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IEEE Transactions on Electrical Insulation Vol. EI-21 No.

3, June 1986 511

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 struc-
tural network, while the piezoelectric properties of epider-
mis appear to originate from partially oriented a-helical
keratin-like tonofibrils. The highest piezoelectric coef-
ficients 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 con- skin samples both in vitro and in vivo, reaching the
vert mechanical and thermal stimuli into electric sig- conclusion that the observed electrical signals ob-
nals [1]. Extensive studies are available [2], exam- tained in response to mechanical or thermal stimuli are
ining mechanoelectrical properties of bone both in the intrinsically of piezo- and pyroelectric nature. The
dry and in the moist, physiological state. same authors reported measurements performed on dry
skin observing a reduced (20 to 60% less) mechanoelec-
The hypothesis ascribing bone mechanoelectric trans- trical activity compared to moist samples.
duction to piezoelectric properties of the collagenous
structure in the dry state and to electrokinetic phe- It is worthwhile noting that, while Shamos and Lavine
nomena (streaming potentials) in the moist state nowa- ascribe the piezoelectric properties of human skin to
days has a large consensus [3]. The eventual role of dermal collagen network, Athenstaedt et al. suggest
these phenomena on bone regrowth and healing is pre- that these properties originate-from uniaxially orien-
sently largely debated. However, the mechanoelectrical ted polar keratin filaments in the basal cells layer of
properties of human skin have been very little studied epidermis. To clarify the nature of mechanoelectrical
and their origin is largely unknown. transduction phenomena in human skin and to comprehend
better their microscopic origin, a systematic study of
Shamos and Lavine [41 have reported observations of these properties both in the dry and moist state has
direct piezoelectric effects in dry, whole human skin been undertaken. We report here results obtained on
samples from the forearm and callus from the sole. dry human skin samples.
These authors, by analogy with the behavior of bone
and tendons, ascribe the piezoelectric properties of
human skin to oriented collagen fibrils in dermis. SAMPLE PREPARATION
Athenstaedt et al. [5] have examined fresh human Several samples of human skin from breast, thigh, pre-

0018-9367/86/0600-0511$01.00 @ 1986 IEEE


5I2 IEEE Transactions on Electrical Insulation Vol. EI-211 No3` June 1986

puce, and callus from sole have been obtained from pa- have been performed by applying square wave stress
tients undergoing plastic surgery. Prepuce samples pulses generated by a flat circular plastic pin, driven
were used because they are almost entirely composed of by an electromagnetic shaker. Load readings have been
true epidermal tissue (the horny layer is virtually performed by means of a miniature load cell (Type 9201,
absent). Kistler Instrumente AG, Winterthur, Switzerland) me-
chanically in series with the sample, while charge gen-
The samples were rinsed in distilled water, cut into erated by skin samples were detected by means of a
circular shape (2 cm diameter) and separated into their charge amplifier (Type 5007, Kistler Instrumente AG,
dermal, epidermal and horny layer components by micro- Winterthur, Switzerland). Two different methods have
surgical operations. The samples were dehydrated in been used to determine the eventual pyroelectricity of
vacuum for 12 h. skin samples. The first method, also called the static
method [9], is the only one capable of giving absolute
Typical dehydrated sample thickness was 300 to 400 values of the pyroelectric coefficient. The measure-
vim for whole epidermis, 100 to 200 vm for horny layer ments have been implemented using a Thermo Controller
and 300 to 500 vm for dermis. Electrodes made of con- Unit (Toyo Seiki, Seisaku-sho, Tokyo, Japan) where the
ducting silver-loaded paint (Acheson Colloiden B.V., temperature has been raised at a rate of 2°C per minute.
Scheemda, Holland) were applied by brushing on the sur-
faces of the samples used in piezoelectric measurements. The voltage appearing at the electrodes was measured
Colloidal graphite electrodes were sprayed on the sam- with a very high input impedance (1015 Q) voltmeter
ples used in thermal pulse experiments. After appli- built around a FET-input electrometer operational am-
cation of the electrodes the samples were again vacuum plifier (AD 515 J, Analog Devices, Norwood, MA, USA).
dried for two hours.
This method, however, is known to be effected by er-
rors related to voltages not of pyroelectric origin
EXPERIMENTAL METHODS which are spontaneously generated by the sample and by
voltages generated by any piezoelectric material when it
is nonuniformly heated (tertiary pyroelectric effect).
Dry skin is an anisotropic material which contains To provide an alternative measuring techniques, the
oriented polar crystallites in an amorphous organic rectangular pulse heating method [9] has been used,
matter, and its piezoelectric characterization would in although this method is capable of providing only rela-
principle require determination of 18 components of the tive values of the pyroelectric coefficient.
piezoelectric coefficient third-rank tensor d.. (the
reduced matrix notation [6] has been used in iie pre- A sharply focused 50 W incandescent lamp was used as
sent work). di are the proportionality constants be- light source and light pulses of 1 s duration were de-
tween the applied mechanical stress T and the generated livered to the skin samples to change the temperature.
electrical polarization P: However, both the static method and the classical
rectangular pulse heating method are only capable of
6 providing pyroelectric informations integrated over the
i i i (l sample thickness.
=1 _j
To probe the spatial distribution of polarization
When studying piezoelectric properties of biopolymers across the thickness of the epidermis sample, as re-
it is customary [7] to define a cartesian coordinate quired to evaluate the hypotesis of a pyroelectric acti-
system where the z-3 axis coincides with the assumed vity in the basal cell layer tonofibrils, the Collins'
prevailing orientation of electric dipoles, which for thermal pulse method [10] has been used.
a-helical proteins, is colinear with the helix long
axis. The x_1 axis is assumed to be perpendicular to A very short (1 ms) duration light pulse, generated by
to the skin surface. an electronic flash lamp, was delivered to the sample
located in a shielded, hermetic cell through a glass
Following these definitions, d14 represents the window; voltage at the electrodes was amplified with the
shear piezoelectric coefficient obtained by measuring Ad 515 J operational amplifier and recorded by means of
the electrical charges on electrodes deposited on skin a 7912AD Tektronix transient recorder.
surfaces, generated by applying an uniaxial mechanical
stress in the skin plane directed 450 from the prefer- The physical basis of this method resides in produc-
ential orientation of piezoelectric protein fibers. ing, by means of thermal diffusion, a transient inhomo-
geneous strain across the sample, in order to measure
Because skin shows relaxational dispersion [8], the its inho-moc,neous pyroelectric res-ponsc. Altlhough the
d coefficients are in fact complex quantities having information about the polarization distribution is con-
an in-phase d' real part and an out-of phase d " complex voluted with a time-dependent temperature distribution,
part. A frequency dependence of the piezoelectric co- a deconvolution process is typically applied to the ex-
efficients in this case has to be expected. perimental data to obtain the first few Fourier coef-
ficients of the polarization distribution [11]. For
Angular dependence in the plane of the samples (der- the purpose of the present work, however, we were only
mis, true epidermis and horny layer) of d' and of the interested to detect a limiting case of spatial distri-
real part of the elastic modulus c' have been measured bution of polarization inside epidermis where the pyro-
at 25°C and at the frequencies of 1, 10, and 30 Hz using electric response may be eventually concentrated only
a Rheolograph Piezo (Toyo Seiki Seisaku-sho, Tokyo, at one very superficial layer of the sample.
Japan). The dependence of real d' and imaginary part
d" of shear piezoelectric coefficient on temperature In this simple case, qualitative inspection of the
from -100°C to 1000C at 10 Hz have also been measured, volatage-time responses obtained by alternating the side
using the same apparatus. of the sample in respect to the impinging light is suf-
ficient to determine eventual strong asymmetry in the
Thickness-compression piezoelectric measurements pyroelectricity spatial distribution [11].
De Rossi et al.: Piezoelectric properties of dry human skin 513

Referring to Fig. 1, if we assume the angle of average


RESULTS direction of collagen crystallites orientation corre-
sponds to the maximum of angular response of the real
Dermis part of elastic modulus, 8c=90 '. The relationship d(e)
should be hence represented by the function:
Typical recordings of the angular dependence of the
real part of the piezoelectric shear coefficient and d' = 0.5d1c v F sin[2(O - 2J] (4)
elastic modulus are shown in Fig. 1 for dermal samples.
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 ultrastructur-
al observations [15]. To obtain further evidence of
collagen being at the origin of piezoelectric proper-
ties 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.
Fig. 1: In-pZane anguZar dependence of the reaZ part
of eZastic modulus (c') and piezoeZectric shear co- Epidermis
efficient (d') for a sanple of dermis from the
breast. Typical recording of c' and d' angular dependence
are shown in Fig. 3 for samples of whole epidermis
(horny layer was not removed).
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 value of d'(max) at room temperature has been
found to be typically of the order of 0.01 to 0.03
The presence of one or two maxima in the in-plane pC/N. As in the case of dermis, piezoelectric re-
polar behavior of c' obtained for different samples sponse can be described in terms of in plane shear
from different anatomical sites indicates slight pre- stress piezoelectricity originating from slight pre-
ferential uniaxial or biaxial orientation of collagen ferential orientation (uniaxial or biaxial) of fibrous
fibrils in the dermal three-dimensional structural net- proteins in the tissue.
work. The invariably observed bisinusoidal behavior of
d' polar response is similar to the one observed in In Fig. 4 the temperature dependences of d' and d"
oriented collagen structures and uniaxially oriented are reported for true epidermis and horny layer, to-
synthetic polypeptides [7]. gether with rhinoceros horn samples. Close similari-
ties can be observed. It appears that, in analogy
This kind of anisotropy can be generally expressed with rhinoceros horn samples, the piezoelectric re-
through the relation [12] sponse of human epidermis can be ascribed to keratin-
like a-helical fibers. True piezoelectric response
(polar) to uniaxial thickness compression has not been
d' = 0.5 dl4sin(2e) (2) observed in epidermal samples, although erratic stress-
generated potentials usually were observed.
In the case of prevailing uniaxial anisotropy, such as Thermal pulse experiments were performed on samples
shown in Fig. 1, for a composite piezoelectric materi- of epidermis to eventually verify the suggested hy-
al where the degree of orientation is low, the follow- pothesis [5] of basal cell layer tonofibrils being re-
ing expression can be used [12], assuming collagen to sponsible for the suggested piezo- and pyroelectric
originate piezoelectric activity: properties of epidermis. Thermally generated electric
signals were not clearly pyroelectric in nautre, and
sample reversal in respect to the radiant heat source
d' = 0.5 d04 1cF sin[2(O - 0 )] (3) did not show any marked asymmetry in charge response.

where dC'4
is the shear piezoelectric coefficient for Horny Layer
the single crystallite, b the volume fraction of the
paracrystalline piezoelecYric component (collagen) in The characteristic features of piezoelectric response
the sample, Fc the degree of orientation of collagen of the horny layer have been found to be very similar
to those of true epidermis. However, d'(max) of the
fibers, and 0c the angle of average direction of colla-
gen crystallites orientation.
horny layer has been found to be of the order of 0.1
5;14 IEEE Transactions on Electrical Insulation Vol. EI-21 No.3, June 1986

They are, in the epidermal cells or in the form of ful-


ly developed keratin in the horny layer or finally as
a three-dimensional network of collagen filaments in
dermis (also containing elastin and reticulin) [15].

E
_- 4 z
i
0.5
13
o

2
z

-0.5

Fig. 3: In-pZane anguZar dependence of the reaZ


part of elastic moduZus (c') and piezoeZectric co-
efficient (dT) for samples of epidermis from the
thigh.

The organization and orientation of fibrous proteins


show distinctive features in the three cutaneous sec-
tions which may prove to be related strictly to the
particular tensorial form assumed by the piezoelectric
e1 coefficients and to the eventual presence of local sym-
metry in the orientational arrangement, which may be
T(C)
>1
compatible with pyroelectric activity.
Fig. S shows a schematic drawing of skin, where the
arrangement of fibrous proteins, as determined from
-Dermis
/ X-ray analysis or ultrastructural observations [15], is
-Oriented Collagen
/
clearly evident.
The collagen network of dermis, as compared to the
collagenous structural frame of other connective tis-
sues such as bone and tendons, appears to be less or-
dered and oriented. Some degree of orientation, how-
ever, 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
Fag. 2: Temrperature dependence of reaZ (dLf) and collagen network is compatible with shear piezoelec-
imaginary (d"' ) parts of shear stress piezoeZectric tricity, but does not support any pyroelectric activi-
coefficient ot human dermis and pure coZZagen ty. These findings have been indeed observed in the
(coZZagen data from [13]). present study as previously described.
A more complex picture needs to be analyzed for what
to 0.2 pC/N, factor 5 to 10 times higher than the
a fibrous proteins arrangement is applicable to human
typical value of true epidermis. Neither pyroelectri c epidermis. It appears that piezoelectric properties in
response nor thickness compression piezoelectricity epidermis originate from a-helical keratin-like tono-
were detected in the horny layer samples. fibrils, and their orientational arrangement is crucial
to infer possible structures of their corresponding co-
efficient tensor. An almost uniaxial orientation of
A MODEL OF SKIN PIEZOELECTRICITY BASED ON tonofibrils perpendicular to the plane of the epider-
MICROSTRUCTURAL ORGANIZATION mis is indeed found in the basal cells layer [18],
OF FIBROUS PROTEINS these tonofibrils being seen as precursors of fully
developed keratin. The uniaxial arrangements of tono-
fibrils in the basal cells is progressively lost in up-
Fibrous proteins constitute a major component of skin. wards epidermal areas to assume a more isotropic, star-
De Rossi et al.: Piezoelectric properties of dry human skin 515

- - - Rhinoceros horn
14 _ - Skin horny layer
o\ \ - - True epidermis
1
0
E
10

'N

-100 -50 0 50 T(C)

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 pro-
gressiveZy change their orientation from an aZ-
most uniaxiaZ arrangement perpendicuZar to skin
d4 --- Rhinoceros horn surface in the basaZ ceZZ Zayer to an horizontaZ,
.5 - Skin horny layer aZmost uniplanar arrangement in the horny Zayer.
- - True epidermis

which can be hypothesized is C.co().


E
-
-100
_. -50
\E .
-\ 0 50 T(T)
This symmetry calls for the following form of the
piezoelectric coefficient matrix [7]:
-.5
II0 d14 dl 5 0
'\, /''\ ~~~~~~I
0 0

d =
O O d1 5 -d1 4 ° (5)
-1L d31 d31 d33 0 0

This sort of symmetry would also support pyroelectric


activity [9]. This reasoning is the basis of
Athenstaedt's speculations on the origin of pyroelec-
tric activity he claimed to exist in epidermis [5]. Ex-
cept 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.
Fig. 4: Temperature dependence of real (df4) and
imaginary (dr ) parts of shear stress piezoeZec- The keratin organization in the horny layer allow to
tric coefficient of human true epidermis and suggest a Dm (X22) form of symmetry and consequently [7]
horny Zayer and rhinoceros horn (rhinoceros a very simple form of the d matrix.
horn data from [13]).
0 0 d14 0 0
d - 0 0 0 0 -d14 0 (6)
like arrangement in the spinous layer t15]. 0
0 00 0

In the horny layer the cells become fully cornified


and flattened, and filaments account for almost half of This kind of symmetry supports neither pyroelectric nor
the total protein content [15]. These keratin fila- thickness-compression piezoelectric properties.
ments are predominantly parallel to the plane of skin
[19]. The higher degree of in-plane orientation and the
larger fractional content of fibrous proteins in the
In the case of uniaxially oriented tonofibrils in the horny layer in respect to true epidermis would suggest
basal cell layer, assuming isotropy in the plane per- a higher piezoelectric activity in the horny layer.
pendicular to the helical axis, the kind of symmetry This fact has indeed been observed in the present study,
516 IEEE Transactions on Electrical Insulation Vol. EI-21 No.3, June 1986

[2] C.T. Brighton, J.Black and S.R. Pollack, Elec-


SYNTHETIC POLYMER ANALOGS OF trical properties of bone and cartilage: ex-
PIEZOELECTRIC DRY SKIN perimental effects and clinical applications,
Grune & Stratton NY, 1979.
In the process of investigating the microscopic ori- [3] W.S. Williams, "Piezoelectric effects in biologi-
gin of piezoelectric properties of biological materi- cal materials", Ferroelectrics Vol 41, pp. 225-
als, comparison with artificial piezoelectric material 246, 1982.
of inorganic and organic nature, has often been of
valuable help [3]. To provide further insight into the [4] M.H. Shamos and L.S. Lavine, "Piezoelcetricity as
nature of the piezoelectric activity of true epidermis, a fundamental porperty of biological tissues",
two synthetic polymer analogs have been prepared and Nature Vol 213, pp. 267-269, 1967.
characteri zed.
The first physical model is made of a film of uniaxi-
[5] H. Athenstaedt, H. Claussen and D. Schaper,
"Epidermis of human skin: pyroelectric and piezo-
ally oriented polyhydroxybutyrate (PHB), a semicrystal- electric sensor layer", Science Vol 216, pp.
line biopolymer of bacterial origin which is known to 1018-1020, 1982.
assume a D (c22) symmetry upon mechanical drawing [20].
PHB samples were supplied by Marlborough Ltd., Stockton- [6] J.F. Nye, Physical properties of crystals, The
on-Tees, U.K. in the form of 200pm thick films, uniaxi- Clarendon Press, Oxford 1957, Chapter 7.
ally stretched to 3.7 times.
[7] E. Fukada, "Piezoelectric properties of biologi-
The second analog is made of a 120pm thick polyvi- cal polymers", Quart. Rev. Biophys. Vol 16, pp.
nylidene fluoride (PVDF) film which has been purposely 59-87, 1983.
poled under a temperature gradient of 40%C and at a low
electric field (0.5 MV/cm) following the method indi- [8] D. De Rossi, P. Dario and C. Domenici, "The
cated by Marcus [211 to concentrate its piezo- and py- electret nature of human skin: a model for arti-
roelectric activity in a very thin layer close to one ficial tactile sensor arrays" (Abstr.), IVth
of the electrodes. This would in some aspect model the Meeting of the European Society of Biomechanics,
given picture of basal cell layer piezo- and pyroelec- Davos (Switzerland), September 1984.
tric properties. Comparative evaluation of the two
polymers with true epidermis samples, performed by the [9] S.B. Lang, "Pyroelectric effect in biological ma-
experimental procedures used in the present work, has terials." in Electronic conduction and mechano-
shown a very marked phenomenological analogy between electrical transduction in biological materials,
PHB and epidermis piezoelectric properties. B. Linpinski Ed., M. Dekker Inc. NY, 1982.
[10] R.E. Collins, "Measurement of charge distribution
CONCLUSION in electrets", Rev. Sci. Instrum. Vol 48, pp. 83-
91, 1977.
Human dermis, true epidermis, and horny layer, all [11] A,S. De Reffi, C.M. Guttman, F.I. Mopsik, G.T.
show piezoelectric activity. The preponderant contri- Davis and M.G. Broadhurst, "Determination of
bution appears to originate from shear piezoelectricity charge or polarization distribution across poly-
of collagen network in dermis, and a-helical keratin- mer electrets by the thermal pulse method and
like fibrils in epidermis and horny layer. The horny Fourier analysis", Phys. Rev. Lett. Vol 40, pp.
layer typically shows the highest activity. 413-416, 1978.
No experimental evidence has been found for the sug- [12] T. Furukawa and E. Fukada, "Piezoelectric relaxa-
gested hypothesis [5] of pyroelectric response in the tion in poly(y-benzyl-gluamate)", J. Polym. Sci.
epidermis arising from uniaxially oriented tonofibrils Phys. Ed. Vol 14, pp. 1979-2010, 1976.
in the basal cell layer being perpendicular to the der-
mal-epidermal junction. This hypothesis, however, can- [13] E. Fukada, "Piezoelectricity of biological ma-
not be totally discarded because more refined measuire- terials." in Electronic conduction and mechano-
ment techniques are possibly needed to detect the very electrical transduction in biological materials,
low level of pyroelectric activity and thickness com- B. Lipinski Ed., M. Dekker Inc. NY, 1982.
pression piezoelectric response originating from a
single cell layer. Strong contribution to electro- [14] R.D. Harkness, "Mechanical properties of skin in
mechanical or thermomechanical response of human skin relation to its biological function and its chemi-
in the dry state has been found to arise from trapped cal components" in Biophysical properties of the
charges, as is to be expected, because of the high ion- skin, H.TR. Elden Ed., Wiley & Sons NY, 1971.
ic content of skin tissue. Finally, we observed piezo-
electric decay with increasing moisture content. This [15] W. Montagna and P.F. Parakkal, The structure and
fact does not corroborate the hypothesis [5] of piezo- function of skin, 3rd Edition, Academic Press NY,
and pyroelectricity being a major effect in moist skin 1974.
electromechanical properties.
[16] E. Fukada, H. Ueda and R, Rinaldi, "Piezoelectric
and related properties if hydrated collagen",
REFERENCES Biophys. J. Vol 16, pp. 911-918, 1976.
[17] H. Maeda and E. Fukada, "Effect of water on piezo-
[1] A.J. Grodzinsky, "Electromechanical and physico- electric, dielectric and elastic properties of
chemical properties of connective tissue" CRC bone", Biopolymers Vol 21, pp, 2055-2068, 1982.
Crit. Rev. Biomed. Eng. Vol 9, pp. 133-197, 1983.
De Rossi et al.: Piezoelectric properties of dry human skin 517

[18] G.F. Oldland, "The fine structure of the interre-


lationship of cells in the human epidermis", J.
Biophys. Biochem. Cytol. Vol 4, pp. 529-538,
1958.
[19] A.C. Park and C.B. Baddiel, "Rheology of the stra-
tum corneum I0: A molecular interpretation of
the stress strain curves", J. Soc. Cosmet. Chem.
Vol 23, pp. 3-12, 1972.
[20] E. Fukada, "Piezoelectricity of natural biomateri-
als'", Ferroelectrics Vol 60, pp. 285-296, 1984.
[21] M.A. Marcus, "Controlling the piezoelectric acti-
vity distribution in poly(vinylidene fluoride)
transducers", Ferroelectrics Vol 32, pp. 149-155,
1981.

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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