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AN APPROACH OF LINEAR VISCOELASTIC MODEL TO DYNAMIC ANALYSIS OF


HUMAN TYMPANIC MEMBRANE

Article  in  Acta científica venezolana · November 2016

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PHYSICS

AN APPROACH OF LINEAR VISCOELASTIC MODEL TO


DYNAMIC ANALYSIS OF HUMAN TYMPANIC MEMBRANE

Luis Caminos1*, María Torres1, Fernando González1, Wilber Rosales1, Juan


Colmenares1, Jesús Ramirez-Pastran1 y Antonio González-Herrera2

1
Departamento de Ingeniería Mecánica, Universidad Nacional Experimental del Táchira,
Venezuela. 2Departamento de Ingeniería Civil, Materiales y Fabricación, Universidad de Málaga,
España.

Recibido: 06/10/2016 Corregido: 14/11/2016 Aceptado: 25/11/2016

ABSTRACT The human tympanic membrane (TM) plays a key role in driving
sound from the air to the fluid inside the cochlea. It transforms the acoustic
energy into mechanical vibratory energy. The mechanism involved in this
transformation is currently under study, being numerical modeling one of the
common strategies. The proper knowledge of the mechanical properties for the
different components is the main limitation for the validity of these models. It is
especially relevant the dynamic response in the frequency range of audible
sound. In this study, a viscoelastic model is used to simulate the dynamic
behavior of the TM. The tissue is characterized assuming viscoelastic linear
behaviour based in the generalized Maxwell model. Experimental
measurements of complex modulus on samples of the TM are used to
determine the parameters of the viscoelastic model. Once the constitutive
equation of the material has been determined it is implemented into a complete
middle ear finite element model (FEM), composed of the TM, the ossicular chain
and the suspensory ligaments and tendons. The middle ear transfer function is
obtained by means of a harmonic analysis and it is used to evaluate the
viscoelastic model. Finally, numerical results are compared with other
experimental results. KEYWORDS Tympanic membrane, Viscoelastic behavior,
Finite element analysis, Transfer function.

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FÍSICA

UN ENFOQUE DE MODELO VISCOELÁSTICO LINEAL PARA EL


ANÁLISIS DINÁMICO DE LA MEMBRANA TIMPÁNICA HUMANA

RESUMEN La membrana timpánica humana (MT) juega un papel clave


en la conducción de sonido desde el aire hasta el fluido dentro de la cóclea.
Ésta transforma la energía acústica en energía mecánica vibratoria. El
mecanismo implicado en esta transformación está actualmente en estudio,
siendo el modelado numérico una de las estrategias comúnmente utilizadas.
El desconocimiento de las propiedades mecánicas de los diferentes
componentes es la principal limitación para validar estos modelos. Resulta
especialmente importante la respuesta dinámica dentro del rango de
frecuencias de sonido audible. En este estudio, un modelo viscoelástico se
utiliza para simular el comportamiento dinámico de la MT. El tejido se
caracteriza suponiendo un comportamiento viscoelástico lineal usando el
modelo generalizado de Maxwell. Medidas experimentales del módulo
complejo en muestras de la TM se usaron para determinar los parámetros
del modelo viscoelástico. Una vez determinada la ecuación constitutiva del
material, ésta se implementa en un modelo de elementos finitos (MEF) del
oído medio, compuesto por la MT, cadena de huesecillos, ligamentos
suspensorios y tendones. La función de transferencia del oído medio se
obtiene por medio de un análisis armónico y se utiliza para evaluar el modelo
viscoelástico. Finalmente, los resultados numéricos se comparan con otros
resultados experimentales. PALABRAS CLAVES Membrana timpánica,
Comportamiento viscoelástico. Análisis de elementos finitos, Función de
transferencia.

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INTRODUCTION

The middle ear mechanic focuses on the principles of sound transmission


from the TM to the oval window, which is the gateway to the cochlea (inner
ear). This area of study includes the transformation of sound energy implicit in
the sound waves in mechanical vibrational energy that includes the eardrum
movement and vibration transmission to the ossicles and finally the cochlea.
The use of numerical models has led to significant advances in the study of
the biomechanics of the middle ear. Specifically, the FEM has become a
widely accepted method for modeling the human hearing system. However,
the knowledge of the dynamic properties of the materials is essential to
simulate correctly its dynamic behaviour under stimulus of a sound wave.
Current research is focused to determine more precisely the mechanical
properties of the tissues of the human ear under different working conditions,
in order to obtain numerical models that adequately simulate their actual
behavior.
The first goal of the present research was to characterize the tissue of the
human tympanic membrane, considering its dynamic behavior as a linear
viscoelastic material in the audible frequency range (20 Hz to 20 kHz). For
this purpose, the values for the storage modulus (E')18 and loss modulus
(E'')18 are used with the corresponding hypotheses.

METHODOLOGY

In this section, the methodology for the characterization of TM is presented. It


is based on Wiechert (or generalized Maxwell model) constitutive equation.
Its implementation in the simulation of the dynamic behavior of TM with a
virtual model it is also described.

Definition of the model parameters


In this study, the TM tissue is considered isotropic and homogeneous.
Moreover, recent studies10,19 have observed typical viscoelastic behavior.
These studies suggest that theories developed about polymers can be used
to characterize live tissue; hence, the present study propose a generalized
Maxwell model for modelling of dynamic behavior of TM, in the frequencies of
audible sound. This model consists of one Standard Linear Solid (SLS)
connected with three Maxwell solids (Figure 1).
The characterization of TM tissue is made by means of the complex

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modulus, which is defined in the frequency domain as4:

(1)

where is the storage modulus, is the loss modulus, is the


frequency, and and can be expressed as:

(2)

(3)

where ( =1, 2 ,3 ,4) is the relaxation modulus of the jth spring, is the
viscosity of the jth dashpot, is the relaxation time of the jth
dashpot, and is the spring stiffness connected in parallel at Maxwell solid
which provides a balance or elastic stiffness after the stress relaxation.

Figure 1 Wiechert viscoelastic model of the TM


Standard Linear Solid (SLS) connected with three Maxwell solids

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The loss factor is defined in the Equation (4) as the ratio of the storage
modulus to the loss modulus:

(4)

where is the phase angle of the complex modulus.


For the model parameters, the mean experimental values18 of and
are used; they were extrapolated to 20,000 Hz using a logarithmic curve with
coefficients of determination r2 of 0.9558 and 0.9203 for and
respectively.
Using the reference logarithmic curve, a nonlinear regression method was
applied to calculate the 9 parameters of the model: e = 17.41 MPa; 1 = 7.92
MPa; 2 = 4.92 MPa; 3 = 4.36 MPa; 4 = 3.46 MPa; 1 = 0.00756 x 10-3s; 2
-3 -3 -3
= 0.0582 x 10 s; 3 = 0.47 x 10 s; 4 = 4.79 x 10 s.
The values of r2 found with the Wiechert model with respect to logarithmic
referential curve are: 0.9860 and 0.9944 for and respectively
between 20 to 20000 Hz. The parameter is approximated to a constant
value equal to 0.14 in the same frequency range.

Finite element model


The geometric model of the middle ear was developed based on
measurements taken in temporal bones without pathology and published in
different references (1for details).
The TM was modeled with shell (SHELL181) elements assuming uniform
thickness of 0.075 mm. The tympanic annulus is considered as a band (0.2
mm wide and 0.2 mm thick) around the eardrum. For the ossicular chain,
posterior incudal ligament, incudomalleolar and incudostapedial joints, solid
(SOLID185) elements are used.
The ligaments and tendon support of the malleus are modeled with beam
(BEAM182) elements. The stapedial annular ligament is assumed as a band
around of stapedial footplate (0.05 mm wide and 0.05 mm thick) also using
shell (SHELL181) elements.
The boundary conditions of the model include the suspensory ligaments and
tendons of the ossicular chain, which are joined at one end with the nodes at
the intersection of each bone and, at the other end, are fixed to simulate the

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union with the middle ear cavity. The nodes of the outer edge of the tympanic
annulus as well as nodes of the periphery of stapedius annular ligament are
fixed to simulate the connection with the middle ear cavity.
The cochlear load on stapedial footplate was modeled with mass block
dashpot system6. The Figure 2 shows the FEM of middle ear generated with
ANSYS program.
The simulations were made using harmonic analysis in the audible
frequency range (20 Hz to 20 kHz) by applying pressure sound at 90 dBSPL on
the TM. Thus, the assumption is that the materials are isotropic and
have a linear viscoelastic behavior in the case of the eardrum and other soft
tissues, whereas the ossicular chain is assumed a linear elastic solid. This
hypothesis is commonly accepted and has been tested experimentally5.
The mechanical properties of the components of the model, excepting the
Young's modulus of the TM, were taken from the mean values commonly
accepted in the literature and are shows in Table I. Most of the information
comes from calibration with numerical models.

Figure 2 Finite element model of the human middle The model is composed of the
TM (eardrum), the ossicular chain (malleus, incus and stapes) and the suspensory ligaments
and tendons

Otherwise, in order to simplify the simulations, the same damping factor is

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53

used for the TM ( = 0.14) and the other soft tissue components (ligaments,
tendons and joints). This consideration is valid according to the results
obtained in previous researches1,2 where a sensitivity analysis were made. It
was proved that there is a strong dependence of the results with the
mechanical properties of the TM compared with the properties of other
elements of the middle ear, especially in terms of the movements of umbo
and stapes.

Table I Materials properties


Young’s modulus Loss
Density Poisson’s
Component E factor
 (Kg/m3) ratio 𝝼

Eardrum:
2
Pars tensa 1.2x103 (a) (N/m
[18.3 -) 33.8]x106 0.3 (d) 0.14
Pars flaccida 1.2x103 (a)
[18.3 - 33.8]x106 0.3 (d) 0.14
(0.020 - 20 kHz)
Malleus 1.9x103 (b)
1.41x1010 (e)
0.3 (d) 0
Incus 1.9x103 (b)
1.41x1010 (e)
0.3 (d) 0
Stapes 1.9x103 (b)
1.41x1010 (e)
0.3 (d) 0
3
1.2x10
Tympanic annulus 6x105 (d)
0.3 (d) 0.14
(assumed)
Manubrium 1.0x103 (c)
4.7x109 (c)
0.3 (d) 0.14

Tensor tympani tendon 2.5x103 (c)


2.6x106 (c)
0.3 (d) 0.14

Lateral mallear
2.5x103 (c)
6.7x104 (d)
0.3 (d) 0.14
ligament
Anterior mallear
2.5x103 (c)
2.1x106 (d)
0.3 (d) 0.14
ligament
Superior mallear
2.5x103 (c)
4.9x104 (d)
0.3 (d) 0.14
ligament
Posterior incudal
2.5x103 (c)
6.5x106 (h)
0.3 (d) 0.14
ligament
Stapedial tendon 2.5x103 (c)
5.2x105 (c)
0.3 (d) 0.14
Stapedial annular
2.5x103 (c)
2x105 (f)
0.3 (d) 0.14
ligament
Incudomalleolar
3.2x103 (d)
1.41x1010 (d)
0.3 (d) 0.14
joint

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Incudostapedial
1.2x103 (d)
6x105 (g)
0.3 (d) 0.14
joint
References: (a)17, (b)16, (c)9, (d)14, (e)13, (f)7, (g)(11), (h)(6)

Governing equations
One of the contributions of this research is related to the approach of damping
system. As noted in a study about the evolution of numerical modeling of the
TM15, Rayleigh damping is a classic and probably the most common method to
easily build the damping matrix of a numerical model. However in this
investigation, the Rayleigh damping is replaced by the hysteretic or structural
damping, which leads to intrinsic losses due to internal friction of the material,
which can be quantified by the loss factor η. This factor can be included in the
elastic properties of the material through the complex modulus as follows:

(5)

With this kind of damping representation, the motion governing equation is:

(6)

where vectors , y are acceleration, velocity and complex


displacement of the nodes respectively, and the vector represents the
harmonic external force applied to the system and in this study is made equal to
the nodal forces generated due to harmonic sound pressure on the surface of
the eardrum. The matrix corresponds to the structural mass matrix and
is the complex stiffness matrix of the structure, which is determined as:

(7)

The matrixs and are the real and imaginary parts of the complex
stiffness matrix respectively. The matrix is calculated using the storage
modulus and is determined using the imaginary part of the complex
modulus
Equation (6) allows calculating the displacements and velocities (magnitude
and phase angle), corresponding to the node located in the umbo (see Figure
2)This node serves as a reference for measuring the dynamic response of the
system through harmonic analysis.

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RESULTS AND DISCUSSION

In order to validate the proposed model, two studies are used as a standard for
comparison with the results of the simulations. The first3 two fresh temporal
bones (TB1 and TB2) without otologic diseases to calculate the transfer function
of the umbo using Laser Doppler Vibrometry (LDV). The external canal, cochlea,
incus, stapes, tensor tympani tendon, stapedial annular ligament, posterior
incudal ligament were removed of the bones. Only the TM with malleus,
tympanic annulus and anterior mallear ligament were left intact.
To simulate this experiment through the numerical model, we used only the
components involved. A harmonic pressure load equal to 90 dBSPL, equivalent
to 0.632 Pa, on the outer face of the TM was applied, and then we made
harmonic analysis covering from 20 to 20000 Hz. Complex displacements and
velocities were calculated on the node located in the umbo area (Figure 2).
These displacements and velocities are expressed in magnitude and angle
phase. Finally, the umbo transfer function module is obtained by dividing the
velocity by the pressure on the TM (0.632 Pa).
The Figure 3 shows comparative curves between the values obtained
experimentally and with the numerical model for the magnitude and the angle
phase of the umbo transfer function (velocity/pressure). As can be seen, both
experimental measurements (TB1 and TB2) differ quantitatively, but exhibit
similar behavior in the frequency range studied. Both curves are consistent with
similar measurements made by other authors3.
In each one of the experimental measurements, a characteristic peak (about
300 Hz and 600 Hz at TB1 and TB2) exists, where the transfer function reaches
a maximum magnitude and phase angle of zero crossing occurs.
We can also observe that there are three particular frequency ranges in both
measurements: the first one occurs below the frequency where the peak occurs;
here, umbo movement is in-phase with the pressure wave due that the phase
between the transfer function and the pressure is maintained at approximately
0.25 periods, which is consistent with the in-phase behavior between the
pressure and the displacement and in turn the response is consistent with
dynamic behavior of a simple mechanical oscillator that is dominated by
stiffness.
The second range is located between peak frequency and 2 - 3 kHz, where
phase becomes more negative by the damping effect and is consistent with the
increase in reactance due to the inertia of the system. The third range appears

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after 2 - 3 kHz; the transfer function phase drops below -0.25 periods, which
implies more complex patterns of vibration that cannot be explained by simple
mechanical elements.
Regarding the model results, a behavior closer to TB2 curve can be observed,
both qualitatively and quantitatively, between 100 and 7000 Hz. After 7000 Hz
the curve model is more damped; however, it has the three characteristics areas
described above for the two experimental curves.
From these results, we can conclude that the viscoelastic model used with a
constant loss factor η = 0.14 to simulate the dynamic behavior of the TM is
reasonably acceptable within of the audible frequency range.
The second experimental study12, the authors used a different methodology to
the previous: Opto-electronic stroboscopic holography was used to measure the
magnitude and phase of the transfer function of the umbo on temporal bones
without pathology. The temporal bone was kept intact in this study, including the
cochlea and all other components of the middle ear.
The finite element simulation was applied to the complete middle ear model.
The material properties are shown in Table I, and the boundary conditions
described above were used. Figure 4 shows the curves for the modulus of the
transfer function of the umbo (a) and phase (b), the corresponding experimental
measurements on two temporal bones (TB10_05 and TB09_11) and the results
of the finite element model.

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(a)

(b)
Figure 3 Umbo transfer function: (a) Magnitude (b) Phase

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(a)

(b)
Figure 4 Umbo transfer function: (a) Magnitude (b) Phase

It can be seen that both experimental curves are very similar with only a slight
difference from a quantitative point of view. Similarly to previous experimental
measurements, the three characteristics areas are also seen in the frequency
range studied; however, the transfer function magnitude values are lower due to
the inertia and damping of the ossicles, ligaments and tendons, as well as
the effect of the load of the cochlea.
Regarding the model curve, can be observed that the umbo transfer function
presents a similar shape to the experimental to 4000 Hz, but differs
quantitatively. The peak frequency is 800 Hz, which is very close to the 1000 Hz
of TB09_11. It also presents greater damping in the high-frequency (> 4000 Hz).
One possible explanation is that the mechanical properties of the other
component elements coupled to the TM, particularly ligaments and tendons, are
taken of the mean values obtained through calibration of numerical models for
frequency ranges until 8000 Hz; futhermore, the vibration complex patterns at
high frequency of the system can be cause of this behavior too.
Another potential source for discrepancies is the influence of the acoustic
cavities. In this model, the effect of the fluid has not been included. In an recent
study, where the middle ear cavity was modelled with fluid element, the

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presence of an additional peak was observed8. In that study classic Rayleigh


damping was used. This phenomenon is related to coupled mechano-acoustics
effect which are not considered in this model.

CONCLUSIONS

The methodology used in this investigation allowed us to characterize the


tissue of TM based on measurements of storage modulus and loss made with
TM samples using a dynamic test.
The characterization was done assuming dynamic viscoelastic behavior, which
is analogous to the response Wiechert model, or generalized Maxwell model,
which consists of simple mechanical elements (springs and dampers). After
defining the constitutive equation model, it was implemented in a finite element
program to simulate the dynamic response of an average human ear when it is
stimulated by a pressure wave.
The model results indicate that the calculated parameters reproduce
adequately the trend curves of the values measured for the storage modulus
and loss of membrane tissue within the audible frequency range, therefore we
found that the theoretical foundations applied to the dynamic behavior of
polymers can be used to explain the behavior of biological tissue.
Finally, it may be noted that findings of this research represent an important
advancement in the study of the dynamic behavior of the human tympanic
membrane by taking into account values of complex modulus and loss factor
within a finite element model. This will expand the application of computational
models for other purposes such as prosthesis design and detection of tympanic
membrane pathologies.

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Biomechanics, 45: S182, 2012.
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J., Dirckx, J. Viscoelastic properties of the human tympanic membrane


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Correspondencia: *Dr. Luis Francisco Caminos Gámez. Universidad


Nacional Experimental del Táchira, Avenida Universidad, Paramillo, San
Cristóbal, CP. : 5001. Correo electrónico: lcaminos@unet.edu.ve

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