A triaxial force-sensitive microrobot was developed to dynamically perturb skin in multiple deformation modes, in vivo. Wiener static nonlinear identification was used to extract the linear dynamics and static nonlinearity of the force–displacement behavior of skin. Stochastic input forces were applied to the volar forearm and thenar eminence of the hand, producing probe tip perturbations in indentation and tangential extension. Wiener static nonlinear approaches reproduced the resulting displacements with variances accounted for (VAF) ranging 94–97%, indicating a good fit to the data. These approaches provided VAF improvements of 0.1–3.4% over linear models. Thenar eminence stiffness measures were approximately twice those measured on the forearm. Damping was shown to be significantly higher on the palm, whereas the perturbed mass typically was lower. Coefficients of variation (CVs) for nonlinear parameters were assessed within and across individuals. Individual CVs ranged from 2% to 11% for indentation and from 2% to 19% for extension. Stochastic perturbations with incrementally increasing mean amplitudes were applied to the same test areas. Differences between full-scale and incremental reduced-scale perturbations were investigated. Different incremental preloading schemes were investigated. However, no significant difference in parameters was found between different incremental preloading schemes. Incremental schemes provided depth-dependent estimates of stiffness and damping, ranging from 300 N/m and 2 Ns/m, respectively, at the surface to 5 kN/m and 50 Ns/m at greater depths. The device and techniques used in this research have potential applications in areas, such as evaluating skincare products, assessing skin hydration, or analyzing wound healing.

References

References
1.
Hendriks
,
F. M.
,
Brokken
,
D.
,
Oomens
,
C. W. J.
,
Bader
,
D. L.
, and
Baaijens
,
F. P. T.
,
2006
, “
The Relative Contributions of Different Skin Layers to the Mechanical Behavior of Human Skin In Vivo Using Suction Experiments
,”
Med. Eng. Phys.
,
28
(
3
), pp.
259
266
.
2.
Delalleau
,
A.
,
Josse
,
G.
,
Lagarde
,
J.-M.
,
Zahouani
,
H.
, and
Bergheau
,
J.-M.
,
2008
, “
A Nonlinear Elastic Behavior to Identify the Mechanical Parameters of Human Skin In Vivo
,”
Skin Res. Technol.
,
14
(
2
), pp.
152
164
.
3.
Delalleau
,
A.
,
Josse
,
G.
,
George
,
J.
,
Yassine
,
M.
,
Ossant
,
F.
, and
Lagarde
,
J.-M.
,
2009
, “
A Human Skin Ultrasonic Imaging to Analyse Its Mechanical Properties
,”
Eur. J. Comput. Mech.
,
18
(
1
), pp.
105
116
.
4.
Krueger
,
N.
,
Luebberding
,
S.
,
Oltmer
,
M.
,
Streker
,
M.
, and
Kerscher
,
M.
,
2011
, “
Age-Related Changes in Skin Mechanical Properties: A Quantitative Evaluation of 120 Female Subjects
,”
Skin Res. Technol.
,
17
(
2
), pp.
141
148
.
5.
Sutradhar
,
A.
, and
Miller
,
M. J.
,
2012
, “
In Vivo Measurement of Breast Skin Elasticity and Breast Skin Thickness
,”
Skin Res. Technol.
, (
11
), pp.
1
9
.
6.
Escoffier
,
C.
,
de Rigal
,
J.
,
Rochefort
,
A.
,
Vasselet
,
R.
,
Leveque
,
J. L.
, and
Agache
,
P.
,
1989
, “
Age-Related Mechanical Properties of Human Skin: An In Vivo Study
,”
J. Invest. Dermatol.
,
93
(
3
), pp.
353
357
.
7.
Leveque
,
J. L.
,
Corcuff
,
P.
,
de Rigal
,
J.
, and
Agache
,
P.
,
1984
, “
In Vivo Studies of the Evolution of Physical Properties of the Human Skin With Age
,”
Int. J. Dermatol.
,
23
(
5
), pp.
322
329
.
8.
Zahouani
,
H.
,
Pailler-Mattei
,
C.
,
Sohm
,
B.
,
Vargiolu
,
R.
,
Cenizo
,
V.
, and
Debret
,
R.
,
2009
, “
Characterization of the Mechanical Properties of a Dermal Equivalent Compared With Human Skin In Vivo by Indentation and Static Friction Tests
,”
Skin Res. Technol.
,
15
(
1
), pp.
68
76
.
9.
Flynn
,
C.
,
Taberner
,
A. J.
,
Nielsen
,
P. M. F.
, and
Fels
,
S.
,
2013
, “
Simulating the Three-Dimensional Deformation of In Vivo Facial Skin
,”
J. Mech. Behav. Biomed. Mater.
,
28
, pp.
484
494
.
10.
Pailler-Mattéi
,
C.
,
Bec
,
S.
, and
Zahouani
,
H.
,
2008
, “
In Vivo Measurements of the Elastic Mechanical Properties of Human Skin by Indentation Tests
,”
Med. Eng. Phys.
,
30
(
5
), pp.
599
606
.
11.
Delalleau
,
A.
,
Josse
,
G.
,
Lagarde
,
J. M.
,
Zahouani
,
H.
, and
Bergheau
,
J. M.
,
2008
, “
Characterization of the Mechanical Properties of Skin by Inverse Analysis Combined With an Extensometry Test
,”
Wear
,
264
(
5–6
), pp.
405
410
.
12.
Woo
,
M. S.
,
Moon
,
K. J.
,
Jung
,
H. Y.
,
Park
,
S. R.
,
Moon
,
T. K.
,
Kim
,
N. S.
, and
Lee
,
B. C.
,
2014
, “
Comparison of Skin Elasticity Test Results From the Ballistometer® and Cutometer®
,”
Skin Res. Technol.
,
20
(
4
), pp.
422
428
.
13.
Sandrin
,
L.
,
Tanter
,
M.
,
Gennisson
,
J.-L.
,
Catheline
,
S.
, and
Fink
,
M.
,
2002
, “
Shear Elasticity Probe for Soft Tissues With 1-D Transient Elastography
,”
IEEE Trans. Ultrason. Ferroelectr. Freq. Control
,
49
(
4
), pp.
436
446
.
14.
Zhang
,
X.
, and
Greenleaf
,
J. F.
,
2007
, “
Estimation of Tissue's Elasticity With Surface Wave Speed
,”
J. Acoust. Soc. Am.
,
122
(
5
), pp.
2522
2525
.
15.
Verhaegen
,
P. D. H. M.
,
Res
,
E. M.
,
van Engelen
,
A.
,
Middelkoop
,
E.
, and
van Zuijlen
,
P. P. M.
,
2010
, “
A Reliable, Non-Invasive Measurement Tool for Anisotropy in Normal Skin and Scar Tissue
,”
Skin Res. Technol.
,
16
(
3
), pp.
325
331
.
16.
Coutts
,
L.
,
Bamber
,
J.
, and
Miller
,
N.
,
2013
, “
Multi-Directional In Vivo Tensile Skin Stiffness Measurement for the Design of a Reproducible Tensile Strain Elastography Protocol
,”
Skin Res. Technol.
,
19
(
1
), pp.
37
44
.
17.
Lim
,
K. H.
,
Chew
,
C. M.
,
Chen
,
P. C. Y.
,
Jeyapalina
,
S.
,
Ho
,
H. N.
,
Rappel
,
J. K.
, and
Lim
,
B. H.
,
2008
, “
New Extensometer to Measure In Vivo Uniaxial Mechanical Properties of Human Skin
,”
J. Biomech.
,
41
(
5
), pp.
931
936
.
18.
Jacquet
,
E.
,
Josse
,
G.
,
Khatyr
,
F.
, and
Garcin
,
C.
,
2008
, “
A New Experimental Method for Measuring Skin's Natural Tension
,”
Skin Res. Technol.
,
14
(
1
), pp.
1
7
.
19.
Diridollou
,
S.
,
Berson
,
M.
,
Vabre
,
V.
,
Black
,
D.
,
Karlsson
,
B.
,
Auriol
,
F.
,
Gregoire
,
J. M.
,
Yvon
,
C.
,
Vaillant
,
L.
,
Gall
,
Y.
, and
Patat
,
F.
,
1998
, “
An In Vivo Method for Measuring the Mechanical Properties of the Skin Using Ultrasound
,”
Ultrasound Med. Biol.
,
24
(
2
), pp.
215
224
.
20.
Sandford
,
E.
,
Chen
,
Y.
,
Hunter
,
I.
,
Hillebrand
,
G.
, and
Jones
,
L.
,
2012
, “
Capturing Skin Properties From Dynamic Mechanical Analyses
,”
Skin Res. Technol.
,
19
(
1
), pp.
e339
48
.
21.
Kennedy
,
B. F.
,
Hillman
,
T. R.
,
McLaughlin
,
R. A.
,
Quirk
,
B. C.
, and
Sampson
,
D. D.
,
2009
, “
In Vivo Dynamic Optical Coherence Elastography Using a Ring Actuator
,”
Opt. Express
,
17
(
24
), pp.
21762
21772
.
22.
Boyer
,
G.
,
Zahouani
,
H.
,
Le Bot
,
A.
, and
Laquieze
,
L.
,
2007
, “
In Vivo Characterization of Viscoelastic Properties of Human Skin Using Dynamic Micro-Indentation
,” 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (
EMBS 2007
), Lyon, France, Aug. 22–26, pp.
4584
4587
.
23.
Boyer
,
G.
,
Laquièze
,
L.
,
Le Bot
,
A.
,
Laquièze
,
S.
, and
Zahouani
,
H.
,
2009
, “
Dynamic Indentation on Human Skin In Vivo: Ageing Effects
,”
Skin Res. Technol.
,
15
(
1
), pp.
55
67
.
24.
Chen
,
Y.
, and
Hunter
,
I. W.
,
2013
, “
Nonlinear Stochastic System Identification of Skin Using Volterra Kernels
,”
Ann. Biomed. Eng.
,
41
(
4
), pp.
847
862
.
25.
Chen
,
Y.
, and
Hunter
,
I. W.
,
2012
, “
Stochastic System Identification of Skin Properties: Linear and Wiener Static Nonlinear Methods
,”
Ann. Biomed. Eng.
,
40
(
10
), pp.
2277
2291
.
26.
Holzapfel
,
G. A.
, and
Ogden
,
R. W.
,
2008
, “
On Planar Biaxial Tests for Anisotropic Nonlinearly Elastic Solids. A Continuum Mechanical Framework
,”
Math. Mech. Solids
,
14
(
5
), pp.
474
489
.
27.
Chen
,
Y.
, and
Hunter
,
I. W.
,
2009
, “
In Vivo Characterization of Skin Using a Weiner Nonlinear Stochastic System Identification Method
,” Annual International Conference of the IEEE Engineering in Medicine and Biology Society (
EMBC 2009
), Minneapolis, MN, Sept. 3–6, pp.
6010
6013
.
28.
Flynn
,
C.
,
Taberner
,
A.
, and
Nielsen
,
P.
,
2011
, “
Mechanical Characterisation of In Vivo Human Skin Using a 3D Force-Sensitive Micro-Robot and Finite Element Analysis
,”
Biomech. Model. Mechanobiol.
,
10
(
1
), pp.
27
38
.
29.
Flynn
,
C.
,
Taberner
,
A.
, and
Nielsen
,
P.
,
2011
, “
Measurement of the Force–Displacement Response of In Vivo Human Skin Under a Rich Set of Deformations
,”
Med. Eng. Phys.
,
33
(
5
), pp.
610
619
.
30.
Sandford
,
E.
,
Chen
,
Y.
,
Hunter
,
I.
,
Hillebrand
,
G.
, and
Jones
,
L.
,
2013
, “
Capturing Skin Properties From Dynamic Mechanical Analyses
,”
Skin Res. Technol.
,
19
(
1
), pp.
e339
e348
.
31.
Finlay
,
B.
,
1970
, “
Dynamic Mechanical Testing of Human Skin “In Vivo
,”
J. Biomech.
,
3
(
6
), pp.
557
568
.
32.
Liang
,
X.
, and
Boppart
,
S. A.
,
2010
, “
Biomechanical Properties of In Vivo Human Skin From Dynamic Optical Coherence Elastography
,”
IEEE Trans. Biomed. Eng.
,
57
(
4
), pp.
953
959
.
33.
Kearney
,
S. P.
,
Khan
,
A.
,
Dai
,
Z.
, and
Royston
,
T. J.
,
2015
, “
Dynamic Viscoelastic Models of Human Skin Using Optical Elastography
,”
Phys. Med. Biol.
,
60
(
17
), pp.
6975
6990
.
34.
Khatyr
,
F.
, and
Imberdis
,
C.
,
2004
, “
Model of the Viscoelastic Behaviour of Skin In Vivo and Study of Anisotropy
,”
Skin Res. Technol.
,
10
(
2
), pp.
96
103
.
35.
Weickenmeier
,
J.
,
Jabareen
,
M.
, and
Mazza
,
E.
,
2015
, “
Suction Based Mechanical Characterization of Superficial Facial Soft Tissues
,”
J. Biomech.
,
48
(
16
), pp.
4279
4286
.
36.
Jemec
,
G. B. E.
,
Selvaag
,
E.
,
Agren
,
M.
, and
Wulf
,
H. C.
,
2001
, “
Measurement of the Mechanical Properties of Skin With Ballistometer and Suction Cup
,”
Skin Res. Technol.
,
7
(
2
), pp.
122
126
.
37.
Li
,
C.
,
Guan
,
G.
,
Reif
,
R.
,
Huang
,
Z.
, and
Wang
,
R. K.
,
2012
, “
Determining Elastic Properties of Skin by Measuring Surface Waves From an Impulse Mechanical Stimulus Using Phase-Sensitive Optical Coherence Tomography
,”
J. R. Soc. Interface
,
9
(
70
), pp.
831
841
.
38.
Raveh Tilleman
,
T.
,
Tilleman
,
M. M.
, and
Neumann
,
M. H. A.
,
2004
, “
The Elastic Properties of Cancerous Skin: Poisson's Ratio and Young's Modulus
,”
Isreal Med. Assoc. J.
,
6
(
12
), pp.
753
755
.http://www.ima.org.il/FilesUpload/IMAJ/0/52/26480.pdf
39.
Hendriks
,
F. M.
,
Brokken
,
D.
,
van Eemeren
,
J. T. W. M.
,
Oomens
,
C. W. J.
,
Baaijens
,
F. P. T.
, and
Horsten
,
J. B. A. M.
,
2003
, “
A Numerical–Experimental Method to Characterize the Non-Linear Mechanical Behaviour of Human Skin
,”
Skin Res. Technol.
,
9
(
3
), pp.
274
283
.
40.
Tran
,
H. V.
,
Charleux
,
F.
,
Rachik
,
M.
,
Ehrlacher
,
A.
, and
Ho Ba Tho
,
M. C.
,
2007
, “
In Vivo Characterization of the Mechanical Properties of Human Skin Derived From MRI and Indentation Techniques
,”
Comput. Methods Biomech. Biomed. Eng.
,
10
(
6
), pp.
401
407
.
41.
Geerligs
,
M.
,
van Breemen
,
L.
,
Peters
,
G.
,
Ackermans
,
P.
,
Baaijens
,
F.
, and
Oomens
,
C.
,
2011
, “
In Vitro Indentation to Determine the Mechanical Properties of Epidermis
,”
J. Biomech.
,
44
(
6
), pp.
1176
1181
.
42.
Hatefi
,
A.
, and
Amsden
,
B.
,
2002
, “
Biodegradable Injectable In Situ Forming Drug Delivery Systems
,”
J. Controlled Release
,
80
(
1–3
), pp.
9
28
.
43.
Sanders
,
R.
,
1973
, “
Torsional Elasticity of Human Skin In Vivo
,”
Pflugers Arch.
,
342
(
3
), pp.
255
260
.
44.
Grahame
,
R.
, and
Holt
,
P. J. L.
,
1969
, “
The Influence of Ageing on the In Vivo Elasticity of Human Skin
,”
Gerontology
,
15
(
2–3
), pp.
121
139
.
45.
Khatyr
,
F.
,
Imberdis
,
C.
,
Vescovo
,
P.
,
Varchon
,
D.
, and
Lagarde
,
J.-M.
,
2004
, “
Model of the Viscoelastic Behaviour of Skin In Vivo and Study of Anisotropy
,”
Skin Res. Technol.
,
10
(
2
), pp.
96
103
.
46.
Langer
,
K.
,
1978
, “
On the Anatomy and Physiology of the Skin—I: The Cleavability of the Cutis
,”
Br. J. Plast. Surg.
,
31
(
1
), pp.
3
8
.
47.
Nizet
,
J. L.
,
Piérard-Franchimont
,
C.
, and
Piérard
,
G. E.
,
2001
, “
Influence of Body Posture and Gravitational Forces on Shear Wave Propagation in the Skin
,”
Dermatology
,
202
(
2
), pp.
177
180
.
48.
Fung
,
Y.
,
1993
, Biomechanics: Mechanical Properties of Living Tissues,
Springer-Verlag
,
New York
.
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