Biosensors and Bioelectronics 17 (2002) 835 /841

www.elsevier.com/locate/bios

‘Missing mass’ effect in biosensor’s QCM applications

M.V. Voinova *, M. Jonson, B. Kasemo
Department of Applied Physics, Chalmers University of Technology and Göteborg University, S-412 96 Göteborg, Sweden

Received 25 May 2001; received in revised form 11 January 2002; accepted 21 January 2002

Abstract

Nowadays, liquid applications of quartz crystal microbalance (QCM) opened a way for in situ studies of proteins, vesicles and
cells adsorbed from the solution onto the QCM surface. The sensitivity of QCM to the viscoelasticity of the adsorbed biomaterial
can be a reason of the experimentally observed deviation from a linear dependence of QCM resonant frequency on mass deposition
(the so-called Sauerbrey relation) and can limit its application for biosensoring. Presented here rigorous theoretical analysis explains
the deviation from ideal mass response of soft overlayers in the contact with liquid. The fundamental result of the theory is the
analog of Sauerbrey relation for layered viscous/viscoelastic medium which can be exploited for the correct physical interpretation
of QCM experimental data in biofluids, in particular for measurements of the ‘true’ surface mass of adsorbed biomolecular films.
We predict a new physical effect ‘missing mass’ of the sample in liquid phase measurements and compare the results given by our
theory with QCM measurements on supported membranes. # 2002 Elsevier Science B.V. All rights reserved.

Keywords: Acoustical biosensors; Quartz crystal microbalance; Supported membranes; Viscoelasticity

1. Introduction Fredriksson et al., 1998; Höök et al., 1999; Keller and

Successful characterization of biomolecular systems
in their natural aqueous environment is the important
objective of biosensoring. The quartz crystal microba-
lance (QCM) which can operate in fluids, offers such
straightforward possibility (Rodahl and Kasemo, 1996).
Polymer coated or biochemically modified quartz sur-
face forms a ‘tolerant’ biological interface which is
available for further mounting of biomolecular com-
plexes exposed to water solution. Recently, the applica-
tion of QCM as a sensor element for the electronic nose
(DiNatale et al., 2000) and affinity immunosensor has
been reported elsewhere (Sakti et al., 1999, 2000).
Biosensor systems based on a QCM have become a
suitable tool for in situ measurements in biofluids, in
particular, for on-line detection of immunological reac-
tions (Hengerer et al., 1999; Sakti et al., 2000; Kößlinger
et al., 1995). for surface bioelectrochemistry of redox
enzymes (Buttry, 1991). adsorption of proteins, and
adhesion of vesicles and living cell (Rodahl et al., 1997;
* Corresponding author. Tel.: /46-31-772-3115; fax: /46-31-41-
6884
E-mail address: voinova@fy.chalmers.se (M.V. Voinova).
0956-5663/02/$ - see front matter # 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 9 5 6 - 5 6 6 3 ( 0 2 ) 0 0 0 5 0 - 7
Kasemo, 1998).
The experimental fact that the quartz crystal resona-
tors are sensitive to viscoelastic properties of tested
material (Voinova et al., 1997, 1999a,b Reed et al., 1990;
Rodahl et al., 1997; Bandley et al., 1997 Lucklum and
Hauptmann, 1997; Johannsmann et al., 1992; Nwankwo
and Durning, 1998), limits their application as a
microbalance, i.e. for the precisious mass detection of
biological materials in liquid phase measurements. It
seems crucial that, an adequate physical model is chosen
for a quantitative interpretation of experimentally ob-
served deviation from ideal Sauerbrey behavior in
biosensor’s QCM measurements. A vast literature on
QCM experiments and theory (see, for review, Hengerer
et al., 1999; Rodahl and Kasemo, 1996; Voinova et al.,
1999a,b) reveals a sharp interest to this topic. However,
the analog of Sauerbrey’s relation for systems with
complex rheology as to our knowledge has not been
reported yet.
In this communication, we present rigorous formulae
for QCM response in liquids for soft deposits when the
Sauerbrey’s relation is not valid. The main result in the
present work */the effect of ‘missing mass’, predicts the
reduction in liquid phase measurements of surface mass
836 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841

Ms comparing with the ‘true’ mass M of the film:


hrv Gƒ
Ms  M 1 2 2 ; M r1 h1 ; (1)
r1 G?2  Gƒ2
In the section, ‘Comparison with experiments and
discussion’ we verify our theoretical results on QCM
measurements on supported membranes (Fig. 1) pub-
lished elsewhere (Rodahl et al., 1997; Johannsmann et
al., 1992; Höök et al., 1999; Keller and Kasemo, 1998).
2. Theoretical considerations of the QCM surface mass
measurements. Resonant frequency and damping of QCM
in complex fluids
Let us consider a QCM oscillating in a thickness-
shear mode and on one side covered by a soft adsorbed
layer (the geometry is depicted schematically in Fig. 1).
We describe the motion of the QCM as the forced
vibration of a damped oscillator driven by periodic force
(Rodahl and Kasemo, 1996; Voinova et al., 1999a,b).
When mass is deposited onto the crystal surface, the
resonance frequency changes, For a small amount of
mass deposited onto the QCM surface, the shift of
resonance frequency Df is proportional to the surface
mass M of the deposit (Sauerbrey, 1959):
M 1997). which holds in QCM dynamic measurements.
Df˜ f0 : (2)
mq
This equation known as Sauerbrey’s decrease of the
resonant frequency (Sauerbrey, 1959), can only be used
for thin films rigidly attached to the QCM surface.
When a rigid film is replaced by Newtonian bulk liquid
of shear viscosity h , the QCM resonant frequency shift
is given by Kanazawa and Cordon’s expression (Kana-
zawa and Gordon, 1985):
sffiffiffiffiffiffiffiffiffiffi
1 rhv
Df : ; (3)
2pmq 2
so the total response Df for the system of QCM rigid
film-immersed-in-water is a sum of film surface mass
(Eq. (2)) and viscous contribution of water (Eq. (3)).
However, our theoretical analysis ((Voinova et al., 1997,
1999a,b) shows that for non-rigid deposits that is not
valid. We found that the viscous loss of energy in the
overlayers causes the deviation from Sauerbrey behavior
and results in non-trivial reduction in measured surface
mass of the film, Ms /M (1/a ), where M is the ‘true’
film mass and the viscous correction factor a depends
both on mechanical properties both of overlayer mate-
rial and of aqueous solution h , r . This reduction in Df
has been predicted by us for the first, time for the special
case of pure viscous layers (Voinova et al., 1997).
Now consider a soft (viscoelastic) material which
contacts the solution and effects the Df of the quartz
oscillator. The material is assumed to exhibit linear
viscoelasticity if both deformations and deformation
rates are small (Panizza et al., 1996; Lekkerkerker,
In the linear viscoelastic regime, there is proportionality
between stored energy and strain and between strain
rate and dissipated energy (Doi and Edwards, 1989).
When the oscillatory shear stress of constant frequency
v is applied to the viscoelastic material, the general

Fig. 1. Sketch of different types of supported membranes. We also display the geometry of shear wave propagation in the system: k is the wave
vector, u denotes the in-plane displacement vector. (a) Flat lipid bilayer; (b) Langmuir /Blodgett film composed from rod-like organic molecules.
Adlayer formed by dense packed (c) small unilamellar lipid vesicles and (d) multilamellar liposomes (‘onion phase’, top view).
 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841
strain/stress relation can be written as following:
sik 2Guik : (4)
Here sik , is the shear stress tensor, uik is the strain
tensor, G *(v )/G ?(v )/iGƒ(v ) is the complex fre-
quency-dependent shear modulus of viscoelastic fluid;
the real part G ?(v ) is a storage modulus while the
imaginary one G ƒ(v ) is a loss modulus, v is a circular
frequency. The most well known mathematical formula-
tions of linear viscoelasticity are the Maxwell model of
relaxation in highly viscous fluids and the Kelvin/Voight
model of viscoelastic solids. Below we consider an
arbitrary viscoelastic material characterized by a shear
complex modulus G *(v ) and discuss the results for the
special cases of supported membranes in the next
Section.
The shift of resonant frequency Df and dissipation
factor DD , due to the soft deposit on the quartz surface,
can be calculated as a real and imaginary parts of the
frequency shift of viscoelastically loaded quartz oscilla-
tor with no-slip boundary conditions (since in present
communication, we use the model developed by us
earlier, we will not repeat here the details of calculations
and refer our readers to Voinova et al., 1997). Within
this model, using the balance between dissipated and
stored energy in the system of the soft film exposure to
one side of the crystal and to another one of the
solution, we found the following expression for Df:
h2 hrv
Dftotal :  1 1
2pmq d2 2pmq

  
2 h2 2 Gƒ
 1 ; (5)
r1 d2 G?2  Gƒ2
where the index ‘1’ corresponds to the thin soft overlayer
and index ‘2’ denotes liquid bulk phase, respectively,
d2 //2h2/r2v is a viscous length of bulk newtonian
liquid (Landau and Lifshitz, 1997). Note that in (Eq.
(5)) the viscous term appears in first order correction in
the film thickness h . Then the reduction (Eq. (1)) in
measured surface mass Ms in comparison with the ‘true’
mass M of the film, is due to the viscous loss of energy
of the quartz oscillator both in the soft overlays (/G ƒ)
and in the liquid bulk phase (h2r2). A simple analysis of
the expression (Eq. (5)) shows, that the resonance
frequency has a minimum when the viscoelastic ratio
X /G ?/G ƒ is equal to unity. (It should be pointed out,
since in biofluid’s QCM measurements the thickness h
of adlayer and its viscoelasticity G* can both vary
during the adsorption process, one has to monitor. e.g.
h independently by other method while G ? and G ƒ can
be derived from Df and DD measured simultaneously).
In Figs. 2 and 3, we display the calculated resonant
frequency and dissipation factor versus film thickness
and loss moduli for viscoelastic film in liquid environ-
ment.
837
When the viscosity of the top bulk liquid vanishes,
viscoelastic corrections to the equivalent surface mass
appear only in higher order corrections in the film
thickness:


hrv h2 rv2 G?
Df : 1 (6)
2pmq 3 G?2  Gƒ2
Let us discuss now the physical origin of damping in
biofluid’s QCM measurements. While a rigid film
attached to the quartz surface shows no dissipation at
no-slip conditions, a damping due to a bulk viscous
liquid (as was originally reported by Stockbridge, 1966
and later revealed by Rodahl and Kasemo, 1996)
depends on its density r and shear viscosity h :
sffiffiffiffiffiffiffiffi
1 2rh
DD : :
mq v
In case of a layered viscous (viscoelastic) medium, DD
is a complex functions of thickness, mass and viscoelas-
tic properties of the material. We found that the
dissipation factor of the quartz oscillator covered with
soft overlayer in liquid phase measurements is:

 2 
1 h2 h2 h1 vG?
DD̃ : 2 (7)
pfmq d2 d2 G?2  Gƒ2
From (Eq. (7)). viscous corrections due to the
dissipation in liquid phase /h2d2 appear already in
the first order in the film thickness, while in a gas phase
or vacuum the same thin overlayer will dissipate much
smaller energy /h3:
h3 r2 v3 Gƒ
DD̃ : (8)
3pfmq G?2  Gƒ2
Comparing formulae (Eqs. (5) and (7)) and (Eqs. (6)
and (8)), we conclude that viscoelastic effects become
more pronounced when the system operates in a bulk
liquid phase and thus one can determine storage G? and
loss G ƒ moduli of soft deposits with higher accuracy
even for ultrathin films.
3. Comparison with experiments and discussion
In this section, we verify our theoretical results (a
‘missing mass’ effect) by comparing the QCM response
predicted in the theory with experimental data on
Langmuir /Blodgett /Kuhn films and supported mem-
branes published elsewhere (Voinova et al., 1999a,b;
Rodahl et al., 1997; Keller and Kasemo, 1998). In
contrast with Langmuir /Blodgett films, water environ-
ment is essential for lipid bilayer membranes since it
maintains the structure and fluidity of lipid membrane
via a balance of hydrophobic and hydrophilic forces.
838 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841
Fig. 2. Calculated resonance frequency shift df of 3 MHz quartz crystal versus overlayer thickness and loss modulus G ?? at given elastic modulus
G ?/106 dyn cm 2; system operates in a bulk water solution (bulk water contribution was subtracted).
Supported membranes is a convenient model system
whose physical properties are similar to those of lipid
bilayer of the biological membranes (Sackmann, 1996).
Membranes-planar (Fig. 1a) or of closed type (vesicles;
Fig. 1c) form a soft biological interface, with peculiar
viscoelastic properties. In the supported membranes
technology, viscosity and elasticity of lipid bilayer play
a key role in membrane assembling on surfaces (Sack-
mann, 1996). Strongly adhesive surfaces can give rise to
membrane failure and subsequent fusion of vesicles or to
appearance of single bilayers with free edges. Alterna-
tively, adsorption of vesicles on moderately adhesive
substrates can result in morphological transformations
or formation of an intact vesicles monolayer (Höök et
al., 1999; Keller and Kasemo, 1998; Sackmann, 1996).
It was found by Keller and Kasemo, 1998, that the
adsorption of lipid vesicles (egg phosphatidylcholine
(PC) small unilamellar vesicles of radius R /12.5 nm)
onto an oxidized gold surface is accompanied by a large
resonant frequency shift (Df//90 Hz) and a large
dissipation (DD /3 /106). Now let us estimate the
‘ideal’ pure mass response of this system (assuming that
a bulk water contribution (Eq. (3)) has already been
subtracted front Df). Sauerbrey’s formula (Eq. (2)) gives
Df /Dfmh1/hm //141 Hz where h1 / 2, R /2.5 /10 6
cm is the thickness of the adlayer r1 :/1 g cm 3 (PC
bilayer density at room temperatures (Petrov, 1999)),
hm /0.23 /106 cm is a monolayer thickness and
Dfm /13 Hz is the frequency shift monitored for the
monolayer (Keller and Kasemo, 1998). Thus, the
reduction in frequency response is df /51 Hz. This
deviation from Sauerbrey behavior and a large dissipa-
tion DD can be explained by ‘missing mass’ effect
predicted in our theory. By setting for adlayer of
vesicles X /G? /G ƒ :/0.1 and G? :/105 dyne cm 2, we
find from (Eq. (5)) that df :/50 Hz and from (Eq. (7))
that. dD /3:/106 which is consistent with experi-
mental data.
Since at the same time the lipid bilayer of thickness
2hm demonstrated a pure viscous response (DD /0/
Dfm /2Dfm //26 Hz (Keller and Kasemo, 1998)), we
conclude that flat bilayers and intact dense packed
vesicles differ in mechanical properties: flat bilayer
behaves as 2D pure viscous fluid with negligible
resistance to shear in-plane stress (Helfrich, 1973) while
adlayer built up from vesicles demonstrates a pro-
nounced viscoelasticity. Apparent viscoelasticity of the
latter can lie attributed to the assumption that dense
packed vesicles onto the oxidized gold forms a viscoe-
lastic ‘supramolecular fluid’ where individual vesicles
play role of the ‘supramolecules’ (Voinova, unpub-
lished). (The formation of strong, weak and metastable
liquids from colloidal ‘supramolecules’ has recently been
discussed in detail by Lekkerkerker (1997).)
 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841
Fig. 3. Calculated damping of 3 MHz quartz crystal versus overlayer thickness and loss modulus G ?? for the same conditions as in Fig. 2.
Another example of supported membranes-the so-
called onion phase, is shown schematically on Fig. 1d.
Panizza et al. (1996) provided a clear evidence that dense
packed multi-lamellar liposomes (onion phase) exhibit
viscoelastic properties. They have measured the elastic
(storage) shear modulus G ?(v ) and a loss modulus G ƒ
(v ) of the onion phase by means of a low frequency
rheometry. It should be mentioned that the QCM
measurements of shear elastic moduli of biomaterials
can provide essential information about their dynamical
behavior at high frequencies.
It is useful to compare a response of QCM to
viscoelastic fluid and viscoelastic solid films in gas phase
(or vacuum). For the special case of the viscoelastic
(Maxwell) fluid, we found that the resonant frequency
shift is a function on the film shear elasticity GM :


hrv h2 rv2
DfM : 1 (9)
2pmq 3GM
while the viscoelastic solid (Voight/Kelvin) film is a
function of both viscous h and elastic G moduli [9]:
 
hrv h2 Gv2 r
Dfv : 1 : (10)
2pmq 3(G2  h2 v2 )
The results of our model for gas phase are in
agreement with those of Johannsmann et al. (1992)
839
who calculated and measured the frequencies of QCM
resonances and the corresponding damping constants of
viscoelastic Langmuir /Blodgett /Kuhn films (sketched
in Fig. 1b). The authors (Johannsmann et al., 1992)
suggested to measure the equivalent mass on various
harmonics and then plot this characteristic versus the
square of the frequency to estimate the viscoelastic
compliance J(v )/1/G * of the film and to study
whether viscous and elastic compliance arc frequency-
dependent. As an extension of their idea, we noticed that
in gas phase measurements, the frequency behavior of
the QCM characteristics in the linear viscoelasticity
region, viz. Df(v ), can also test for the type of material-
either viscoelastic fluid or viscoelastic solid. From our
results (Eq. (9) and Eq. (10)) for DfM and Dfv , it follows
that we expect a straight line if Df(v ) is plotted versus
v2 for the case of a Maxwell fluid and a deviation from
a straight line for other types of viscoelastic materials. In
the case of Maxwell fluid, the slope of the straight line
gives the equilibrium shear elastic modulus GM of the
material (the viscosity h of the Maxwell film can then be
deduced directly from the measured values of DD if the
film thickness and density are known).
The usage of QCM for biological arid biomedical
purposes brings out the problem of accounting for the
complex rheology of the biological interface, which is
840 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841

dominated by viscous effects. In some special cases or road to biosensoring, is QCM-immunosensor and QCM
for particular type of shear deformations, the linear as mechanical spectroscopy device assembled in arrays.
viscoelasticity of polymers can be treated within either
the Maxwell or the Voight/Kelvin schemes. The results
of the Yoight/Kelvin model can readily be applied to 4. List of symbols
quartz crystal acoustic measurements of adsorbed
proteins, which conserve their shape during adsorption D dissipation factor
and do not flow under shear deformation as well as to f0 fundamental resonant frequency of QCM
polymer films far from the glass transition region. The G* shear complex modulus
Maxwell fluid scheme is appropriate for polymer solu- G? storage modulus
tions that are pure liquids (at low shear rates) and Gƒ loss modulus
polymers in the amorphous state and in the vicinity of J* viscoelastic compliance
the polymer liquid-glass transition (Sperling, 1986). h overlayer thickness
Viscoelastic materials with more complex rheology mq (surface) mass of the quartz plate
(e.g. cells, membranes, liquid crystal polymers etc.) can M (surface) mass of the deposit
be described by a combination of these two basic R radius of lipid vesicles
viscoelastic schemes. They can be analyzed in a similar nik strain tensor
as we have done here way by substitution of the
corresponding expressions for the complex shear mod- Greek letters
ulus G * in the general results (Eqs. (5) /(8)). For a viscous correction factor
instance, the complex shear modulus: d viscous length
h shear viscosity coefficient
G1  ivh1 1
G1   : (11) r density
ivh1 G1 G2  ivh2 sik stress tensor
t relaxation time
well describes, a viscoelasticity of the lyotropic multi- v circular frequency
lamellar vesicles. [26] (‘onion phase’) sketched in Fig. 1d.
It is convenient to describe the frequency behavior of Indices
a complex viscous medium exhibiting a spectrum of / corresponding to the non-slip conditions
relaxation times in terms of the three-parameter model M monolayer
h* /h /(1/ivt)b of the complex viscosity suggested by M maxwell viscoelastic fluid
Reed et al. (1990). In this model, h is the viscosity of the V Voight/Kelvin viscoelastic solid
liquid; b is a characteristic exponent related to the s surface
distribution of relaxation times t. In the same manner,
we can introduce in our model a complex shear modulus
of the form:

G Acknowledgements
G
(1  i=wt)b
One of us (M.V. Voinova) is indebted to P. Haupt-
mann for his discussion of QCM immnnosensor’s
which is a generalization for the case of a relaxation time
applications, to E. Terentjev for his fruitful comments
distribution characterized by the exponent b . In parti-
to our model of supramolecular viscoelastic fluid and
cular, the Maxwell fluid corresponds to the value b/1.
C.-Y.D. Lu for the important correspondence and
Besides the experimental concern on viscoelastic
demonstration of their rheometric frequency-dependent
corrections of surface mass measurements, an important
measurements on onion multilamellar liposomes. This
problem for the application of the QCM technique to
work was supported financially by the Royal Swedish
biosensoring remains. How can the device recognize
Academy of Sciences (KVA) and the Swedish TFR.
what type of material is being probed except by
detection of an ‘anonymous’ deposited mass? We
suggest here a mechanical test of how to distinguish
Maxwell viscoelastic materials among others by measur- References
ing the QCM response on different frequencies. Another
Bandley, H.L., Hillman, A.R., Brown, M.J., Martin, S.J., 1997.
way is a direct biochemical modification of quartz
Viscoelastic characterization of etectroactive polymer films at the
surface for selective binding of tested biological mole- electrode/solution interface. Faraday Discuss. 107, 214 /228.
cules (Hengerer et al., 1999; Sakti et al., 1999; Sakti et al. Buttry, D.A., 1991. The quartz crystal microbalance as an situ tool in
2000; Kößlinger et al., 1995). Perhaps the successful electrochemistry. In: Abruña, II.D. (ed.), Electrochemical inter-
 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841
faces: modern technique for in-situ interface characterization,
VCII.
Doi, M., Edwards, S.F., 1989. The Theory of Polymer Dynamics.
Clarendon Press, Oxford.
Fredriksson, C., Kihlman, S., Rodahl, M., Kasemo, B., 1998. The
piezoelectric quartz crystal mass and dissipation sensor: a means of
studying cell adhesion. Langmuir 14, 248 /251.
Helfrich, W., 1973. Elastic properties of lipid bilayers: theory and
possible experiments. Z. Naturforsch. 28C, 693 /703.
Hengerer, A., Decker, J., Prohaska, E., Hauck, S., Kößlinger, C.,
Wolf, H., 1999. Quartz crystal microbalance (QCM) as a device for
the screening of phage libraries. Biosens. Bioelectron. 14, 139 /144.
Höök, F., Rodahl, M., Keller, C., Glasmästar, K., Fredriksson, C.,
Dahlqvist, P., Kasemo, B., 1999. The dissipative QCM-D techni-
que: interfacial phenomena, and sensor applications for proteins,
membranes, living cells and polymers. 1999 Joint Meeting EFTF-
IEEE IFCS, 966 /972.
Johannsmann, D., Mathauer, K., Wegner, C., Knoll, W., 1992.
Viscoelastic properties of thin films probed with a quartz-crystal
resonator. Phys. Rev. B46, 7808.
Kanazawa, K.K., Gordon, J.G., 1985. The oscillation frequency of a
quartz resonator in contact with a liquid. Anal. Chim. Acta 175,
99 /105.
Keller, C., Kasemo, B., 1998. Surface specific kinetics of lipid vesicle
adsorption measured with a quartz crystal microbalance. Biophys.
J. 75, 1397 /1402.
Kößlinger, C., Uttenthaler, F., Drost, S., Alberl, F., Wolf, H., Brink,
G., Stanglmair, A., Sackmann, E., 1995. Comparison of the QCM
and the SPR method for surface studies and immunological
applications. Sens. Actuators B. 24 /25, 107 /112.
Landau, L.D., Lifshitz, E.M. 1997. Course of Theoretical Physics,
three ed. vol. 6. Fluid mechanics.
Lekkerkerker, H.N.W., 1997. Strong, weak and metastable liquids.
Physica A. 244, 227 /237.
Lucklum, R., Hauptmann, P., 1997. Determination of polymer shear
modulus with quartz crystal resonators. Faraday Discuss. 107,
112 /202.
DiNatale, C., Paolesse, R., Macagnano, A., Mantini, A., D’Amico, A.,
Legin, A., Lvova, L., Rudnitskaya, A., Vlasov, Y., 2000. Electronic
nose and electronic tonque integration for improved classification
of clinical and food samples. Sens. Actuators B. 64 (1 /3), 15 /22.
Nwankwo, E., Durning, C.J., 1998. Mechanical response of thickness-
shear mode quartz-crystal resonators to linear viscoelastic fluids.
Sens. Actuators A. 64, 119 /124.
841
Panizza, P., Roux, D., Vuillaume, V., Lu, C.-Y., Cates, M.F., 1996.
Viscoelasticity of the onion phase. Langmuir 12, 248 /252.
Petrov, A.G., 1999. The Lyotropic State of Matter. Gordon and
Breach publication.
Reed, C.E., Kanazawa, K.K., Kaufman, J.H., 1990. Physical descrip-
tion of a viscoelastically loaded AT-cut quartz resonators. J. Appl.
Phys. 68, 1993.
Rodahl, M., Höök, F., Fredriksson, C., Keller, C.A., Krozer, A.,
Brzezinski, P., Voinova, M., Kasemo, B., 1997. Simultaneous
frequency arid dissipation factor QCM measurements of biomole-
cular adsorption and cell adhesion. Faraday Discuss. 107, 229 /
246.
Rodahl, M., Kasemo, B., 1996. On the measurement of thin liquid
overlayers with the quartz crystal microbalance. Sens. Actuators A.
54, 448 /462.
Sackmann, E., 1996. Supported membranes: scientific and practical
applications. Science 271, 43 /48.
Sakti, S.P., Röstler, S., Lucklum, R., Hauptmann, P., Bühling, F.,
Ansorge, S., 1999. Thick polystyrene-coated quartz crystal micro-
balance as a basis of a cost effective immunosensor. Sens.
Actuators 76, 98 /102.
Sakti, S.P., Hauptmann, P., Zimmermann, B., Bühling, F., Ansorge,
S., 2000. Disposable QCM-immunosensor for practical qualitative
and quantitative diagnosis. Eurosensors XIV. Gopenhagen, 475 /
476.
Sauerbrey, G., 1959. Verwendung von Schwingquarzen zur
Wägung Dünner Schichten und zur Mikrowägung. Z. Physik
155, 206 /222.
Sperling, L.H., 1986. Introduction to Physical Polymer Science. Wiley.
Stockbridge, C.D., 1966. Effects of gas pressure on quartz-crystal
microbalances. In: Vacuum Microbalance Techniques, vol. 5.
Plenum Press, pp. 147 /148.
Voinova, M.V., Jonson, M., Kasemo, B., 1997. Dynamics of viscous
amphiphilic films supported by elastic solid sub-strates. J. Phys.
Condens Matter 9, 7799 /7808.
Voinova, M.V., Rodahl, M., Jonson, M., Kasemo, B., 1999a.
Viscoelastic acoustic response of layered polymer films at fluid-
solid interfaces: continuum mechanics approach. Physica Scripta
59, 391 /396.
Voinova, M.V., Rodahl, M., Jonson, M., Kasemo, B., 1999b.
Viscoelastic acoustic response of layered polymer films at fluid-
solid interfaces: continuum mechanics approach. Physica Scripta
59, 391 /396.