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Elasticity and viscosity of surface tissues of the human chest wall

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DOI: 10.15593/RJBiomech/2017.2.06

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 ISSN 1812-5123. Russian Journal of Biomechanics. 2017. Vol. 21, No. 2: 164-174

DOI: 10.15593/RJBiomech/2017.2.06

ELASTICITY AND VISCOSITY OF SURFACE TISSUES

OF THE HUMAN CHEST WALL

A.I. Dyachenko1–4, M.V. Veremyeva1, 2, E.S. Fomina1, 2

1
Prokhorov General Physics Institute of Russian Academy of Sciences, 38 Vavilova Street, Moscow, Russia, e-mail:
mar33567736@yandex.ru
2
Bauman Moscow State Technical University, 14 Brigadirskiy Pereulok, Moscow, Russia, e-mail:
fomina153@mail.ru
3
Institute of Biomedical Problems of Russian Academy of Sciences, 76 а Khoroshevskoe Shosse, Moscow,
Russia.
4
Moscow Institute of Physics and Technology, 9 Institutskiy Pereulok, Dolgoprudniy, Russia, e-mail: alexander-
dyachenko@yandex.ru

Abstract. The purpose of this work was a study of viscoelasticity of the human chest wall
soft tissues. By virtue of vibrational viscoelastometer VVEM-5, we have measured
elasticity and viscosity of soft tissue surface layer beneath an indenter, oscillating at a
frequency 40 Hz. Voight rheological model was accepted. A shear elasticity modulus µ
and a shear viscosity η of a soft tissue surface layer attached to a rigid basement were
obtained. Twelve normal male volunteers aged from 19 to 22 years participated in the
study. In 6 different locations of the right chest wall surface of each volunteer, we
measured viscosity, elasticity and thickness of the soft tissue layer. To provide more vivid
presentation of soft tissue elasticity and viscosity distributions over chest wall surface, we
presented elasticity and viscosity in the original dimensional data as well as in relative
values normalized to mean elasticity and viscosity of each test subject. In total, we
obtained 323 values of elasticity and viscosity of chest wall surface tissues. Distributions
of elasticity and viscosity were not normal, they resembled log-normal distributions. In all
test subjects, there were the same five locations of measurements. We searched if there
are differences of elasticity and viscosity in those five locations and observed these
differences. Viscosity of chest wall surface tissues located closer to an axillary crease
was greater than viscosity in other studied positions over chest wall surface. We
considered effects of chest wall surface tissue viscoelasticity on measurements of soft
tissue vibrations by virtue of contact sensors.

Key words: shear elasticity and viscosity, viscoelastometer, surface soft tissues, chest
wall, surface vibration measurement, vibrational viscoelastometry.

INTRODUCTION
Rheological properties of biological tissues determine the stress-strain reaction of these
tissues on exposure to different mechanical loads on the body surface. The main rheological
parameters are the elasticity and viscosity of tissues that are considered in the framework of
some rheological model. These parameters are important for diagnostic purposes. By a
deviation of the parameters from the "normal" values or by dynamics of their change, a
progression or disease treatment can be evaluated [5, 11, 15, 18].
The viscoelastic properties of human chest wall surface tissues in many respects
determine the reaction of the chest to percussion and vibration impact. At the acoustic

© Dyachenko A.I., Veremyeva M.V., Fomina E.S., 2017

Alexander I. Dyachenko, Ph.D., Head of Physics of Living System Laboratory, Moscow
Maria V. Veremyeva, Student of Biomedical Technics Faculty, Moscow
Ekaterina S. Fomina, Student of Biomedical Technics Faculty, Moscow
 Elasticity and viscosity of surface tissues of the human chest wall

frequencies, the viscoelastic properties affect the sound propagation through tissues and
applicability of acoustic methods for diagnostics [3].
To describe the viscoelastic properties of soft biological tissue, different rheological
models are applied, and different experimental methods are used to measure the parameters of
these models [16]. Note that different methods may give very different values of viscoelastic
parameters [4, 16]. For example, muscle stretching methods give several orders of the
Young's modulus magnitude greater than the indentation methods. This follows from the
smaller size of deformed areas in the vicinity of pressed indenter and from lighter overflow of
extracellular fluid as compared with difficult overflow in large sizes of stretched tissue [16].
At large deformations, it is necessary to use nonlinear models of soft tissue. Small
deformations allow us to apply linear models, in which the magnitude of stresses and strains,
as well as their time derivatives are related by linear equations. On rheological diagrams, such
models are presented as a combination of several elastic and viscous elements. Examples of
such models are the Voigt viscoelastic model, Maxwell, Kelvin (also called Kelvin–Zener),
Burger’s, Brankov’s models containing from two to five elements [10]. To solve the problem
of parameter identification, it is expedient to choose simple models describing the main
features of a tissue under load. The simplest models are the Maxwell and Voigt models, each
of which contains one elastic and one viscous element. Both models describe properties of
elasticity and viscosity, the presence of a phase shift between the strains and stresses, but not
adequately describe the behavior of soft tissues under certain conditions. Voigt model
describes the fluidity to a certain strain at constant stress, but in this model it can not be a
stress relaxation at a constant strain. In the Maxwell model at constant stress, deformation
increases indefinitely, and at a constant strain stress relaxes to zero. To describe the properties
of the muscle tissue with covering by skin and subcutaneous tissues, the Voigt model is the
most appropriate [6, 8], although Maxwell model is also applied [10]. We use the Voigt
model further.
In the non-invasive methods of vibration diagnostics [4–6, 8, 9], the vibrations are
created on the surface of soft tissue, then the surface impedance is measured [9]; another kind
of non-invasive methods is analysis, either by ultrasound or other means, of vibration of tissue
located deep below the surface [6].
Earlier in the literature, the results of individual measurements of the viscoelastic
properties of the human chest wall surface soft tissues were presented [5, 12] but systematic
research, especially in different parts of the thorax surface, have not been considered.
The purpose of our work is to measure the elasticity and viscosity of soft tissues in
several areas on the surface of the chest of healthy men by the impedance method. Results of
this study were previously presented at the conference [13].

MATERIALS AND METHODS

Method of measurement
The viscoelastic characteristics of tissues were determined using a hardware-software
complex "Vibration Viscoelastometer (VVEM-05)" developed by E.M. Timanin [9]. In this
device, specialized vibration sensor is easily pressed to the surface of the body by indenter.
Cylindrical indenter (diameter 8 mm) oscillates with a frequency 40 Hz and an amplitude
about 0.1 mm. Vibration sensor consists of an accelerometer for registering indenter
acceleration A, as well as force sensors for registration of indenter’s static pressure force
exerted on the tissue F and tissue resistance force to indenter oscillatory motion P. For each
period of indenter oscillation, the real and imaginary parts of the dynamic stiffness K of
tissues are determined

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 A.I. Dyachenko, M.V. Veremyeva, E.S. Fomina

−ω2 P
K= , (1)
A
where ω is an angular frequency of indenter vibrations. The effective modules of shear
elasticity E and viscosity V in a model of a viscoelastic half-space (for Voigt body) are
determined:
Re K
E= , (2)
4d
Im K
V= , (3)
4d ω
here d is a diameter of indenter. The force of the indenter static pressure on tissue F is
recorded synchronously with the values of E and V and is used to stabilize the conditions of
their measurement by audio biofeedback signalling due to F.
If a tissue layer is thick (i.g. semi-infinite space) and has uniform mechanical
properties, the effective shear modules of elasticity E and the viscosity V are respectively
equal to the shear modules of elasticity µ and viscosity η tissue. If a tissue layer is uniform
and has a known finite thickness h, then the elastic µ and the viscosity η at modules of tissue
are associated with the values E, V, h, d by more complex relationships. They were calculated
by VEM5 software included in the hardware-software complex VVEM-05, by the model of a
single layer of Voigt tissue with constant thickness, located on a flat hard surface. Compared
with compliant layer of soft tissue (skin, subcutaneous fat), the rib cage lying under this layer
is solid. Although the surface of the rib cage is not completely flat, the distance between the
ribs is several times more than the diameter of the indenter and "depth" of intercostal recesses.
Therefore, the model of soft tissue layer positioned on a solid foundation is applicable to the
lateral surface of the chest.
The thickness of the soft tissue layer on the chest wall surface was determined as half-
thickness of the fold obtained after easy pinching of tissues.

The subjects and areas of viscoelasticity measurement

Measurements of viscoelastic properties of the chest wall soft tissues were performed
involving healthy volunteers, the group included 12 male subjects with age 19–22 years,
height 179.8 ± 6.9 cm, weight 72.6 ± 8.9 kg, body mass index 22.4 ± 2.1 kg/m2. The
circumference of the chest after a maximum inspiration, normal and maximum expiration
were 96.3 ± 5.6 cm; 91.2 ± 6.7 cm; 88.4 ± 6.9 cm, respectively.
In each volunteer, tissue elasticity and viscosity were measured in intercostal spaces in
six different points located on the right side surface of the chest wall. One point, further called
the "central", was chosen over intercostal space at a certain distance from the axillary crease,
which was from 8 to 13 cm vertically and from 0 to 3 cm across. Then, around the "central"
point, positions of the other four major points were chosen above the intercostal spaces as
well (Fig. 1).
Along the same intercostal space, where the "central point" was located, at distances
of 5.1 ± 0.5 cm and 5.0 ± 0.8 cm (mean ± SD) "along up" and "along down" points were
placed respectively. Perpendicular to the intercostal space, where "central" point was located,
at distances of 4.5 ± 1.0 cm and 4.6 ± 1.0 cm from the "central" point "across up" and "across
down", the points were located respectively. For each volunteer, except the five points
arranged systematically on the right side of the chest, viscoelastic properties of tissues were
measured in another arbitrarily chosen point on the right side of the chest. Since arrangement
of measurement points of the subjects slightly differed, then in the analysis of group data we
will talk about their respective fields on the surface of the right side of the chest.

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 Elasticity and viscosity of surface tissues of the human chest wall

Fig. 1. The typical arrangement of the five main

points of measurement of the viscoelastic properties
of the chest wall surface tissues. The numbers refer
to the points: 1 is "along up", 3 is "along down", 2 is
"across up", 4 is "across down", 5 is "central point"

Measurements and data processing

Operator pressed the vibrosensor to the selected points of the surface of the chest with
a pressing force of 20 ± 2 g. At each point from two to six tests were conducted (recording the
values E and V with the total duration of 2–3 minutes. In each test from 10 to 400 values of
the quantities E and V were obtained, on average about 100 values per test. In each test,
the program VEM-5 calculated mean E, V values of the test and standard deviation SD
values of E, V.
Further, according to each test data, program VEM-5 determined shear modulus µ and
shear viscosity η in a single-layer model of a viscoelastic soft tissue (Voigt body), set on a
solid surface.
Then for each point of the chest wall surface and for each subject, the characteristics
of distributions of values E, V, µ, η were found (maximum and minimum values, medians,
quartiles, mean values, interquartile range and SD).
Further, obtained median and the mean values of E, V, µ, η, the interquartile range and
SD values of E, V, µ, η determined for each point of the chest surface for each person were
considered as the primary experimental data. For statistical analysis of these data,
nonparametric methods and application package Statistica 8 were used. As the border of
statistical significance the value of P = 0.05 was selected.

RESULTS
In total for 12 people in all six (five major and one extra) areas of the chest surface,
323 measurements of viscosity and elasticity were carried out.
For a more visual representation of the character of the tissue elasticity and viscosity
distribution on the surface of the chest, the values of elasticity and viscosity are presented in

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 A.I. Dyachenko, M.V. Veremyeva, E.S. Fomina

the form of a relative, "normalized" values. To do this for each person, the mean individual E,
V were found using all values measured at the surface of the chest, i.e. Esrind , Vsrind for each
subject. Then, we found
E
En = , (4)
Esrind
V
Vn = , (5)
Vsrind
which were named "normalized values E, V".
The results of all obtained data are shown in Table. The data spread is caused mainly
by differences in elasticity and viscosity in different areas of the chest surface for different
people. For a fixed measurement point for one person on average for all test points and
subjects the interquartile ranges are 0.76 kPa, 1.37 Pa·s, 0.31 kPa and 0.64 Pa·s for E, V, µ, η
respectively. It can be seen that it is considerably smaller than the corresponding interquartile
ranges in Table.
Distributions of viscosity and elasticity parameters (E, V, µ, η and the corresponding
normalized parameters) are not normal (Gaussian) and better fit the log-normal functions. An
assessment of the "chi-squared" test showed that the probability of compliance of the µ
distribution with normal distribution is less than 10–5, and the probability of agreement with
the log-normal distribution is equal to 0.19. For the same value of µ according to
Kolmogorov–Smirnov test, the statistic criterion D is equal to 0.041 (difference not
significant, p > 0.05) and 0.099 (significant difference, p < 0.01) for the log-normal and
normal distributions respectively. Distributions of the normalized and non-normalized
elasticity are shown in Figs. 2, 3. It is seen that the distributions are not the normal, they are
more like the log-normal.
Next, we will consider the data obtained in the five main areas of the chest surface.
The distributions of the normalized values of elasticity and viscosity in these areas are shown
in Fig. 4.

The effective modules of shear elasticity E and viscosity V, the modules of shear elasticity µ and
viscosity η of tissue, also values normalized to the individual mean values of these parameters
En , Vn , µ n , ηn , , in total there are 323 measurements for 12 subjects in six points of the chest wall

Variable Mean Меdian Min Маx LQ HQ SD HQ–LQ

E, kPa 4.3 3.8 0.9 17.4 2.4 5.6 2.4 3.2
V, Pa·s 9.1 8.4 2.3 41.6 6.5 10.8 4.0 4.23
µ, kPa 1.39 1.16 0.16 5.70 0.83 1.72 0.84 0.89
η, Pa·s 2.9 2.7 0.10 17.7 1.70 3.7 2.0 2.0
En 1.00 0.91 0.30 3.39 0.71 1.17 0.42 0.46
Vn 1.00 0.95 0.35 2.23 0.82 1.13 0.29 0.31
µn 1.00 0.95 0.22 2.80 0.73 1.18 0.41 0.45
ηn 1.00 0.95 0.09 2.64 0.71 1.20 0.42 0.49

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 Elasticity and viscosity of surface tissues of the human chest wall

Number of measurements

µn, rel. un.

Fig. 2. The histogram of distribution of the normalized values of the

shear modulus and the best normal 1 and the lognormal 2
approximation curves (n = 323)
The density of the probability distribution

µ, kPa

Fig. 3. The probability density function of distribution of values µ

In the "along up" area, viscosities are mainly located in the right half of the figure
plane, and in the "central" area they are shifted to the left. In the "across down" area, only one
value En is greater than one, the other values are arranged in the bottom half of the figure
plane. These findings suggest that in different areas properties of the chest wall surface tissues
may vary.
To analyze the statistical significance of differences in the viscoelastic properties of
the soft tissue on the chest surface, we used the Friedman analysis of variance by ranks -
nonparametric version of repeated measures ANOVA [1, 14].

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 A.I. Dyachenko, M.V. Veremyeva, E.S. Fomina

Fig. 4. The normalized values of elasticity and viscosity in five areas on the
right side of the chest surface: "along up" (1), "across up" (2), "along down"
(3), "across down" (4), "central" (5)

Using the Friedman test, the values obtained at different points from one subject were
considered as repeated measurements at one and the same person. Values determined in the
same area of right side of the chest from all 12 subjects form a sample consisting of
12 numbers. Values determined in another area from the same 12 people form another
sample. Therefore, we have related samples. And it was continued in all areas on the surface
of the chest. Finally, we got five data samples for each of the considered parameters E, V, µ, η
and their corresponding normalized values. Samples of normalized values are shown in Fig. 5.
The probability of the null hypothesis (that the measured values in all five areas on the
surface of the chest belong to the same general set of data) for the values E, V, µ, η are
p = 0.16; 0.0044; 0.47; 0.026 respectively. Concordance coefficients are 0.14; 0.32; 0.07; 0.23
respectively. The probability of the null hypothesis and the concordance coefficients for the
normalized values are similar to nonnormalized. In this case, for the values V, Vn and η, ηn the
probabilities are 0.0044 and 0.026, which are less than 0.05. It assumes that the data are not
included in the same general set, i.e. these parameters vary in different regions of the thorax.
Fig. 5 shows that the viscosity in the "along up" area is larger than in other areas, and in a
"center" it is less than in other areas.
Application of Friedman's test to the data, in which one of the areas is excluded,
indicates that for the parameters V, Vn after exclusion of the area "along up" a null hypothesis
probability is greater than 0.05 and after exclusion of any other region, except the "along up",
the null hypothesis probability is less than 0.05. Thus, the values of V, Vn parameters in the
"along up" differ from values in other areas, which are not statistically different between

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 Elasticity and viscosity of surface tissues of the human chest wall

Fig. 5. The values of normalized values E, V, µ, η in five areas of the right half of
the chest: "along up" (1), "across up" (2), "along down" (3), "across down" (4),
"center" (5)

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 A.I. Dyachenko, M.V. Veremyeva, E.S. Fomina

Fig. 5. Ending

themselves, including the "center" area. Similar estimates for the parameters η, ηn show that
the exclusion of any area (including the "along up" and "central") increases the probability of
the null hypothesis to a value greater than 0.05, so it cannot be specified a certain area that is
significantly different from the rest in the parameters η, ηn.
In summary, Friedman’s test indicates on regional differences in the effective modules
of viscosity V, Vn and modules of viscosity η, ηn.
In order to clarify a difference between area "along up" and other areas, all these
parameters were compared in pairs: the area "across up" and one of the other four areas,
applying the Wilcoxon test with Bonferroni correction [1, 14]. Since there were 4
comparisons, the Bonferroni correction consisted that the probability of the null hypothesis
was considered significant, satisfying condition 4·p < 0.05. It was revealed that the values of
the parameters V, Vn in the area "along up" are significantly higher than "across down" and
"center" areas. But values of η, ηn in the area "along up" significantly higher than in the area
"center". The rest of the areas are not statistically different between themselves in other
considered parameters.

DISCUSSION
The obtained results show that there are regional differences in viscosity of the chest
wall surface tissues. Apparently, this is due to regional differences of properties of the skin
and/or subcutaneous fat. Histological studies may reveal the causes for these differences.
As we have already pointed out in the introduction, in the literature there are only
scattered data of the viscoelastic properties of the chest wall surface tissues. Viscoelasticity
value obtained earlier by the same method and instrument, which were used in this study,
correspond to the new data.
Dynamic surface tissues modulus was measured at several points of surface tissues of
one subject by registration of tissue resistance to torsional vibrations [5]. In doing so, tests
were carried out one by one at each point of the surface. Modulus values differed in
magnitude by five orders in different points of the chest, practically it does not enable to
compare our results with the results of [5].
So, we compared the viscosity and elasticity values of the chest wall surface tissues
obtained in our study, with the values found in other areas of the body surface.

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 Elasticity and viscosity of surface tissues of the human chest wall

Using the Voigt body and the same model of viscoelastometer like in our research, the
characteristic values of elasticity E and viscosity V were found for different muscles covered
with skin and subcutaneous fat (the trapezius muscles of the neck, biceps of shoulders,
quadriceps of thighs, calf muscles), in the case of relaxation and after the muscular load, in
normal state and at Parkinson's disease, constituting about 5–30 kPa and 10–90 Pa·s
respectively [8]. The obtained values of the elasticity and viscosity of the chest wall surface
tissues are close to the low limit of specified range for the muscles.
Determination of the mechanical properties of viscoelastic layer of Voigt tissue based
on the impedance measurements in the frequency range from 120 to 260 Hz [6] for forearm
surface tissues using stamp with diameter 8 mm gave the value of Young's modulus 8kPa.
Neglecting the small tissue volume compressibility, at which the shear modulus is three times
less than the Young's modulus, from the data [6], we obtained µ = 2.7 kPa. For the same
stamp from data of the same article, we obtained η = 2.9 Pa·s. Thus, the magnitude of the
shear viscosity of the chest wall surface tissue, that we have obtained, and the shear viscosity
of the forearm tissue estimated in [6] are the same.
The obtained values of viscosity and elasticity of the chest wall surface tissues may be
helpful in solving the problems of diagnostics of these tissue state. Diagnostic significance of
viscoelasticity was shown for many kinds of tissues [10, 11, 16–18]. If there is more than
50% of malignant cells in prostate tissues, their Young's modulus is several times greater than
normal, the difference increases with frequency by 2.1 times at 0.1 Hz and by 2.5 times
at 150 Hz [15]. On average, a complex Young's modulus of the malignant tissue is in
3.1 times greater than modulus of the benign tissue for the same prostate [18]. It should be
noted that in [15, 18] a modified Voigt model was used.
The viscoelastic properties of surface tissues are important not only for assessing the
state of tissue. They in many ways determine possibility of registration of the surface tissue
vibration using contact sensors [3]. Viscoelastic tissues present an viscoelastic suspension, on
which the sensor case of a certain weight is housing [3]. Therefore, vibrations of sensor are
different from tissue vibrations which were before attachment of the sensor. The presence of
the viscoelastic suspension of the sensor case is not always taken into account in the analysis
of possibility of registration of lung sounds using contact sensors [2]. Estimates have shown
that the viscoelastic properties of the chest wall surface tissue quantitatively and qualitatively
affect the amplitude-frequency and phase-frequency characteristics of contact sensors in the
frequency range of lung sounds and percussion vibrations of the chest [13].
Also viscoelastic properties of surface tissues are important for assessing the sound
field arising on the tissue surface by the impact of surface or deep sources of acoustic
vibrations.

CONCLUSIONS
Viscoelasticity of human chest wall surface tissues was measured and the potential
distortion of contact methods of tissue vibration registration was estimated. Using vibration
viscoelastometer VVEM-5, the viscosity V and the elasticity E of human chest wall surface
tissues were measured at frequency 40 Hz. Individual differences of elasticity and viscosity
parameters and local differences in viscosity of tissues were identified. The problem of the
effect of surface tissue viscoelasticity on results of tissues vibration measurements using
contact sensors was discussed.

ACKNOWLEDGMENTS
The work was supported financially by the Russian Foundation for Basic Research
(project No. 15-01-06246).

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 A.I. Dyachenko, M.V. Veremyeva, E.S. Fomina

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Received 23 March 2017

174 ISSN 1812-5123. Russian Journal of Biomechanics. 2017. Vol. 21, No. 2: 164-174

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