Microfluidics for Biofilm Studies

Literature Cited

1. 1.

   Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95–108
   [Google Scholar]
2. 2.

   Nadell CD, Foster KR, Xavier JB. 2010. Emergence of spatial structure in cell groups and the evolution of cooperation. PLOS Comput. Biol. 6:31000716
   [Google Scholar]
3. 3.

   Lopez D, Vlamakis H, Kolter R. 2010. Biofilms. Cold Spring Harb. Perspect. Biol. 2:7a000398
   [Google Scholar]
4. 4.

   Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:41140–54
   [Google Scholar]
5. 5.

   Hoffman MD, Zucker LI, Brown PJB, Kysela DT, Brun YV, Jacobson SC. 2015. Timescales and frequencies of reversible and irreversible adhesion events of single bacterial cells. Anal. Chem. 87:2412032–39
   [Google Scholar]
6. 6.

   Okshevsky M, Regina VR, Meyer RL. 2015. Extracellular DNA as a target for biofilm control. Curr. Opin. Biotechnol. 33:73–80
   [Google Scholar]
7. 7.

   Suarez C, Piculell M, Modin O, Langenheder S, Persson F, Hermansson M. 2019. Thickness determines microbial community structure and function in nitrifying biofilms via deterministic assembly. Sci. Rep. 9:5110
   [Google Scholar]
8. 8.

   Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14:9563–75
   [Google Scholar]
9. 9.

   Yang L, Hu Y, Liu Y, Zhang J, Ulstrup J, Molin S. 2011. Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ. Microbiol. 13:71705–17
   [Google Scholar]
10. 10.

    Macfarlane S, Dillon JF. 2007. Microbial biofilms in the human gastrointestinal tract. J. Appl. Microbiol. 102:51187–96
    [Google Scholar]
11. 11.

    Lewis K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45:4999–1007
    [Google Scholar]
12. 12.

    Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:54181318–22
    [Google Scholar]
13. 13.

    Wi YM, Patel R. 2018. Understanding biofilms and novel approaches to the diagnosis, prevention, and treatment of medical device-associated infections. Infect. Dis. Clin. N. Am. 32:4915–29
    [Google Scholar]
14. 14.

    Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8:9881–90
    [Google Scholar]
15. 15.

    Campoccia D, Mirzaei R, Montanaro L, Arciola CR. 2019. Hijacking of immune defences by biofilms: a multifront strategy. Biofouling 35:101055–74
    [Google Scholar]
16. 16.

    Römling U, Balsalobre C. 2012. Biofilm infections, their resilience to therapy and innovative treatment strategies. J. Intern. Med. 272:6541–61
    [Google Scholar]
17. 17.

    Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:6964306–10
    [Google Scholar]
18. 18.

    Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:4322–32
    [Google Scholar]
19. 19.

    Cantón R, Morosini MI. 2011. Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiol. Rev. 35:5977–91
    [Google Scholar]
20. 20.

    Stewart PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:9276135–38
    [Google Scholar]
21. 21.

    Tolker-Nielsen T, Sternberg C. 2011. Growing and analyzing biofilms in flow chambers. Curr. Protoc. Microbiol. 21:B2.1–17
    [Google Scholar]
22. 22.

    Convery N, Gadegaard N. 2019. 30 Years of microfluidics. Micro Nano Eng. 2:76–91
    [Google Scholar]
23. 23.

    Dittrich PS, Manz A. 2006. Lab-on-a-chip: microfluidics in drug discovery. Nat. Rev. Drug Discov. 5:3210–18
    [Google Scholar]
24. 24.

    Xia Y, Whitesides GM. 1998. Soft lithography. Angew. Chem. Int. Ed. 37:5550–75
    [Google Scholar]
25. 25.

    Diaz De Rienzo MA, Stevenson PS, Marchant R, Banat IM. 2016. Effect of biosurfactants on Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a BioFlux channel. Appl. Microbiol. Biotechnol. 100:5773–79
    [Google Scholar]
26. 26.

    Volpatti LR, Yetisen AK. 2014. Commercialization of microfluidic devices. Trends Biotechnol. 32:7347–50
    [Google Scholar]
27. 27.

    Scott SM, Ali Z 2021. Fabrication methods for microfluidic devices: an overview. Micromachines 12:3319
    [Google Scholar]
28. 28.

    Byun CK, Abi-Samra K, Cho YK, Takayama S. 2014. Pumps for microfluidic cell culture. Electrophoresis 35:2–3245–57
    [Google Scholar]
29. 29.

    Pérez-Rodríguez S, García-Aznar JM, Gonzalo-Asensio J. 2022. Microfluidic devices for studying bacterial taxis, drug testing and biofilm formation. Microb. Biotechnol. 15:2395–414
    [Google Scholar]
30. 30.

    Straub H, Eberl L, Zinn M, Rossi RM, Maniura-Weber K, Ren Q. 2020. A microfluidic platform for in situ investigation of biofilm formation and its treatment under controlled conditions. J. Nanobiotechnol. 18:166
    [Google Scholar]
31. 31.

    Balagaddé FK, You L, Hansen CL, Arnold FH, Quake SR. 2005. Long-term monitoring of bacteria undergoing programmed population control in a microchemostat. Science 309:5731137–40
    [Google Scholar]
32. 32.

    Liao Z, Wang J, Zhang P, Zhang Y, Miao Y et al. 2018. Recent advances in microfluidic chip integrated electronic biosensors for multiplexed detection. Biosens. Bioelectron. 121:272–80
    [Google Scholar]
33. 33.

    Son K, Brumley DR, Stocker R. 2015. Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics. Nat. Rev. Microbiol. 13:12761–75
    [Google Scholar]
34. 34.

    Stoodley P, DeBeer D, Lewandowski Z. 1994. Liquid flow in biofilm systems. Appl. Environ. Microbiol. 60:82711–16
    [Google Scholar]
35. 35.

    Scheler O, Postek W, Garstecki P. 2019. Recent developments of microfluidics as a tool for biotechnology and microbiology. Curr. Opin. Biotechnol. 55:60–67
    [Google Scholar]
36. 36.

    Recupido F, Toscano G, Tatè R, Petala M, Caserta S et al. 2020. The role of flow in bacterial biofilm morphology and wetting properties. Colloid Surf. B Biointerfaces 192:111047
    [Google Scholar]
37. 37.

    Lauga E. 2016. Bacterial hydrodynamics. Annu. Rev. Fluid Mech. 48:105–30
    [Google Scholar]
38. 38.

    Guttenplan SB, Kearns DB. 2013. Regulation of flagellar motility during biofilm formation. FEMS Microbiol. Rev. 37:6849–71
    [Google Scholar]
39. 39.

    Lauga E, DiLuzio WR, Whitesides GM, Stone HA. 2006. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90:2400–12
    [Google Scholar]
40. 40.

    Kaya T, Koser H. 2012. Direct upstream motility in Escherichia coli. Biophys. J. 102:71514–23
    [Google Scholar]
41. 41.

    Persat A, Nadell CD, Kim MK, Ingremeau F, Siryaporn A et al. 2015. The mechanical world of bacteria. Cell 161:5988–97
    [Google Scholar]
42. 42.

    Belas R. 2014. Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 22:9517–27
    [Google Scholar]
43. 43.

    Berne C, Ellison CK, Ducret A, Brun YV. 2018. Bacterial adhesion at the single-cell level. Nat. Rev. Microbiol. 16:10616–27
    [Google Scholar]
44. 44.

    Thomas W. 2008. Catch bonds in adhesion. Annu. Rev. Biomed. Eng. 10:39–57
    [Google Scholar]
45. 45.

    Thomas WE, Vogel V, Sokurenko E. 2008. Biophysics of catch bonds. Annu. Rev. Biophys. 37:399–416
    [Google Scholar]
46. 46.

    Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V. 2004. Shear-dependent “stick-and-roll” adhesion of type 1 fimbriated Escherichia coli. Mol. Microbiol. 53:51545–57
    [Google Scholar]
47. 47.

    Yakovenko O, Sharma S, Forero M, Tchesnokova V, Aprikian P et al. 2008. FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J. Biol. Chem. 283:1711596–605
    [Google Scholar]
48. 48.

    Rodesney CA, Roman B, Dhamani N, Cooley BJ, Katira P et al. 2017. Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. PNAS 114:235906–11
    [Google Scholar]
49. 49.

    Newell PD, Boyd CD, Sondermann H, O'Toole GA. 2011. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLOS Biol. 9:2e1000587
    [Google Scholar]
50. 50.

    Sanfilippo JE, Lorestani A, Koch MD, Bratton BP, Siryaporn A et al. 2019. Microfluidic-based transcriptomics reveal force-independent bacterial rheosensing. Nat. Microbiol. 4:81274–81
    [Google Scholar]
51. 51.

    De La Fuente L, Montanes E, Meng Y, Li Y, Burr TJ et al. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 73:82690–96
    [Google Scholar]
52. 52.

    Kim MK, Ingremeau F, Zhao A, Bassler BL, Stone HA. 2016. Local and global consequences of flow on bacterial quorum sensing. Nat. Microbiol. 1:15005
    [Google Scholar]
53. 53.

    De Grazia A, LuTheryn G, Meghdadi A, Mosayyebi A, Espinosa-Ortiz EJ et al. 2020. A microfluidic-based investigation of bacterial attachment in ureteral stents. Micromachines 11:4408
    [Google Scholar]
54. 54.

    Boedicker JQ, Vincent ME, Ismagilov RF. 2009. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Ed. 121:326022–25
    [Google Scholar]
55. 55.

    Lin N, Valiei A, McKay G, Nguyen D, Tufenkji N, Moraes C. 2022. Microfluidic study of bacterial attachment on and detachment from zinc oxide nanopillars. ACS Biomater. Sci. Eng. 8:73122–31
    [Google Scholar]
56. 56.

    Valentin JDP, Straub H, Pietsch F, Lemare M, Ahrens CH et al. 2022. Role of the flagellar hook in the structural development and antibiotic tolerance of Pseudomonas aeruginosa biofilms. ISME J. 16:41176–86
    [Google Scholar]
57. 57.

    Nadell CD, Bassler BL. 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. PNAS 108:3414181–85
    [Google Scholar]
58. 58.

    Xia Y, Jayathilake PG, Li B, Zuliani P, Deehan D et al. 2022. Coupled CFD-DEM modeling to predict how EPS affects bacterial biofilm deformation, recovery and detachment under flow conditions. Biotechnol. Bioeng. 119:2551–63
    [Google Scholar]
59. 59.

    Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319–46
    [Google Scholar]
60. 60.

    Stanley NR, Lazazzera BA. 2004. Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52:4917–24
    [Google Scholar]
61. 61.

    Zheng S, Bawazir M, Dhall A, Kim HE, He L et al. 2021. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front. Bioeng. Biotechnol. 9:643722
    [Google Scholar]
62. 62.

    Tuson HH, Weibel DB. 2013. Bacteria-surface interactions. Soft Matter 9:174368–80
    [Google Scholar]
63. 63.

    Krasowska A, Sigler K. 2014. How microorganisms use hydrophobicity and what does this mean for human needs?. Front. Cell. Infect. Microbiol. 4:112
    [Google Scholar]
64. 64.

    Zhou J, Khodakov DA, Ellis AV, Voelcker NH. 2012. Surface modification for PDMS-based microfluidic devices. Electrophoresis 33:189–104
    [Google Scholar]
65. 65.

    Salta M, Capretto L, Carugo D, Wharton JA, Stokes KR. 2013. Life under flow: a novel microfluidic device for the assessment of anti-biofilm technologies. Biomicrofluidics 7:6064118
    [Google Scholar]
66. 66.

    Ofek I, Hasty DL, Sharon N 2003. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol. Med. Microbiol. 38:3181–91
    [Google Scholar]
67. 67.

    Buhmann MT, Stiefel P, Maniura-Weber K, Ren Q. 2016. In vitro biofilm models for device-related infections. Trends Biotechnol. 34:12945–48
    [Google Scholar]
68. 68.

    Carniello V, Peterson BW, van der Mei HC, Busscher HJ 2018. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv. Colloid Interface Sci. 261:1–14
    [Google Scholar]
69. 69.

    Wilson WW, Wade MM, Holman SC, Champlin FR. 2001. Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J. Microbiol. Methods 43:3153–64
    [Google Scholar]
70. 70.

    Gottenbos B, Grijpma DW, van der Mei HC, Feijen J, Busscher HJ. 2001. Antimicrobial effects of positively charged surfaces on adhering Gram-positive and Gram-negative bacteria. J. Antimicrob. Chemother. 48:7–13
    [Google Scholar]
71. 71.

    Hamadi F, Latrache H, Zahir H, Elghmari A, Timinouni M, Ellouali M. 2008. The relation between Escherichia coli surface functional groups’ composition and their physiochemical properties. Braz. J. Microbiol. 39:10–15
    [Google Scholar]
72. 72.

    Zhu J, Wang M, Zhang H, Yang S, Song KY et al. 2020. Effects of hydrophilicity, adhesion work, and fluid flow on biofilm formation of PDMS in microfluidic systems. ACS Appl. Bio Mater. 3:128386–94
    [Google Scholar]
73. 73.

    Renner LD, Weibel DB. 2011. Physicochemical regulation of biofilm formation. MRS Bull. 36:5347–55
    [Google Scholar]
74. 74.

    Yang K, Shi J, Wang L, Chen Y, Liang C et al. 2022. Bacterial anti-adhesion surface design: surface patterning, roughness and wettability: a review. J. Mater. Sci. Technol. 99:82–100
    [Google Scholar]
75. 75.

    Sharma S, Jaimes-Lizcano YA, McLay RB, Cirino PC, Conrad JC. 2016. Subnanometric roughness affects the deposition and mobile adhesion of Escherichia coli on silanized glass surfaces. Langmuir 32:215422–33
    [Google Scholar]
76. 76.

    Mitik-Dineva N, Wang J, Mocanasu RC, Stoddart PR, Crawford RJ, Ivanova EP. 2008. Impact of nano-topography on bacterial attachment. Biotechnol. J. 3:4536–44
    [Google Scholar]
77. 77.

    Zhu Y, Gu Y, Qiao S, Zhou L, Shi J, Lai H. 2017. Bacterial and mammalian cells adhesion to tantalum-decorated micro-/nano-structured titanium. J. Biomed. Mater. Res. A 105:3871–78
    [Google Scholar]
78. 78.

    Velic A, Hasan J, Li Z, Yarlagadda PKDV. 2021. Mechanics of bacterial interaction and death on nanopatterned surfaces. Biophys. J. 120:2217–31
    [Google Scholar]
79. 79.

    Valiei A, Lin N, Bryche JF, McKay G, Canva M et al. 2020. Hydrophilic mechano-bactericidal nanopillars require external forces to rapidly kill bacteria. Nano Lett. 20:85720–27
    [Google Scholar]
80. 80.

    Li L, Tian F, Chang H, Zhang J, Wang C et al. 2019. Interactions of bacteria with monolithic lateral silicon nanospikes inside a microfluidic channel. Front. Chem. 7:483
    [Google Scholar]
81. 81.

    Doll PW, Doll K, Winkel A, Thelen R, Ahrens R et al. 2022. Influence of the available surface area and cell elasticity on bacterial adhesion forces on highly ordered silicon nanopillars. ACS Omega 7:2117620–31
    [Google Scholar]
82. 82.

    Siddiqui S, Chandrasekaran A, Lin N, Tufenkji N, Moraes C. 2019. Microfluidic shear assay to distinguish between bacterial adhesion and attachment strength on stiffness-tunable silicone substrates. Langmuir 35:268840–49
    [Google Scholar]
83. 83.

    Valentin JDP, Qin XH, Fessele C, Straub H, van der Mei HC et al. 2019. Substrate viscosity plays an important role in bacterial adhesion under fluid flow. J. Colloid Interface Sci. 552:247–57
    [Google Scholar]
84. 84.

    Nagy K, Dukic B, Hodula O, Ábrahám Á, Csákvári E et al. 2022. Emergence of resistant Escherichia coli mutants in microfluidic on-chip antibiotic gradients. Front. Microbiol. 13:820738
    [Google Scholar]
85. 85.

    Tang P-C, Eriksson O, Sjögren J, Fatsis-Kavalopoulos N, Kreuger J, Andersson DI. 2022. A microfluidic chip for studies of the dynamics of antibiotic resistance selection in bacterial biofilms. Front. Cell. Infect. Microbiol. 12:896149
    [Google Scholar]
86. 86.

    Qiu Y, Zhang J, Li B, Wen X, Liang P, Huang X. 2018. A novel microfluidic system enables visualization and analysis of antibiotic resistance gene transfer to activated sludge bacteria in biofilm. Sci. Total Environ. 642:582–90
    [Google Scholar]
87. 87.

    Li B, Qiu Y, Zhang J, Huang X, Shi H, Yin H. 2018. Real-time study of rapid spread of antibiotic resistance plasmid in biofilm using microfluidics. Environ. Sci. Technol. 52:1911132–41
    [Google Scholar]
88. 88.

    Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6:3199–210
    [Google Scholar]
89. 89.

    Zhang K, Qin S, Wu S, Liang Y, Li J. 2020. Microfluidic systems for rapid antibiotic susceptibility tests (ASTs) at the single-cell level. Chem. Sci. 11:256352–61
    [Google Scholar]
90. 90.

    Kim KP, Kim YG, Choi CH, Kim HE, Lee SH et al. 2010. In situ monitoring of antibiotic susceptibility of bacterial biofilms in a microfluidic device. Lab Chip 10:233296–99
    [Google Scholar]
91. 91.

    Hou Z, An Y, Hjort K, Hjort K, Sandegren L, Wu Z. 2014. Time lapse investigation of antibiotic susceptibility using a microfluidic linear gradient 3D culture device. Lab Chip 14:173409–18
    [Google Scholar]
92. 92.

    Tran VN, Khan F, Han W, Luluil M, Truong VG et al. 2022. Real-time monitoring of mono- and dual-species biofilm formation and eradication using microfluidic platform. Sci. Rep. 12:19678
    [Google Scholar]
93. 93.

    Blanco-Cabra N, López-Martínez MJ, Arévalo-Jaimes BV, Martin-Gómez MT, Samitier J, Torrents E. 2021. A new BiofilmChip device for testing biofilm formation and antibiotic susceptibility. npj Biofilms Microbiomes 7:62
    [Google Scholar]
94. 94.

    Nance WC, Dowd SE, Samarian D, Chludzinski J, Delli J et al. 2013. A high-throughput microfluidic dental plaque biofilm system to visualize and quantify the effect of antimicrobials. J. Antimicrob. Chemother. 68:112550–60
    [Google Scholar]
95. 95.

    Shin S, Ahmed I, Hwang J, Seo Y, Lee E et al. 2016. A microfluidic approach to investigating a synergistic effect of tobramycin and sodium dodecyl sulfate on Pseudomonas aeruginosa biofilms. Anal. Sci. 32:167–73
    [Google Scholar]
96. 96.

    Imran M, Jha SK, Hasan N, Insaf A, Shrestha J et al. 2022. Overcoming multidrug resistance of antibiotics via nanodelivery systems. Pharmaceutics 14:3586
    [Google Scholar]
97. 97.

    Artzy-Schnirman A, Lehr CM, Sznitman J. 2020. Advancing human in vitro pulmonary disease models in preclinical research: opportunities for lung-on-chips. Expert Opin. Drug Deliv. 17:5621–25
    [Google Scholar]
98. 98.

    Kim HJ, Li H, Collins JJ, Ingber DE. 2016. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. PNAS 113:1E7–15
    [Google Scholar]
99. 99.

    Yuan L, De Haan P, Peterson BW, De Jong ED, Verpoorte E et al. 2020. Visualization of bacterial colonization and cellular layers in a gut-on-a-chip system using optical coherence tomography. Microsc. Microanal. 26:61211–19
    [Google Scholar]
100. 100.

     Kim HJ, Huh D, Hamilton G, Ingber DE. 2012. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12:122165–74
     [Google Scholar]
101. 101.

     Plebani R, Potla R, Soong M, Bai H, Izadifar Z et al. 2021. Modeling pulmonary cystic fibrosis in a human lung airway-on-a-chip: cystic fibrosis airway chip. J. Cyst. Fibros. 21:4606–15
     [Google Scholar]
102. 102.

     Maschmeyer I, Lorenz AK, Schimek K, Hasenberg T, Ramme AP et al. 2015. A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents. Lab Chip 15:122688–99
     [Google Scholar]
103. 103.

     Skardal A, Shupe T, Atala A. 2016. Organoid-on-a-chip and body-on-a-chip systems for drug screening and disease modeling. Drug Discov. Today 21:91399–1411
     [Google Scholar]
104. 104.

     Lee JH, Gu Y, Wang H, Lee WY. 2012. Microfluidic 3D bone tissue model for high-throughput evaluation of wound-healing and infection-preventing biomaterials. Biomaterials 33:4999–1006
     [Google Scholar]
105. 105.

     Lee JH, Wang H, Kaplan JB, Lee WY. 2010. Microfluidic approach to create three-dimensional tissue models for biofilm-related infection of orthopaedic implants. Tissue Eng. C Methods 17:139–48
     [Google Scholar]
106. 106.

     Xu Y, Dhaouadi Y, Stoodley P, Ren D. 2020. Sensing the unreachable: challenges and opportunities in biofilm detection. Curr. Opin. Biotechnol. 64:79–84
     [Google Scholar]
107. 107.

     Doll K, Jongsthaphongpun KL, Stumpp NS, Winkel A, Stiesch M. 2016. Quantifying implant-associated biofilms: comparison of microscopic, microbiologic and biochemical methods. J. Microbiol. Methods 130:61–68
     [Google Scholar]
108. 108.

     Hazan R, Que YA, Maura D, Rahme LG 2012. A method for high throughput determination of viable bacteria cell counts in 96-well plates. BMC Microbiol. 12:259
     [Google Scholar]
109. 109.

     Garcia-Betancur JC, Yepes A, Schneider J, Lopez D. 2012. Single-cell analysis of Bacillus subtilis biofilms using fluorescence microscopy and flow cytometry. J. Vis. Exp. 60:e3796
     [Google Scholar]
110. 110.

     Behera B, Anil Vishnu GK, Chatterjee S, Sitaramgupta VSN, Sreekumar N et al. 2019. Emerging technologies for antibiotic susceptibility testing. Biosens. Bioelectron. 142:111552
     [Google Scholar]
111. 111.

     Persat A, Stone HA, Gitai Z. 2014. The curved shape of Caulobacter crescentus enhances surface colonization in flow. Nat. Commun. 5:3824
     [Google Scholar]
112. 112.

     Wang P, Robert L, Pelletier J, Dang WL, Taddei F et al. 2010. Robust growth of Escherichia coli. Curr. Biol. 20:121099–1103
     [Google Scholar]
113. 113.

     Hassanpourfard M, Sun X, Valiei A, Mukherjee P, Thundat T et al. 2014. Protocol for biofilm streamer formation in a microfluidic device with micro-pillars. J. Vis. Exp. 90:e51732
     [Google Scholar]
114. 114.

     Mukherjee M, Menon NV, Liu X, Kang Y, Cao B. 2016. Confocal laser scanning microscopy-compatible microfluidic membrane flow cell as a nondestructive tool for studying biofouling dynamics on forward osmosis membranes. Environ. Sci. Technol. Lett. 3:8303–9
     [Google Scholar]
115. 115.

     Cattoni DI, Fiche J-B, Valeri A, Mignot TM, Nöllmann M. 2013. Super-resolution imaging of bacteria in a microfluidics device. PLOS ONE 8:10e76268
     [Google Scholar]
116. 116.

     Okumus B, Landgraf D, Lai GC, Bakhsi S, Arias-Castro JC et al. 2016. Mechanical slowing-down of cytoplasmic diffusion allows in vivo counting of proteins in individual cells. Nat. Commun. 7:11641
     [Google Scholar]
117. 117.

     Endesfelder U. 2019. From single bacterial cell imaging towards in vivo single-molecule biochemistry studies. Essays Biochem. 63:2187–96
     [Google Scholar]
118. 118.

     Chin LK, Lee CH, Chen BC. 2016. Imaging live cells at high spatiotemporal resolution for lab-on-a-chip applications. Lab Chip 16:112014–24
     [Google Scholar]
119. 119.

     Priester JH, Horst AM, Van De Werfhorst LC, Saleta JL, Mertes LAK, Holden PA. 2007. Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J. Microbiol. Methods 68:3577–87
     [Google Scholar]
120. 120.

     Hizal F, Rungraeng N, Lee J, Jun S, Busscher HJ et al. 2017. Nanoengineered superhydrophobic surfaces of aluminum with extremely low bacterial adhesivity. ACS Appl. Mater. Interfaces 9:1312118–29
     [Google Scholar]
121. 121.

     Boehm DA, Gottlieb PA, Hua SZ. 2007. On-chip microfluidic biosensor for bacterial detection and identification. Sens. Actuators B Chem. 126:2508–14
     [Google Scholar]
122. 122.

     Radke SM, Alocilja EC. 2004. Design and fabrication of a microimpedance biosensor for bacterial detection. IEEE Sens. J. 4:4434–40
     [Google Scholar]
123. 123.

     Pousti M, Zarabadi MP, Amirdehi MA, Paquet-Mercier F, Greener J. 2019. Microfluidic bioanalytical flow cells for biofilm studies: a review. Analyst 144:68–86
     [Google Scholar]
124. 124.

     Goikoetxea E, Routkevitch D, de Weerdt A, Green JJ, Steenackers H, Braeken D. 2018. Impedimetric fingerprinting and structural analysis of isogenic E. coli biofilms using multielectrode arrays. Sens. Actuators B Chem. 263:319–26
     [Google Scholar]
125. 125.

     Schultze LB, Maldonado A, Lussi A, Sculean A, Eick S. 2020. The impact of the pH value on biofilm formation. Monogr. Oral Sci. 29:19–29
     [Google Scholar]
126. 126.

     Gashti MP, Asselin J, Barbeau J, Boudreau D, Greener J. 2016. A microfluidic platform with pH imaging for chemical and hydrodynamic stimulation of intact oral biofilms. Lab Chip 16:81412–19
     [Google Scholar]
127. 127.

     Zarabadi MP, Charette SJ, Greener J. 2018. Flow-based deacidification of Geobacter sulfurreducens biofilms depends on nutrient conditions: a microfluidic bioelectrochemical study. ChemElectroChem 5:233645–53
     [Google Scholar]
128. 128.

     Grist SM, Chrostowski L, Cheung KC. 2010. Optical oxygen sensors for applications in microfluidic cell culture. Sensors 10:9286–9316
     [Google Scholar]
129. 129.

     Tahirbegi IB, Ehgartner J, Sulzer P, Zieger S, Kasjanow A et al. 2017. Fast pesticide detection inside microfluidic device with integrated optical pH, oxygen sensors and algal fluorescence. Biosens. Bioelectron. 88:188–95
     [Google Scholar]
130. 130.

     Kühl M, Rickelt LF, Thar R. 2007. Combined imaging of bacteria and oxygen in biofilms. Appl. Environ. Microbiol. 73:196289–95
     [Google Scholar]
131. 131.

     Altintas Z, Akgun M, Kokturk G, Uludag Y. 2018. A fully automated microfluidic-based electrochemical sensor for real-time bacteria detection. Biosens. Bioelectron. 100:541–48
     [Google Scholar]
132. 132.

     Johannessen EA, Weaver JMR, Cobbold PH. 2002. Heat conduction nanocalorimeter for pl-scale single cell measurements. Appl. Phys. Lett. 80:112029–31
     [Google Scholar]
133. 133.

     Pinck S, Ostormujof LM, Teychené S, Erable B. 2020. Microfluidic microbial bioelectrochemical systems: an integrated investigation platform for a more fundamental understanding of electroactive bacterial biofilms. Microorganisms 8:111841
     [Google Scholar]