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Towards Biofilm Spectroscopy – A Novel Microfluidic Approach for Characterizing Biofilm Subpopulation by Microwave-Based Electrical Impedance Spectroscopy

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Published/Copyright: March 28, 2018
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Abstract

In this work three disciplines – microfluidics, microbiology and microwave engineering – are utilized to develop a system for analyzing subpopulations of biofilms and their reaction to antibiotic treatment. We present handling strategies to destabilize a biofilm inside a microfluidic system down to aggregate sizes of<10 µm2 as well as microfluidic structures for the flow-through filtration of the resulting cell suspensions. For the analysis of the cell populations by microwave electrical impedance spectroscopy, two novel calibration schemes are demonstrated to cover both, reflection as well as transmission measurements of dielectric fluids. The broadband calibration strategies are solely based on liquid standards and allow a precise long-term monitoring with a resolution up to Δε=6 ‰, while the error is kept below Δ=1.5 ‰ at5GHz. Combining these three research topics therefore will open up new ways for analyzing biofilm effects.


Christiane Richter, Sönke Schmidt, Julia Bruchmann These authors contributed equally.


Funding statement: Funder Name: Deutsche Forschungsgemeinschaft, Funder Id: 10.13039/501100001659, Grant Number: SPP 1857 Essence.

Acknowledgements

Julia Bruchmann, Christiane Richter and Sönke Schmidt were funded by the German Research Foundation (DFG) as part of the SPP 1857 “Elektromagnetische Sensoren für Life Sciences (ESSENCE)”.

References

[1] J. Costerton, L. Montanaro, and C. Arciola. (2005). Biofilm in implant infections: Its production and regulation. Int. J. Artif. Organs. 28(11), 1062–1068.10.1177/039139880502801103Search in Google Scholar

[2] P. S. Stewart and J. W. Costerton. (2001). Antibiotic resistance of bacteria in biofilms. The Lancet. 358(9276), 135–138.10.1016/S0140-6736(01)05321-1Search in Google Scholar

[3] E. M. Hetrick and M. H. Schoenfisch. (2006). Reducing implant-related infections: Active release strategies. Chem. Soc. Rev. 35(9), 780–789.10.1039/b515219bSearch in Google Scholar PubMed

[4] J. W. Costerton, P. S. Stewart, and E. P. Greenberg. (1999). Bacterial biofilms: A common cause of persistent infections. Science. 284(5418), 1318–1322.10.1126/science.284.5418.1318Search in Google Scholar PubMed

[5] M. Willcox et al., (2008). A novel cationic‐peptide coating for the prevention of microbial colonization on contact lenses. J. Appl. Microbiol. 105(6), 1817–1825.10.1111/j.1365-2672.2008.03942.xSearch in Google Scholar PubMed

[6] P. D. Fey and M. E. Olson. (2010). Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol. 5(6), 917–933.10.2217/fmb.10.56Search in Google Scholar PubMed PubMed Central

[7] C. C. De Carvalho. (2007). Biofilms: Recent developments on an old battle. Recent Pat. Biotechnol. 1(1), 49–57.10.2174/187220807779813965Search in Google Scholar PubMed

[8] K. Lewis. (2001). Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45(4), 999–1007.10.1128/AAC.45.4.999-1007.2001Search in Google Scholar PubMed PubMed Central

[9] D. R. Monteiro et al., (2009). The growing importance of materials that prevent microbial adhesion: Antimicrobial effect of medical devices containing silver. Int. J. Antimicrob. Agents. 34(2), 103–110.10.1016/j.ijantimicag.2009.01.017Search in Google Scholar PubMed

[10] J. Davies, G. B. Spiegelman, and G. Yim. (2006). The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9(5), 445–453.10.1016/j.mib.2006.08.006Search in Google Scholar PubMed

[11] D. Reyes-Romero et al., (2014). Dynamic thermal sensor for biofilm monitoring. Sensors Actuators A: Phy. 213, 43–51.10.1016/j.sna.2014.03.032Search in Google Scholar

[12] F. Mariana et al., (2013). Chip-calorimetric monitoring of biofilm eradication with antibiotics provides mechanistic information. Int. J. Med. Microbiol. 303(3), 158–165.10.1016/j.ijmm.2012.12.009Search in Google Scholar PubMed

[13] R. Maurício et al., (2013). Biofilm thickness measurement using an ultrasound method in a liquid phase. Environ. Monit. Assess. 185(10), 8125–8133.10.1007/s10661-013-3160-0Search in Google Scholar PubMed

[14] N. Saber et al., (2013). A feasibility study on the application of microwaves for online biofilm monitoring in the pipelines. Int. J. Press. Vessels Piping. 111, 99–105.10.1016/j.ijpvp.2013.05.005Search in Google Scholar

[15] R. Ghodssi, M. T. Meyer, and Y. W. Kim. Microsystems for sensing and characterization of bacterial biofilms, in SENSORS, 2013 IEEE. 2013. IEEE.10.1109/ICSENS.2013.6688300Search in Google Scholar

[16] T. Sakata and R. Fukuda. (2013). Simultaneous biosensing with quartz crystal microbalance with a dissipation coupled-gate semiconductor device. Anal. Chem. 85(12), 5796–5800.10.1021/ac400468mSearch in Google Scholar PubMed

[17] T. Sun et al., (2007). Analytical electric field and sensitivity analysis for two microfluidic impedance cytometer designs. Iet Nanobiotechnology. 1(5), 69–79.10.1049/iet-nbt:20070019Search in Google Scholar

[18] E. Ghafar-Zadeh and M. Sawan. (2007). A hybrid microfluidic/CMOS capacitive sensor dedicated to lab-on-chip applications. IEEE Trans. Biomed. Circuits Syst. 1(4), 270–277.10.1109/TBCAS.2008.915641Search in Google Scholar PubMed

[19] G. Facer, D. Notterman, and L. Sohn. (2001). Dielectric spectroscopy for bioanalysis: From 40 Hz to 26.5 GHz in a microfabricated wave guide. Appl. Phys. Lett. 78(7), 996–998.10.1063/1.1347020Search in Google Scholar

[20] K. Grenier et al., (2009). Integrated broadband microwave and microfluidic sensor dedicated to bioengineering. IEEE Trans. Microw. Theory Tech. 57(12), 3246–3253.10.1109/TMTT.2009.2034226Search in Google Scholar

[21] K. Grenier, et al. Resonant based microwave biosensor for biological cells discrimination, in Radio and Wireless Symposium (RWS), 2010 IEEE. 2010. IEEE.10.1109/RWS.2010.5434223Search in Google Scholar

[22] K. Grenier, et al. Microwave signatures of alive B-lymphoma cells suspensions, in 2011 IEEE Topical Conference on Biomedical Wireless Technologies, Networks, and Sensing Systems (BioWireleSS), 2011. IEEE.10.1109/BIOWIRELESS.2011.5724351Search in Google Scholar

[23] J. Liu and D. Xue. (2011). Rapid and scalable route to CuS biosensors: A microwave-assisted Cu-complex transformation into CuS nanotubes for ultrasensitive nonenzymatic glucose sensor. J. Mater. Chem. 21(1), 223–228.10.1039/C0JM01714KSearch in Google Scholar

[24] A. Treizebre and B. Bocquet. (2008). Nanometric metal wire as a guide for THz investigation of living cells. Int. J. Nanotechnology. 5(6–8), 784–795.10.1504/IJNT.2008.018697Search in Google Scholar

[25] A. C. Ward, P. Connolly, and N. P. Tucker. (2014). Pseudomonas aeruginosa can be detected in a polymicrobial competition model using impedance spectroscopy with a novel biosensor. PloS One. 9(3), e91732.10.1371/journal.pone.0091732Search in Google Scholar PubMed PubMed Central

[26] J. Paredes et al., (2013). Interdigitated microelectrode biosensor for bacterial biofilm growth monitoring by impedance spectroscopy technique in 96-well microtiter plates. Sensors Actuators B: Chemical. 178, 663–670.10.1016/j.snb.2013.01.027Search in Google Scholar

[27] L. Pires et al., (2013). Online monitoring of biofilm growth and activity using a combined multi-channel impedimetric and amperometric sensor. Biosens. Bioelectron. 47, 157–163.10.1016/j.bios.2013.03.015Search in Google Scholar PubMed

[28] J. Bruchmann et al., (2015). Multi-channel microfluidic biosensor platform applied for online monitoring and screening of biofilm formation and activity. PloS One. 10(2), e0117300.10.1371/journal.pone.0117300Search in Google Scholar PubMed PubMed Central

[29] H. C. Flemming, T. R. Neu, and D. J. Wozniak. (2007). The EPS matrix: The house of biofilm cells. J. Bacteriol. 189(22), 7945–7947.10.1128/JB.00858-07Search in Google Scholar PubMed PubMed Central

[30] P. Chaignon et al., (2007). Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl. Microbiol. Biotechnol. 75(1), 125–132.10.1007/s00253-006-0790-ySearch in Google Scholar PubMed

[31] S. K. Shukla and T. S. Rao. (2012). Dispersal of Bap-mediated Staphylococcus aureus biofilm by proteinase K. J. Antibiot. 66, 55–60.10.1038/ja.2012.98Search in Google Scholar PubMed

[32] J. B. Kaplan et al., (2012). Recombinant human DNase I decreases biofilm and increases antimicrobial susceptibility in staphylococci. J. Antibiot. 65(2), 73–77.10.1038/ja.2011.113Search in Google Scholar PubMed PubMed Central

[33] C. B. Whitchurch et al., (2002). Extracellular DNA required for bacterial biofilm formation. Science. 295(5559), 1487.10.1126/science.295.5559.1487Search in Google Scholar PubMed

[34] S. Wang et al., (2013). A spider web strategy of type IV pili‐mediated migration to build a fibre‐like Psl polysaccharide matrix in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 15(8), 2238–2253.10.1111/1462-2920.12095Search in Google Scholar PubMed PubMed Central

[35] L. Friedman and R. Kolter. (2004). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51(3), 675–690.10.1046/j.1365-2958.2003.03877.xSearch in Google Scholar PubMed

[36] J. Nett et al., (2007). Putative role of β-1, 3 glucans in Candida albicans biofilm resistance. Antimicrob. Agents Chemother. 51(2), 510–520.10.1128/AAC.01056-06Search in Google Scholar PubMed PubMed Central

[37] A. Boyd and A. Á. Chakrabarty. (1994). Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60(7), 2355–2359.10.1128/aem.60.7.2355-2359.1994Search in Google Scholar PubMed PubMed Central

[38] J. B. Kaplan et al., (2003). Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J. Bacteriol. 185(16), 4693–4698.10.1128/JB.185.16.4693-4698.2003Search in Google Scholar PubMed PubMed Central

[39] L. R. Huang et al., (2004). Continuous particle separation through deterministic lateral displacement. Science. 304(5673), 987–990.10.1126/science.1094567Search in Google Scholar PubMed

[40] J. A. Davis, Microfluidic Separation of Blood Components through Deterministic Lateral Displacement. Princeton University, 2008.Search in Google Scholar

[41] F. Artis et al., (2015). Microwaving biological cells: Intracellular analysis with microwave dielectric spectroscopy. IEEE Microw. Mag. 16(4), 87–96.10.1109/MMM.2015.2393997Search in Google Scholar

[42] J.-C. Chien, et al. A 6.5/17.5-GHz dual-channel interferometer-based capacitive sensor in 65-nm CMOS for high-speed flow cytometry, in Microwave Symposium (IMS), 2014 IEEE MTT-S International. 2014. IEEE.10.1109/MWSYM.2014.6848507Search in Google Scholar

[43] S. Schmidt, M. Schüßler, and R. Jakoby. All liquid based calibration scheme for microwave dielectrometry, in 2017 IEEE MTT-S International Microwave Symposium (IMS). 2017. IEEE.10.1109/MWSYM.2017.8058839Search in Google Scholar

[44] F. Michler, et al. Calibration scheme for microwave biosensors using exclusively liquid calibration standards, in 2016 IEEE Topical Conference on Biomedical Wireless Technologies, Networks, and Sensing Systems (BioWireleSS), 2016. IEEE.10.1109/BIOWIRELESS.2016.7445564Search in Google Scholar

[45] K. Nörtemann, J. Hilland, and U. Kaatze. (1997). Dielectric properties of aqueous NaCl solutions at microwave frequencies. J. Phys. Chem. 101(37), 6864–6869.10.1021/jp971623aSearch in Google Scholar

[46] T. M. Nargang et al., (2014). Liquid polystyrene: A room-temperature photocurable soft lithography compatible pour-and-cure-type polystyrene. Lab Chip. 14(15), 2698–2708.10.1039/C4LC00045ESearch in Google Scholar

[47] F. Kotz et al., (2017). Three-dimensional printing of transparent fused silica glass. Nature. 544(7650), 337–339.10.1038/nature22061Search in Google Scholar PubMed

Received: 2018-1-3
Published Online: 2018-3-28
Published in Print: 2018-3-26

© 2018 Walter de Gruyter GmbH, Berlin/Boston

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