype of Pseudomonas fluorescens biofilms. Biofouling 2007, 23:249-258.
58. Simões L., Simões M., Vieira M. Adhesion and biofilm formation on polystyrene by drinking water-isolated bacteria. Antonie Van Leeuwenhoek 2010, 98:317-329.
59. Smith K., Perez A., Ramage G., Lappin D., Gemmell C.G., Lang S. Biofilm formation by Scottish clinical isolates of Staphylococcus aureus. J. Med. Microbiol. 2008, 57:1018-1023.
60. Stepanovic S., Vukovic D., Dakic I., Savic B., Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods 2000, 40:175-179.
61. Stewart P.S., Murga R., Srinivasan R., de Beer D. Biofilm structural heterogeneity visualized by three microscopic methods. Water Res. 1995, 29:2006-2009.
62. Stoodley P., Wilson S., Hall-Stoodley L., Boyle J.D., Lappin-Scott H.M., Costerton J.W. Growth and detachment of cell clusters from mature mixed-species biofilms. Appl. Environ. Microbiol. 2001, 67:5608-5613.
63. Stoodley P., Sauer K., Davies D.G., Costerton J.W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 2002, 56:187-209.
64. Surman S.B., Walker J.T., Goddard D.T., Morton L.H.G., Keevil C.W., Weaver W., Skinner A., Hanson K., Caldwell D., Kurtz J. Comparison of microscope techniques for the examination of biofilms. J. Microbiol. Methods 1996, 25:57-70.
65. Tambyah P., Maki D. Catheter-associated urinary tract infection is rarely symptomatic: a prospective study of 1497 catheterized patients. Arch. Intern. Med. 2000, 160:678-682.
66. Teodósio J.S., Simões M., Melo L.F., Mergulhão F.J. Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 2011, 27:1-11.
67. Teodósio J.S., Silva F.C., Moreira J.M.R., Simões M., Melo L.F., Alves M.A., Mergulhão F.J. Flow cells as quasi ideal systems for biofouling simulation of industrial piping systems. Biofouling 2013, 1-14.
68. Thorn R.M.S., Greenman J. A novel in vitro flat-bed perfusion biofilm model for determining the potential antimicrobial efficacy of topical wound treatments. J. Appl. Microbiol. 2009, 107:2070-2079.
69. Toté K., Berghe D.V., Maes L., Cos P. A new colorimetric microtitre model for the detection of Staphylococcus aureus biofilms. Lett. Appl. Microbiol. 2008, 46:249-254.
70. van Loosdrecht M.C.M., Eikelboom D., Gjaltema A., Mulder A., Tijhuis L., Heijnen J.J. Biofilm structures. Water Sci. Technol. 1995, 32:35-43.
71. Vertes A., Hitchins V., Phillips K.S. Analytical challenges of microbial biofilms on medical devices. Anal. Chem. 2012, 84:3858-3866.
72. Wang Y., Zhang W., Wu Z., Zhu X., Lu C. Functional analysis of luxS in Streptococcus suis reveals a key role in biofilm formation and virulence. Vet. Microbiol. 2011, 152:151-160.
73. Wäsche S., Horn H., Hempel D.C. Influence of growth conditions on biofilm development and mass transfer at the bulk/biofilm interface. Water Res. 2002, 36:4775-4784.
74. Xia B., Sun D.-W. Applications of computational fluid dynamics (CFD) in the food industry: a review. Comput. Electron. Agric. 2002, 34:5-24.
75. Youngs D.L. Time-dependent multi-material flow with large fluid distortion. Numerical Methods for Fluid Dynamics 1982, 273-285. Academic Press, New York (USA). K.W. Morton, M.J. Baibnes (Eds.).