PIEZOELECTRIC PROPERTIES OF DRY HUMAN SKIN

IEEE Transactions on Electrical Insulation Vol. EI-21 No.3, June 1986
PIEZOELECTRIC PROPERTIES OF DRY HUMAN SKIN
D. De Rossi, C. Domenici
Centro "E. Piaggio"
Universita di Pisa
and
Istituto di Fisiologia Clinica del C. N. R.
Pisa, Italy
and
P. Pastacaldi
Divisione di Chirurgia Plastica
USL 12, Pisa, Italy
ABSTRACT
Mechanoelectrical conversion properties of dry human skin
have been examined and their origin investigated in dermis,
epidermis and horny layer. Shear stress piezoelectricity
is observed in all three cutaneous sections. Piezoelectric
properties of dermis can be ascribed to its collagen structural
network, while the piezoelectric properties of epidermis
appear to originate from partially oriented a-helical
keratin-like tonofibrils. The highest piezoelectric coefficients
have been found in horny layer samples. The values
of thickness-compression piezoelectric coefficients were so
low that they were not discernable from the intrinsic noise
of the measuring system. Although thermally generated
currents have been observed in the course of thermal pulse
experiments, no evidence of relevant contributions from
pyroelectric (polar) responses has been noticed in all
cutaneous compartments.
INTRODUCTION
Different biological tissues show the ability to convert
mechanical and thermal stimuli into electric signals
[1]. Extensive studies are available [2], examining
mechanoelectrical properties of bone both in the
dry and in the moist, physiological state.
The hypothesis ascribing bone mechanoelectric transduction
to piezoelectric properties of the collagenous
structure in the dry state and to electrokinetic phenomena
(streaming potentials) in the moist state nowadays
has a large consensus [3]. The eventual role of
these phenomena on bone regrowth and healing is presently
largely debated. However, the mechanoelectrical
properties of human skin have been very little studied
and their origin is largely unknown.
Shamos and Lavine [41 have reported observations of
direct piezoelectric effects in dry, whole human skin
samples from the forearm and callus from the sole.
These authors, by analogy with the behavior of bone
and tendons, ascribe the piezoelectric properties of
human skin to oriented collagen fibrils in dermis.
Athenstaedt et al. [5] have examined fresh human
0018-9367/86/0600-0511$01.00 @ 1986 IEEE
skin samples both in vitro and in vivo, reaching the
conclusion that the observed electrical signals obtained
in response to mechanical or thermal stimuli are
intrinsically of piezo- and pyroelectric nature. The
same authors reported measurements performed on dry
skin observing a reduced (20 to 60% less) mechanoelectrical
activity compared to moist samples.
It is worthwhile noting that, while Shamos and Lavine
ascribe the piezoelectric properties of human skin to
dermal collagen network, Athenstaedt et al. suggest
that these properties originate-from uniaxially oriented
polar keratin filaments in the basal cells layer of
epidermis. To clarify the nature of mechanoelectrical
transduction phenomena in human skin and to comprehend
better their microscopic origin, a systematic study of
these properties both in the dry and moist state has
been undertaken. We report here results obtained on
dry human skin samples.
SAMPLE PREPARATION
511
Several samples of human skin from breast, thigh, pre-
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5 I 2
puce, and callus from sole have been obtained from patients
undergoing plastic surgery. Prepuce samples
were used because they are almost entirely composed of
true epidermal tissue (the horny layer is virtually
absent).
The samples were rinsed in distilled water, cut into
circular shape (2 cm diameter) and separated into their
dermal, epidermal and horny layer components by microsurgical
operations. The samples were dehydrated in
vacuum for 12 h.
Typical dehydrated sample thickness was 300 to 400
vim for whole epidermis, 100 to 200 vm for horny layer
and 300 to 500 vm for dermis. Electrodes made of conducting
silver-loaded paint (Acheson Colloiden B.V.,
Scheemda, Holland) were applied by brushing on the surfaces
of the samples used in piezoelectric measurements.
Colloidal graphite electrodes were sprayed on the samples
used in thermal pulse experiments. After application
of the electrodes the samples were again vacuum
dried for two hours.
EXPERIMENTAL METHODS
Dry skin is an anisotropic material which contains
oriented polar crystallites in an amorphous organic
matter, and its piezoelectric characterization would in
principle require determination of 18 components of the
piezoelectric coefficient third-rank tensor d.. (the
reduced matrix notation [6] has been used in iie present
work). di are the proportionality constants between
the applied mechanical stress T and the generated
electrical polarization P:
i
6
=1 i _j
IEEE Transactions on Electrical Insulation Vol. EI-211 No3` June 1986
i (l
When studying piezoelectric properties of biopolymers
it is customary [7] to define a cartesian coordinate
system where the z-3 axis coincides with the assumed
prevailing orientation of electric dipoles, which for
a-helical proteins, is colinear with the helix long
axis. The x_1 axis is assumed to be perpendicular to
to the skin surface.
Following these definitions, d14 represents the
shear piezoelectric coefficient obtained by measuring
the electrical charges on electrodes deposited on skin
surfaces, generated by applying an uniaxial mechanical
stress in the skin plane directed 450 from the preferential
orientation of piezoelectric protein fibers.
Because skin shows relaxational dispersion [8], the
d coefficients are in fact complex quantities having
an in-phase d' real part and an out-of phase d" complex
part. A frequency dependence of the piezoelectric coefficients
in this case has to be expected.
Angular dependence in the plane of the samples (dermis,
true epidermis and horny layer) of d' and of the
real part of the elastic modulus c' have been measured
at 25°C and at the frequencies of 1, 10, and 30 Hz using
a Rheolograph Piezo (Toyo Seiki Seisaku-sho, Tokyo,
Japan). The dependence of real d' and imaginary part
d" of shear piezoelectric coefficient on temperature
from -100°C to 1000C at 10 Hz have also been measured,
using the same apparatus.
Thickness-compression piezoelectric measurements
have been performed by applying square wave stress
pulses generated by a flat circular plastic pin, driven
by an electromagnetic shaker. Load readings have been
performed by means of a miniature load cell (Type 9201,
Kistler Instrumente AG, Winterthur, Switzerland) mechanically
in series with the sample, while charge generated
by skin samples were detected by means of a
charge amplifier (Type 5007, Kistler Instrumente AG,
Winterthur, Switzerland). Two different methods have
been used to determine the eventual pyroelectricity of
skin samples. The first method, also called the static
method [9], is the only one capable of giving absolute
values of the pyroelectric coefficient. The measurements
have been implemented using a Thermo Controller
Unit (Toyo Seiki, Seisaku-sho, Tokyo, Japan) where the
temperature has been raised at a rate of 2°C per minute.
The voltage appearing at the electrodes was measured
with a very high input impedance (1015 Q) voltmeter
built around a FET-input electrometer operational amplifier
(AD 515 J, Analog Devices, Norwood, MA, USA).
This method, however, is known to be effected by errors
related to voltages not of pyroelectric origin
which are spontaneously generated by the sample and by
voltages generated by any piezoelectric material when it
is nonuniformly heated (tertiary pyroelectric effect).
To provide an alternative measuring techniques, the
rectangular pulse heating method [9] has been used,
although this method is capable of providing only relative
values of the pyroelectric coefficient.
A sharply focused 50 W incandescent lamp was used as
light source and light pulses of 1 s duration were delivered
to the skin samples to change the temperature.
However, both the static method and the classical
rectangular pulse heating method are only capable of
providing pyroelectric informations integrated over the
sample thickness.
To probe the spatial distribution of polarization
across the thickness of the epidermis sample, as required
to evaluate the hypotesis of a pyroelectric activity
in the basal cell layer tonofibrils, the Collins'
thermal pulse method [10] has been used.
A very short (1 ms) duration light pulse, generated by
an electronic flash lamp, was delivered to the sample
located in a shielded, hermetic cell through a glass
window; voltage at the electrodes was amplified with the
Ad 515 J operational amplifier and recorded by means of
a 7912AD Tektronix transient recorder.
The physical basis of this method resides in producing,
by means of thermal diffusion, a transient inhomogeneous
strain across the sample, in order to measure
its inho-moc,neous pyroelectric res-ponsc. Altlhough the
information about the polarization distribution is convoluted
with a time-dependent temperature distribution,
a deconvolution process is typically applied to the experimental
data to obtain the first few Fourier coefficients
of the polarization distribution [11]. For
the purpose of the present work, however, we were only
interested to detect a limiting case of spatial distribution
of polarization inside epidermis where the pyroelectric
response may be eventually concentrated only
at one very superficial layer of the sample.
In this simple case, qualitative inspection of the
volatage-time responses obtained by alternating the side
of the sample in respect to the impinging light is sufficient
to determine eventual strong asymmetry in the
pyroelectricity spatial distribution [11].
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De Rossi et al.: Piezoelectric properties of dry human skin
Dermis
RESULTS
Typical recordings of the angular dependence of the
real part of the piezoelectric shear coefficient and
elastic modulus are shown in Fig. 1 for dermal samples.
Fig. 1: In-pZane anguZar dependence of the reaZ part
of eZastic modulus (c') and piezoeZectric shear coefficient
(d') for a sanple of dermis from the
breast.
The values of d'(max) at room temperature have been
found to be of the order of 0.05 to 0.1 pC/N.
The presence of one or two maxima in the in-plane
polar behavior of c' obtained for different samples
from different anatomical sites indicates slight preferential
uniaxial or biaxial orientation of collagen
fibrils in the dermal three-dimensional structural network.
The invariably observed bisinusoidal behavior of
d' polar response is similar to the one observed in
oriented collagen structures and uniaxially oriented
synthetic polypeptides [7].
This kind of anisotropy can be generally expressed
through the relation [12]
d' = 0.5 dl4sin(2e) (2)
In the case of prevailing uniaxial anisotropy, such as
shown in Fig. 1, for a composite piezoelectric material
where the degree of orientation is low, the following
expression can be used [12], assuming collagen to
originate piezoelectric activity:
d' = 0.5 d04 1cF sin[2(O -
0 )] (3)
where dC'4 is the shear piezoelectric coefficient for
the single crystallite, b the volume fraction of the
paracrystalline piezoelecYric component (collagen) in
the sample, Fc the degree of orientation of collagen
fibers, and 0c the angle of average direction of collagen
crystallites orientation.
Referring to Fig. 1, if we assume the angle of average
direction of collagen crystallites orientation corresponds
to the maximum of angular response of the real
part of elastic modulus, 8c=90 '. The relationship d(e)
should be hence represented by the function:
d' = 0.5d1c v F sin[2(O - 2J] (4)
As the maa itude of d 4 has been measured to be 6 pC/N
(18.2xlO- cgsesu) [13], the volume fraction of collagen
4v in dried dermis is approximately 0.75 [14] and the
measured d'(O) for dermis has been found to be 3.3xlO09
cgsesu, it follows from Eq. 4 that F..= 0.05. This low
value of F.
would indeed imply an almost random distri-
bution of collagen fiber orientation in the plane of
the dermis.
This finding is indeed compatible with ultrastructural
observations [15]. To obtain further evidence of
collagen being at the origin of piezoelectric properties
of dermis, the temperature dependence of the real
and imaginary components of d of dried dermis have been
measured and compared with the temperature dependence
of df4 and d'c4 of pure, uniaxially oriented collagen
at the relative humidity of 39% [16]. As shown in
Fig. 2, the pattern of the two curves is very similar,
although a shift is present along the temperature axis.
It is known [17] that increasing water content shifts
the d'(T) curve toward lower temperature, so we ascribe
this discrepancy to the higher water content of the
pure collagen sample.
Epidermis
Typical recording of c' and d' angular dependence
are shown in Fig. 3 for samples of whole epidermis
(horny layer was not removed).
The value of d'(max) at room temperature has been
found to be typically of the order of 0.01 to 0.03
pC/N. As in the case of dermis, piezoelectric response
can be described in terms of in plane shear
stress piezoelectricity originating from slight preferential
orientation (uniaxial or biaxial) of fibrous
proteins in the tissue.
In Fig. 4 the temperature dependences of d' and d"
are reported for true epidermis and horny layer, together
with rhinoceros horn samples. Close similarities
can be observed. It appears that, in analogy
with rhinoceros horn samples, the piezoelectric response
of human epidermis can be ascribed to keratinlike
a-helical fibers. True piezoelectric response
(polar) to uniaxial thickness compression has not been
observed in epidermal samples, although erratic stressgenerated
potentials usually were observed.
Thermal pulse experiments were performed on samples
of epidermis to eventually verify the suggested hypothesis
[5] of basal cell layer tonofibrils being responsible
for the suggested piezo- and pyroelectric
properties of epidermis. Thermally generated electric
signals were not clearly pyroelectric in nautre, and
sample reversal in respect to the radiant heat source
did not show any marked asymmetry in charge response.
Horny Layer
513
The characteristic features of piezoelectric response
of the horny layer have been found to be very similar
to those of true epidermis. However, d'(max) of the
horny layer has been found to be of the order of 0.1
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5;14
i
13
z
e1
>1
-Dermis
-Oriented Collagen
Fag. 2: Temrperature dependence of reaZ (dLf) and
imaginary (d"' ) parts of shear stress piezoeZectric
coefficient ot human dermis and pure coZZagen
(coZZagen data from [13]).
to 0.2 pC/N, a factor 5 to 10 times higher than the
typical value of true epidermis. Neither pyroelectri c
response nor thickness compression piezoelectricity
were detected in the horny layer samples.
A MODEL OF SKIN PIEZOELECTRICITY BASED ON
MICROSTRUCTURAL ORGANIZATION
OF FIBROUS PROTEINS
Fibrous proteins constitute a major component of skin.
IEEE Transactions on Electrical Insulation Vol. EI-21 No.3,
/
T(C)
/
June 1986
They are, in the epidermal cells or in the form of fully
developed keratin in the horny layer or finally as
a three-dimensional network of collagen filaments in
dermis (also containing elastin and reticulin) [15].
M
_-
0.5
0
-0.5
E
4 z
Fig. 3: In-pZane anguZar dependence of the reaZ
part of elastic moduZus (c') and piezoeZectric coefficient
(dT) for samples of epidermis from the
thigh.
The organization and orientation of fibrous proteins
show distinctive features in the three cutaneous sections
which may prove to be related strictly to the
particular tensorial form assumed by the piezoelectric
coefficients and to the eventual presence of local symmetry
in the orientational arrangement, which may be
compatible with pyroelectric activity.
Fig. S shows a schematic drawing of skin, where the
arrangement of fibrous proteins, as determined from
X-ray analysis or ultrastructural observations [15], is
clearly evident.
The collagen network of dermis, as compared to the
collagenous structural frame of other connective tissues
such as bone and tendons, appears to be less ordered
and oriented. Some degree of orientation, however,
exists and it varies from one area to the next.
For the sake of formulating a structural model of
piezoelectricity in dermis, a loose, slightly oriented
collagen network is compatible with shear piezoelectricity,
but does not support any pyroelectric activity.
These findings have been indeed observed in the
present study as previously described.
A more complex picture needs to be analyzed for what
fibrous proteins arrangement is applicable to human
epidermis. It appears that piezoelectric properties in
epidermis originate from a-helical keratin-like tonofibrils,
and their orientational arrangement is crucial
to infer possible structures of their corresponding coefficient
tensor. An almost uniaxial orientation of
tonofibrils perpendicular to the plane of the epidermis
is indeed found in the basal cells layer [18],
these tonofibrils being seen as precursors of fully
developed keratin. The uniaxial arrangements of tonofibrils
in the basal cells is progressively lost in upwards
epidermal areas to assume a more isotropic, star-
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2
o

De Rossi et al.: Piezoelectric properties of dry human skin
0
E
10
'N
1
E
-
.5
-.5
-1L
- - - Rhinoceros horn
14 _ - Skin horny layer
o\\\ - - True epidermis
-100 -50 0 50 T(C)
d4 --- Rhinoceros horn
- Skin horny layer
- - True epidermis
-100 -50 -\ 0 50 T(T)
_. \E .
'\, /''\ ~~~~~~I
Fig. 4: Temperature dependence of real (df4) and
imaginary (dr ) parts of shear stress piezoeZectric
coefficient of human true epidermis and
horny Zayer and rhinoceros horn (rhinoceros
horn data from [13]).
like arrangement in the spinous layer t15].
In the horny layer the cells become fully cornified
and flattened, and filaments account for almost half of
the total protein content [15]. These keratin filaments
are predominantly parallel to the plane of skin
[19].
In the case of uniaxially oriented tonofibrils in the
basal cell layer, assuming isotropy in the plane perpendicular
to the helical axis, the kind of symmetry
Fig. 5: Schematic diagram showing the Layering of
skin where the fibrous proteins organization is
evident. ExtraceZZuZar coZZagenous mesh of dermis
is shown in the bottom, while the intracelZular
tonofibriZs in the epidermis are shown to progressiveZy
change their orientation from an aZmost
uniaxiaZ arrangement perpendicuZar to skin
surface in the basaZ ceZZ Zayer to an horizontaZ,
aZmost uniplanar arrangement in the horny Zayer.
which can be hypothesized is C.co().
This symmetry calls for the following form of the
piezoelectric coefficient matrix [7]:
II0 0 0 d14 dl 5 0
d = O O d1 5 -d1 4 °
d31 d31 d33 0
This sort of symmetry would also support pyroelectric
activity [9]. This reasoning is the basis of
Athenstaedt's speculations on the origin of pyroelectric
activity he claimed to exist in epidermis [5]. Except
for a layer of one cell thickness (the basal layer)
a more comples form of d should be postulated, were
probably all the 18 d coefficients should be non-zero.
The keratin organization in the horny layer allow to
suggest a Dm (X22) form of symmetry and consequently [7]
a very simple form of the d matrix.
0 0 d14 0 0
d - 0 0 0 0 -d14 0
0 00 0 0
This kind of symmetry supports neither pyroelectric nor
thickness-compression piezoelectric properties.
The higher degree of in-plane orientation and the
larger fractional content of fibrous proteins in the
horny layer in respect to true epidermis would suggest
a higher piezoelectric activity in the horny layer.
This fact has indeed been observed in the present study,
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0
(5)
(6)
515

516
SYNTHETIC POLYMER ANALOGS OF
PIEZOELECTRIC DRY SKIN
In the process of investigating the microscopic origin
of piezoelectric properties of biological materials,
comparison with artificial piezoelectric material
of inorganic and organic nature, has often been of
valuable help [3]. To provide further insight into the
nature of the piezoelectric activity of true epidermis,
two synthetic polymer analogs have been prepared and
characteri zed.
The first physical model is made of a film of uniaxially
oriented polyhydroxybutyrate (PHB), a semicrystalline
biopolymer of bacterial origin which is known to
assume a D (c22) symmetry upon mechanical drawing [20].
PHB samples were supplied by Marlborough Ltd., Stocktonon-Tees,
U.K. in the form of 200pm thick films, uniaxially
stretched to 3.7 times.
The second analog is made of a 120pm thick polyvinylidene
fluoride (PVDF) film which has been purposely
poled under a temperature gradient of 40%C and at a low
electric field (0.5 MV/cm) following the method indicated
by Marcus [211 to concentrate its piezo- and pyroelectric
activity in a very thin layer close to one
of the electrodes. This would in some aspect model the
given picture of basal cell layer piezo- and pyroelectric
properties. Comparative evaluation of the two
polymers with true epidermis samples, performed by the
experimental procedures used in the present work, has
shown a very marked phenomenological analogy between
PHB and epidermis piezoelectric properties.
CONCLUSION
Human dermis, true epidermis, and horny layer, all
show piezoelectric activity. The preponderant contribution
appears to originate from shear piezoelectricity
of collagen network in dermis, and a-helical keratinlike
fibrils in epidermis and horny layer. The horny
layer typically shows the highest activity.
No experimental evidence has been found for the suggested
hypothesis [5] of pyroelectric response in the
epidermis arising from uniaxially oriented tonofibrils
in the basal cell layer being perpendicular to the dermal-epidermal
junction. This hypothesis, however, cannot
be totally discarded because more refined measuirement
techniques are possibly needed to detect the very
low level of pyroelectric activity and thickness compression
piezoelectric response originating from a
single cell layer. Strong contribution to electromechanical
or thermomechanical response of human skin
in the dry state has been found to arise from trapped
charges, as is to be expected, because of the high ionic
content of skin tissue. Finally, we observed piezoelectric
decay with increasing moisture content. This
fact does not corroborate the hypothesis [5] of piezoand
pyroelectricity being a major effect in moist skin
electromechanical properties.
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De Rossi et al.: Piezoelectric properties of dry human skin
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Manuscript was received 4 November 1985.
This paper was presented at the 5th InternationaZ
Symposium on EZectrets, HeideZberg, Germany, 4-6
September 1985.
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