Critical review on biofilm methods

Critical Reviews in Microbiology

Volumn 43, Issue 3, 2017, Pages 313-351

  Azeredo, Joana ^a   Azevedo, Nuno F ^b   Briandet, Romain ^c   Cerca, Nuno ^a   Coenye, Tom ^d   Costa, Ana Rita ^a   Desvaux, Mickaël ^e   Di Bonaventura, Giovanni ^f   Hébraud, Michel ^e   Jaglic, Zoran ^g   Kačániová, Miroslava ^h   Knøchel, Susanne ⁱ   Lourenço, Anália ^j   Mergulhão, Filipe ^b   Meyer, Rikke Louise ^k   Nychas, George ^l   Simões, Manuel ^b   Tresse, Odile ^m   Sternberg, Claus ⁿ  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d GHENT UNIVERSITY   (Belgium)

^e CEMAGREF   (France)

^f UNIVERSITY OF CHIETI   (Italy)

^g VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^h SLOVAK UNIVERSITY OF AGRICULTURE IN NITRA   (Slovakia)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

^j UNIVERSITY OF VIGO   (Spain)

^k AARHUS UNIVERSITY   (Denmark)

^l AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^m LUNAM UNIVERSITÉ   (France)

ⁿ TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

more..

Author keywords

biofilm data analysis; Biofilm formation; biofilm formation devices; biofilm measurement; biofilm omics

Indexed keywords

BIOFILM; BIOFILM REACTOR; BIOMASS; CELL ADHESION; CONSENSUS; DRIP FLOW BIOFILM REACTOR; FLUORESCENCE IN SITU HYBRIDIZATION; IMAGE PROCESSING; MICROBIAL ADHESION; MICROFLUIDICS; MICROSCOPY; MICROTITER PLATE ASSAY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; ROTARY BIOFILM REACTOR; VALIDATION PROCESS; BACTERIUM ADHERENCE; DEVICES; EQUIPMENT DESIGN; FACTUAL DATABASE; GROWTH, DEVELOPMENT AND AGING; LAB ON A CHIP; MICROBIOLOGICAL EXAMINATION; MOLECULAR BIOLOGY; PROCEDURES; SOFTWARE;

BACTERIAL ADHESION; BIOFILMS; DATABASES, FACTUAL; EQUIPMENT DESIGN; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION, FLUORESCENCE; LAB-ON-A-CHIP DEVICES; MICROBIOLOGICAL TECHNIQUES; MICROSCOPY; MOLECULAR BIOLOGY; SOFTWARE;

EID: 85014963888     PISSN: 1040841X     EISSN: 15497828     Source Type: Journal    
DOI: 10.1080/1040841X.2016.1208146     Document Type: Review

References (349)

1. Abràmoff MD, Magalhães PJ, Ram SJ., (2004). Image processing with Image. J Biophotonics Int 11:36–41.
2. Adav SS, Lee DJ., (2008). Extraction of extracellular polymeric substances from aerobic granule with compact interior structure. J Hazard Mater 154:1120–6.
3. Agostinho AM, Hartman A, Lipp C, et al. (2011). An in vitro model for the growth and analysis of chronic wound MRSA biofilms. J Appl Microbiol 111:1275–82.
4. Ahimou F, Semmens MJ, Novak PJ, Haugstad G., (2007). Biofilm cohesiveness measurement using a novel atomic force microscopy methodology. Appl Environ Microbiol 73:2897–904.
5. Akiyama H, Hamada T, Huh WK, et al. (2003). Confocal laser scanning microscopic observation of glycocalyx production by Staphylococcus aureus in skin lesions of bullous impetigo, atopic dermatitis and pemphigus foliaceus. Br J Dermatol 148:526–32.
6. Alhede M, Qvortrup K, Liebrechts R, et al. (2012). Combination of microscopic techniques reveals a comprehensive visual impression of biofilm structure and composition. FEMS Immunol Med Microbiol 65:335–42.
7. Alvarez G, Gonzalez M, Isabal S, et al. (2013). Method to quantify live and dead cells in multi-species oral biofilm by real-time PCR with propidium monoazide. AMB Express 3:1. doi:10.1186/2191-0855-3-1.
8. Amann RI, Krumholz L, Stahl DA., (1990). Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–70.
9. Ammons MC, Ward LS, James GA., (2011). Anti-biofilm efficacy of a lactoferrin/xylitol wound hydrogel used in combination with silver wound dressings. Int Wound J 8:268–73.
10. An D, Parsek MR., (2007). The promise and peril of transcriptional profiling in biofilm communities. Curr Opin Microbiol 10:292–6.
11. Ansari MJ, Al-Ghamdi A, Usmani S, et al. (2013). Effect of jujube honey on Candida albicans growth and biofilm formation. Arch Med Res 44:352–60.
12. Aquino SF, Stuckey DC., (2004). Soluble microbial products formation in anaerobic chemostats in the presence of toxic compounds. Water Res 38:255–66.
13. Aquino SF, Stuckey DC., (2008). Integrated model of the production of soluble microbial products (SMP) and extracellular polymeric substances (EPS) in anaerobic chemostats during transient conditions. Biochem Eng J 38:138–46.
14. Araujo JC, Teran FC, Oliveira RA, et al. (2003). Comparison of hexamethyldisilazane and critical point drying treatments for SEM analysis of anaerobic biofilms and granular sludge. J Electron Microsc (Tokyo) 52:429–33.
15. Arnold JW., (2008). Colorimetric assay for biofilms in wet processing conditions. J Ind Microbiol Biotechnol 35:1475–80.
16. Asally M, Kittisopikul M, Rue P, et al. (2012). Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci USA 109:18891–6.
17. ASTM (2012a). ASTM e2196-12 standard test method for quantification of Pseudomonas aeruginosa biofilm grown with medium shear and continuous flow using rotating disk reactor. ASTM International.
18. ASTM (2012b). ASTM e2562-12 standard test method for quantification of Pseudomonas aeruginosa biofilm grown with high shear and continuous flow using CDC biofilm reactor. ASTM International.
19. Au AK, Lai HY, Utela BR, Folch A., (2011). Microvalves and micropumps for BioMEMS. Micromachines 2:179–220.
20. Auerbach ID, Sorensen C, Hansma HG, Holden PA., (2000). Physical morphology and surface properties of unsaturated Pseudomonas putida biofilms. J Bacteriol 182:3809–15.
21. Azeredo J, Oliveira R, Lazarova V., (1998). A new method for extraction of exopolymers from activated sludges. Water Sci Technol 37:367–70.
22. Azevedo NF, Lopes SP, Keevil CW, et al. (2009). Time to “go large” on biofilm research:advantages of an omics approach. Biotechnol Lett 31:477–85.
23. Azevedo NF, Vieira MJ, Keevil CW., (2003). Establishment of a continuous model system to study Helicobacter pylori survival in potable water biofilms. Water Sci Technol 47:155–60.
24. Badel S, Laroche C, Gardarin C, et al. (2008). New method showing the influence of matrix components in Leuconostoc mesenteroides biofilm formation. Appl Biochem Biotechnol 151:364–70.
25. Badel S, Laroche C, Gardarin C, et al. (2011). A new method to screen polysaccharide cleavage enzymes. Enzyme Microb Technol 48:248–52.
26. Bakke R, Kommedal R, Kalvenes S., (2001). Quantification of biofilm accumulation by an optical approach. J Microbiol Methods 44:13–26.
27. Bakker DP, Van Der Plaats A, Verkerke GJ, et al. (2003). Comparison of velocity profiles for different flow chamber designs used in studies of microbial adhesion to surfaces. Appl Environ Microbiol 69:6280–7.
28. Bansal T, Englert D, Lee J, et al. (2007). Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75:4597–607.
29. Baro AM, Reifenberger RG., (2012). Atomic force microscopy in liquid:biological applications. Weinheim, Germany:Wiley-VCH.
30. Beaussart A, El-Kirat-Chatel S, Sullan RM, et al. (2014). Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy. Nat Protoc 9:1049–55.
31. Becker H, Gartner C., (2008). Polymer microfabrication technologies for microfluidic systems. Anal Bioanal Chem 390:89–111.
32. Beech IB, Smith JR, Steele AA, et al. (2002). The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces. Colloids Surf B Biointerfaces 23:231–47.
33. Behrens S, Losekann T, Pett-Ridge J, et al. (2008). Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl Environ Microbiol 74:3143–50.
34. Beier BD, Quivey RG, Berger AJ., (2012). Raman microspectroscopy for species identification and mapping within bacterial biofilms. AMB Express 2:35. doi:10.1186/2191-0855-2-35.
35. Benoit MR, Conant CG, Ionescu-Zanetti C, et al. (2010). New device for high-throughput viability screening of flow biofilms. Appl Environ Microbiol 76:4136–42.
36. Berry D, Mader E, Lee TK, et al. (2015). Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc Natl Acad Sci USA 112:E194–203.
37. Beyenal H, Donovan C, Lewandowski Z, Harkin G., (2004). Three-dimensional biofilm structure quantification. J Microbiol Methods 59:395–413.
38. Bhardwaj C, Moore JF, Cui Y, et al. (2013). Laser desorption VUV postionization MS imaging of a cocultured biofilm. Anal Bioanal Chem 405:6969–77.
39. Bjarnsholt T, Jensen PO, Fiandaca MJ, et al. (2009). Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547–58.
40. Bleck CK, Merz A, Gutierrez MG, et al. (2010). Comparison of different methods for thin section EM analysis of Mycobacterium smegmatis. J Microsc 237:23–38.
41. Bleich R, Watrous JD, Dorrestein PC, et al. (2015). Thiopeptide antibiotics stimulate biofilm formation in Bacillus subtilis. Proc Natl Acad Sci USA 112:3086–91.
42. Bos R, Van Der Mei HC, Busscher HJ., (1999). Physico-chemistry of initial microbial adhesive interactions-its mechanisms and methods for study. FEMS Microbiol Rev 23:179–230.
43. Boyd CD, Smith TJ, El-Kirat-Chatel S, et al. (2014). Structural features of the Pseudomonas fluorescens biofilm adhesin LapA required for LapG-dependent cleavage, biofilm formation, and cell surface localization. J Bacteriol 196:2775–88.
44. Bremer PJ, Geesey GG, Drake B., (1992). Atomic force microscopy examination of the topography of a hydrated bacterial biofilm on a copper surface. Curr Microbiol 24:223–30.
45. Bressan E, Tessarolo F, Sbricoli L, et al. (2014). Effect of chlorhexidine in preventing plaque biofilm on healing abutment:a crossover controlled study. Implant Dent 23:64–8.
46. Bridier A, Briandet R, Bouchez T, Jabot F., (2014). A model-based approach to detect interspecific interactions during biofilm development. Biofouling 30:761–71.
47. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F., (2011a). Resistance of bacterial biofilms to disinfectants:a review. Biofouling 27:1017–32.
48. Bridier A, Dubois-Brissonnet F, Boubetra A, et al. (2010). The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J Microbiol Meth 82:64–70.
49. Bridier A, Dubois-Brissonnet F, Greub G, et al. (2011b). Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55:2648–54.
50. Bridier A, Meylheuc T, Briandet R., (2013). Realistic representation of Bacillus subtilis biofilms architecture using combined microscopy (CLSM, ESEM and FESEM). Micron 48:65–9.
51. Bridier A, Sanchez-Vizuete Mdel P, Le Coq D, et al. (2012). Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS One 7:e44506. doi:10.1371/journal.pone.0044506.
52. Brown MJ, Lester JN., (1980). Comparison of bacterial extracellular polymer extraction methods. Appl Environ Microbiol 40:179–85.
53. Brul S, Coote P, Oomes S, et al. (2002). Physiological actions of preservative agents:prospective of use of modern microbiological techniques in assessing microbial behaviour in food preservation. Int J Food Microbiol 79:55–64.
54. Buckingham-Meyer K, Goeres DM, Hamilton MA., (2007). Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods 70:236–44.
55. Bulut F, Meric F, Yorgancilar E, et al. (2014). Effects of N-acetyl-cysteine and acetylsalicylic acid on the tonsil bacterial biofilm tissues by light and electron microscopy. Eur Rev Med Pharmacol Sci 18:3720–5.
56. Burgess C, Desvaux M, Olmez H., (2014). 1st conference of BacFoodNet:mitigating bacterial colonisation in the food chain:bacterial adhesion, biocide resistance and microbial safety of fresh produce. Res Microbiol 165:305–10.
57. Busscher HJ, Van Der Mei HC., (2006). Microbial adhesion in flow displacement systems. Clin Microbiol Rev 19:127–41.
58. Cabral V, Znaidi S, Walker LA, et al. (2014). Targeted changes of the cell wall proteome influence Candida albicans ability to form single- and multi-strain biofilms. PLoS Pathog 10:e1004542. doi:10.1371/journal.ppat.1004542.
59. Cachet H, El Moustafid T, Herbert-Guillou D, et al. (2001). Characterization of deposits by direct observation and by electrochemical methods on a conductive transparent electrode. Application to biofilm and scale deposit under cathodic protection. Electrochimica Acta 46:3851–7.
60. Camesano TA, Liu Y, Datta M., (2007). Measuring bacterial adhesion at environmental interfaces with single-cell and single-molecule techniques. Adv Water Res 30:1470–91.
61. Carlson RP, Taffs R, Davison WM, Stewart PS., (2008). Anti-biofilm properties of chitosan-coated surfaces. J Biomater Sci Polym Ed 19:1035–46.
62. Carvalhais V, Delgado-Rastrollo M, Melo LD, Cerca N., (2013). Controlled RNA contamination and degradation and its impact on qPCR gene expression in S. epidermidis biofilms. J Microbiol Methods 95:195–200.
63. Cerca F, Trigo G, Correia A, et al. (2011). SYBR green as a fluorescent probe to evaluate the biofilm physiological state of Staphylococcus epidermidis, using flow cytometry. Can J Microbiol 57:850–6.
64. Ceresa C, Tessarolo F, Caola I, et al. (2015). Inhibition of Candida albicans adhesion on medical-grade silicone by a Lactobacillus-derived biosurfactant. J Appl Microbiol 118:1116–25.
65. Ceri H, Olson ME, Stremick C, et al. (1999). The calgary biofilm device:new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–6.
66. Cerqueira L, Azevedo NF, Almeida C, et al. (2008). DNA mimics for the rapid identification of microorganisms by fluorescence in situ hybridization (fish). Int J Mol Sci 9:1944–60.
67. Chagnot C, Zorgani MA, Astruc T, Desvaux M., (2013). Proteinaceous determinants of surface colonization in bacteria:bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 4:303. doi:10.3389/fmicb.2013.00303.
68. Chatterjee S, Biswas N, Datta A, et al. (2014). Atomic force microscopy in biofilm study. Microscopy (Oxf) 63:269–78.
69. Chauhan A, Sakamoto C, Ghigo JM, Beloin C., (2013). Did I pick the right colony? Pitfalls in the study of regulation of the phase variable antigen 43 adhesin. PLoS One 8:e73568. doi:10.1371/journal.pone.0073568.
70. Chavant P, Gaillard-Martinie B, Talon R, et al. (2007). A new device for rapid evaluation of biofilm formation potential by bacteria. J Microbiol Methods 68:605–12.
71. Chen NT, Chang CW., (2010). Rapid quantification of viable legionellae in water and biofilm using ethidium monoazide coupled with real-time quantitative PCR. J Appl Microbiol 109:623–34.
72. Chen V, Li H, Fane AG., (2004). Noninvasive observation of synthetic membrane processes–a review of methods. J Membrane Sci 241:23–44.
73. Choi AH, Slamti L, Avci FY, et al. (2009). The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-beta-1-6-N-acetylglucosamine, which is critical for biofilm formation. J Bacteriol 191:5953–63.
74. Christensen BB, Sternberg C, Andersen JB, et al. (1999). Molecular tools for study of biofilm physiology. Meth Enzymol 310:20–42.
75. Christensen GD, Simpson WA, Bisno AL, Beachey EH., (1982). Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 37:318–26.
76. Christensen GD, Simpson WA, Younger JJ, et al. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates:a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006.
77. Chu H, Yu H, Tan X, et al. (2015). Extraction procedure optimization and the characteristics of dissolved extracellular organic matter (dEOM) and bound extracellular organic matter (bEOM) from Chlorella pyrenoidosa. Colloids Surf B Biointerfaces 125:238–46.
78. Coenye T, Nelis HJ., (2010). In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Methods 83:89–105.
79. Comte S, Guibaud G, Baudu M., (2006). Relations between extraction protocols for activated sludge extracellular polymeric substances (EPS) and EPS complexation properties. Enzyme Microb Technol 38:237–45.
80. Cooper MA, Singleton VT., (2007). A survey of the 2001 to 2005 quartz crystal microbalance biosensor literature:applications of acoustic physics to the analysis of biomolecular interactions. J Mol Recognit 20:154–84.
81. Corbin A, Pitts B, Parker A, Stewart PS., (2011). Antimicrobial penetration and efficacy in an in vitro oral biofilm model. Antimicrob Agents Chemother 55:3338–44.
82. Costerton JW, Geesey GG, Cheng KJ., (1978). How bacteria stick. Sci Am 238:86–95.
83. Costerton JW, Stewart PS, Greenberg EP., (1999). Bacterial biofilms:a common cause of persistent infections. Science 284:1318–22.
84. Cramton SE, Gerke C, Schnell NF, et al. (1999). The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427–33.
85. Crusz SA, Popat R, Rybtke MT, et al. (2012). Bursting the bubble on bacterial biofilms:a flow cell methodology. Biofouling 28:835–42.
86. Daddi Oubekka S, Briandet R, Fontaine-Aupart MP, Steenkeste K., (2012). Correlative time-resolved fluorescence microscopy to assess antibiotic diffusion-reaction in biofilms. Antimicrob Agents Chemother 56:3349–58.
87. Daims H, Lucker S, Wagner M., (2006). daime, a novel image analysis program for microbial ecology and biofilm research. Environ Microbiol 8:200–13.
88. Dall L, Herndon B., (1989). Quantitative assay of glycocalyx produced by viridans group streptococci that cause endocarditis. J Clin Microbiol 27:2039–41.
89. Daniels KJ, Park YN, Srikantha T, et al. (2013). Impact of environmental conditions on the form and function of Candida albicans biofilms. Eukaryotic Cell 12:1389–402.
90. Danin PE, Girou E, Legrand P, et al. (2015). Description and microbiology of endotracheal tube biofilm in mechanically ventilated subjects. Respir Care 60:21–9.
91. Darby C, Hsu JW, Ghori N, Falkow S., (2002). Caenorhabditis elegans:plague bacteria biofilm blocks food intake. Nature 417:243–4.
92. Das T, Sharma PK, Krom BP, et al. (2011). Role of eDNA on the adhesion forces between Streptococcus mutans and substratum surfaces:influence of ionic strength and substratum hydrophobicity. Langmuir 27:10113–18.
93. Davis SC, Ricotti C, Cazzaniga A, et al. (2008). Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 16:23–9.
94. Davison WM, Pitts B, Stewart PS., (2010). Spatial and temporal patterns of biocide action against Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 54:2920–7.
95. De Angelis M, Siragusa S, Campanella D, et al. (2015). Comparative proteomic analysis of biofilm and planktonic cells of Lactobacillus plantarum db200. Proteomics 15:2244–57.
96. De Brouwer JF, Cooksey KE, Wigglesworth-Cooksey B, et al. (2006). Time of flight-secondary ion mass spectrometry on isolated extracellular fractions and intact biofilms of three species of benthic diatoms. J Microbiol Meth 65:562–72.
97. De Carvalho C, Da Fonseca MM., (2007). Assessment of three-dimensional biofilm structure using an optical microscope. BioTechniques 42:616–20.
98. Delatolla R, Tufenkji N, Comeau Y, et al. (2009). In situ characterization of nitrifying biofilm:minimizing biomass loss and preserving perspective. Water Res 43:1775–87.
99. Desvaux M, Hebraud M, Talon R, Henderson IR., (2009). Secretion and subcellular localizations of bacterial proteins:a semantic awareness issue. Trends Microbiol 17:139–45.
100. Di Bonaventura G, Piccolomini R, Paludi D, et al. (2008). Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces:relationship with motility and cell surface hydrophobicity. J Appl Microbiol 104:1552–61.
101. Di Bonaventura G, Pompilio A, Picciani C, et al. (2006). Biofilm formation by the emerging fungal pathogen Trichosporon asahii:development, architecture, and antifungal resistance. Antimicrob Agents Chemother 50:3269–76.
102. Di Bonaventura G, Spedicato I, D'antonio D, et al. (2003). Biofilm formation by Stenotrophomonas maltophilia:modulation by quinolones, trimethoprim-sulfamethoxazole, and ceftazidime. Antimicrob Agents Chemother 48:151–60.
103. Di Luca M, Maccari G, Maisetta G, Batoni G., (2015). BaAMPs:the database of biofilm-active antimicrobial peptides. Biofouling 31:193–9.
104. Djordjevic D, Wiedmann M, Mclandsborough LA., (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–8.
105. Dominguez-Benetton X, Sevda S, Vanbroekhoven K, Pant D., (2012). The accurate use of impedance analysis for the study of microbial electrochemical systems. Chem Soc Rev 41:7228–46.
106. Doroshenko N, Tseng BS, Howlin RP, et al. (2014). Extracellular DNA impedes the transport of vancomycin in Staphylococcus epidermidis biofilms preexposed to subinhibitory concentrations of vancomycin. Antimicrob Agents Chemother 58:7273–82.
107. Doulgeraki AI, Iliopoulos V, Nychas GE., (2014). Metabolomic analysis of Salmonella enterica cells in vitro and in situ. Plant Microbe Interaction, July 6–10 2014. Rhodes, Greece:MPMI.
108. Dufrene YF., (2002). Atomic force microscopy, a powerful tool in microbiology. J Bacteriol 184:5205–13.
109. Dugat-Bony E, Straub C, Teissandier A, et al. (2015). Overview of a surface-ripened cheese community functioning by meta-omics analyses. PLoS One 10:e0124360. doi:10.1371/journal.pone.0124360.
110. Edmonds JM, Collett PJ, Valdes ER, et al. (2009). Surface sampling of spores in dry-deposition aerosols. Appl Environ Microbiol 75:39–44.
111. Eguia E, Trueba A, Rio-Calonge B, et al. (2008). Combined monitor for direct and indirect measurement of biofouling. Biofouling 24:75–86.
112. Fittipaldi M, Nocker A, Codony F., (2012). Progress in understanding preferential detection of live cells using viability dyes in combination with DNA amplification. J Microbiol Methods 91:276–89.
113. Flemming HC, Wingender J., (2010). The biofilm matrix. Nat Rev Microbiol 8:623–33.
114. Fletcher M., (1977). The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Can J Microbiol 23:1–6.
115. Fontenete S, Leite M, Guimaraes N, et al. (2015). Towards fluorescence in vivo hybridization (FIVH) detection of H. Pylori in gastric mucosa using advanced LNA probes. PLoS One 10:e0125494. doi:10.1371/journal.pone.0125494.
116. Franca A, Carvalhais V, Maira-Litran T, et al. (2014). Alterations in the Staphylococcus epidermidis biofilm transcriptome following interaction with whole human blood. Pathog Dis 70:444–8.
117. Francius G, Lebeer S, Alsteens D, et al. (2008). Detection, localization, and conformational analysis of single polysaccharide molecules on live bacteria. ACS Nano 2:1921–9.
118. Freiberg JA, Mciver KS, Shirtliff ME., (2014). In vivo expression of Streptococcus pyogenes immunogenic proteins during tibial foreign body infection. Infect Immun 82:3891–9.
119. Gallaher TK, Wu S, Webster P, Aguilera R., (2006). Identification of biofilm proteins in non-typeable Haemophilus influenzae. BMC Microbiol 6:65. doi:10.1186/1471-2180-6-65.
120. Garcez AS, Nunez SC, Azambuja N, Jr, et al. (2013). Effects of photodynamic therapy on gram-positive and gram-negative bacterial biofilms by bioluminescence imaging and scanning electron microscopic analysis. Photomed Laser Surg 31:519–25.
121. Gerke C, Kraft A, Sussmuth R, et al. (1998). Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273:18586–93.
122. Ghosh P, Ben-Jacob E, Levine H., (2013). Modeling cell-death patterning during biofilm formation. Phys Biol 10:066006. doi:10.1088/1478-3975/10/6/066006.
123. Glass NR, Tjeung R, Chan P, et al. (2011). Organosilane deposition for microfluidic applications. Biomicrofluidics 5:36501–365017.
124. Goeres DM, Hamilton MA, Beck NA, et al. (2009). A method for growing a biofilm under low shear at the air–liquid interface using the drip flow biofilm reactor. Nat Protoc 4:783–8.
125. Gomez-Suarez C, Busscher HJ, Van Der Mei HC., (2001). Analysis of bacterial detachment from substratum surfaces by the passage of air–liquid interfaces. Appl Environ Microbiol 67:2531–7.
126. Gong AS, Bolster CH, Benavides M, Walker SL., (2009). Extraction and analysis of extracellular polymeric substances:comparison of methods and extracellular polymeric substance levels in Salmonella pullorum sa 1685. Environ Eng Sci 26:1523–32.
127. Grand I, Bellon-Fontaine MN, Herry JM, et al. (2011). Possible overestimation of surface disinfection efficiency by assessment methods based on liquid sampling procedures as demonstrated by in situ quantification of spore viability. Appl Environ Microbiol 77:6208–14.
128. Guilbaud M, Piveteau P, Desvaux M, et al. (2015). Exploring the diversity of Listeria monocytogenes biofilm architecture by high-throughput confocal laser scanning microscopy and the predominance of the honeycomb-like morphotype. Appl Environ Microbiol 81:1813–19.
129. Haagensen JA, Klausen M, Ernst RK, et al. (2007). Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J Bacteriol 189:28–37.
130. Hannig C, Follo M, Hellwig E, Al-Ahmad A., (2010). Visualization of adherent micro-organisms using different techniques. J Med Microbiol 59:1–7.
131. Harz M, Rosch P, Peschke KD, et al. (2005). Micro-Raman spectroscopic identification of bacterial cells of the genus Staphylococcus and dependence on their cultivation conditions. Analyst 130:1543–50.
132. Hasan S, Danishuddin M, Khan AU., (2015). Inhibitory effect of Zingiber officinale towards Streptococcus mutans virulence and caries development:in vitro and in vivo studies. BMC Microbiol 15:1. doi:10.1186/s12866-014-0320-5.
133. Hassanpourfard M, Sun X, Valiei A, et al. (2014). Protocol for biofilm streamer formation in a microfluidic device with micro-pillars. J Vis Exp e51732. doi:10.3791/51732.
134. Henderson IR, Owen P, Nataro JP., (1999). Molecular switches–the ON and OFF of bacterial phase variation. Mol Microbiol 33:919–32.
135. Heydorn A, Ersboll B, Kato J, et al. (2002). Statistical analysis of Pseudomonas aeruginosa biofilm development:impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 68:2008–17.
136. Heydorn A, Ersboll BK, Hentzer M, et al. (2000a). Experimental reproducibility in flow-chamber biofilms. Microbiology 146:2409–15.
137. Heydorn A, Nielsen AT, Hentzer M, et al. (2000b). Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395–407.
138. Hinterdorfer P, Dufrene YF., (2006). Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 3:347–55.
139. Hochbaum AI, Kolodkin-Gal I, Foulston L, et al. (2011). Inhibitory effects of d-amino acids on Staphylococcus aureus biofilm development. J Bacteriol 193:5616–22.
140. Hochstim CJ, Choi JY, Lowe D, et al. (2010). Biofilm detection with hematoxylin–eosin staining. Arch Otolaryngol Head Neck Surg 136:453–6.
141. Hong SD, Dhong HJ, Chung SK, et al. (2014). Hematoxylin and eosin staining for detecting biofilms:practical and cost-effective methods for predicting worse outcomes after endoscopic sinus surgery. Clin Exp Otorhinolaryngol 7:193–7.
142. Hope CK, Clements D, Wilson M., (2002). Determining the spatial distribution of viable and nonviable bacteria in hydrated microcosm dental plaques by viability profiling. J Appl Microbiol 93:448–55.
143. Hu YF, Zhang JD, Ulstrup J., (2011). Investigation of Streptococcus mutans biofilm growth on modified Au(111)-surfaces using AFM and electrochemistry. J Electroanal Chem 656:41–9.
144. Hua X, Marshall MJ, Xiong Y, et al. (2015). Two-dimensional and three-dimensional dynamic imaging of live biofilms in a microchannel by time-of-flight secondary ion mass spectrometry. Biomicrofluidics 9:031101. doi:10.1063/1.4919807.
145. Hua X, Yu XY, Wang Z, et al. (2014). In situ molecular imaging of a hydrated biofilm in a microfluidic reactor by ToF-SIMS. Analyst 139:1609–13.
146. Huang WE, Stoecker K, Griffiths R, et al. (2007). Raman-fish:combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 9:1878–89.
147. Hung C, Zhou Y, Pinkner JS, et al. (2013). Escherichia coli biofilms have an organized and complex extracellular matrix structure. MBio 4:e00645–13.
148. Iliescu C, Taylor H, Avram M, et al. (2012). A practical guide for the fabrication of microfluidic devices using glass and silicon. Biomicrofluidics 6:16505–1650516.
149. Jackson S, Coulthwaite L, Loewy Z, et al. (2014). Biofilm development by blastospores and hyphae of Candida albicans on abraded denture acrylic resin surfaces. J Prosthet Dent 112:988–93.
150. Janakiraman V, Englert D, Jayaraman A, Baskaran H., (2009). Modeling growth and quorum sensing in biofilms grown in microfluidic chambers. Ann Biomed Eng 37:1206–16.
151. Jarrett CO, Deak E, Isherwood KE, et al. (2004). Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J Infect Dis 190:783–92.
152. Jiao Y, Cody GD, Harding AK, et al. (2010). Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76:2916–22.
153. Johnson ME, Landers JP., (2004). Fundamentals and practice for ultrasensitive laser-induced fluorescence detection in microanalytical systems. Electrophoresis 25:3513–27.
154. Jorge P, Pérez-Pérez M, Rodríguez GP, et al. (2016). Reconstruction of the network of experimentally validated AMP-drug combinations against Pseudomonas aeruginosa infections. Curr Bioinform, 11. [Epub ahead of print]. doi:10.2174/1574893611666160617093955.
155. Kang S, Elimelech M., (2009). Bioinspired single bacterial cell force spectroscopy. Langmuir 25:9656–9.
156. Karcz J, Bernas T, Nowak A, et al. (2012). Application of lyophilization to prepare the nitrifying bacterial biofilm for imaging with scanning electron microscopy. Scanning 34:26–36.
157. Kim BI, Boehm RD., (2012). Force-feedback high-speed atomic force microscope for studying large biological systems. Micron 43:1372–9.
158. Kim J, Hegde M, Kim SH, et al. (2012). A microfluidic device for high throughput bacterial biofilm studies. Lab Chip 12:1157–63.
159. Kindaichi T, Ito T, Okabe S., (2004). Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiography-fluorescence in situ hybridization. Appl Environ Microbiol 70:1641–50.
160. Klausen M, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T., (2003b). Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50:61–8.
161. Klausen M, Heydorn A, Ragas P, et al. (2003a). Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–24.
162. Klein MI, Scott-Anne KM, Gregoire S, et al. (2012). Molecular approaches for viable bacterial population and transcriptional analyzes in a rodent model of dental caries. Mol Oral Microbiol 27:350–61.
163. Koban I, Matthes R, Hubner NO, et al. (2012). Xtt assay of ex vivo saliva biofilms to test antimicrobial influences. GMS Krankenhhyg Interdiszip 7:Doc06. doi:10.3205/dgkh000190.
164. Kornegay BH, Andrews JF., (1968). Kinetics of fixed-film biological reactors. J Water Pollut Con F 40:R460–8.
165. Korstgens V, Flemming HC, Wingender J, Borchard W., (2001). Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. J Microbiol Methods 46:9–17.
166. Kotra LP, Amro NA, Liu GY, Mobashery S., (2000). Visualizing bacteria at high resolution. ASM News 66:675–81.
167. Kragh KN, Alhede M, Jensen PO, et al. (2014). Polymorphonuclear leukocytes restrict growth of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Infect Immun 82:4477–86.
168. Kruger NJ, Buhler C, Iwobi AN, et al. (2014). “Limits of control”–crucial parameters for a reliable quantification of viable campylobacter by real-time PCR. PLoS One 9:e88108. doi:10.1371/journal.pone.0088108.
169. Kuhn TS., (1970). The structure of scientific revolutions. Chicago (MI):University of Chicago Press.
170. Kunacheva C, Stuckey DC., (2014). Analytical methods for soluble microbial products (SMP) and extracellular polymers (ECP) in wastewater treatment systems:a review. Water Res 61:1–18.
171. Kuypers MM, Jorgensen BB., (2007). The future of single-cell environmental microbiology. Environ Microbiol 9:6–7.
172. Larsen P, Nielsen JL, Otzen D, Nielsen PH., (2008). Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge. Appl Environ Microbiol 74:1517–26.
173. Laspidou CS, Rittmann BE., (2002). A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res 36:2711–20.
174. Lau PC, Dutcher JR, Beveridge TJ, Lam JS., (2009). Absolute quantitation of bacterial biofilm adhesion and viscoelasticity by microbead force spectroscopy. Biophys J 96:2935–48.
175. Lawrence JR, Korber DR, Hoyle BD, et al. (1991). Optical sectioning of microbial biofilms. J Bacteriol 173:6558–67.
176. Lawrence JR, Swerhone GD, Neu TR., (2000). A simple rotating annular reactor for replicated biofilm studies. J Microbiol Methods 42:215–24.
177. Lee JH, Kaplan JB, Lee WY., (2008). Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms. Biomed Microdevices 10:489–98.
178. Lee N, Nielsen PH, Andreasen KH, et al. (1999). Combination of fluorescent in situ hybridization and microautoradiography-a new tool for structure–function analyses in microbial ecology. Appl Environ Microbiol 65:1289–97.
179. Lenz AP, Williamson KS, Pitts B, et al. (2008). Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74:4463–71.
180. Lewandowski Z, Beyenal H, Stookey D., (2004). Reproducibility of biofilm processes and the meaning of steady state in biofilm reactors. Water Sci Technol 49:359–64.
181. Lewandowski Z, Beyenal H., (2014). Quantifying biofilm structure. Fundamentals of biofilm research. 2nd ed. Boca Raton (FL):CRC Press.
182. Li L, Mendis N, Trigui H, et al. (2014). The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 5:258. doi:10.3389/fmicb.2014.00258.
183. Li T, Wu TD, Mazeas L, et al. (2008). Simultaneous analysis of microbial identity and function using NanoSIMS. Environ Microbiol 10:580–8.
184. Li YF, Sun HW, Gao R, et al. (2015). Inhibited biofilm formation and improved antibacterial activity of a novel nanoemulsion against cariogenic Streptococcus mutans in vitro and in vivo. Int J Nanomedicine 10:447–62.
185. Lilledahl MB, Stokke BT., (2015). Novel imaging technologies for characterization of microbial extracellular polysaccharides. Front Microbiol 6:525.
186. Lim J, Cui Y, Oh YJ, et al. (2011). Studying the effect of alginate overproduction on Pseudomonas aeruginosa biofilm by atomic force microscopy. J Nanosci Nanotechnol 11:5676–81.
187. Linkert M, Rueden CT, Allan C, et al. (2010). Metadata matters:access to image data in the real world. J Cell Biol 189:777–82.
188. Linton CJ, Sherriff A, Millar MR., (1999). Use of a modified Robbins device to directly compare the adhesion of Staphylococcus epidermidis RP62A to surfaces. J Appl Microbiol 86:194–202.
189. Long T, Ford RM., (2009). Enhanced transverse migration of bacteria by chemotaxis in a porous T-sensor. Environ Sci Technol 43:1546–52.
190. Lourenço A, Coenye T, Goeres DM, et al. (2014). Minimum information about a biofilm experiment (MIABiE):standards for reporting experiments and data on sessile microbial communities living at interfaces. Pathog Dis 70:250–6.
191. Lourenço A, De Las Heras A, Scortti M, et al. (2013). Comparison of Listeria monocytogenes exoproteomes from biofilm and planktonic state:Lmo2504, a protein associated with biofilms. Appl Environ Microbiol 79:6075–82.
192. Lourenço A, Ferreira A, Veiga N, et al. (2012). BiofOmics:a web platform for the systematic and standardized collection of high-throughput biofilm data. PLoS One 7:e39960.
193. Lower SK., (2011). Atomic force microscopy to study intermolecular forces and bonds associated with bacteria. Advances in experimental medicine and biology. Dordrecht, The Netherlands:Springer Science + Business Media.
194. Luo Q, Shang J, Feng X, et al. (2013). PrfA led to reduced biofilm formation and contributed to altered gene expression patterns in biofilm-forming Listeria monocytogenes. Curr Microbiol 67:372–8.
195. Madou MJ., (2011). Fundamentals of microfabrication and nanotechnology. Boca Raton:CRC Press.
196. Malic S, Hill KE, Hayes A, et al. (2009). Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA fish). Microbiology (Reading, Engl.) 155:2603–11.
197. Mangalappalli-Illathu AK, Vidovic S, Korber DR., (2008). Differential adaptive response and survival of Salmonella enterica serovar enteritidis planktonic and biofilm cells exposed to benzalkonium chloride. Antimicrob Agents Chemother 52:3669–80.
198. Manz W, Szewzyk U, Ericsson P, et al. (1993). In situ identification of bacteria in drinking water and adjoining biofilms by hybridization with 16s and 23s rRNA-directed fluorescent oligonucleotide probes. Appl Environ Microbiol 59:2293–8.
199. Mao H, Cremer PS, Manson MD., (2003). A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc Natl Acad Sci USA 100:5449–54.
200. Marchal M, Briandet R, Halter D, et al. (2011). Subinhibitory arsenite concentrations lead to population dispersal in Thiomonas sp. PLoS One 6:e23181. doi:10.1371/journal.pone.0023181.
201. Mccoy WF, Bryers JD, Robbins J, Costerton JW., (1981). Observations of fouling biofilm formation. Can J Microbiol 27:910–17.
202. Mcdonald JC, Duffy DC, Anderson JR, et al. (2000). Fabrication of microfluidic systems in poly(dimethylsiloxane). Electrophoresis 21:27–40.
203. Meyer MT, Roy V, Bentley WE, Ghodssi R., (2011). Development and validation of a microfluidic reactor for biofilm monitoring via optical methods. J Micromech Microeng 21:054023. doi:10.1088/0960-1317/21/5/054023.
204. Meyer RL, Zhou X, Tang L, et al. (2010). Immobilization of living bacteria for AFM imaging under physiological conditions. Ultramicroscopy 110:1349–57.
205. Moller S, Sternberg C, Andersen JB, et al. (1998). In situ gene expression in mixed-culture biofilms:evidence of metabolic interactions between community members. Appl Environ Microbiol 64:721–32.
206. Mueller LN, De Brouwer JF, Almeida JS, et al. (2006). Analysis of a marine phototrophic biofilm by confocal laser scanning microscopy using the new image quantification software PHLIP. BMC Ecol 6:1.
207. Muller DJ, Krieg M, Alsteens D, Dufrene YF., (2009). New frontiers in atomic force microscopy:analyzing interactions from single-molecules to cells. Curr Opin Biotechnol 20:4–13.
208. Muller P, Guggenheim B, Attin T, et al. (2011). Potential of shock waves to remove calculus and biofilm. Clin Oral Investig 15:959–65.
209. Musat N, Foster R, Vagner T, et al. (2012). Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev 36:486–511.
210. Musat N, Halm H, Winterholler B, et al. (2008). A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci USA 105:17861–6.
211. Muscariello L, Rosso F, Marino G, et al. (2005). A critical overview of ESEM applications in the biological field. J Cell Physiol 205:328–34.
212. Nagant C, Tre-Hardy M, Devleeschouwer M, Dehaye JP., (2010). Study of the initial phase of biofilm formation using a biofomic approach. J Microbiol Methods 82:243–8.
213. Nandakumar K, Obika H, Utsumi A, et al. (2004). In vitro laser ablation of laboratory developed biofilms using an Nd:YAG laser of 532 nm wavelength. Biotechnol Bioeng 86:729–36.
214. Neu TR, Lawrence JR., (2014a). Advanced techniques for in situ analysis of the biofilm matrix (structure, composition, dynamics) by means of laser scanning microscopy. Methods Mol Biol 1147:43–64.
215. Neu TR, Lawrence JR., (2014b). Investigation of microbial biofilm structure by laser scanning microscopy. Adv Biochem Eng Biotechnol 146:1–51.
216. Neu TR, Lawrence JR., (2015). Innovative techniques, sensors, and approaches for imaging biofilms at different scales. Trends Microbiol 23:233–42.
217. Nickel JC, Ruseska I, Wright JB, Costerton JW., (1985). Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 27:619–24.
218. Nielsen PE, Egholm M, Berg RH, et al. (1991). Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science 254:1497–500.
219. Nishitani K, Sutipornpalangkul W, De Mesy Bentley KL, et al. (2015). Quantifying the natural history of biofilm formation in vivo during the establishment of chronic implant-associated Staphylococcus aureus osteomyelitis in mice to identify critical pathogen and host factors. J Orthop Res 33:1311–19.
220. Nocker A, Camper AK., (2009). Novel approaches toward preferential detection of viable cells using nucleic acid amplification techniques. FEMS Microbiol Lett 291:137–42.
221. Nocker A, Mazza A, Masson L, et al. (2009). Selective detection of live bacteria combining propidium monoazide sample treatment with microarray technology. J Microbiol Meth 76:253–61.
222. Nocker A, Sossa KE, Camper AK., (2007). Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. J Microbiol Methods 70:252–60.
223. Oates A, Bowling FL, Boulton AJ, et al. (2014). The visualization of biofilms in chronic diabetic foot wounds using routine diagnostic microscopy methods. J Diabetes Res 2014:153586. doi:10.1155/2014/153586.
224. O'brien J, Wilson I, Orton T, Pognan F., (2000). Investigation of the alamar blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 267:5421–6.
225. Okabe S, Satoh H, Kindaichi T., (2011). A polyphasic approach to study ecophysiology of complex multispecies nitrifying biofilms. Meth Enzymol 496:163–84.
226. Okshevsky M, Meyer RL., (2014). Evaluation of fluorescent stains for visualizing extracellular DNA in biofilms. J Microbiol Methods 105:102–4.
227. Oli MW, Mcarthur WP, Brady LJ., (2006). A whole cell BIAcore assay to evaluate p1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. J Microbiol Meth 65:503–11.
228. Oliveira F, Lima CA, Bras S, et al. (2015). Evidence for inter- and intraspecies biofilm formation variability among a small group of coagulase-negative staphylococci. FEMS Microbiol Lett 362. doi:10.1093/femsle/fnv175.
229. Olofsson AC, Hermansson M, Elwing H., (2005). Use of a quartz crystal microbalance to investigate the antiadhesive potential of N-acetyl-l-cysteine. Appl Environ Microbiol 71:2705–12.
230. Olson ME, Ceri H, Morck DW, et al. (2002). Biofilm bacteria:formation and comparative susceptibility to antibiotics. Can J Vet Res 66:86–92.
231. Orsinger-Jacobsen SJ, Patel SS, Vellozzi EM, et al. (2013). Use of a stainless steel washer platform to study Acinetobacter baumannii adhesion and biofilm formation on abiotic surfaces. Microbiology (Reading, Engl.) 159:2594–604.
232. O'toole GA, Kolter R., (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304.
233. Otto K, Elwing H, Hermansson M., (1999). Effect of ionic strength on initial interactions of Escherichia coli with surfaces, studied on-line by a novel quartz crystal microbalance technique. J Bacteriol 181:5210–18.
234. Otto K, Silhavy TJ., (2002). Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci USA 99:2287–92.
235. Ovchinnikova ES, Krom BP, Harapanahalli AK, et al. (2013). Surface thermodynamic and adhesion force evaluation of the role of chitin-binding protein in the physical interaction between Pseudomonas aeruginosa and Candida albicans. Langmuir 29:4823–9.
236. Pallandre A, De Lambert B, Attia R, et al. (2006). Surface treatment and characterization:perspectives to electrophoresis and lab-on-chips. Electrophoresis 27:584–610.
237. Pan X, Liu J, Zhang D, et al. (2010). A comparison of five extraction methods for extracellular polymeric substances (EPS) from biofilm by using three dimensional excitation-emission matrix (3DEEM) fluorescence spectroscopy. Water SA 36:111–116.
238. Pan Y, Breidt F, Jr.(2007). Enumeration of viable Listeria monocytogenes cells by real-time PCR with propidium monoazide and ethidium monoazide in the presence of dead cells. Appl Environ Microbiol 73:8028–31.
239. Patzold R, Keuntje M, Anders-Von Ahlften A., (2006). A new approach to non-destructive analysis of biofilms by confocal Raman microscopy. Anal Bioanal Chem 386:286–92.
240. Pavarina AC, Dovigo LN, Sanitá PV, et al. (2011). Dynamic models for in vitro biofilm formation. In:Bailey WC, ed. Biofilms:formation, development and properties. 1st ed. Hauppauge, NY:Nova Science Publishers, Inc.
241. Pavlekovic M, Schmid MC, Schmider-Poignee N, et al. (2009). Optimization of three fish procedures for in situ detection of anaerobic ammonium oxidizing bacteria in biological wastewater treatment. J Microbiol Meth 78:119–26.
242. Peeters E, Nelis HJ, Coenye T., (2008). Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 72:157–65.
243. Perez-Osorio AC, Williamson KS, Franklin MJ., (2010). Heterogeneous rpoS and rhlR mRNA levels and 16s rRNA/rDNA (rRNA gene) ratios within Pseudomonas aeruginosa biofilms, sampled by laser capture microdissection. J Bacteriol 192:2991–3000.
244. Perez-Rodriguez G, Glez-Pena D, Azevedo NF, et al. (2015). Enabling systematic, harmonized and large-scale biofilms data computation:the biofilms experiment workbench. Comput Meth Programs Biomed 118:309–21.
245. Pernthaler A, Pernthaler J, Amann R., (2002). Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–101.
246. Peterson BW, He Y, Ren Y, et al. (2015). Viscoelasticity of biofilms and their recalcitrance to mechanical and chemical challenges. FEMS Microbiol Rev 39:234–45.
247. Peterson SB, Irie Y, Borlee BR, et al. (2011). Different methods for culturing biofilms in vitro. In:Bjarnsholt T, Jensen PØ, Moser C, Høiby N, eds. Biofilm infections. New York:Springer.
248. Pettit RK, Weber CA, Kean MJ, et al. (2005). Microplate alamar blue assay for Staphylococcus epidermidis biofilm susceptibility testing. Antimicrob Agents Chemother 49:2612–17.
249. Pettit RK, Weber CA, Pettit GR., (2009). Application of a high throughput alamar blue biofilm susceptibility assay to Staphylococcus aureus biofilms. Ann Clin Microbiol Antimicrob 8:28. doi:10.1186/1476-0711-8-28.
250. Peulen TO, Wilkinson KJ., (2011). Diffusion of nanoparticles in a biofilm. Environ Sci Technol 45:3367–73.
251. Pinkart HC, Ringelberg DB, Piceno YM, et al. (2002). Biochemical approaches to biomass measurements and community structure analysis. In:Hurst CJ, Crawford RL, Mcinerney MJ, et al., eds. Manual of environmental microbiology. Washington (DC):ASM Press.
252. Pinzon-Arango PA, Liu Y, Camesano TA., (2009). Role of cranberry on bacterial adhesion forces and implications for Escherichia coli-uroepithelial cell attachment. J Med Food 12:259–70.
253. Pitts B, Hamilton MA, Zelver N, Stewart PS., (2003). A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Methods 54:269–76.
254. Planchon S, Desvaux M, Chafsey I, et al. (2009). Comparative subproteome analyses of planktonic and sessile Staphylococcus xylosus C2a:new insight in cell physiology of a coagulase-negative Staphylococcus in biofilm. J Proteome Res 8:1797–809.
255. Pompilio A, De Nicola S, Crocetta V, et al. (2015). New insights in Staphylococcus pseudintermedius pathogenicity:antibiotic-resistant biofilm formation by a human wound-associated strain. BMC Microbiol 15:109. doi:10.1186/s12866-015-0449-x.
256. Potthoff E, Ossola D, Zambelli T, Vorholt JA., (2015). Bacterial adhesion force quantification by fluidic force microscopy. Nanoscale 7:4070–9.
257. Puig C, Domenech A, Garmendia J, et al. (2014). Increased biofilm formation by nontypeable Haemophilus influenzae isolates from patients with invasive disease or otitis media versus strains recovered from cases of respiratory infections. Appl Environ Microbiol 80:7088–95.
258. Qin Z, Zhang J, Hu Y, et al. (2009). Organic compounds inhibiting S. epidermidis adhesion and biofilm formation. Ultramicroscopy 109:881–8.
259. Raes J, Bork P., (2008). Molecular eco-systems biology:towards an understanding of community function. Nat Rev Microbiol 6:693–9.
260. Ramage G, Vande Walle K, Wickes BL, Lopez-Ribot JL., (2001). Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45:2475–9.
261. Ramage G., (2016). Comparing apples and oranges:considerations for quantifying candidal biofilms with xtt [2,3-bis(2-methoxy-4-nitro-5-sulfo-phenyl)-2h-tetrazolium-5-carboxanilide] and the need for standardized testing. J Med Microbiol 65:259–60.
262. Remis JP, Wei D, Gorur A, et al. (2014). Bacterial social networks:structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol 16:598–610.
263. Renier S, Chagnot C, Deschamps J, et al. (2014). Inactivation of the SecA2 protein export pathway in Listeria monocytogenes promotes cell aggregation, impacts biofilm architecture and induces biofilm formation in environmental condition. Environ Microbiol 16:1176–92.
264. Reynolds TB, Fink GR., (2001). Bakers' yeast, a model for fungal biofilm formation. Science 291:878–81.
265. Richardson N, Mordan NJ, Figueiredo JA, et al. (2009). Microflora in teeth associated with apical periodontitis:a methodological observational study comparing two protocols and three microscopy techniques. Int Endod J 42:908–21.
266. Rodahl M, Hook F, Krozer A, et al. (1995). Quartz-crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments. Rev Sci Instrum 66:3924–30.
267. Rodrigues D, Banobre-Lopez M, Espina B, et al. (2013). Effect of magnetic hyperthermia on the structure of biofilm and cellular viability of a food spoilage bacterium. Biofouling 29:1225–32.
268. Rueden CT, Eliceiri KW., (2007). Visualization approaches for multidimensional biological image data. BioTechniques 43:33–6.
269. Sabaeifard P, Abdi-Ali A, Soudi MR, Dinarvand R., (2014). Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J Microbiol Methods 105:134–40.
270. Salanitro JP, Hokanson JS., (1990). Tubular biofilm reactor–biofilm samples are connected in series to monitor biofouling by microorganisms in continuous flow stream. US831-H US039851 20 Apr 1987.
271. Salminen A, Loimaranta V, Joosten JA, et al. (2007). Inhibition of p-fimbriated Escherichia coli adhesion by multivalent galabiose derivatives studied by a live-bacteria application of surface plasmon resonance. J Antimicrob Chemother 60:495–501.
272. Salta M, Capretto L, Carugo D, et al. (2013). Life under flow:a novel microfluidic device for the assessment of anti-biofilm technologies. Biomicrofluidics 7:64118. doi:10.1063/1.4850796.
273. Salunke GR, Ghosh S, Santosh Kumar RJ, et al. (2014). Rapid efficient synthesis and characterization of silver, gold, and bimetallic nanoparticles from the medicinal plant Plumbago zeylanica and their application in biofilm control. Int J Nanomedicine 9:2635–53.
274. Samaranayake YH, Cheung BP, Yau JY, et al. (2013). Human serum promotes Candida albicans biofilm growth and virulence gene expression on silicone biomaterial. PLoS One 8:e62902. doi:10.1371/journal.pone.0062902.
275. Sanchez-Romero MA, Cota I, Casadesus J., (2015). DNA methylation in bacteria:from the methyl group to the methylome. Curr Opin Microbiol 25:9–16.
276. Sanchez-Vizuete P, Le Coq D, Bridier A, et al. (2015). Identification of ypqP as a new Bacillus subtilis biofilm determinant that mediates the protection of Staphylococcus aureus against antimicrobial agents in mixed-species communities. Appl Environ Microbiol 81:109–18.
277. Sandberg ME, Schellmann D, Brunhofer G, et al. (2009). Pros and cons of using resazurin staining for quantification of viable Staphylococcus aureus biofilms in a screening assay. J Microbiol Methods 78:104–6.
278. Sawant SN, Selvaraj V, Prabhawathi V, Doble M., (2013). Antibiofilm properties of silver and gold incorporated PU, PCLm, PC and PMMA nanocomposites under two shear conditions. PLoS One 8:e63311. doi:10.1371/journal.pone.0063311.
279. Scherr TD, Roux CM, Hanke ML, et al. (2013). Global transcriptome analysis of Staphylococcus aureus biofilms in response to innate immune cells. Infect Immun 81:4363–76.
280. Schneider CA, Rasband WS, Eliceiri KW., (2012). NIH image to ImageJ:25 years of image analysis. Nat Methods 9:671–5.
281. Schultz MP, Swain GW., (1999). The effect of biofilms on turbulent boundary layers. J Fluid Eng-T Asme 121:44–51.
282. Sharma S, Cross SE, Hsueh C, et al. (2010). Nanocharacterization in dentistry. Int J Mol Sci 11:2523–45.
283. Sim STV, Suwarno SR, Chong TH, et al. (2013). Monitoring membrane biofouling via ultrasonic time-domain reflectometry enhanced by silica dosing. J Membrane Sci 428:24–37.
284. Sjollema J, Busscher HJ, Weerkamp AH., (1989). Experimental approaches for studying adhesion of microorganisms to solid substrata:applications and mass transport. J Microbiol Meth 9:79–90.
285. Skolimowski M, Nielsen MW, Emneus J, et al. (2010). Microfluidic dissolved oxygen gradient generator biochip as a useful tool in bacterial biofilm studies. Lab Chip 10:2162–9.
286. Skolimowski M, Weiss Nielsen M, Abeille F, et al. (2012). Modular microfluidic system as a model of cystic fibrosis airways. Biomicrofluidics 6:34109. doi:10.1063/1.4742911.
287. Skovager A, Whitehead K, Siegumfeldt H, et al. (2012). Influence of flow direction and flow rate on the initial adhesion of seven Listeria monocytogenes strains to fine polished stainless steel. Int J Food Microbiol 157:174–81.
288. Sousa AM, Pereira MO, Azevedo NF, Lourenço A., (2014). An harmonised vocabulary for communicating and interchanging biofilms experimental results. J Integr Bioinform 11:249.
289. Speziale P, Pietrocola G, Foster TJ, Geoghegan JA., (2014). Protein-based biofilm matrices in staphylococci. Front Cell Infect Microbiol 4:171. doi:10.3389/fcimb.2014.00171.
290. Stepanović S, Vuković D, Dakić I, et al. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Meth 40:175–9.
291. Stepanovic S, Vukovic D, Hola V, et al. (2007). Quantification of biofilm in microtiter plates:overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891–9.
292. Sternberg C, Christensen BB, Johansen T, et al. (1999). Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol 65:4108–17.
293. Stewart PS, Franklin MJ., (2008). Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210.
294. Stewart PS, Rayner J, Roe F, Rees WM., (2001). Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol 91:525–32.
295. Stingu CS, Rodloff AC, Jentsch H, et al. (2008). Rapid identification of oral anaerobic bacteria cultivated from subgingival biofilm by MALDI-TOF-MS. Oral Microbiol Immunol 23:372–6.
296. Stipetic LH, Dalby MJ, Davies RL, et al. (2016). A novel metabolomic approach used for the comparison of Staphylococcus aureus planktonic cells and biofilm samples. Metabolomics 12:75. doi:10.1007/s11306-016-1002-0.
297. Stoecker K, Dorninger C, Daims H, Wagner M., (2010). Double labeling of oligonucleotide probes for fluorescence in situ hybridization (DOPE-FISH) improves signal intensity and increases rRNA accessibility. Appl Environ Microbiol 76:922–6.
298. Stoodley P, Dodds I, Boyle JD, Lappin-Scott HM., (1998). Influence of hydrodynamics and nutrients on biofilm structure. J Appl Microbiol 85:19S–28S.
299. Storey MV, Ashbolt NJ., (2002). A comparison of methods and models for the analysis of water distribution pipe biofilms. In:Wilderer P, Amy G, Arvin E, et al., eds. 2nd World Water Congress:water distribution and water services management. London, UK:IWA Publishing, 73–80.
300. Strauber H, Muller S., (2010). Viability states of bacteria-specific mechanisms of selected probes. Cytometry A 77:623–34.
301. Sun L, Liao K, Wang D., (2015). Effects of magnolol and honokiol on adhesion, yeast-hyphal transition, and formation of biofilm by Candida albicans. PLoS One 10:e0117695. doi:10.1371/journal.pone.0117695.
302. Sutherland IW., (2001). Exopolysaccharides in biofilms, flocs and related structures. Water Sci Technol 43:77–86.
303. Szlavik J, Paiva DS, Mork N, et al. (2012). Initial adhesion of Listeria monocytogenes to solid surfaces under liquid flow. Int J Food Microbiol 152:181–8.
304. Tapia JM, Munoz JA, Gonzalez F, et al. (2009). Extraction of extracellular polymeric substances from the acidophilic bacterium Acidiphilium 3.2sup(5). Water Sci Technol 59:1959–67.
305. Tavernier S, Coenye T., (2015). Quantification of Pseudomonas aeruginosa in multispecies biofilms using PMA-qPCR. PeerJ 3:e787. doi:10.7717/peerj.787.
306. Taylor MJ, Bentham RH, Ross KE., (2014). Limitations of using propidium monoazide with qPCR to discriminate between live and dead Legionella in biofilm samples. Microbiol Insights 7:15–24.
307. Teodosio J, Simoes M, Mergulhão F., (2013a). Platforms for in-vitro biofilm studies. In:Simoes M, Mergulhão F, eds. Biofilms in bioengineering. New York:Nova Science Publishers.
308. Teodosio JS, Silva FC, Moreira JM, et al. (2013b). Flow cells as quasi-ideal systems for biofouling simulation of industrial piping systems. Biofouling 29:953–66.
309. Teodosio JS, Simoes M, Melo LF, Mergulhao FJ., (2011). Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 27:1–11.
310. Teodosio JS, Simoes M, Mergulhao FJ., (2012). The influence of nonconjugative Escherichia coli plasmids on biofilm formation and resistance. J Appl Microbiol 113:373–82.
311. Terry J, Neethirajan S., (2014). A novel microfluidic wound model for testing antimicrobial agents against Staphylococcus pseudintermedius biofilms. J Nanobiotechnol 12:1. doi:10.1186/1477-3155-12-1.
312. Timp W, Matsudaira P., (2008). Electron microscopy of hydrated samples. Meth Cell Biol 89:391–407.
313. Tolker-Nielsen T, Sternberg C., (2011). Growing and analyzing biofilms in flow chambers. Curr Protoc Microbiol Chapter 1:Unit 1B.2. doi:10.1002/9780471729259.mc01b02s21.
314. Tolker-Nielsen T, Sternberg C., (2014). Methods for studying biofilm formation:flow cells and confocal laser scanning microscopy. Methods Mol Biol 1149:615–29.
315. Tote K, Vanden Berghe D, Levecque S, et al. (2009). Evaluation of hydrogen peroxide-based disinfectants in a new resazurin microplate method for rapid efficacy testing of biocides. J Appl Microbiol 107:606–15.
316. Toth L, Csomor P, Sziklai I, Karosi T., (2011). Biofilm detection in chronic rhinosinusitis by combined application of hematoxylin–eosin and gram staining. Eur Arch Otorhinolaryngol 268:1455–62.
317. Trulear MG, Characklis WG., (1982). Dynamics of biofilm processes. J Water Pollut Con F 54:1288–301.
318. Turonova H, Neu TR, Ulbrich P, et al. (2016). The biofilm matrix of Campylobacter jejuni determined by fluorescence lectin-binding analysis. Biofouling 32:597–608.
319. Valm AM, Mark Welch JL, Rieken CW, et al. (2011). Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc Natl Acad Sci USA 108:4152–7.
320. Van Den Driessche F, Rigole P, Brackman G, Coenye T., (2014). Optimization of resazurin-based viability staining for quantification of microbial biofilms. J Microbiol Methods 98:31–4.
321. Van Laar TA, Chen T, You T, Leung KP., (2015). Sublethal concentrations of carbapenems alter cell morphology and genomic expression of Klebsiella pneumoniae biofilms. Antimicrob Agents Chemother 59:1707–17.
322. Verma V, Harjai K, Chhibber S., (2010). Structural changes induced by a lytic bacteriophage make ciprofloxacin effective against older biofilm of Klebsiella pneumoniae. Biofouling 26:729–37.
323. Vester B, Wengel J., (2004). LNA (locked nucleic acid):high-affinity targeting of complementary RNA and DNA. Biochemistry 43:13233–41.
324. Villacorte LO, Ekowati Y, Neu TR, et al. (2015). Characterisation of algal organic matter produced by bloom-forming marine and freshwater algae. Water Res 73:216–30.
325. Vogel C, Marcotte EM., (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13:227–32.
326. Vorregaard M., (2008). Comstat2–a modern 3D image analysis environment for biofilms. Master of Science [Master thesis]. Technical University of Denmark.
327. Wallace PK, Arey B, Mahaffee WF., (2011). Subsurface examination of a foliar biofilm using scanning electron- and focused-ion-beam microscopy. Micron 42:579–85.
328. Wang S, Liu X, Liu H, et al. (2015). The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Rep 7:330–40.
329. Waring MJ., (1965). Complex formation between ethidium bromide and nucleic acids. J Mol Biol 13:269–82.
330. Watrous JD, Dorrestein PC., (2011). Imaging mass spectrometry in microbiology. Nat Rev Microbiol 9:683–94.
331. Webb JS, Thompson LS, James S, et al. (2003). Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185:4585–92.
332. Weissbrodt DG, Neu TR, Kuhlicke U, et al. (2013). Assessment of bacterial and structural dynamics in aerobic granular biofilms. Front Microbiol 4:175. doi:10.3389/fmicb.2013.00175.
333. Willcock L, Gilbert P, Holah J, et al. (2000). A new technique for the performance evaluation of clean-in-place disinfection of biofilms. J Ind Microbiol Biot 25:235–41.
334. Winther B, Gross BC, Hendley JO, Early SV., (2009). Location of bacterial biofilm in the mucus overlying the adenoid by light microscopy. Arch Otolaryngol Head Neck Surg 135:1239–45.
335. Wirtanen G, Mattila-Sandholm T., (1993). Epifluorescence image-analysis and cultivation of foodborne biofilm bacteria grown on stainless-steel surfaces. J Food Protect 56:678–83.
336. Wolfaardt GM, Lawrence JR, Robarts RD, et al. (1994). Multicellular organization in a degradative biofilm community. Appl Environ Microbiol 60:434–46.
337. Yasunaga A, Yoshida A, Morikawa K, et al. (2013). Monitoring the prevalence of viable and dead cariogenic bacteria in oral specimens and in vitro biofilms by qPCR combined with propidium monoazide. BMC Microbiol 13:157. doi:10.1186/1471-2180-13-157.
338. Yawata Y, Toda K, Setoyama E, et al. (2010). Monitoring biofilm development in a microfluidic device using modified confocal reflection microscopy. J Biosci Bioeng 110:377–80.
339. You Y, Moreira BG, Behlke MA, Owczarzy R., (2006). Design of LNA probes that improve mismatch discrimination. Nucleic Acids Res 34:e60. doi:10.1093/nar/gkl175.
340. Zeng G, Muller T, Meyer RL., (2014). Single-cell force spectroscopy of bacteria enabled by naturally derived proteins. Langmuir 30:4019–25.
341. Zeng G, Vad BS, Dueholm MS, et al. (2015). Functional bacterial amyloid increases Pseudomonas biofilm hydrophobicity and stiffness. Front Microbiol 6:1099. doi:10.3389/fmicb.2015.01099.
342. Zhang RY, Neu TR, Bellenberg S, et al. (2015a). Use of lectins to in situ visualize glycoconjugates of extracellular polymeric substances in acidophilic archaeal biofilms. Microb Biotechnol 8:448–61.
343. Zhang W, Sun J, Ding W, et al. (2015b). Extracellular matrix-associated proteins form an integral and dynamic system during Pseudomonas aeruginosa biofilm development. Front Cell Infect Microbiol 5:40. doi:10.3389/fcimb.2015.00040.
344. Zhang Z, Han D, Zhang S, et al. (2009). Biofilms and mucosal healing in postsurgical patients with chronic rhinosinusitis. Am J Rhinol Allergy 23:506–11.
345. Zhao B, Van Der Mei HC, Subbiahdoss G, et al. (2014). Soft tissue integration versus early biofilm formation on different dental implant materials. Dent Mater 30:716–27.
346. Zhu H, Isikman SO, Mudanyali O, et al. (2013). Optical imaging techniques for point-of-care diagnostics. Lab Chip 13:51–67.
347. Zielinski JS, Zielinska AK, Bouaynaya N, et al. (2011). Automated biofilm region recognition and morphology quantification from confocal laser scanning microscopy imaging. Biomedical Sciences and Engineering Conference (BSEC); 2011 Mar 15–17, 1–4.
348. Zippel B, Neu TR., (2011). Characterization of glycoconjugates of extracellular polymeric substances in tufa-associated biofilms by using fluorescence lectin-binding analysis. Appl Environ Microbiol 77:505–16.
349. Zlatanova J, Lindsay SM, Leuba SH., (2001). Single molecule force spectroscopy in biology using the atomic force microscope. Prog Biophys Mol Biol 74:37–61.