See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/247836284

A comparison of Young's modulus for normal and diseased human eardrums

at high strain rates

Article  in  International Journal of Experimental and Computational Biomechanics · January 2009

DOI: 10.1504/IJECB.2009.022856

CITATIONS READS

19 134

4 authors, including:

Huiyang Luo Chenkai Dai

University of Texas at Dallas Johns Hopkins University
61 PUBLICATIONS   728 CITATIONS    33 PUBLICATIONS   797 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

AFOSR Sand View project

NSF CNT wrapped carbon fiber to reinforce interface strength of composite View project

All content following this page was uploaded by Huiyang Luo on 16 October 2014.

The user has requested enhancement of the downloaded file.

Int. J. Experimental and Computational Biomechanics, Vol. 1, No. 1, 2009 1

A comparison of Young’s modulus for normal and

diseased human eardrums at high strain rates

Huiyang Luo and Hongbing Lu*

School of Mechanical and Aerospace Engineering,
Oklahoma State University,
Stillwater, OK 74078, USA
Fax: 1-405-744-7873
E-mail: huiynag.luo@okstate.edu
E-mail: hongbing.lu@okstate.edu
*Corresponding author

Chenkai Dai and Rong Zhu Gan

School of Aerospace and Mechanical Engineering,
University of Oklahoma,
Norman, OK73019, USA
E-mail: chenkaidai@ou.edu
E-mail: rgan@ou.edu

Abstract: The viscoelastic properties of a human eardrum or tympanic

membrane (TM) have not been fully characterised in the auditory frequency
range, despite the fact that these properties are critical data as input in
modelling the acoustic transmission in a human ear. In this paper using a
miniature split Hopkinson tension bar (SHTB), we investigated the mechanical
behaviour of TM at high strain rates, corresponding approximately to the
behaviour at high frequency. The Young’s modulus values of diseased human
TMs are determined as 63.4–79.2 MPa in the radial direction, and 33.1–42.8
MPa in the circumferential direction at strain rates 300–2000 s–1, results are
compared with those for normal TMs. The comparison indicates that normal
human TMs show stronger dependence on high strain rates. The measured
Young’s modulus is converted into complex Young’s modulus in the frequency
domain in the frequency range of 300–2000 Hz.

Keywords: diseased human eardrum; Young’s modulus; high strain rate; split
Hopkinson tension bar; SHTB; complex modulus; frequency domain.

Reference to this paper should be made as follows: Luo, H., Lu, H., Dai, C.
and Gan, R.Z. (2009) ‘A comparison of Young’s modulus for normal and
diseased human eardrums at high strain rates’, Int. J. Experimental and
Computational Biomechanics, Vol. 1, No. 1, pp.1–22.

Biographical notes: Huiyang Luo received his PhD in Mechanical

Engineering at the University of Arizona, Tucson, USA in 2005. He is
currently a Research Associate in the Polymer Mechanics Laboratory at
Oklahoma State University, Stillwater, USA.

Copyright © 2009 Inderscience Enterprises Ltd.

2 H. Luo et al.

Hongbing Lu received his PhD in Aeronautics at Caltech in 1997. He is a Full

Professor of Mechanical and Aerospace Engineering at Oklahoma State
University since 2006. His research is focused on the viscoelastic behaviour of
polymers, polymer nanoencapsulated aerogels and biomedical materials. He is
on the editorial boards of Mechanics of Time-Dependent Materials and
International Journal of Theoretical and Applied Multiscale Mechanics.

Chenkai Dai received his MD and MS from Tongji Medical College, Huazhong
University of Science and Technology, China. He is currently a PhD candidate
in Biomedical Engineering Laboratory in the Bioengineering Center at the
University of Oklahoma, Norman, USA.

Rong Zhu Gan received her PhD in Biomechanical Engineering at University

of Memphis in 1992. She is a Full Professor and Charles E. Foster Chair in
Mechanical Engineering at the University of Oklahoma. Her recent research
interests are on the implantable devices, middle ear mechanics and transfer
functions. She is on the editorial board of International Journal of
Experimental and Computational Biomechanics.

1 Introduction

About 15% of US population suffers from different levels of hearing loss induced by
various diseases and pathological conditions. In most cases of conductive hearing loss,
the change of tympanic membrane (TM) plays an important role in the hearing loss
development. For instance, the otitis media, one of the most common diseases in pediatric
population, causes TM edema or perforation and initiate the hearing loss. Hence, the
effective implants and surgical treatments with minimum trials are necessary to improve
or restore the hearing loss. It is essential to understand the roles of the individual
components in ear, the hearing aid devices and surgical procedures in acoustic
transmission. Towards this goal, a complete human ear model, with the consideration of
the accurate structures and mechanical properties (capable of taking into account of
properties of normal and diseased tissues) needs to be constructed for analysis of acoustic
transmission in human ears. The eardrum, or TM, separates the middle ear from the outer
ear, receives the sound waves collected by the outer ear and transmits them to the middle
ear. TM plays an important role in coupling the pressure wave in the external ear with the
acoustic wave in the middle ear. Any damage on the eardrum, such as perforation, trauma
and infection, can affect sound transmission and result in conductive hearing loss (Eiber
and Schiehlen, 1996; Puria et al., 2003; Ferris and Prendergast, 2000; Voss et al., 2001).
The eardrum is a multi-layer membrane including the epidermal, collagen fibrous and
mucosal layers. The collagen fibres, which provide primarily the mechanical stiffness of
the TM, is arranged into the matrix of ground substance primarily along radial (~22 µm
thick fibre layer) and circumferential (~15 µm thick fibre layer) directions (Lim, 1995).
The pars tensa is the major part of the TM within tympanic annulus and malleus
manubrium. The small size of the TM (about 0.07 mm in thickness and 9 mm in
diameter) induces difficulties in measuring the mechanical properties. Numerous
investigations of the mechanical behaviour of human TMs have been performed.
However, the data are limited to low strain rates or low frequencies under 100 Hz (von
Békésy, 1960; Dirckx and Decraemer, 2001; Fay et al. 2005; Cheng et al., 2007; Gaihede
 A comparison of Young’s modulus 3

et al., 2007; Huang et al. 2007; Daphalapurkara et al., 2008). For example, the Young’s
modulus of a human TM was reported as ~20 MPa in the radial direction at 0.005 Hz
through bending test of the dissected TM strip (von Békésy, 1960) and at each quadrant
of TM using nanoindentation (Huang et al. 2007) and as 13–22 MPa in the
circumferential direction under quasi-static tension (Daphalapurkara et al., 2008). Some
of these property values are often used as input data to model sound transmission and
hearing sensitivity in middle ear (Gan et al., 2004, 2006; Wang et al., 2007). Accurate
measurements of TM dynamic properties will also help to understand the effects of
structural changes of the TM, such as perforation, trauma and infection, on the sound
transmission and conductive hearing loss through modelling (Eiber and Schiehlen, 1996;
Puria et al., 2003; Ferris and Prendergast, 2000; Voss et al., 2001).
The eardrum is subjected to loading in the frequency domain; its Young’s modulus,
however, has not been well investigated in the frequency domain, corresponding
approximately to the behaviour at high strain rates. To the best of our knowledge, the
only data reported at high frequency was given by Kirikae (1960), who showed a
Young’s modulus of 40 MPa in a rectangular eardrum specimen cut along a direction
perpendicular to the malleus manubrium at a frequency 890 Hz. Since the TM performs
its function in the frequency domain, its mechanical properties must be characterised
within the auditory frequency range, or high strain rates, for use to model the acoustic
wave transmission in a human ear. It is well known that for most biological living tissues,
the mechanical properties are not sensitive to strain rates under relatively low strain rate
range (Fung, 1993), usually less than 10 s–1. Recently, the mechanical properties of some
human tissues have been investigated within high strain rate range (100–5000 s–1) using
split Hopkinson bars (Weiss et al., 2002; Shergold et al., 2006; Song et al., 2007; Saraf et
al., 2007). The results show a strong rate-dependent behaviour. In this paper, we use a
miniature split Hopkinson tension bar (SHTB) to measure the mechanical properties of
diseased (or abnormal) eardrum at high strain rates, corresponding approximately to the
behaviour at high frequencies and compare the properties with the corresponding results
from normal TMs. The normal and diseased human TM specimens were prepared in
either radial or circumstantial direction; they were pre-conditioned, tested on the SHTB
to measure the stress-strain relationship at high strain rates. The results are converted to
the complex modulus in the frequency domain. The properties of diseased TMs are
compared and discussed with normal TMs.

2 Experiments

2.1 Preparation of human TM strip specimens

The TM samples with the tympanic annulus and malleus attached [as shown in
Figures 1(a) and 1(b)], were harvested from fresh-frozen human temporal bones through
the Willed Body Program at the University of Oklahoma Health Sciences Center. The
samples were immersed in 0.9% saline solution. Each TM sample was cut into 1–1.5 mm
wide and 4–5 mm long rectangular strip specimens along either the radial [Figure 1(a)] or
circumferential [Figure 1(b)] direction in the pars tensa part of the TM using surgical
knifes. The specimens for measurement of Young’s modulus in the radial direction were
cut along the radial fibres emanating from the umbo to annulus and the specimens for
measurement of circumferential direction were cut nearly along the local circular fibre
4 H. Luo et al.

direction. After cutting, each strip specimen was placed immediately in saline solution
again and was used in experiment within 5–10 minutes. During experiments, saline was
added to the TM specimen to ensure that it was saturated with saline at all the time.
Orientations of the TM strips cut from a TM sample are shown in Figures 1(a) and 1(b);
each grid in the rulers at the bottom of the figure is 1 mm × 1 mm. The pars tensa part of
the normal TM of right ear of a 71-year old male appears smooth and thin [Figure 1(a)]
and the diseased TM of left ear of an 83-year old female appears rough and thick
[Figure 1(b)]. In each TM sample with ~9 mm diameter, up to eight pieces of radial
[Figure 1(a)] or circumferential [Figure 1(b)] specimens were prepared. In this
investigation, 11 normal (thin) and six diseased (thick) TMs were used. A list of diseased
TM specimens with the age and side was given in Table 1, prepared from six diseased
TM samples used in this study. The list of normal TM specimens was given in reference
by Luo et al. (2008a), prepared from 11 normal TM samples as comparison.

Figure 1 Schematic of the TM strip specimens cut from TM samples, (a) in the radial direction
(normal TM: TB07-27) (b) in the circumferential direction (diseased TM: TB07-24)

(a) (b)
Note: Each grid at the bottom represents a scale of 1 mm × 1 mm.

2.2 SHTB experiments

A miniature SHTB was developed for tensile tests of TM strip specimen at high strain
rates. A schematic diagram for the SHTB setup is shown in Figure 2. The incident bar is
3.66 meter long aluminum 7075-T6 bar with 6.4 mm diameter. The transmission bar is
2.74 meter long hollow 6061-T6 bar with 5 mm inner diameter (ID) and 6.4 mm outer
diameter (OD). Two clamp fixtures were used to grip a TM strip specimen. An X-cut
quartz crystal disk (Boston Piezo-Optics) was inserted and mounted between the clamped
end of the fixture and the incident bar end to measure the front force applied on the TM
specimen. The aluminum tubing striker bar, launched manually by hand, made impact
with the flange thread-connected to the incident bar, generating a tensile wave travelling
along the incident bar to load the specimen. Two semiconductor strain gages with a gage
 A comparison of Young’s modulus 5

factor 176 were mounted on opposite surfaces in the middle of the hollow transmission
bar to measure the weak strain signal representing the transmitted wave. A Nicolet
Sigma-30 digital oscilloscope was used to acquire all strain signals on bars through a
Wheatstone bridge and Vishay 2310A signal-conditioning amplifier, as well as from the
force signal on the X-cut quartz through a Kistler 5010B charge amplifier. A plastic
collar was used as a pulse shaper to assist to reach dynamic stress equilibrium and a
constant strain rate condition, necessary in a valid SHTB experiment. Further details on
the experimental setup and technique have been documented elsewhere (Lu et al., 2007;
Luo et al., 2006, 2008a, 2008b).

Figure 2 Schematic of the miniature SHTB (see online version for colours)
Impact flange
Semiconductor Sample X-Cut quartz crystals Strain gauge (εi , εr)
V
strain gauge (εt )

Transmission bar - + Incident bar

Wheatstone bridge Wheatstone bridge

Clamp fixtures Tubing striker Pulse shaper

Signal amplifier Charge amplifier Signal amplifier

Sigma-30
Oscilloscope

The working principle of SHTB has been well documented in literature (Gray, 2000;
Chen et al., 1999, 2002). With the use of a clamping fixture between the TM strip
specimen and a bar end, under a valid SHTB experiment, formulas (Gray, 2000; Cheng
and Chen, 2003) for the stress and strain rate in a specimen are modified as
At
σ s (t ) = Et ε t (t ) (1)
As

1
ε&s (t ) = [(ci − ct β )ε i (t ) − (ci + ct β )ε r (t ) − K c F (t )] (2)
Ls

where β = Ei Ai / ( Et At ) ; E, c, ε, σ, A and L are Young’s modulus, bar wave speed,

strain, stress, cross-sectional area and length, respectively; F(t) is the force applied on the
specimen, calculated as F (t ) = Et At ε t (t ) ; Kc is the coefficient of clamping correction; the
subscripts i, t, r represent the incident, transmitted, reflected signals, respectively. The
subscript s indicates specimen.
6 H. Luo et al.

Table 1 Mechanical properties of diseased human TM strip specimens

Notes: R: radial direction; C: circumferential direction; in the first column, TB07-xx is

U U U U

the code of TM; the number in the second column is the age; M: male; F: female;
R: right ear; L: left ear.
*The strains are the maximum strain reached in experiments, not the failure strain.
The strain history is obtained through the integration of strain rate with respect to time.
For the soft TM tissue with Young’s modulus in the neighbourhood of tens of MPa, the
typical strains involved in measurement are relatively high, on the order of 6% to 20–
30% (Luo et al., 2008b) and the compliance of the metal clamp fixtures, represented by
 A comparison of Young’s modulus 7

the last term in equation (2) on strain measurement, is low so that the effect of fixture
compliance can be neglected.
On the clamping fixtures mounted on two bar ends, machine screws were used to
tighten aluminum end plates to grip a TM strip specimen. A surgical microscope (Zeiss
OPMI1) was used to monitor the TM specimen during clamping. The width, thickness
and gage length (the distance between two fixture ends) of specimens were within 1.1–
2.0 mm, 62.5–75.4 μm, 0.42–1.48 mm for a normal TM specimen, respectively, and 1.1–
2.3 mm, 84.2–121.5 μm, 0.42–1.3 mm for diseased TM specimen, respectively. The
dimensions of diseased specimens measured in this study are given in Table 1. The
tensile tests were conducted at room temperature 23 ± 2 °C under relative humidity 40 ±
5%.
Each TM specimen was pre-conditioned through pre-stretching by several cycles
(Cheng et al., 2007) prior to testing on SHTB in order to simulate the loading condition
on a TM in service and allow biological soft tissues to reach a steady state in mechanical
behaviour. In quasi-static tension tests, the pre-conditioning of TM specimens could be
accurately controlled with the load applied by MTS machine (Cheng et al., 2007). In this
work, in order to apply consistent pre-conditioning, we used the SHTB to apply the
pre-conditioning at small amplitude of stress, approximately 20% of the maximum stress
used in actual testing, using the multiple incident/reflected waves inside the incident bar,
to load a TM specimen at high strain rates (Luo et al., 2008a). After pre-conditioning, the
TM specimen was adjusted to the initial length (stretch ratio 1.0) for tensile tests at high
strain rates. Tensile tests for normal and diseased TM specimens were conducted within
three ranges of strain rates, namely, 100–500 s–1, 500–1000s–1 and 1000–2500 s–1.

3 Results

The typical recorded data for the incident, transmitted, reflected and quartz signals on the
bars in an SHTB experiment are plotted in Figure 3. When the incident wave reaches the
TM specimen, only a small fraction of the wave was transmitted to the transmission bar,
majority of the wave was reflected back to the incident bar. Therefore, the magnitude of
reflected signal is very close to that of the incident signal and the transmitted signal is
very weak. The X-cut crystal shows the actual force history as experienced by the quartz
crystal; two peaks are present during loading and unloading stages. For the measurement
of the front force applied on the TM specimen, the quartz actually measured the wave
signal in the form of incident wave plus the delayed reflected wave. With the
consideration of the time delay in the reflected wave as recorded by the quartz, the force
representing the front force of the specimen can be determined through analysis of the
stress wave propagation (Luo et al., 2008b). The front force recorded by the X-cut quartz
was corrected to remove two peaks representing the inertia effects of the quartz.
Following the 1-wave, 2-wave method (Gray, 2000), the dynamic equilibrium condition
was examined. Since the mechanical impedance of the TM is much less than that of the
bars, it takes 4–5 μs for the stress wave to complete one round trip transit in the gage
length of a TM specimen and about 20 times of round trip transits of the stress wave in
the TM specimen to reach dynamic stress equilibrium state.
8 H. Luo et al.

Figure 3 Typical recorded signals from incident bar, transmission bar and X-cut crystal
(normal TM specimen: TB07-32, #1)

In Figure 4, the back force applied on the specimen as recorded from the semiconductor
strain gages attached to the hollow transmission bar is very close to the front force
determined from X-cut force, except during the rise-up stage (0–100 μs) and the final
unloading stage (330–420 μs). Hence, the dynamic stress equilibrium condition was
nearly established during the loading duration period (100–330 μs) when the strain rate
was constant and data representing the properties of TM was analysed. A plastic washer
was used as a pulse shaper for the incident wave so that the strain rate was kept nearly
constant during the loading. Under the valid testing conditions, bar strain data was
processed further to determine the stress-strain relation under a given high strain rate.
The typical stress-strain curves for TM strips in both radial and circumferential
directions are shown in Figure 5 for TM strip specimens after pre-conditioning for
normal TMs. The curves are in general linear prior to reaching their peak values. The
Young’s modulus increases with the increase of strain rate. The TM specimen was not
broken at strain rates less than 500 s–1 but failed at strain rates higher than 500 s–1. For the
given incident bar length loaded by the tubing striker of 900 mm long, a constant loading
duration 360 μs was induced on a TM strip specimen at all strain rates. At a lower strain
rate, the maximum strains that could be attained within 360 μs were small so that the
specimen did not reach the failure strain, while at a high strain rate the maximum strain
that could be attained within the same time (360 μs) was high enough to induce failure in
the TM specimen. An error bar representing the variation of Young’s modulus is plotted
with the stress-strain curves (Figure 5). It is noted that in tensile tests, the actual strain
rate that could be reached was limited by the experimental setup, the maximum strain rate
that could be reached with this setup was ~2500 s–1. For diseased TM strip specimens in
the radial and circumferential directions, the Young’s modulus values are summarised in
Table 1.
 A comparison of Young’s modulus 9

Figure 4 Typical dynamic force equilibrium check and strain rate history on a TM specimen
(TB07-32, #1)

Figure 5 Typical stress-strain curves of TM strip specimens at high strain rates

Notes: TM specimens represent (340 s–1: TB07-23, #6; 600 s–1: TB07-32, #5; 1600 s–1:
TB07-29, #3) in the radial direction and (300 s–1: TB07-31, #2; 850 s–1: TB07-31,
#5; 1130 s–1: TB07-38, #5) in the circumferential direction.
In order to compare the experimental data at different strain rates, the Young’s modulus
values are averaged within one of the three strain rate ranges, 100–500 s–1,
10 H. Luo et al.

500–1000 s–1 and 1000–2500 s–1, respectively. In the quasi-static testing at low strain
rates, the specimens from the same TM show statistical similarity on four quadrants while
the modulus could vary significantly from different individuals (Daphalapurkara et al.,
2008). The average Young’s modulus values of normal TM within different strain rate
ranges in this work are given in Table 2. Within each range of strain rate, the Young’s
modulus tends to be close, so that the results are averaged and are representative of the
data within that strain rate range.
Table 2 Mechanical properties of normal human TM (67 pieces of TM strip specimens)

Testing Strain rate Young’s modulus Ultimate stress Specimen

Strain
number (s–1) (MPa) (MPa) orientation
11 309 ± 77 45.2 ± 10.2 6.3 ± 3.4a 11 ± 3%b R
U U

15 714 ± 146 51.4 ± 16.6 10.4 ± 3.4 20 ± 7% R

U U

7 1654 ± 381 58.9 ± 18.5 15.9 ± 7.3 41 ± 10% R

U U

21 333 ± 68 34.1 ± 11.2 4.3 ± 1.8 a 11 ± 2% b C

U U

6 772 ± 176 40.6 ± 7.6 7.7 ± 2.5 14 ± 8% C

U U

7 1353 ± 362 56.8 ± 15.7 13.7 ± 5.5 37 ± 10% C

U U

Notes: R: radial direction; C: circumferential direction; the normal TM had a thickness of

U U U U

70.2 ± 3.9 μm.

a
the stress was the maximum stress reached in tests, not the tensile strength
b
the strain was the maximum strain reached in tests, not the failure strain
From Table 2, the data shows about 20–30% variation in Young’s modulus obtained from
different TM specimens. In the radial direction, the Young’s modulus increases from 45.2
± 10.2 MPa, to 51.4 ± 16.6 MPa and to 58.9 ± 18.5 MPa with increasing strain rates from
309 s–1, to 714 s–1 and to 1654 s–1, respectively. In the circumferential direction, the
Young’s modulus increases from 34.1 ± 11.2 MPa, 40.6 ± 7.6 MPa to 56.8 ± 15.7 MPa
with increasing strain rates from 333 s–1, 772 s–1 to 1353 s–1, respectively. The results
show that in general, the Young’s modulus of TM in the radial direction is higher than
that in the circumferential direction. The Young’s modulus in the circumferential
direction tends to be close to that in the radial direction at higher strain rates (1000–2500
s–1), showing nearly isotropic behaviour at higher strain rates. From these results, the
Young’s modulus as a function of strain rate is plotted in Figures 6(a) and 6(b) for normal
TMs in radial and circumferential directions, respectively. The y-axis error bars represent
standard deviation of Young’s modulus between the experimental data and the fitted
curves.
The normal TM usually appears as a smooth, translucent thin membrane tissue
[Figure 1(a)]. The TMs of the diseased ears are dark and opaque in appearance under
otoscope. The diseased TMs are thicker due to inflammation. Overall, 26 valid tests were
conducted on SHTB for diseased TM strip specimens in an effort to obtain results to
compare with those of normal TMs. The stress-strain curves for normal TMs are similar
to those of diseased TMs except the difference in slopes (Young’s modulus). The
Young’s modulus data of diseased TMs under high strain rates are summarised in
Table 3. In the radial direction, the Young’s modulus increases from 63.4 ± 14.0 MPa, to
66.0 ± 3.1 MPa and to 79.2 ± 42.3 MPa with increasing strain rates from 282 s–1, to
727 s–1 and to 1173 s–1, respectively. In the circumferential direction, the Young’s
modulus increases from 33.1 ± 7.6 MPa to 42.8 ± 9.0 MPa with increasing strain rates
 A comparison of Young’s modulus 11

from 750 s–1 to 1289 s–1, respectively. The data of diseased TMs also show 20–30%
deviation from each other. Due to the limitation in supply of diseased TMs, there were no
valid tests of diseased TMs in the circumferential direction on SHTB under 100–500 s–1,
the Young’s modulus within this range of strain rates was not obtained. The Young’s
modulus of both normal and diseased TMs as a function of strain rate is plotted in
Figure 6(c). The results of diseased TM show that its Young’s modulus is higher than
normal TMs in the radial direction and its modulus is lower than that of normal TMs in
the circumferential direction [Figure 6(d)].
Table 3 Mechanical properties of diseased human eardrum (31 pieces of TM strip specimens)

Testing Strain rate Young’s modulus Ultimate stress Specimen

Strain
number (s–1) (MPa) (MPa) orientation
6 286 ± 105 64.4 ± 11.1 6.6 ± 2.6a 10 ± 3%b R
U U

6 727 ± 152 66.0 ± 3.1 9.2 ± 3.9 20 ± 9% R

U U

3 1173 ± 117 79.2 ± 42.3 15.0 ± 2.3 33 ± 7% R

U U

9 762 ± 172 34.7 ± 6.9 9.7 ± 5.6 24 ± 7% C

U U

7 1289 ± 195 42.8 ± 9.0 14.9 ± 9.0 40 ± 9% C

U U

Notes: R: radial direction; C: circumferential direction; the diseased TM had a thickness

U U U U

98.4 ± 15.4 μm.

a
the stress was the maximum stress reached in tests, not the tensile strength
b
the strain was the maximum strain reached in tests, not the failure strain

Figure 6 Comparison of Young’s modulus of TMs at different strain rates, (a) normal TMs in
radial direction (b) normal TMs in circumferential direction (c) diseased (abnormal)
TMs in both radial and circumferential direction (d) summary of fitted curves for
normal and diseased (abnormal) TMs

(a)
12 H. Luo et al.

Figure 6 Comparison of Young’s modulus of TMs at different strain rates, (a) normal TMs in
radial direction (b) normal TMs in circumferential direction (c) diseased (abnormal)
TMs in both radial and circumferential direction (d) summary of fitted curves for
normal and diseased (abnormal) TMs (continued)

(b)

(c)
 A comparison of Young’s modulus 13

Figure 6 Comparison of Young’s modulus of TMs at different strain rates, (a) normal TMs in
radial direction (b) normal TMs in circumferential direction (c) diseased (abnormal)
TMs in both radial and circumferential direction (d) summary of fitted curves for
normal and diseased (abnormal) TMs (continued)

(d)

Four typical failed TM strip specimens after tensile testing at strain rates higher than
500 s–1 are shown in Figure 7.

Figure 7 Typical failed TM strip specimens after tensile tests on a SHTB, (a) normal TM
specimen in circumferential direction (b) normal TM specimen in radial direction
(c) diseased TM specimen in circumferential direction (d) diseased TM specimen in
radial direction

(a) (b)

(c) (d)
14 H. Luo et al.

At the bottom, each grid in the rulers represents 1 mm × 1 mm. All TM strip specimens
broke in the middle sections of the specimens, indicating valid tests. For the specimen in
the circumferential direction [Figure 7(a)], most circumferential fibres were elongated
and broke at ultimate strain 32.7 ± 10.2% except for a small number of fibres that
remained connected. For normal TM specimens in the radial direction [Figure 7(b)], they
broke at ultimate strain 38.7 ± 8.7% in the 45º direction with respect to loading direction,
indicating a shear-dominant failure, associated with ductile failure mode. However,
diseased TM specimens in both circumferential and radial directions broke at ultimate
strains 30.8 ± 6.1 % and 36.6 ± 9.4%, respectively, on a plane perpendicular to the
loading axis as shown in Figures 7(c) and 7(d), respectively. The diseased TMs appear to
have failed in brittle mode, indicating that the failure mode changes from ductile mode
for normal TMs to brittle mode for diseased TMs.

4 Discussions

An abnormal TM commonly appears in middle ear diseases such as chronic otitis media,
acute otitis media, tympanosclerosis, TM atrophy and atelectasis (da Costa et al., 1992).
The diseases induce various changes of the TM thickness and shape including thickening
or thinning of the TM, formation of retraction pockets, cholesteatoma and
metalloproteinase inflammation (Yoon et al., 1990; Oktay et al., 2005; Wilmoth et al.,
2003). The change of TM structure results in a change of mechanical properties, which
directly affects the auditory function and causes conductive hearing loss (Hunter and
Margolis, 1997). Since the TM samples used for this study do not have a complete record
on otological pathology history of the human temporal bones, it is difficult to trace each
sample to the original disease. The Young’s modulus values measured in some TMs
could become higher or lower than a normal TM based on different type of middle ear
disease. However, the difference of Young’s modulus between the normal and abnormal
TMs is clearly demonstrated in Figure 6. Doner et al. (2003) observed an increase of
collagen and fibrous fibres in the TM as well as the hyaline degeneration, calcification
and occasional ossification in the TMs with tympanosclerosis. Structural changes could
occur and disrupt frequently the circular fibrous layer (Ruah et al., 1995) which might
explain the lower modulus of abnormal TM than the normal TM in circumferential
direction as shown in Figure 6(d).
The relationship between structure and properties is still not well understood in
diseased TM (Jaisinghani et al., 1999). The Young’s modulus of the TM could decrease
in some diseased TMs (induced by such diseases as purulent otitis media, serious otitis
media). However, middle ears with tympanosclerosis or chronic otitis media have stiffer
TM due to the changes of fibres and possible hyaline degeneration and calcification.
The higher stiffness of diseased TM in the radial direction could indicate that the
external pressure wave may not be transmitted effectively to the middle ear so that
hearing loss could occur. In general, for normal TM, the middle ear converts the sound
pressure into relatively large displacement of the TM as well as the displacement of the
stapes, thus the cochlear sensitivity of acoustic transmission is normal. The hair cells on
the basilar membrane receive the vibration, convert it into nerve impulses and send it to
the brain (Yost, 2007). Under the same magnitude of the sound pressure in the ear canal,
a diseased TM with higher stiffness (due to higher modulus in the radial direction and
thicker TM) induces vibration with lower amplitude at low frequency (Dai and Gan,
 A comparison of Young’s modulus 15

2008; Dai et al., 2008). The lower stiffness of diseased TM (von Unge et al., 1995) in the
circumferential direction could lead to lower vibration amplitude at high frequency (Dai
and Gan, 2008) and distortion in acoustic wave transmission. Further experimental and
numerical investigations on the transfer function for acoustic transmission are needed in
this area.
The results shown in Section 3 indicate that the Young’s modulus of TM depends on
the strain rate within high strain rate range. This indicates that TM is a viscoelastic
material, with its viscosity contributing to the change of Young’s modulus with strain
rate. Since data for the Young’s modulus has been obtained within three ranges of high
strain rates (300–2000 s–1), we model the mechanical behaviour of the TM as a standard
linear solid with three undetermined parameters. Figure 8 shows the standard linear
model consisting of two springs, with spring constants E∞, E1 and a dashpot with
viscosity η. The relaxation time of the model is τ = η/E1. For the standard linear solid
under the uniaxial tension, the Young’s relaxation modulus E(t) is given as

E (t ) = E∞ + E1e−t /τ (3)

For a linear viscoelastic material at a constant strain rate ε&0 , the strain history is
ε (t ) = ε&0 t . The average relaxation modulus E (t ) is determined between initial time and
the ending time of nearly linear stress-strain curve. From an experimental stress-strain
curve, the Young’s modulus is determined before the limit of linearity, εe. The time t is
determined by t = ε e / ε&0 . Considering the standard linear solid model in equation (3), the
average relaxation modulus E (t ) as a function of time t (i.e., terminal time
corresponding to εe) and the Young’s modulus E (ε&) as a function of strain rate ε& 0 are
given as

E (t ) = E∞ + E1 (1 − e−t /τ )τ / t and E (ε&) = E∞ + E1 (1 − e−ε e / ετ )τε& / ε e

&
(4)

Figure 8 A standard linear solid model

All the individual Young’s modulus data (as shown in Table 1) at the actual strain rates
measured in SHTB tests are used as inputs to fit into one of the above equations, to
search for the three best-fit parameters E∞, E1 and η. Table 4 summarises the three
best-fit parameters for both normal and diseased TMs in radial and circumferential
directions. Hence, the best-fit Young’s modulus is plotted in Figure 6 as a function of
strain rate (102–2 × 103 s–1). It is seen that the mechanical property data points are
16 H. Luo et al.

scattered, a characteristics with bio-tissues. Nevertheless, the curves still agree

reasonably well with the experimental data. With these curves, the Young’s modulus can
be determined at other strain rates within 300–2000 s–1. At strain rates (300–1500 s–1), the
Young’s modulus of normal TMs in the radial direction is in general higher than that in
the circumferential direction. At strain rates 1500–2000 s–1 the modulus values in both
radial and circumferential directions are close to each other. The normal TMs show more
pronounced viscoelastic effects in the circumferential direction so that its modulus shows
higher change with the increase of strain rates. However, the modulus of the diseased
TMs in the radial direction is higher than that of normal TMs while the modulus of the
diseased TMs in the circumferential direction is lower than that of normal TMs.
Table 4 Best-fit parameters for Young’s relaxation modulus

Eardrum
Modulus number Modulus number Relaxation time τ Specimen
E∞ (MPa) E1 (MPa) (10–5 s) orientation
Normal 41.52 25.44 5.069 R
U U

Normal 30.04 69.08 2.533 C

U U

Diseased 55.64 186.28 1.036 R

U U

Diseased 28.24 78.97 1.278 C

U U

Notes: R: radial direction; C: circumferential direction.

U U U U

With the parameters in equation (4) determined, the Young’s relaxation modulus E(t) can
be determined. The Young’s relaxation modulus was obtained for TM in both radial and
circumferential directions, as shown in Figure 9.

Figure 9 Young’s relaxation modulus of TM in time domain

From Figure 9, the relaxation modulus can be determined for other times. At relatively
long times (3 × 10–4 – 10–3 s) relaxation modulus of normal TM in the radial direction is
higher than that in the circumferential direction and lower than that of diseased TM in the
 A comparison of Young’s modulus 17

radial direction. The relaxation modulus of diseased TMs in the circumferential direction
is lower than that of normal TMs. As for the relatively short times (e.g., < ~ 2 × 10–5 s),
relaxation modulus of normal TMs in the radial direction tends to be lower than that in
the circumferential direction. The relaxation modulus of diseased TMs in the radial
direction shows the highest value among the four.
We next convert the relaxation modulus in time domain to the complex modulus in
frequency domain. The complex modulus is expressed as E% (ω ) = E ' (ω ) + iE " (ω ) , with
E′(ω) being the storage modulus and E″(ω) the loss modulus. The loss tangent is
tan θ = E ′′ / E ′ . For the standard linear solid in frequency domain, storage modulus E′(ω)
and loss modulus E″(ω) are calculated as (Knauss et al., 2008)

E ′(ω ) = E∞ + E1τ 2ω 2 / (1 + τ 2ω 2 ) and E ′′(ω ) = E1τω / (1 + τ 2ω 2 ) (5)

where ω is angular frequency, ω = 2πf, f is the frequency. The frequency f corresponds

approximately to the strain rate (Emri et al., 2005) in the calculation of viscoelastic
properties. At a frequency 890 Hz, the complex modulus values are calculated as
E% R ( f = 890 Hz ) = 43.41 + 6.67i MPa and E%C ( f = 890 Hz ) = 31.40 + 9.59i MPa for TMs
in the radial and the circumferential directions, respectively. For a normal TM, the
magnitudes of the complex modulus functions at 890 Hz are 32.83 MPa in
circumferential directions, 43.92 MPa in the radial direction, which is very close to
40 MPa, the Young’s modulus reported by Kirikae (1960) measured at 890 Hz. For
diseased TM at 890 Hz, the magnitudes of the complex modulus values are 55.09 MPa
and 26.98 MPa for the radial and circumferential directions, respectively, indicating a
higher stiffness in the radial direction and lower stiffness in the circumferential direction
in comparison with the corresponding values for normal TMs. The storage and loss
moduli of TM are shown in Figures 10(a) and 10(b) determined using equation (5),
respectively. The loss tangent values of TM in both radial and circumferential directions
are shown Figure 11. Both moduli show slow increase in low frequency range
(300–1000 Hz) and a rapid increase in the middle frequency range (1000–2000 Hz). For
normal TMs in the circumferential direction, the storage modulus shows lower value than
that for TMs in the radial direction [Figure 10(a)]. For diseased TMs in the radial
direction, storage modulus is higher than that of normal TMs. The loss modulus of TMs
in the circumferential direction shows a more rapid increase than that of TMs in the radial
direction. In the circumferential direction, both diseased and normal TMs show similar
behaviour in loss modulus [Figure 10(b)]. In the circumferential direction, diseased TMs
show more pronounced viscoelastic behaviour than normal TMs. The analysis presented
here is appropriate for frequency range of 300–2000 Hz. In Figure 11, diseased TMs
show more pronounced viscoelastic behaviour than normal TMs in the radial direction
and less pronounced viscoelastic behaviour than normal TMs in the circumferential
direction. In Figure 11, the loss tangents of diseased TMs in both radial and
circumferential directions are nearly overlapped. Further experimental investigation is
needed to determine the storage modulus and loss modulus at different frequency range
(20–100 Hz and 2000–20000 Hz) and differentiate effects of various middle ear diseases
on the mechanical properties of TM at high strain rates in the future.
18 H. Luo et al.

Figure 10 Complex modulus of both normal and diseased (abnormal) TMs in frequency domain,
(a) storage modulus (b) loss modulus

(a)

(b)
 A comparison of Young’s modulus 19

Figure 11 Loss tangent of normal and diseased (abnormal) TMs

5 Conclusions

A new miniature SHTB was used to apply tension on small specimens of

saline-saturated human normal and diseased TM samples (1.5 mm × 4.5 mm) along both
radial and circumferential directions for measurements of Young’s modulus at high strain
rates. The Young’s modulus data at high strain rates was determined to increase with
strain rate. The Young’s modulus of normal TM in the radial direction is
45.2–58.9 MPa and the modulus in the circumferential direction is 34.1–56.8 MPa under
high strain rates 300–2000 s–1. The Young’s modulus of diseased TM in the radial
direction is 63.4–79.2 MPa and the modulus in the circumferential direction is
33.1–42.8 MPa under high strain rates 300–1300 s–1.The values of normal TMs are more
than twice of the modulus obtained at quasi-static loading condition, showing significant
rate-dependence or viscoelastic behaviour of TMs. These properties are modelled with
the consideration of the TM as a linear viscoelastic material and fitted into a standard
linear solid model. The Young’s relaxation modulus was obtained and was converted into
complex Young’s modulus in frequency domain. The conversion indicates that the
Young’s modulus falls into the range 45.2–58.9 MPa under frequency ~300–2000 Hz.
The magnitude of the complex modulus of a normal TM in the radial direction is
determined to be 43.9 MPa at 890 Hz, close to the modulus of 40 MPa reported by
Kirikae (1960). The TM in the circumferential direction shows more pronounced
viscoelastic behaviour than in the radial direction. The diseased TM shows more
pronounced viscoelastic behaviour than normal TM in the radial direction and less
pronounced viscoelastic behaviour than normal eardrums in the circumferential direction.
The TM specimens in the radial and circumferential directions broke at ultimate strains
38.7 ± 8.7% and 32.7 ± 10.2%, respectively. The diseased TM specimens in the radial
20 H. Luo et al.

and circumferential directions broke at ultimate strains 36.6 ± 9.4% and 30.8 ± 6.1 %,
respectively.

Acknowledgements

We acknowledge the support of NSF (CMMI-0510563) and NIH

(NIDCDR01DC006632).

References
Chen, W., Lu, F. and Cheng, M. (2002) ‘Tension and compression tests of two polymers under
quasi-static and dynamic loading’, Polym. Test., Vol. 21, pp.113–121.
Chen, W., Zhang, B. and Forrestal, M.J. (1999) ‘A split Hopkinson bar technique for
low-impendance materials’, Exp. Mech., Vol. 39, pp.81–85.
Cheng, M. and Chen, W. (2003) ‘Experimental investigation of the stress-stretch behavior of
EPDM rubber with loading rate effects’, Int. J. Solids Struct., Vol. 40, pp.4749–4768.
Cheng, T. and Gan R.Z. (2007) ‘Mechanical properties of anterior malleolar ligament from
experimental measurement and material modelling analysis’, Biomech. Model Mechanobiol.,
Vol. 7, pp.387–394.
Cheng, T., Dai, C. and Gan, R.Z. (2007) ‘Viscoelastic properties of human tympanic membrane’,
Ann. Biomed. Eng., Vol. 35, pp.305–314.
da Costa, S.S., Paparella, M.M., Schachern, P.A., Yoon, T.H. and Kimberley, B.P. (1992)
‘Temporal bone histopathology in chronically infected ears with intact and perforated
tympanic membranes’, Laryngoscope, Vol. 102, pp.1229–1236.
Dai, C. and Gan, R.Z. (2008) ‘Change of middle ear transfer function in otitis media with effusion
model of guinea pigs’, Hear. Res., August 2008, Online published.
Dai, C., Wood, M.W. and Gan, R.Z. (2008) ‘Combined effect of fluid and pressure on middle ear
function’, Hear. Res., Vol. 236, pp.22–32.
Daphalapurkar, N.P., Dai, C., Gan, R.Z. and Lu, H. (2008) ‘Characterization of the linearly
viscoelastic behavior of human tympanic membrane by nanoindentation’, J. Mech. Behav.
Biomed. Mater., DOI: 10.1016/j.jmbbm.2008.05.008.
Dirckx, J.J. and Decraemer, W.F. (2001) ‘Effect of middle ear components on eardrum quasi-static
deformation’, Hearing Res., Vol. 157, pp.124–137.
Doner, F., Yariktas, M., Dogru, H., Uzun, H., Aydin, S. and Delibas, N. (2003) ‘The biochemical
analysis of tympanosclerotic plaques’, Otolaryngol, Head Neck Surg., Vol. 128, pp.742–745.
Eiber, A. and Schiehlen, W. (1996) ‘Reconstruction of hearing by mechatronical devices’, Robot,
Autonom Syst., Vol.19, pp.199–204.
Emri, I., von Bernstorff, B.S., Cvelbar, R. and Nikonov, A. (2005) ‘Re-examination of the
approximate methods for interconversion between frequency- and time-dependent material
functions’, J. Non-Newtonian Fluid Mech., Vol. 129, pp.75–84.
Fay, J., Puria, S., Decraemer, W.F. and Steele, C. (2005) ‘Three approaches for estimating the
elastic modulus of the tympanic membrane’, J. Biomech., Vol. 38, pp.1807–1815.
Ferris, P. and Prendergast, P.J. (2000) ‘Middle-ear dynamics before and after ossicular
replacement’, J. Biomech., Vol.33, pp.581–590.
Fung, Y.C. (1993) Biomechanics: Mechanical Properties of Living Tissues, 2nd ed., Springer, New
York.
Gaihede, M., Liao, D. and Gregersen, H. (2007) ‘In vivo a real modulus of elasticity estimation of
the human tympanic membrane system: modelling of middle ear mechanical function in
normal young and aged ears’, Phys. Med. Biol., Vol. 52, pp.803–814.
 A comparison of Young’s modulus 21

Gan, R.Z., Feng, B. and Sun, Q. (2004) ‘Three-dimensional finite modelling of human ear for
sound transmission’, Ann. Biomed. Eng., Vol. 32, pp.847–859.
Gan, R.Z., Sun, Q., Feng, B. and Wood, M.W. (2006) ‘Acoustic-structural coupled finite element
analysis for sound transmission in human ear-pressure distributions’, Med. Eng. Phys.,
Vol. 28, pp.395–404.
Gray, G.T. (2000) ‘Classic split Hopkinson pressure bar technique’, Mechanical Testing and
Evaluation, ASM, Vol. 8, pp.462–476.
Huang, G., Daphalapurkar, N.P., Gan, R.Z. and Lu, H. (2007) ‘A method for measuring linearly
viscoelastic properties of human tympanic membrane using nanoindentation’, J. Biomech.
Eng.-Trans. ASME, Vol. 130, 014501-1.
Hunter, L.L and Margolis, R.H. (1997) ‘Effects of tympanic membrane abnormalities on auditory
function’, J. Am. Acad. Audiol., Vol. 8, pp.431–446.
Jaisinghani, V.J., Paparella, M.M., Schachern, P.A. and Le, C.T. (1999) ‘Tympanic
membrane/middle ear pathologic correlates in chronic otitis media’, Laryngoscope, Vol. 109,
pp.712–716.
Kirikae, I. (1960) The Structure and Function of the Middle Ear, University of Tokyo Press,
Tokyo.
Knauss, W.G., Emri I. and Lu, H. (2008) ‘Mechanics of polymers: viscoelasticity’, in Sharpe, Jr.
and William, N. (Eds.): Handbook of Experimental Solid Mechanics, pp.49–95, Springer,
USA, ISBN 978-0-387-26883-5.
Lim, D.J. (1995) ‘Structure and function of tympanic membrane: a review’, Acta Oto-rhino-
laryngolog. Belg., Vol. 49, pp.101–115.
Lu, H., Luo, H. and Gan, R. (2007) ‘Measurements of Young’s modulus of human eardrum at high
strain rates using a miniature split Hopkinson tension bar’, Proc. 2007 SEM Ann. Conf.,
Vol. 1, pp.190–194.
Luo, H., Dai, C., Gan, R. and Lu, H. (2008a) ‘Measurement of Young’s modulus of human
tympanic membrane at high strain rates’, J. Biomech Eng. – Trans ASME, submitted.
Luo, H., Chen, W. and Lu, H. (2008b) ‘Tensile behavior of a polymer film at high strain rates’,
Proc. 2008 SEM Ann. Conf., 2–5 June, Orlando, Florida, paper #253 in conf. CD.
Luo, H., Lu, H. and Leventis, N. (2006) ‘The compressive behavior of isocyanate-crosslinked silica
aerogel at high strain rates’, Mech. Time-Depend. Mater., Vol. 10, pp.83–111.
Oktay, M.F., Cureoglu, S., Schachern, P.A., Paparella, M.M., Kariya, S. and Fukushima, H. (2005)
‘Tympanic membrane changes in central tympanic membrane perforations‘, Am. J.
Otolaryngol, Vol. 26, pp.393–397.
Puria, S. (2003) ‘Measurements of human middle ear forward and reverse acoustics: implications
for otoacoustic emissions’, J. Acoust. Soc. Am., Vol. 113, pp.2773–2789.
Ruah, C., Penha, R., Schachern, P. and Paparella, M. (1995) ‘Tympanic membrane and otitis
media’, Acta Oto-rhino-laryngologica Belg., Vol. 49, pp.173–180.
Saraf, H., Ramesh, K.T., Lennon, A.M., Merkle, A.C. and Roberts, J.C. (2007) ‘Mechanical
properties of soft human tissues under dynamic loading’, J. Biomech., Vol. 40, pp.1960–1967.
Shergold, O.A., Fleck N.A. and Radford, D. (2006) ‘The uniaxial stress versus strain response of
pig skin and silicone rubber at low and high strain rates’, Int. J. Impact Eng., Vol. 32,
pp.1384–1402.
Song, B., Chen, W., Ge, Y. and Weerasooriya, T. (2007) ‘Dynamic and quasi-static compressive
response of porcine muscle’, J. Biomech., Vol. 40, pp.2999–3005.
von Békésy, G. (1960) Experiments in Hearing, McGraw Hill, New York.
von Unge, M., Decraemer, W.F., Dirckx, J.J. and Bagger-Sjoback, D. (1995) ‘Shape and
displacement patterns of the gerbil tympanic membrane in experimental otitis media with
effusion’, Hear. Res., Vol. 82, pp.184–196.
 22 H. Luo et al.

Voss, S.E., Rosowski, J.J., Merchant, S.N. and Peake, W.T. (2001) ‘Middle-ear function with
tympanic-membrane perforations, I. Measurements and mechanisms’, J. Acoust. Soc. Am.,
Vol. 110, pp.1432–1444.
Wang, X., Cheng, T. and Gan, R.Z. (2007) ‘Finite-element analysis of middle-ear pressure effects
on static and dynamic behavior of human ear’, J. Acoust. Soc. Am., Vol. 122, pp.906–917.
Weiss, J.A., Gardiner, J.C. and Bonifasi-Lista, C. (2002) ‘Ligament material behavior is non-linear,
viscoelastic and rate-independent under shear loading’, J. Biomech., Vol. 35, pp.943–950.
Wilmoth J.G., Schultz, G.S. and Antonelli, P.J. (2003) ‘Tympanic membrane metalloproteinase
inflammatory’, Otolarygol. Head Neck Surg., Vol. 129, pp.647–654.
Yoon, T.H., Schachern, P.A., Paparella, M.M. and Aeppli, D.M. (1990) ‘Pathology and
pathogenesis of tympanic membrane retraction’, Am. J. Otolaryngol., Vol. 11, pp.10–17.
Yost, W.A. (2007) Fundamentals of Hearing: An Introduction, pp.103–120, 5th ed., Elsevier Inc.

View publication stats