Advertisement

pp 1-28 | Cite as

On the Use of the Quartz Crystal Microbalance for Whole-Cell-Based Biosensing

  • D. JohannsmannEmail author
Chapter
Part of the Bioanalytical Reviews book series

Abstract

The quartz crystal microbalance (QCM) can be used and has often been used to study the interactions of cells with man-made surfaces. The instrument as such is simple. For screening purposes, one can easily run numerous resonators in parallel. The main problem is the interpretation of experimental data. Living cells by their very nature are enormously complicated and the limited amount of information obtained from a QCM experiment therefore is not easily turned into a meaningful diagnostic statement. In the first part, the text elaborates on the technical background with special emphasis on quantitative modeling. While thorough quantitative modeling is difficult, simplified models (which have a limited scope and which provide limited answers) can be applied. The text provides checks on consistency and applicability. These simple models are the Sauerbrey film (only applicable to biofilms on torsional resonators), the semi-infinite viscoelastic medium, and the coupled resonance. In search for more depth of information, one may explore novel sensing dimensions, which include the variation of amplitude, exploitation of piezoelectric stiffening, the analysis of temporal variations, and temperature sweeps. Given the instrument’s simplicity, one may combine the QCM with imaging techniques, with optical spectroscopy (even in transmission), and with electrical impedance spectroscopy. The situation is open. Probing whole cells and cell layers with a QCM is already a robust and reliable technique. A better understanding of data interpretation will expand the scope of possible applications.

Keywords

Acoustic sensors Biocolloids Quartz crystal microbalance Whole-cell-based biosensing 

Notes

Acknowledgments

The author has enjoyed a long-standing collaboration with Ilya Reviakine on the application of the QCM to biosystems, which has influenced this chapter in many ways. Astrid Peschel provided the data shown in Fig. 8.

References

  1. 1.
    Janata J (2009) Principles of chemical sensors. Springer, BerlinGoogle Scholar
  2. 2.
    Rock F, Barsan N, Weimar U (2008) Electronic nose: current status and future trends. Chem Rev 108(2):705–725Google Scholar
  3. 3.
    Bousse L (1996) Whole cell biosensors. Sens Actuators B Chem 34(1–3):270–275Google Scholar
  4. 4.
    Gu MB, Mitchell RJ, Kim BC (2004) Whole-cell-based biosensors for environmental biomonitoring and application. Adv Biochem Eng Biotechnol 87:269–305Google Scholar
  5. 5.
    Pancrazio JJ, Whelan JP, Borkholder DA, Ma W, Stenger DA (1999) Development and application of cell-based biosensors. Ann Biomed Eng 27(6):697–711Google Scholar
  6. 6.
    Gryte DM, Ward MD, Hu WS (1993) Real-time measurement of anchorage-dependent cell-adhesion using a quartz crystal microbalance. Biotechnol Prog 9(1):105–108Google Scholar
  7. 7.
    Wegener J, Janshoff A, Galla HJ (1998) Cell adhesion monitoring using a quartz crystal microbalance: comparative analysis of different mammalian cell lines. Eur Biophys J Biophys Lett 28(1):26–37Google Scholar
  8. 8.
    Zhou T, Marx KA, Warren M, Schulze H, Braunhut SJ (2000) The quartz crystal microbalance as a continuous monitoring tool for the study of endothelial cell surface attachment and growth. Biotechnol Prog 16(2):268–277Google Scholar
  9. 9.
    Wegener J, Seebach J, Janshoff A, Galla HJ (2000) Analysis of the composite response of shear wave resonators to the attachment of mammalian cells. Biophys J 78(6):2821–2833Google Scholar
  10. 10.
    Redepenning J, Schlesinger TK, Mechalke EJ, Puleo DA, Bizios R (1993) Osteoblast attachment monitored with a quartz-crystal microbalance. Anal Chem 65(23):3378–3381Google Scholar
  11. 11.
    Wegener J, Janshoff A, Steinem C (2001) The quartz crystal microbalance as a novel means to study cell-substrate interactions in situ. Cell Biochem Biophys 34(1):121–151Google Scholar
  12. 12.
    Heitmann V, Reiss B, Wegener J (2007) The quartz crystal microbalance in cell biology: basics and applications. In: Steinem C, Janshoff A (eds) Piezoelectric sensors. Springer, BerlinGoogle Scholar
  13. 13.
    Saitakis M, Gizeli E (2012) Acoustic sensors as a biophysical tool for probing cell attachment and cell/surface interactions. Cell Mol Life Sci 69(3):357–371Google Scholar
  14. 14.
    Reviakine I, Johannsmann D, Richter RP (2011) Hearing what you cannot see and visualizing what you hear: interpreting quartz crystal microbalance data from solvated interfaces. Anal Chem 83(23):8838–8848Google Scholar
  15. 15.
    Beck R, Pittermann U, Weil KG (1988) Impedance analysis of quartz oscillators, contacted on one side with a liquid. Ber Bunsen Phys Chem 92(11):1363–1368Google Scholar
  16. 16.
    Böttcher A, Peschel A, Johannsmann D (2015) A backing plate for quartz crystal resonators improves the baseline stability and the baseline reproducibility. Meas Sci Technol 26:035303Google Scholar
  17. 17.
    Länge K, Rapp BE, Rapp M (2008) Surface acoustic wave biosensors: a review. Anal Bioanal Chem 391(5):1509–1519Google Scholar
  18. 18.
    Gaso Rocha MA, Jiménez Y, Laurent FA, Arnau A (2013) Love wave biosensors: a review. In: Rinken T (ed) State of the art in biosensors – general aspects. Intech, London.  https://doi.org/10.5772/53077. http://www.intechopen.com/books/state-of-the-art-in-biosensors-general-aspects/love-wave-biosensors-a-review. 17 Dec 2015CrossRefGoogle Scholar
  19. 19.
    March C, Garcia JV, Sanchez A, Arnau A, Jimenez Y, Garcia P, Manclus JJ, Montoya A (2015) High-frequency phase shift measurement greatly enhances the sensitivity of QCM immunosensors. Biosens Bioelectron 65:1–8Google Scholar
  20. 20.
    Zimmermann B, Lucklum R, Hauptmann P, Rabe J, Büttgenbach S (2001) Electrical characterisation of high-frequency thickness-shear-mode resonators by impedance analysis. Sens Actuators B Chem 76(1–3):47–57Google Scholar
  21. 21.
    Wingqvist G, Bjurstrom J, Liljeholm L, Yantchev V, Katardjiev I (2007) Shear mode AlN thin film electro-acoustic resonant sensor operation in viscous media. Sens Actuators B Chem 123(1):466–473Google Scholar
  22. 22.
    Sauerbrey G (1959) Verwendung von Schwingquarzen zur Wägung Dünner Schichten und zur Mikrowagung. Z Phys 155(2):206–222Google Scholar
  23. 23.
    Bruckenstein S, Shay M (1985) Experimental aspects of use of the quartz crystal microbalance in solution. Electrochim Acta 30(10):1295–1300Google Scholar
  24. 24.
    Nomura T, Okuhara M (1982) Frequency-shifts of piezoelectric quartz crystals immersed in organic liquids. Anal Chim Acta 142:281–284Google Scholar
  25. 25.
    Johannsmann D (1999) Viscoelastic analysis of organic thin films on quartz resonators. Macromol Chem Phys 200(3):501–516Google Scholar
  26. 26.
    Voinova MV, Jonson M, Kasemo B (2002) ‘Missing mass’ effect in biosensor’s QCM applications. Biosens Bioelectron 17(10):835–841Google Scholar
  27. 27.
    Tsionsky V, Daikhin L, Zilberman G, Gileadi E (1997) Response of the EQCM for electrostatic and specific adsorption on gold and silver electrodes. Faraday Discuss 107:337–350Google Scholar
  28. 28.
    Johannsmann D (2014) The quartz crystal microbalance in soft matter research: fundamentals and modeling. Springer, BerlinGoogle Scholar
  29. 29.
    Marx KA (2003) Quartz crystal microbalance: a useful tool for studying thin polymer films and complex biomolecular systems at the solution-surface interface. Biomacromolecules 4(5):1099–1120Google Scholar
  30. 30.
    Ward MD, Buttry DA (1990) In situ interfacial mass detection with piezoelectric transducers. Science 249(4972):1000–1007Google Scholar
  31. 31.
    Cooper MA (2003) Label-free screening of bio-molecular interactions. Anal Bioanal Chem 377(5):834–842Google Scholar
  32. 32.
    Homola J (2003) Present and future of surface plasmon resonance biosensors. Anal Bioanal Chem 377(3):528–539Google Scholar
  33. 33.
    Lucklum R, Hauptmann P (2006) Acoustic microsensors-the challenge behind microgravimetry. Anal Bioanal Chem 384(3):667–682Google Scholar
  34. 34.
    Steinem C, Janshoff A (2007) Piezoeletric sensors. Springer, HeidelbergGoogle Scholar
  35. 35.
    Rodahl M, Hook F, Fredriksson C, Keller CA, Krozer A, Brzezinski P, Voinova M, Kasemo B (1997) Simultaneous frequency and dissipation factor QCM measurements of biomolecular adsorption and cell adhesion. Faraday Discuss 107:229–246Google Scholar
  36. 36.
    Johannsmann D, Reviakine I, Rojas E, Gallego M (2008) Effect of sample heterogeneity on the interpretation of QCM(−D) data: comparison of combined quartz crystal microbalance/atomic force microscopy measurements with finite element method modeling. Anal Chem 80(23):8891–8899Google Scholar
  37. 37.
    Kanazawa KK, Gordon JG (1985) Frequency of a quartz microbalance in contact with liquid. Anal Chem 57(8):1770–1771Google Scholar
  38. 38.
    Borovikov AP (1976) Measurement of viscosity of media by means of shear vibration of plane piezoresonators. Instrum Exp Tech 19(1):223–224Google Scholar
  39. 39.
    Tabidze AA, Kazakov RK (1983) High-frequency ultrasonic unit for measuring the complex shear modulus of liquids. Meas Tech USSR 26(1):24–27Google Scholar
  40. 40.
    Stockbridge CD (1966) In: Beckum KH (ed) Vacuum microbalance techniques, vol 5. 4th edn. Plenum Press, New YorkGoogle Scholar
  41. 41.
    Glassford APM (1978) Response of a quartz crystal microbalance to a liquid deposit. J Vac Sci Technol 15(6):1836–1843Google Scholar
  42. 42.
    Mason WP (1948) Piezoelectric crystals and their applications to ultrasonics. Van Nostrand, PrincetonGoogle Scholar
  43. 43.
    Dybwad GL (1985) A sensitive new method for the determination of adhesive bonding between a particle and a substrate. J Appl Phys 58(7):2789–2790Google Scholar
  44. 44.
    Scholz M, Noack V, Pechlivanis I, Engelhardt M, Fricke B, Linstedt U, Brendel B, Schmieder K, Ermert H, Harders A (2005) Vibrography during tumor neurosurgery. J Ultrasound Med 24(7):985–992Google Scholar
  45. 45.
    Hemsel T, Stroop R, Uribe DO, Wallaschek J (2007) Resonant vibrating sensors for tactile tissue differentiation. J Sound Vib 308(3–5):441–446Google Scholar
  46. 46.
    Stroop R, Uribe DO, Martinez MO, Brokelmann M, Hemsel T, Wallaschek J (2008) Tactile tissue characterisation by piezoelectric systems. J Electroceram 20(3–4):237–241Google Scholar
  47. 47.
    Valtorta D, Mazza E (2006) Measurement of rheological properties of soft biological tissue with a novel torsional resonator device. Rheol Acta 45(5):677–692Google Scholar
  48. 48.
    Bressel A, Schultze JW, Khan W, Wolfaardt GM, Rohns HP, Irmscher R, Schoning MJ (2003) High resolution gravimetric, optical and electrochemical investigations of microbial biofilm formation in aqueous systems. Electrochim Acta 48(20–22):3363–3372Google Scholar
  49. 49.
    Tessier L, Patat F, Schmitt N, Lethiecq M, Frangin Y, Guilloteau D (1994) Significance of mass and viscous loads discrimination for an at-quartz blood-group immunosensor. Sens Actuators B Chem 19(1–3):698–703Google Scholar
  50. 50.
    Bandey HL, Cernosek RW, Lee WE, Ondrovic LE (2004) Blood rheological characterization using the thickness-shear mode resonator. Biosens Bioelectron 19(12):1657–1665Google Scholar
  51. 51.
    Muller L, Sinn S, Drechsel H, Ziegler C, Wendel HP, Northoff H, Gehring FK (2010) Investigation of prothrombin time in human whole-blood samples with a quartz crystal biosensor. Anal Chem 82(2):658–663Google Scholar
  52. 52.
    Plunkett MA, Wang ZH, Rutland MW, Johannsmann D (2003) Adsorption of pNIPAM layers on hydrophobic gold surfaces, measured in situ by QCM and SPR. Langmuir 19(17):6837–6844Google Scholar
  53. 53.
    Eggers F, Funck T (1987) Method for measurement of shear-wave impedance in the Mhz region for liquid samples of approximately 1 Ml. J Phys E Sci Instrum 20(5):523–530Google Scholar
  54. 54.
    Bücking W, Du B, Turshatov A, Konig AM, Reviakine I, Bode B, Johannsmann D (2007) Quartz crystal microbalance based on torsional piezoelectric resonators. Rev Sci Instrum 78(7):074903Google Scholar
  55. 55.
    Sievers P, Moss C, Schroeder U, Johannsmann D (2018) Use of torsional resonators to monitor electroactive biofilms. Biosens Bioelectron 110:225–232Google Scholar
  56. 56.
    Bode B (1984) Entwicklung eines Quarzviskometers für Messungen bei hohen Drücken. Clausthal University of Technology, Clausthal-ZellerfeldGoogle Scholar
  57. 57.
    Vaughan RD, O'Sullivan CK, Guilbault GG (2001) Development of a quartz crystal microbalance (QCM) immunosensor for the detection of Listeria monocytogenes. Enzym Microb Technol 29(10):635–638Google Scholar
  58. 58.
    Molino PJ, Hodson OA, Quinn JF, Wetherbee R (2008) The quartz crystal microbalance: a new tool for the investigation of the bioadhesion of diatoms to surfaces of differing surface energies. Langmuir 24(13):6730–6737Google Scholar
  59. 59.
    Poitras C, Fatisson J, Tufenkji N (2009) Real-time microgravimetric quantification of Cryptosporidium parvum in the presence of potential interferents. Water Res 43(10):2631–2638Google Scholar
  60. 60.
    Wang Y, Narain R, Liu Y (2014) Study of bacterial adhesion on different glycopolymer surfaces by quartz crystal microbalance with dissipation. Langmuir 30(25):7377–7387Google Scholar
  61. 61.
    Peschel A, Langhoff A, Johannsmann D (2015) Coupled resonances allow to study the aging of adhesive contacts between a QCM surface and single, micrometer-sized particles. Nanotechnology 26(48):484001–484009Google Scholar
  62. 62.
    Johannsmann D (2016) Towards vibrational spectroscopy on surface-attached colloids performed with a quartz crystal microbalance. Sens Biosens Res 11:86–93Google Scholar
  63. 63.
    Olsson ALJ, van der Mei HC, Johannsmann D, Busscher HJ, Sharma PK (2012) Probing colloid-substratum contact stiffness by acoustic sensing in a liquid phase. Anal Chem 84(10):4504–4512Google Scholar
  64. 64.
    Olsson ALJ, Arun N, Kanger JS, Busscher HJ, Ivanov IE, Camesano TA, Chen Y, Johannsmann D, van der Mei HC, Sharma PK (2012) The influence of ionic strength on the adhesive bond stiffness of oral streptococci possessing different surface appendages as probed using AFM and QCM-D. Soft Matter 8(38):9870–9876Google Scholar
  65. 65.
    Cooper MA, Dultsev FN, Minson T, Ostanin VP, Abell C, Klenerman D (2001) Direct and sensitive detection of a human virus by rupture event scanning. Nat Biotechnol 19(9):833–837Google Scholar
  66. 66.
    Edvardsson M, Rodahl M, Hook F (2006) Investigation of binding event perturbations caused by elevated QCM-D oscillation amplitude. Analyst 131(7):822–828Google Scholar
  67. 67.
    Heitmann V, Wegener J (2007) Monitoring cell adhesion by piezoresonators: impact of increasing oscillation amplitudes. Anal Chem 79(9):3392–3400Google Scholar
  68. 68.
    Nosek J (1999) Drive level dependence of the resonant frequency in BAW quartz resonators and his modeling. IEEE Trans Ultrason Ferroelectr Freq Control 46(4):823–829Google Scholar
  69. 69.
  70. 70.
    Berg S, Johannsmann D (2003) High speed microtribology with quartz crystal resonators. Phys Rev Lett 91(14):145505Google Scholar
  71. 71.
    Mindlin RD, Deresiewicz H (1953) Elastic spheres in contact under varying oblique forces. Trans ASME J Appl Mech 20(3):327–344Google Scholar
  72. 72.
    Leopoldes J, Conrad G, Jia X (2013) Onset of sliding in amorphous films triggered by high-frequency oscillatory shear. Phys Rev Lett 110(24):248301Google Scholar
  73. 73.
    Hanke S, Petri J, Johannsmann D (2013) Partial slip in mesoscale contacts: dependence on contact size. Phys Rev E 88(3):032408Google Scholar
  74. 74.
    Vlachová J, König R, Johannsmann D (2015) Stiffness of sphere–plate contacts at MHz frequencies: dependence on normal load, oscillation amplitude, and ambient medium. Beilstein J Nanotechnol 6:845–856Google Scholar
  75. 75.
    Borovsky B, Booth A, Manlove E (2007) Observation of microslip dynamics at high-speed microcontacts. Appl Phys Lett 91(11):114101Google Scholar
  76. 76.
    Batchelor GK (1967) An introduction to fluid dynamics. Cambridge University Press, Clausthal-ZellerfeldGoogle Scholar
  77. 77.
    Riley N (2001) Steady streaming. Annu Rev Fluid Mech 33:43–65Google Scholar
  78. 78.
    Riley N (1998) Acoustic streaming. Theor Comput Fluid Dyn 10(1–4):349–356Google Scholar
  79. 79.
    Friend J, Yeo LY (2011). Rev Mod Phys 83:647Google Scholar
  80. 80.
    König R, Langhoff A, Johannsmann D (2014) Steady flows above a quartz crystal resonator driven at elevated amplitude. Phys Rev E 89(4):043016Google Scholar
  81. 81.
    Ghosh SK, Ostanin VP, Johnson CL, Lowe CR, Seshia AA (2011) Probing biomolecular interaction forces using an anharmonic acoustic technique for selective detection of bacterial spores. Biosens Bioelectron 29(1):145–150Google Scholar
  82. 82.
    Salazar-Banda GR, Felicetti MA, Goncalves JAS, Coury JR, Aguiar ML (2007) Determination of the adhesion force between particles and a flat surface, using the centrifuge technique. Powder Technol 173(2):107–117Google Scholar
  83. 83.
    Rodahl M, Hook F, Krozer A, Brzezinski P, Kasemo B (1995) Quartz-crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments. Rev Sci Instrum 66(7):3924–3930Google Scholar
  84. 84.
    Driscoll MM, Healey DJ (1971) Voltage-controlled crystal oscillators. IEEE Trans Electron Dev ED18(8):528Google Scholar
  85. 85.
    Shana ZA, Zong H, Josse F, Jeutter DC (1994) Analysis of electrical equivalent-circuit of quartz-crystal resonator loaded with viscous conductive liquids. J Electroanal Chem 379(1–2):21–33Google Scholar
  86. 86.
    Shana ZA, Josse F (1994) Quartz-crystal resonators as sensors in liquids using the acoustoelectric effect. Anal Chem 66(13):1955–1964Google Scholar
  87. 87.
    Zhang C, Vetelino JF (2003) Chemical sensors based on electrically sensitive quartz resonators. Sens Actuators B Chem 91(1–3):320–325Google Scholar
  88. 88.
    Peschel A, Boettcher A, Langhoff A, Johannsmann D (2016) Probing the electrical impedance of thin films on a quartz crystal microbalance (QCM), making use of frequency shifts and piezoelectric stiffening. Rev Sci Instrum 87:115002Google Scholar
  89. 89.
    Vidarsson H, Hyllner J, Sartipy P (2010) Differentiation of human embryonic stem cells to cardiomyocytes for in vitro and in vivo applications. Stem Cell Rev Rep 6(1):108–120Google Scholar
  90. 90.
    Pax M, Rieger J, Eibl RH, Thielemann C, Johannsmann D (2005) Measurements of fast fluctuations of viscoelastic properties with the quartz crystal microbalance. Analyst 130(11):1474–1477Google Scholar
  91. 91.
    Tymchenko N, Kunze A, Dahlenborg K, Svedhem S, Steel D (2013) Acoustical sensing of cardiomyocyte cluster beating. Biochem Biophys Res Commun 435(4):520–525Google Scholar
  92. 92.
    Sapper A, Wegener J, Janshoff A (2006) Cell motility probed by noise analysis of thickness shear mode resonators. Anal Chem 78(14):5184–5191Google Scholar
  93. 93.
    Gutman J, Walker SL, Freger V, Herzberg M (2013) Bacterial attachment and viscoelasticity: physicochemical and motility effects analyzed using quartz crystal microbalance with dissipation (QCM-D). Environ Sci Technol 47(1):398–404Google Scholar
  94. 94.
    Wargenau A, Tufenkji N (2014) Direct detection of the gel-fluid phase transition of a single supported phospholipid bilayer using quartz crystal microbalance with dissipation monitoring. Anal Chem 86(16):8017–8020Google Scholar
  95. 95.
    Losada-Perez P, Khorshid M, Yongabi D, Wagner P (2015) Effect of cholesterol on the phase behavior of solid-supported lipid vesicle layers. J Phys Chem B 119(15):4985–4992Google Scholar
  96. 96.
    Domack A, Prucker O, Ruhe J, Johannsmann D (1997) Swelling of a polymer brush probed with a quartz crystal resonator. Phys Rev E 56(1):680–689Google Scholar
  97. 97.
    Edvardsson M, Svedhem S, Wang G, Richter R, Rodahl M, Kasemo B (2009) QCM-D and reflectometry instrument: applications to supported lipid structures and their biomolecular interactions. Anal Chem 81(1):349–361Google Scholar
  98. 98.
    Laschitsch A, Menges B, Johannsmann D (2000) Simultaneous determination of optical and acoustic thicknesses of protein layers using surface plasmon resonance spectroscopy and quartz crystal microweighing. Appl Phys Lett 77(14):2252–2254Google Scholar
  99. 99.
    Babauta JT, Beasley CA, Beyenal H (2014) Investigation of electron transfer by geobacter sulfurreducens biofilms by using an electrochemical quartz crystal microbalance. ChemElectroChem 1(11):2007–2016Google Scholar
  100. 100.
    Liu Y, Berna A, Climent V, Miguel Feliu J (2014) Real-time monitoring of electrochemically active biofilm developing behavior on bioanode by using EQCM and ATR/FTIR. Sens Actuators B Chem 209:781–789Google Scholar
  101. 101.
    Rabaey K, Angenent L, Schroder U (eds) (2009) Bioelectrochemical systems: from extracellular electron transfer to biotechnological application. IWA Publishing, LondonGoogle Scholar
  102. 102.
    ITO coated resonator crystals are available from microvacuum: http://www.microvacuum.com/
  103. 103.
    Giaever I, Keese CR (1991) Micromotion of mammalian-cells measured electrically. Proc Natl Acad Sci U S A 88(17):7896–7900Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institute of Physical ChemistryClausthal Universtity of TechnologyClausthal-ZellerfeldGermany

Personalised recommendations