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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.

Kasemo, 1998).

Successful characterization of biomolecular systems The experimental fact that the quartz crystal resona-

in their natural aqueous environment is the important tors are sensitive to viscoelastic properties of tested

objective of biosensoring. The quartz crystal microba- material (Voinova et al., 1997, 1999a,b Reed et al., 1990;

lance (QCM) which can operate in fluids, offers such Rodahl et al., 1997; Bandley et al., 1997 Lucklum and

straightforward possibility (Rodahl and Kasemo, 1996). Hauptmann, 1997; Johannsmann et al., 1992; Nwankwo

Polymer coated or biochemically modified quartz sur- and Durning, 1998), limits their application as a

face forms a ‘tolerant’ biological interface which is microbalance, i.e. for the precisious mass detection of

available for further mounting of biomolecular com- biological materials in liquid phase measurements. It

plexes exposed to water solution. Recently, the applica- seems crucial that, an adequate physical model is chosen

tion of QCM as a sensor element for the electronic nose for a quantitative interpretation of experimentally ob-

(DiNatale et al., 2000) and affinity immunosensor has served deviation from ideal Sauerbrey behavior in

been reported elsewhere (Sakti et al., 1999, 2000). biosensor’s QCM measurements. A vast literature on

Biosensor systems based on a QCM have become a QCM experiments and theory (see, for review, Hengerer

suitable tool for in situ measurements in biofluids, in et al., 1999; Rodahl and Kasemo, 1996; Voinova et al.,

particular, for on-line detection of immunological reac- 1999a,b) reveals a sharp interest to this topic. However,

tions (Hengerer et al., 1999; Sakti et al., 2000; Kößlinger the analog of Sauerbrey’s relation for systems with

et al., 1995). for surface bioelectrochemistry of redox complex rheology as to our knowledge has not been

enzymes (Buttry, 1991). adsorption of proteins, and reported yet.

adhesion of vesicles and living cell (Rodahl et al., 1997; 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

* Corresponding author. Tel.: /46-31-772-3115; fax: /46-31-41-

6884 present work */the effect of ‘missing mass’, predicts the

E-mail address: voinova@fy.chalmers.se (M.V. Voinova). reduction in liquid phase measurements of surface mass

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

836 M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841

Ms comparing with the ‘true’ mass M of the film: When a rigid film is replaced by Newtonian bulk liquid

of shear viscosity h , the QCM resonant frequency shift

hrv Gƒ

Ms M 1 2 2 ; M r1 h1 ; (1) is given by Kanazawa and Cordon’s expression (Kana-

r1 G?2 Gƒ2 zawa and Gordon, 1985):

In the section, ‘Comparison with experiments and sﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ

discussion’ we verify our theoretical results on QCM 1 rhv

Df : ; (3)

measurements on supported membranes (Fig. 1) pub- 2pmq 2

lished elsewhere (Rodahl et al., 1997; Johannsmann et

al., 1992; Höök et al., 1999; Keller and Kasemo, 1998). 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,

2. Theoretical considerations of the QCM surface mass 1999a,b) shows that for non-rigid deposits that is not

measurements. Resonant frequency and damping of QCM valid. We found that the viscous loss of energy in the

in complex fluids overlayers causes the deviation from Sauerbrey behavior

and results in non-trivial reduction in measured surface

Let us consider a QCM oscillating in a thickness- mass of the film, Ms /M (1/a ), where M is the ‘true’

shear mode and on one side covered by a soft adsorbed film mass and the viscous correction factor a depends

layer (the geometry is depicted schematically in Fig. 1). both on mechanical properties both of overlayer mate-

We describe the motion of the QCM as the forced rial and of aqueous solution h , r . This reduction in Df

vibration of a damped oscillator driven by periodic force has been predicted by us for the first, time for the special

(Rodahl and Kasemo, 1996; Voinova et al., 1999a,b). case of pure viscous layers (Voinova et al., 1997).

When mass is deposited onto the crystal surface, the Now consider a soft (viscoelastic) material which

resonance frequency changes, For a small amount of contacts the solution and effects the Df of the quartz

mass deposited onto the QCM surface, the shift of oscillator. The material is assumed to exhibit linear

resonance frequency Df is proportional to the surface viscoelasticity if both deformations and deformation

mass M of the deposit (Sauerbrey, 1959): rates are small (Panizza et al., 1996; Lekkerkerker,

M 1997). which holds in QCM dynamic measurements.

Df˜ f0 : (2) In the linear viscoelastic regime, there is proportionality

mq

between stored energy and strain and between strain

This equation known as Sauerbrey’s decrease of the rate and dissipated energy (Doi and Edwards, 1989).

resonant frequency (Sauerbrey, 1959), can only be used When the oscillatory shear stress of constant frequency

for thin films rigidly attached to the QCM surface. 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 /841 837

strain/stress relation can be written as following: When the viscosity of the top bulk liquid vanishes,

sik 2Guik : (4) viscoelastic corrections to the equivalent surface mass

appear only in higher order corrections in the film

Here sik , is the shear stress tensor, uik is the strain thickness:

tensor, G *(v )/G ?(v )/iGƒ(v ) is the complex fre-

hrv h2 rv2 G?

quency-dependent shear modulus of viscoelastic fluid; Df : 1 (6)

the real part G ?(v ) is a storage modulus while the 2pmq 3 G?2 Gƒ2

imaginary one G ƒ(v ) is a loss modulus, v is a circular Let us discuss now the physical origin of damping in

frequency. The most well known mathematical formula- biofluid’s QCM measurements. While a rigid film

tions of linear viscoelasticity are the Maxwell model of attached to the quartz surface shows no dissipation at

relaxation in highly viscous fluids and the Kelvin/Voight no-slip conditions, a damping due to a bulk viscous

model of viscoelastic solids. Below we consider an liquid (as was originally reported by Stockbridge, 1966

arbitrary viscoelastic material characterized by a shear and later revealed by Rodahl and Kasemo, 1996)

complex modulus G *(v ) and discuss the results for the depends on its density r and shear viscosity h :

special cases of supported membranes in the next sﬃﬃﬃﬃﬃﬃﬃﬃ

Section. 1 2rh

The shift of resonant frequency Df and dissipation DD : :

mq v

factor DD , due to the soft deposit on the quartz surface,

can be calculated as a real and imaginary parts of the In case of a layered viscous (viscoelastic) medium, DD

frequency shift of viscoelastically loaded quartz oscilla- is a complex functions of thickness, mass and viscoelas-

tor with no-slip boundary conditions (since in present tic properties of the material. We found that the

communication, we use the model developed by us dissipation factor of the quartz oscillator covered with

earlier, we will not repeat here the details of calculations soft overlayer in liquid phase measurements is:

and refer our readers to Voinova et al., 1997). Within 2

1 h2 h2 h1 vG?

this model, using the balance between dissipated and DD̃ : 2 (7)

stored energy in the system of the soft film exposure to pfmq d2 d2 G?2 Gƒ2

one side of the crystal and to another one of the From (Eq. (7)). viscous corrections due to the

solution, we found the following expression for Df: dissipation in liquid phase /h2d2 appear already in

h2 hrv the first order in the film thickness, while in a gas phase

Dftotal : 1 1 or vacuum the same thin overlayer will dissipate much

2pmq d2 2pmq

smaller energy /h3:

2 h2 2 Gƒ

1 ; (5) h3 r2 v3 Gƒ

r1 d2 G?2 Gƒ2 DD̃ : (8)

3pfmq G?2 Gƒ2

where the index ‘1’ corresponds to the thin soft overlayer

Comparing formulae (Eqs. (5) and (7)) and (Eqs. (6)

and index ‘2’ denotes liquid bulk phase, respectively,

and (8)), we conclude that viscoelastic effects become

d2 //2h2/r2v is a viscous length of bulk newtonian

more pronounced when the system operates in a bulk

liquid (Landau and Lifshitz, 1997). Note that in (Eq.

liquid phase and thus one can determine storage G? and

(5)) the viscous term appears in first order correction in

loss G ƒ moduli of soft deposits with higher accuracy

the film thickness h . Then the reduction (Eq. (1)) in

even for ultrathin films.

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 3. Comparison with experiments and discussion

frequency has a minimum when the viscoelastic ratio

X /G ?/G ƒ is equal to unity. (It should be pointed out, In this section, we verify our theoretical results (a

since in biofluid’s QCM measurements the thickness h ‘missing mass’ effect) by comparing the QCM response

of adlayer and its viscoelasticity G* can both vary predicted in the theory with experimental data on

during the adsorption process, one has to monitor. e.g. Langmuir /Blodgett /Kuhn films and supported mem-

h independently by other method while G ? and G ƒ can branes published elsewhere (Voinova et al., 1999a,b;

be derived from Df and DD measured simultaneously). Rodahl et al., 1997; Keller and Kasemo, 1998). In

In Figs. 2 and 3, we display the calculated resonant contrast with Langmuir /Blodgett films, water environ-

frequency and dissipation factor versus film thickness ment is essential for lipid bilayer membranes since it

and loss moduli for viscoelastic film in liquid environ- maintains the structure and fluidity of lipid membrane

ment. 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 hm /0.23 /106 cm is a monolayer thickness and

whose physical properties are similar to those of lipid Dfm /13 Hz is the frequency shift monitored for the

bilayer of the biological membranes (Sackmann, 1996). monolayer (Keller and Kasemo, 1998). Thus, the

Membranes-planar (Fig. 1a) or of closed type (vesicles; reduction in frequency response is df /51 Hz. This

Fig. 1c) form a soft biological interface, with peculiar deviation from Sauerbrey behavior and a large dissipa-

viscoelastic properties. In the supported membranes tion DD can be explained by ‘missing mass’ effect

technology, viscosity and elasticity of lipid bilayer play predicted in our theory. By setting for adlayer of

a key role in membrane assembling on surfaces (Sack- vesicles X /G? /G ƒ :/0.1 and G? :/105 dyne cm 2, we

mann, 1996). Strongly adhesive surfaces can give rise to find from (Eq. (5)) that df :/50 Hz and from (Eq. (7))

membrane failure and subsequent fusion of vesicles or to that. dD /3:/106 which is consistent with experi-

appearance of single bilayers with free edges. Alterna- mental data.

tively, adsorption of vesicles on moderately adhesive Since at the same time the lipid bilayer of thickness

substrates can result in morphological transformations 2hm demonstrated a pure viscous response (DD /0/

or formation of an intact vesicles monolayer (Höök et Dfm /2Dfm //26 Hz (Keller and Kasemo, 1998)), we

al., 1999; Keller and Kasemo, 1998; Sackmann, 1996). conclude that flat bilayers and intact dense packed

It was found by Keller and Kasemo, 1998, that the vesicles differ in mechanical properties: flat bilayer

adsorption of lipid vesicles (egg phosphatidylcholine behaves as 2D pure viscous fluid with negligible

(PC) small unilamellar vesicles of radius R /12.5 nm) resistance to shear in-plane stress (Helfrich, 1973) while

onto an oxidized gold surface is accompanied by a large adlayer built up from vesicles demonstrates a pro-

resonant frequency shift (Df//90 Hz) and a large nounced viscoelasticity. Apparent viscoelasticity of the

dissipation (DD /3 /106). Now let us estimate the latter can lie attributed to the assumption that dense

‘ideal’ pure mass response of this system (assuming that packed vesicles onto the oxidized gold forms a viscoe-

a bulk water contribution (Eq. (3)) has already been lastic ‘supramolecular fluid’ where individual vesicles

subtracted front Df). Sauerbrey’s formula (Eq. (2)) gives play role of the ‘supramolecules’ (Voinova, unpub-

Df /Dfmh1/hm //141 Hz where h1 / 2, R /2.5 /10 6 lished). (The formation of strong, weak and metastable

cm is the thickness of the adlayer r1 :/1 g cm 3 (PC liquids from colloidal ‘supramolecules’ has recently been

bilayer density at room temperatures (Petrov, 1999)), discussed in detail by Lekkerkerker (1997).)

M.V. Voinova et al. / Biosensors and Bioelectronics 17 (2002) 835 /841 839

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- who calculated and measured the frequencies of QCM

called onion phase, is shown schematically on Fig. 1d. resonances and the corresponding damping constants of

Panizza et al. (1996) provided a clear evidence that dense viscoelastic Langmuir /Blodgett /Kuhn films (sketched

packed multi-lamellar liposomes (onion phase) exhibit in Fig. 1b). The authors (Johannsmann et al., 1992)

viscoelastic properties. They have measured the elastic suggested to measure the equivalent mass on various

(storage) shear modulus G ?(v ) and a loss modulus G ƒ harmonics and then plot this characteristic versus the

(v ) of the onion phase by means of a low frequency square of the frequency to estimate the viscoelastic

rheometry. It should be mentioned that the QCM compliance J(v )/1/G * of the film and to study

measurements of shear elastic moduli of biomaterials whether viscous and elastic compliance arc frequency-

can provide essential information about their dynamical dependent. As an extension of their idea, we noticed that

behavior at high frequencies. in gas phase measurements, the frequency behavior of

It is useful to compare a response of QCM to the QCM characteristics in the linear viscoelasticity

viscoelastic fluid and viscoelastic solid films in gas phase

region, viz. Df(v ), can also test for the type of material-

(or vacuum). For the special case of the viscoelastic

either viscoelastic fluid or viscoelastic solid. From our

(Maxwell) fluid, we found that the resonant frequency

results (Eq. (9) and Eq. (10)) for DfM and Dfv , it follows

shift is a function on the film shear elasticity GM :

that we expect a straight line if Df(v ) is plotted versus

hrv h2 rv2 v2 for the case of a Maxwell fluid and a deviation from

DfM : 1 (9)

2pmq 3GM a straight line for other types of viscoelastic materials. In

the case of Maxwell fluid, the slope of the straight line

while the viscoelastic solid (Voight/Kelvin) film is a gives the equilibrium shear elastic modulus GM of the

function of both viscous h and elastic G moduli [9]: material (the viscosity h of the Maxwell film can then be

deduced directly from the measured values of DD if the

hrv h2 Gv2 r

Dfv : 1 : (10) film thickness and density are known).

2pmq 3(G2 h2 v2 )

The usage of QCM for biological arid biomedical

The results of our model for gas phase are in purposes brings out the problem of accounting for the

agreement with those of Johannsmann et al. (1992) 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

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