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Is the time-dependent behaviour of the aortic valve intrinsically quasi-linear? Afshin Anssari-Benam 1,* 1 School of Engineering, University of Portsmouth, Anglesea Road, Portsmouth PO1 3DJ United Kingdom * Address for correspondence: Afshin Anssari-Benam, School of Engineering, University of Portsmouth, Anglesea Road, Portsmouth PO1 3DJ United Kingdom Tel: +44 (0)23 9284 2187 E-mail: [email protected]

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Page 1: The hereditary integral constitutive equation for … · Web viewThese indications put forward a more fundamental question: Is the time-dependent behaviour of the aortic valve intrinsically

Is the time-dependent behaviour of the aortic valve intrinsically quasi-

linear?

Afshin Anssari-Benam1,*

1 School of Engineering, University of Portsmouth, Anglesea Road, Portsmouth PO1 3DJ United Kingdom

* Address for correspondence: Afshin Anssari-Benam, School of Engineering, University of Portsmouth, Anglesea Road, Portsmouth PO1 3DJ United Kingdom

Tel: +44 (0)23 9284 2187 E-mail: [email protected]

Word count (Introduction to conclusion): 2919

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Abstract

The widely popular quasi-linear viscoelasticity (QLV) theory has been employed

extensively in the literature for characterising the time-dependent behaviour of many

biological tissues, including the aortic valve (AV). However, in contrast to other

tissues, application of QLV to AV data has been met with varying success, with studies

reporting discrepancies in the values of the associated quantified parameters for data

collected from different time-scales in experiments. Furthermore, some studies

investigating the stress-relaxation phenomenon in valvular tissues have suggested

discrete relaxation spectra, as an alternative to the continuous spectrum proposed by

the QLV. These indications put forward a more fundamental question: Is the time-

dependent behaviour of the aortic valve intrinsically quasi-linear? In other words, can

the inherent characteristics of the tissue that govern its biomechanical behaviour

facilitate a quasi-linear time-dependent behaviour? This paper attempts to address

these questions by presenting a mathematical analysis to derive the expressions for the

stress-relaxation G(t) and creep J(t) functions for the AV tissue within the QLV theory.

The principal inherent characteristic of the tissue is incorporated into the QLV

formulation in the form of the well-established gradual fibre recruitment model, and

the corresponding expressions for G(t) and J(t) are derived. The outcomes indicate that

the resulting stress-relaxation and creep functions do not appear to voluntarily follow

the observed experimental trends reported in previous studies. These results highlight

that the time-dependent behaviour of the AV may not be quasi-linear, and more

suitable theoretical criteria and models may be required to explain the phenomenon

based on tissue’s microstructure, and for more accurate estimation of the associated

material parameters. In general, these results may further be applicable to other planar

soft tissues of the same class, i.e. with the same representation for fibre recruitment

mechanism and discrete time-dependent spectra.

Keywords: time-dependent behaviour, aortic valve, quasi-linear viscoelasticity (QLV),

stress relaxation, creep, microstructure.

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Is the time-dependent behaviour of the aortic valve intrinsically quasi-

linear?

1. Introduction

In a broad classification, the biomechanical behaviour of soft tissues can be

considered in two distinct categories; quasi-static and time-dependent behaviour.

While quasi-static loading may replicate the main functional mode of many connective

tissues more effectively, characterising time-dependent behaviour is also important,

particularly in tissues that undergo long-term repetitive dynamic loading in vivo, such

as the aortic valve (AV). Structural durability of the AV is generally thought to be

linked to its ability to dampen (relax) the transient stresses created by the sudden

change in pressure gradient at systole during each cardiac cycle (Sacks 2001; Robinson

et al. 2009). Moreover, structural failure of substitute bioprosthetic valves has been

hypothesised to be a consequence of their reduced stress-relaxation characteristics

compared to the native tissue (Sacks 2001).

Time-dependent spectra cannot be measured directly through experimentation alone

(Baumgaertel and Winter 1992), and models are subsequently required to compliment

the estimation of time-dependent parameters. With recent studies underlining the

contribution of the AV microstructure to the bulk tissue quasi-static behaviour (Billiar

and Sacks 2000; Sacks 2003; Stella and Sacks 2007), it is appropriate to model the

time-dependent behaviour of the valve using theoretical criteria and models that are

intrinsic to the tissue microstructure, and to the underlying microstructural mechanisms

facilitating such characteristics. This approach would lead to more accurate and robust

characterisation of AV time-dependent behaviour, with structurally meaningful

material parameters. Such data can subsequently contribute towards gaining better

insights into the in vivo biomechanical function of the valve.

Perhaps the most celebrated microstructural based models applied in studies of tissue

biomechanics were pioneered by Lanir (1979, 1983), addressing structure-function

relationships in fibrous connective tissues under quasi-static loading. These models

were based on the gradual recruitment of collagen fibres as load is applied at the tissue

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level, and have been validated with experimental observations. Following the same

approach, similar models have been proposed to characterise the quasi-static

mechanical behaviour of AV tissue (Sacks 2003). However, microstructural based

models and relationships have been considerably less developed and addressed for

describing the time-dependent behaviour of the AV. Indeed, with studies reporting a

‘no-creep’ behaviour for the tissue under equi-biaxial loading conditions (Stella et al.

2007), and exhibiting both the stress-relaxation and creep phenomena when loaded

uniaxially (Anssari-Benam et al. 2011a), the structural mechanisms and origins of the

AV time-dependent behaviour are yet to be fully understood, and have been a subject

of active research (Stella et al. 2007; Sacks et al. 2009).

Nonetheless, a commonly used criterion in characterising time-dependent behaviour

in soft tissues is the well-established Quasi-Linear Viscoelasticity (QLV) theory,

successfully applied to a wide range of tissues such as ligament (Woo et al. 1993),

tendon (Sarver et al. 2003), and cardiac muscle (Pinto and Patitucci 1980). Under the

assumption that the viscoelastic behaviour of the subject tissue is quasi-linear, QLV

provides a powerful mathematical tool for estimating the time-dependent parameters of

tissues, assuming a continuous relaxation spectrum (Rajagopal and Wineman 2008).

However, experimental procedures to ensure an accurate characterisation of the time-

dependent behaviour of biological tissues by the QLV theory are not straight forward

in practice. For example, for QLV to accurately characterise the experimental

relaxation data, an ideal instantaneous step displacement should be applied in the

experiments, to ensure a complete separation of the elastic and time-dependent

responses (Doehring et al. 2004). However, instantaneous steps are experimentally

difficult to implement, and generally the loading phase is limited to a finite-time ramp,

during the application of which the sample begins to relax. While this may lead to

small errors in estimating the relaxation parameters in unidirectional tissues such as

tendons, in which the population of fibres are already mainly aligned in the principal

loading direction, planar tissues may deviate more notably from the assumption of

complete separation of the elastic and time-dependent responses, since fibre re-

alignment occurs during the application of displacement to the tissue.

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For a planar tissue such as the AV, application of QLV has been met with varying

success, with studies reporting discrepancies in the time-dependent parameters

calculated for different experimental time-scales, as a consequence of the relatively

poor fit of the model to the experimental data (Sauren et al. 1983; Rousseau et al.

1983; Sauren and Rousseau 1983). In a recent study it was shown that the time-

dependent behaviour of the AV, similar to other valvular tissues (Liao et al. 2007),

may be better characterised using discrete spectra than the continuous spectrum offered

by the QLV model (Anssari-Benam et al. 2011a). Such data indicate that the AV tissue

may not fundamentally facilitate quasi-linear viscoelastic behaviour as an intrinsic

feature inherent to the valve’s time-dependent characteristics, and put forward the

important question: Is the time-dependent behaviour of the aortic valve intrinsically

quasi-linear? From a biomechanical perspective, the answer to this question may prove

valuable, as it may further assist a better understanding of the AV time-dependent

behaviour, and highlight the need for development of alternative approaches in order to

obtain more accurate estimations of the associated material parameters.

One analytical way to address this question may be to incorporate the inherent

characteristics of the tissue which govern its biomechanical behaviour into the QLV

formulation, account for the associated mathematics, and analytically derive the

resulting expressions for stress-relaxation and creep functions. The ensuing functions

can then be compared against the experimental data, to investigate and verify the

extent to which they match the observed modes in stress-relaxation and creep tests.

This, in effect, is the crux of the current study. The principal inherent characteristic of

the AV tissue, which has been shown to govern its biomechanical behaviour, is a

feature that is known in the literature as ‘gradual fibre recruitment’ (Billiar and Sacks

2000; Sacks 2003). In the following, the associated well-established gradual fibre

recruitment model is incorporated into the QLV, accounting for the elastic response

in the model. The corresponding stress-relaxation and creep

functions are then mathematically derived, and are compared with the experimental

results previously reported in the literature.

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2. QLV criterion

The hereditary integral constitutive equation for viscoelastic response, under the

assumption that the response to a multi-step strain history can be approximated by a

linear combination of the responses to single strain histories, is (Pipkin and

Rogers 1968; Rajagopal and Wineman):

(1)

where denotes a differential with respect to the first argument of .

With a strain history such that:

for

the stress in equation (1) can be expressed as (Pipkin and Rogers 1968; Rajagopal and

Wineman 2008):

(2)

The QLV model assumes that can be expressed by (Fung 1993):

(3)

where is a stress-relaxation function and is the immediate elastic response

(Fung 1993). It can thus be observed that QLV is a special case of the nonlinear

viscoelastic model in equation (1).

By substituting (3) into (2):

(4)

or to simplify the notation for :

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(5)

The elastic response of the AV tissue has been formulated based on a

stochastic representation of the process of gradual recruitment of the fibres under

deformation by Sacks (2003), based on the general theoretical criterion developed by

Lanir (1979, 1983). In the following, this relationship is employed as the elastic

response of the AV tissue in equation (5), as a representation of the tissue

microstructure. It is then investigated that if the experimentally observed exponential

relaxation and creep modes reported previously in the literature can be mathematically

derived within the QLV criterion.

3. Application to stress-relaxation

For tissues consisting of distributed arrays of wavy collagen fibres, such as the AV,

fibres are generally modelled not to contribute to the load bearing capacity of the tissue

until they are fully straightened. Straightening occurs gradually across the population

of fibres in the tissue continuum, when load or displacement is applied at the tissue

level. Stochastic approaches have been widely popular for modelling this gradual

recruitment of fibres, with a statistical distribution function representing the stretch at

which each fibre becomes uncrimped. Based on these approaches, different distribution

functions including gamma (Sacks 2003; Bischoff 2006), beta (Raz and Lanir 2009)

and Weibull (Hurschler et al. 1997) have been used to model fibre recruitment. Here, a

gamma distribution function of the following form is utilised, consistent with other

related studies of AV biomechanics (Sacks 2003):

(6)

where is the straightening fibre strain. The physical interpretation of is a

straightening strain density distribution function, representing the fraction of fibre fully

straightened at fibre’s current strain (Sacks 2003; Raz and Lanir 2009). is

the cumulative distribution function, which gives the density of the volume fraction of

the fibre population that is straight at (Sacks 2003).

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A fibre can support load only when fully uncrimped, at which point it is considered

to be linearly elastic (Bischoff 2006; Raz and Lanir 2009). Thus, the fibre stress is

related to the fibre true strain, , by:

(7)

where is the elastic modulus. By definition, represents the strain in a fibre with

respect to its uncrimped length. The relationship between , and is (Raz and

Lanir 2009):

(8)

Therefore, the overall Lagrangian elastic stress of the tissue is:

(9)

where is the fibre volume fraction (Aspden 1986). Substituting equation (6) into (9):

(10)

Now, substituting (10) into (5), and assuming that both stress and strain at 0 are equal

to zero, i.e. , , and strain rate is constant upon applying the ramp, i.e.

, one will arrive at:

(11)

From equation (10):

(12)

Thus by substituting (12) into (11):

(13)

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Under the assumption of linear elasticity of the fibre, one can consider that the fibre

straightening strain, , is independent of time. The argument in the parenthesis in

equation (13) will therefore become a constant, leading to:

(14)

In a stress-relaxation test, the left side of equation (14) describes the stress history of

the tissue specimen during relaxation. It has been experimentally observed that the

relaxation modes of the AV tissue typically follow a Maxwellian exponential decay

trend (Stella et al. 2007; Anssari-Benam et al. 2011a), generally represented by Prony

series of the form , where i is the number of Maxwell elements, is

the amplitude of relaxation, and is the characteristic relaxation time (Anssari-Benam

et al. 2011a). Thus, the integral on the right hand side of equation (14) should

mathematically result in the same exponential decay terms. However, the only

mathematically apparent exponential-dependence in equation (14) stems from strain

variables and , and not the time variable t. This demonstrates that is not

automatically constrained by equation (14) to result in an exponential decay function

of t. Thus, not only it contradicts the quasi-linearity assumption by which the stress-

relaxation is independent of the strain, but also introduces arbitration for the choice of

G(t). Therefore, the resulting stress-relaxation function G(t) by the QLV principle does

not mathematically correlate with the relaxation modes incurred in experiments, and

does not conclude a Maxwell type relaxation. This implies that the response of the

tissue may not necessarily be quasi-linear, so that it may not be substituted by

the specific quasi-linear relationship in equation (3). Two representative

stress-relaxation responses reported in Anssari-Benam et al. (2011a) are given in

Figure 1 to highlight examples of discrete Maxwell-type relaxation modes observed in

the experiments.

4. Application to creep

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Corresponding to the stress-relaxation function is a creep function . Under

the assumption of quasi-linear time-dependent behaviour, and are related by

(Rajagopal and Wineman 2008):

=

(15)

By definition, the stress-relaxation at t=0 is . Based on this, one can note

from equation (15) that: . As such, and in light of equation

(15), equation (5) will take the following form when describing creep (Rajagopal and

Wineman 2008):

(16)

Equation (16) can be rearranged by the chain rule as:

(17)

The term can be calculated from equations (10), and will be a constant

according to equation (8), shown hereafter as . Additionally, similar to the

relaxation case, strain rate is assumed constant upon applying the creep loading

protocol, i.e. . Equation (17) can now be re-written as:

(18)

Substituting for in the above equation using equation (8):

(19)

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Under the assumption of linear elasticity of a fibre (equation (7)), one can consider

to be independent of time. Additionally, is an intrinsic property of the subject tissue,

primarily determined by the waviness, initial crimp period and the cross-links of the

fibres. Therefore, is also independent of time. Thus, equation (19) can be rearranged

as:

(20)

where stands for the multiplication of all the constants in (19). The creep function

can then be calculated by:

(21)

The implications of equation (21) are interesting. The right hand-side of the equation

is constant, and independent of time, noting that the creep stress is kept

constant during a creep test. Therefore, equation (21) underlines that the creep function

derived from the relationship furnished by the QLV (equation (15)) calculates a creep

response which remains constant over time. This is inconsistent with the principles of

viscoelasticity and time-dependent behaviour of soft tissues, as well as in contrast to

the reported experimental data. For example, the results reported by Anssari-Benam et

al. (2011a) indicate clear time dependence in the creep response of AV specimens,

both in values and creep stages. The primary creep was reported to be an exponential

function of time, while the secondary creep was observed to be characterised by a

linear relationship of creep rate and time t in the form: , where is

the creep strain in time t. Two representative creep responses reported in that study are

shown in Figure 2. This analysis implies that the relationship between G(t) and J(t) for

the AV tissue could not be characterised under the assumption of quasi-linear time-

dependent behaviour, stated by equation (15).

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5. Concluding remarks

This paper presented a mathematical analysis investigating the assumption of quasi-

linear viscoelasticity in AV time-dependent behaviour. The principal inherent

characteristic of the tissue, namely the gradual fibre recruitment, which primarily

governs its biomechanical behaviour, was incorporated into the QLV model

formulation and the corresponding stress-relaxation and creep functions were derived.

These functions were then compared with the relaxation and creep modes observed in

experiments reported previously in the literature through the works of Stella et al.

(2007) and Anssari-Benam et al. (2011a). The aim of this analysis was not to describe

or model the underlying mechanisms involved in uniaixal and planar stress-relaxation

and creep behaviour of the valve. Rather, this paper attempted to investigate the quasi-

linearity of the AV time-dependent behaviour.

Time-dependent behaviour of soft tissues has proved to be very complex, and

formulating models based on tissue structure that would result in the observed

experimental behaviour remains a challenging task. In a recent study a rheological

model was developed to account for the rate-dependency of the mechanical behaviour

of the AV specimens under tensile deformation (Anssari-Benam et al. 2011b).

However, such models may not elaborate the underlying microstructural mechanisms

that contribute to the overall time-dependent behaviour of the bulk tissue, and therefore

may not be suitable for general application to different tissues and under different

loading conditions. Studies investigating the micromechanics of connective tissues

such as tendons have reported fibre sliding during relaxation experiments, suggesting

that it may be a possible mechanism to contribute to the overall stress-relaxation of the

tissue (Screen 2008; Gupta et al. 2010; Screen et al. 2012). However, analytical models

to directly correlate the observed phenomena to the tissue relaxation modes have less

been addressed. More thorough experimental observations are required to investigate

the possible microstructural origins of the time-dependent behaviour in the AV tissue,

and appropriate models need to be developed to accommodate the identified

mechanisms.

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It was shown here that the assumption of quasi-linear viscoelastic behaviour for AV

tissue does not mathematically correlate with the experimentally observed modes and

trends, and the resulting stress-relaxation and creep functions do not appear to

voluntarily follow the experimental data as reported in the works of Stella et al. (2007)

and Anssari-Benam et al. (2011a). These results suggest that the quasi-linear

viscoelasticity may not be an intrinsic behaviour of the AV, and thus the application of

QLV model to characterise its time-dependent behaviour may not be theoretically

supported. This may be a contributing factor to the limited success of fitting the QLV

model to the AV stress-relaxation data, reported in some studies (Sauren et al. 1983;

Rousseau et al. 1983; Sauren and Rousseau 1983).

Concerning the creep behaviour, previous studies have reported particular poor

outcomes when fitting creep data to the QLV model (Haslach 2005). This is also

reflected in equation (21), as the resulting creep function suggests a constant creep

response, discounting for the primary and the secondary creep behaviours observed in

experimental investigations (Anssari-Benam et al. 2011a).

The stress-relaxation and creep modes exhibited in experiments by other connective

tissues such as tendons have been shown to be interrelated under the assumption of

quasi-linear viscoelasticity, by incorporating the experimentally observed structural

mechanism of gradual fibre recruitment during the both phenomena, into QLV

(Thornton et al. 2001). However, the analysis presented here shows that when the fibre

recruitment model is incorporated for the case of AV, mathematical formulations based

on the quasi-linearity assumption result in two uncoupled functions with no apparent

interrelations (equations 14 and 21), further reflecting on the limitations of such

assumption for the AV tissue.

While the analysis presented here was centred on AV tissue, the mathematical

principles and definitions are generic to all soft tissues of the same class, in which

time-dependent behaviour does not follow a continuous spectrum. Based on this

analysis, it may further be concluded that it is highly unlikely that the time-dependent

behaviour of this class of tissues could be assumed to be quasi-linear.

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Acknowledgment

The author wishes to thank Dr. Hazel Screen for her helpful comments and feedback.

This work was part of a research project funded by the UK Engineering & Physical

Sciences Research Council (EPSRC), a Discipline Bridging Initiative (DBI) grant from

the EPSRC and the Medical Research Council (MRC).

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References

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Anssari-Benam, A., Bader, D. L., Screen, H. R. C.: A combined experimental and modelling approach to aortic valve viscoelasticity in tensile deformation. J. Mater. Sci.: Mater. Med. 22, 253-262 (2011b)

Aspden, R.M.: Relation between structure and mechanical behaviour of fibre-reinforced composite materials at large strains. Proc. R. Soc. Lond. A. 406, 287-298 (1986)

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Billiar, K.L., Sacks, M.S.: Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp - part I: experimental results. J. Biomech. Eng. 122, 23-30 (2000)

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Doehring, T.C., Carew, E.O., Vesely, I.: The effect of strain rate on the viscoelastic response of aortic valve tissue: a direct-fit approach. Ann. Biomed. Eng. 32, 223-232 (2004)

Fung, Y.C.: Biomechanics: Mechanical properties of living tissue, 2nd ed. New York (1993). Springer-Verlag, New York.

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Haslach, H.W.: Nonlinear viscoelastic, thermodynamically consistent, models for biological soft tissue. Biomechan. Model. Mechanobiol. 3, 172-189 (2005)

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Lanir, Y.: A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. J. Biomech. 12, 423-436 (1979)

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Figure legends

Figure 1- Two representative stress-relaxation curves for AV specimens loaded in

circumferential direction. Experimental data points are shown with hollow circles ( ),

and Maxwell relaxation modes in form of Prony series by continuous line. The y axis

represents the reduced stress relaxation G(t). At lower circumferential strains

, single relaxation mode describes the experimental data, while it switches to

double relaxation modes at higher strain levels (e.g. . Data were

collated from Anssari-Benam et al. (2011a).

Figure 2- Two representative creep curves for AV specimens loaded in circumferential

direction: (a) creep under 50% of failure load (50% Ffailure); (b) creep under 70% of

failure load (70% Ffailure). Experimental data points are shown with hollow circles ( ).

Continuous line represents the exponential and linear models used to characterize the

primary and secondary creep phases, respectively. Primary and secondary creep stages

are shown in the graphs. Data were collated from Anssari-Benam et al. (2011a).

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Figure 1

19

Elapsed time (s)

0.5

0.6

0.7

0.8

0.9

1

0 50 100 150 200 250 300

G(t)

Stress-relaxation in circumferential direction

Single exponential decay mode

Double exponential decay modes

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Figure 2

20

Elapsed time (s)

J(t)

Creep in circumferential direction: F = 50% Ffailure

(a)

27

27.5

28

28.5

29

29.5

30

0 50 100 150 200 250 300

Primary creep Secondary creep

Creep in circumferential direction: F = 70% Ffailure

Elapsed time (s)

J(t)

(b)

33

33.5

34

34.5

35

35.5

36

0 50 100 150 200 250 300

Primary creep Secondary creep