Skin Research and Technology 2013; 0: 1–8 Printed in Singapore  All rights reserved doi: 10.1111/srt.12125

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Skin Research and Technology

Experimental and numerical analysis of soft tissue stiffness measurement using manual indentation device – significance of indentation geometry and soft tissue thickness J. T. Iivarinen1,2, R. K. Korhonen1 and J. S. Jurvelin1 1

Department of Applied Physics, University of Eastern Finland, Kuopio, Finland and 2Department of Physical and Rehabilitation Medicine, Kuopio University Hospital, Kuopio, Finland

Background: Indentation techniques haves been applied to measure stiffness of human soft tissues. Tissue properties and geometry of the indentation instrument control the measured response. Methods: Mechanical roles of different soft tissues were characterized to understand the performance of the indentation instrument. An optimal instrument design was investigated. Experimental indentations in forearm of human subjects (N = 11) were conducted. Based on peripheral quantitative computed tomography imaging, a finite element (FE) model for indentation was created. The model response was matched with the experimental data. Results: Optimized values for the elastic modulus of skin and adipose tissue were 130.2 and 2.5 kPa, respectively. The simulated indentation response was 3.9  1.2 (mean  SD) and 4.9  2.0 times more sensitive to changes in the elastic modulus of the skin than to changes in the elastic modulus of

adipose tissue and muscle, respectively. Skin thickness affected sensitivity of the instrument to detect changes in stiffness of the underlying tissues. Conclusion: Finite element modeling provides a feasible method to quantitatively evaluate the geometrical aspects and the sensitivity of an indentation measurement device. Systematically, the skin predominantly controlled the indentation response regardless of the indenter geometry or variations in the volume of different soft tissues.

of human soft tissues can be altered by normal aging (1) or pathological conditions (2). Soft tissue mechanics has been investigated using compression (3–6), suction (7–10), or tension (11, 12) measurements. Compression testing is often conducted for skin (1, 13–15), adipose tissue (16, 17), and muscle (18, 19). Earlier, a hand-held indentation device was designed for the measurement of soft tissue stiffness in vivo (13). At present, it is not known whether the device is optimally designed to detect sensitively the changes in the mechanical characteristics of soft tissues, such as skin, adipose tissue, and muscle. To optimize the instrument design for measurement of soft tissue pathologies, finite element (FE) modeling may be utilized. Even though FE modeling has

actively been used in designs of bioengineered materials, e.g., aortic valve (20), coronary stent (21, 22), hip stem (23), interbody device (24), meniscal implant (25), micropillar arrays (26), and voice-producing prosthesis (27), optimization of the measurement devices has been conducted to a lesser extent. Earlier, the skin layer was proposed to control the indentation response of human forearm (3). However, it is not known how the volume of different soft tissues (skin, adipose tissue, and muscle) affects the overall indentation response, and the sensitivity of such measurement device. Therefore, main aims of this study were to evaluate the importance of the indenter dimensions and soft tissue thickness on the indentation response. For these aims, we conducted experimental indentation measurements

M

ECHANICAL PROPERTIES

Key words: soft tissue – skin – adipose tissue – muscle – finite element analysis – indentation – sensitivity – tissue volume

Ó 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Accepted for publication 21 October 2013

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of human forearm. Using an FE model with realistic geometries of major soft tissues, obtained from peripheral quantitative computed tomography (pQCT) imaging, we simulated the experimental indentation measurements. The effects of thickness and material properties of different soft tissues on the measured biomechanical response were quantified with the model. The present findings could aid to improve the diagnostic sensitivity of the stiffness measurement for soft tissue pathologies.

Materials and Methods Study protocol Mechanical indentations were conducted for the forearm of each subject (N = 11). Then, pQCT images were taken to determine the dimensions of soft tissues at the site of the mechanical measurements. The FE model, based on those mean dimensions, was fitted to the experimental indentation measurements by optimizing the values of model parameters for tissues. Subsequently, sensitivity of the indentation response to changes in the mechanical properties and thickness of different tissues was evaluated using the FE model. Optimal geometry of the indentation device to detect mechanical properties of different tissue layers was also analyzed.

Subjects and measurements Eleven healthy volunteers (nine males, two females, age = 31  7 years, height = 179  9 cm, weight = 84  9 kg, and length of ulna bone = 29  2 cm) participated in this study. All subjects gave their informed consent for the study. The study was approved by the Kuopio University Hospital Committee on Research Ethics (diary number 7/2010). The measurement device was a stiffness (compliance) meter (Fig. 1), a small hand-held indentation device for measuring the transient mechanical response of soft tissues (3, 13). It consists of two coaxial load cells: (i) 10 kg (Honeywell Sensotec load cell 31/1430-04 Mid, Columbus, OH, USA), which measures the force at the end of the rod cover (reference plate); and (ii) 1000 g (Honeywell Sensotec load cell 31/1426-02 Mid), which measures the indenter force. The sum of the reference plate and indenter forces is the total (compressing)

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force. The outer and inner rod diameters were 30.5 and 6.6 mm, respectively. The indenter diameter and length were 2.0 and 1.0 mm, respectively. The instrument was connected to a PC computer for data acquisition. The sampling frequency for the data acquisition was 1000 Hz. The data was recorded through the entire measurement period. During the mechanical measurements, the stiffness meter was pressed instantaneously against the skin surface until a constant pre-defined load (4 N) was reached, similarly as presented earlier (3). The subject’s arm laid on a mechanical support during the test protocol and muscle activity was avoided. The indentation sites were localized in the mid ulna (proximal-distal direction), between the ulna and the radius on the dorsal forearm. During the measurement protocol, 20 repeated measurements were conducted. After measurements, the measurement data were analyzed using Matlab (version 7.12.0; Mathworks Inc., Natick, MA, USA).

pQCT measurements The pQCT imaging of the forearm was performed at the sites of mechanical testing (Stratec XCT 2000, Stratec Medizintechnik GmbH, Pforzheim, Germany). One image slice (thickness = 2.3 mm, pixel size = 0.2 mm 9 0.2 mm, acceleration voltage 58 kV, and current 130 lA) was taken for each subject. Different tissue layers were manually segmented from the images, and the tissue areas were calculated using Matlab, similarly as presented earlier (10).

Fig. 1. Schematic presentation of the stiffness meter. Modified from (13).

Analysis of soft tissue indentation stiffness

FE models and simulations As the exact model geometry from pQCT images led to highly complex model geometry with high element count regions and excessive computation, each tissue cross-section in pQCT was approximated to be of circular shape (Fig. 2), similarly as presented earlier (10). Mean radii of the circular approximation of skin, adipose tissue, muscle, radius (bone), and ulna (bone) were 40.9, 39.3, 36.2, 6.8, and 7.1 mm, respectively. These tissue dimensions were used in the FE models, created using ABAQUS 6.12 (SIMULIA; Dassault Systemes, Providence, RI, USA). In the model geometry, the forearm was 30 cm in length, long enough to exclude all edge effects in the model. Optimal density for the FE mesh was found after running a convergence study. Then, the mesh at the areas of interest (in close proximity of the stiffness meter and skin contact area) was denser to obtain smooth stress/strain distributions. In average, the device consisted of 1900, the skin of 14 000, the adipose tissue of 13 900, and the muscle of 3700 8-node 3D elements with reduced integration (C3D8R) and the skin fibers of 41400 spring elements (SPRINGA). Contact between the stiffness meter and the skin was assumed to be frictionless. The ulna and radius bones in the model were considered to be rigid and static by restricting the movement of the muscle nodes in contact with the bones. The both ends of muscle tissue were fixed. Skin was modeled to be fibril-reinforced hyperelastic and adipose tissue and muscle as hyperelastic (HE) (10, 28, 29). Neo-Hookean material model was used for all soft tissues to imitate the nonlinearity of biological soft tissues, especially skin and adipose tissue, under shortterm loading (3, 5, 30–34). As the Neo-Hookean (a)

material is defined with only two parameters, optimization of the material parameters was straightforward. The strain energy potential function of the Neo-Hookean model is expressed in the form U ¼ C10 ðI1  3Þ þ

1 el ðJ  1Þ2 D1

ð1Þ

where I1 is the first deviatoric strain invariant, J the elastic volume ratio, and C10 and D1 are parameters defining the shear behavior el

C10 ¼

G0 E ¼ 4ð1 þ vÞ 2

ð2Þ

and the bulk behavior D1 ¼

2 6ð1  2vÞ ¼ B0 E

ð3Þ

In equations 2 and 3, G0 is the initial shear modulus, B0 the initial bulk modulus, E the elastic modulus and m the Poisson’s ratio. Therefore, both C10 and D1 can be expressed with E and m. The Poisson’s ratio for each tissue was fixed to 0.4, similarly to previous studies (3, 10, 19, 35–38). Fibril-reinforcement, mimicking collagen mechanics, was added to the skin properties, similarly as presented earlier (10). This was realized using nonlinear springs, which were aligned along tension axes. Mechanical tensile properties of the collagen fibers could then be described by the fibril network modulus Ef = Dr/De (describing the rigidity of straightened fibrils) and the toe limit strain e0 [describing the effect of fibril straightening (10, 11, 39)], where r is stress and e is strain. In the model, we minimized the number of optimized parameters to attain unique results (b)

Fig. 2. (a) A geometry and mesh of the finite element model. (b) A portion of the cross-section geometry of the mid region of the model (mesh hidden). Different tissue areas are indicated with different colors. The model development is explained more in detail in (10).

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from simulations. The mechanical role of the muscles was found to be minimal and the fibril network modulus of skin of more than 50 MPa produced similar tissue deformations (10). Therefore, elastic modulus of the muscle tissue was fixed to 100 kPa (3, 6, 10, 36, 37, 40) and the fibril network modulus of the skin was fixed to a value of 4.4 GPa (41). Optimization of the material properties was conducted for the elastic modulus of skin, toe limit strain of skin fibrils, and elastic modulus of adipose tissue by minimizing the mean squared error between the simulated and experimental responses. A multidimensional unconstrained nonlinear minimization routine, utilizing Nelder-Mead method in Matlab, was used. Sensitivity of the indentation response in the forearm to different soft tissues was investigated using the FE model. In the model, the parameter values of the tissues were changed independently from 50% to 200% of the optimized, reference values, and their effects on the simulated mechanical response were analyzed. Sensitivity is a relative (%) value, calculated by comparing the outcome of simulated reference response with that obtained using altered tissue parameter values. The described sensitivity analysis was conducted separately for different indenter geometries and tissue volumes (~thicknesses). Twelve different indenter geometries were analyzed: indenter width (2 and 2.5 mm), length (0.5, 1.0, and 2.0 mm), and head shape (radius of the rounding 1 mm). The indenter head in the simulations was constructed using different rounding geometries: the first geometry consisted of filleted edges radii of 0.1, 0.2, and 0.4 mm (termed ‘corner’); the second geometry consisted of a sphere using a radius of 1 mm (termed ‘sphere’); the third geometry consisted of a rounded indenter tip that matched the curvature of a sphere that had a radius of 1.625 and 2.5 mm (termed ‘oval’) (Fig. 3). Finally, sensitivity analysis was conducted after the skin and adipose tissue volumes were changed from 50% to 200% of the reference (measured) value.

Results The average experimental indenter force, indicator of tissue stiffness (13), was 0.32  0.07 N (mean  SD, range 0.25–0.47 N, N = 11) under a total force of 3.93 N (Fig. 4). Values of the

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(a)

(b)

(c)

Fig. 3. The head shapes of the simulated indenters (a) corner, (b) sphere, and (c) oval. The illustrations of the circular shaped rounding geometries used for the indenter design are shown. R, indenter shaft radius and r, radius of the rounding geometry.

Fig. 4. Experimental measurement results and model simulations for the subjects (N = 11). The mean error between the experimental measurements and the finite element model was less than 2.5%.

elastic modulus of skin and adipose tissue, as obtained by fitting the model to the experimental data, were 130.2 and 2.5 kPa, respectively. The optimized fibril toe limit strain was 7.19%. The simulated indenter force was most sensitive to changes in the elastic modulus of the skin layer, whereas adipose tissue, muscle, and toe limit strain of the skin fibrils affected less the indentation response of the forearm under all indenter geometries investigated (Fig. 5, Table 1). The simulated response was 3.9  1.2 (mean  SD, range 2.4–6.3), 4.9  2.0 (range 1.7–8.7), and 2.2  0.7 (range 1.4–3.8) times more sensitive to changes in the elastic modulus of the skin than to those of the adipose tissue, muscle, and toe limit strain of the skin fibrils, respectively. The indenters of 0.5 mm in length detected most sensitively the stiffness changes in the skin, whereas indenters with lengths of 1 and 2 mm were 6.5–13.6 and 28.5– 32.4% less sensitive, respectively. Similarly, the

Analysis of soft tissue indentation stiffness

with the modulus of the skin and the fibril toe limit strain (13.5–25.6%) (Fig. 6, Table 2). Also, a similar change in the volume of the adipose tissue had relatively a major effect on the sensitivity of the stiffness meter to measure the elastic modulus of the muscle (69.7%), as compared to the modulus of the adipose tissue and fibril toe limit strain (9.1–9.2%) and the modulus of the skin (5.3%).

Discussion

Fig. 5. Sensitivity of the simulated indenter force to the changes in the elastic modulus of skin, adipose and muscle tissues, and the fibril toe limit strain of the skin fibrils. Responses using 50% or 200% of the optimized material values were examined to analyze sensitivity of the measured indenter force to changes in the values of material parameters (Table 1). Same sensitivity analyses were conducted for indenter lengths of 0.5, 1, and 2 mm.

indenters of 2 mm in diameter revealed the stiffness changes in the skin most sensitively, whereas the indenters of 2.5 mm in diameter were 10.9–15.9% less sensitive. Moreover, the spherical-ended indenters detected the stiffness changes in the skin most sensitively, whereas indenters with oval and corner rounded ends were 0.8–8.3 and 4.4–12.5% less sensitive, respectively. In simulations, changes (50% and 200%) in the skin volume had relatively higher impact for the sensitivity of the stiffness meter to measure the elastic modulus of the adipose tissue and the muscle (53.1–57.4%), as compared

A hand-held indentation instrument, a stiffness meter, may provide a simple method to quantitate changes in the material characteristics of the skin caused by, e.g., aging or pathological tissue swelling. Realistic FE simulations can help to optimize the indentation geometry, as well as to analyze the effect of tissue thickness and mechanical properties on the indentation response. In this study, mechanical responses of human forearm soft tissues were measured using a stiffness meter (3, 13). A HE 3D FE model with the geometry obtained from pQCT imaging was created to determine the mechanical properties of soft tissues (skin, adipose tissue) in forearm. Then, the tissue model was used to evaluate optimal indenter geometry for measurement of the mechanical properties of skin. Finally, sensitivity of the stiffness meter to variations in thickness of different soft tissue layers was analyzed. The present values of elastic modulus for the skin (130.2 kPa) and adipose tissues (2.5 kPa) are well in range with those reported in earlier studies; 8–540 kPa for the skin (3, 7, 10–12, 42) and 0.5–5.6 kPa for the adipose tissue (3, 10, 37,

TABLE 1. Sensitivity of the simulated indentation force for the elastic modulus of the skin Eskin, adipose Eadip.tis., muscle Emuscle tissue, and the toe limit strain e0 for 12 different indenter geometries Indenter characteristics

Sensitivity for parameter

No.

Length (mm)

Diameter (mm)

Head shape (rounding)

Eskin (%)

Eadip.tis. (%)

Emuscle (%)

e0 (%)

1 2 3 4 5 6 7 8 9 10 11 12

0.5 0.5 0.5 0.5 0.5 1 1 1 0.5 1 2 2

2 2 2 2 2 2 2 2 2.5 2.5 2 2.5

Sphere (r = 1 mm) Corner (r = 0.4 mm) Oval (r = 2.5 mm) Corner (r = 0.2 mm) Corner (r = 0.1 mm) Sphere (r = 1 mm) Oval (r = 1.625 mm) Corner (r = 0.4 mm) Corner (r = 0.4 mm) Corner (r = 0.4 mm) Corner (r = 0.4 mm) Corner (r = 0.4 mm)

38.2 35.5 35.1 33.5 33.5 33.1 32.8 31.6 29.9 26.8 24.0 21.4

6.1 7.4 7.2 7.7 7.5 8.3 9.2 9.7 8.4 10.6 9.3 8.9

4.4 5.6 5.4 5.9 5.2 6.7 7.0 7.5 6.4 8.8 11.8 12.4

10.0 13.6 11.5 13.4 13.6 17.5 17.9 18.4 12.1 17.1 16.6 14.8

Highest/lowest sensitivity values are bolded/underlined.

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Iivarinen et al. (a)

(b)

Fig. 6. Sensitivity of the simulated indenter force to the changes in the elastic modulus of skin, adipose and muscle tissues, and the fibril toe limit strain of the skin fibrils. Responses using 50% or 200% of the optimized material values were examined to analyze sensitivity of the measured indenter force to changes in the values of material parameters (Table 2). Same sensitivity analyses were made with the volumes of 50%, 100%, and 200% of the measured volume of the (a) skin and (b) adipose tissue.

TABLE 2. Sensitivity of the simulated indentation force for the elastic modulus of the skin Eskin, adipose Eadip.tis., muscle Emuscle tissue, and the toe limit strain e0 for the reference (100%) and 200 and 50% of the skin and adipose tissue volumes. The simulated indenter length was 1 mm, diameter 2 mm with filleted edges (r = 0.4 mm) Tissue volume

Sensitivity for parameter

No.

Skin

Adipose tissue

Eskin (%)

Eadip.tis. (%)

Emuscle (%)

e0 (%)

1 2 3 4 5

1 2 0.5 1 1

1 1 1 2 0.5

31.6 40.7 24.5 28.7 31.2

9.7 5.5 15.8 8.8 8.9

7.5 4.1 12.7 2.8 13.3

18.4 13.8 18.8 19.9 16.5

Highest/lowest sensitivity values are bolded/underlined.

43, 44). The fibril toe limit strain value (7.19%) is slightly higher than the values we reported earlier 1.86–4.40% (10). However, the fibril toe limit strain is strongly affected by the pre-strain

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of the skin. Also, different mechanical loading, e.g., compression vs. tension, might impact differently the toe limit strain, presumably due to simplifications in the tissue model. In simulations, shorter and spherical-ended the indenter was, more sensitive the stiffness meter was to record changes in the skin properties. However, from a practical point of view, a very short indenter might be prone to measurement uncertainties caused by non-flat skin surface. Also, a short indenter can complicate the measurements at a right angle (perpendicular to the skin). In experiments, a 1-mm long indenter was found to be sensitive enough and userfriendly. Longer indenters could detect more sensitively stiffness changes in the adipose and muscle tissues. However, the impact of the skin on the response was always dominating. Therefore, highly reliable measurements on the stiffness changes in the adipose or the muscle tissue might prove challenging. Based on modeling, an indenter with lower diameter was also more sensitive to changes in the stiffness of skin. A more spherical-ended indenter seemed to improve sensitivity to measure stiffness changes in the skin. At a constant force, a spherical-ended indenter, as compared with a plane-ended indenter, produces larger strains in skin layer. This may lead to higher sensitivity. Thickness of skin layer strongly affected the ability of the indentation technique to detect changes in the mechanical characteristics of the underlying adipose and muscle tissue. Also, simulated thickness of skin layer had medium impact on the sensitivity of the stiffness meter to measure the skin and the fibril toe limit strain. Correspondingly, changes in the amount of adipose tissue affected sensitivity to detect properties of muscle tissue. However, thickness of the adipose tissue had a minimal impact on the sensitivity to record the stiffness of overlying skin. On the other hand, rapid changes in the fat layer thickness (e.g., after losing or gaining weight) may control the initial (“relaxed”) tension level of the skin, and thereby influence the skin stiffness, as recorded using the indentation technique. As the effect of muscle on the indentation response is more significant for people with low body fat, it is essential to avoid all muscle activity during measurements at rest. In the models, ideal perpendicular indentation measurements on the forearm soft tissues were simulated. In the future models, non-opti-

Analysis of soft tissue indentation stiffness

mal measurements with angular errors in indentation approach should be analyzed to reveal some of the uncertainties in practical measurements. The importance of the size of the reference plate on the simulated response was not systematically analyzed and should be conducted in the future. However, it can be noticed (Fig. 4) that the reference plate of the present device (13) is able to deform the soft tissue in the forearm when loaded with forces >0.1 N. With a larger reference plate, this deformation would be decreased. In conclusion, FE modeling provided a feasible method to optimize geometrical aspects of soft tissue meter. The present model was also able to address the significance of variations in tissue volumes on the indentation response. Considering the soft tissue indentation, the skin predominantly affects the indentation response. From simulation point of view, a short and thin indenter is the most optimal for measurement of mechanical characteristics in skin. The present experimental and numerical results suggest that the stiffness meter can be useful in diagnostics of soft tissue disorders, namely those that modify the mechanical consistency of soft tissues,

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Acknowledgements This study was funded by the Finnish Funding Agency for Technology and Innovation (TEKES, funding decision 70011/09), North Savo Regional fund of Finnish Cultural Foundation, Northern Savo Hospital District (EVO – special state subsidy), Doctoral Programme in Medical Physics and Engineering of University of Eastern Finland, Kuopio University Foundation, Foundation for Advanced Technology of Eastern Finland, the Academy of Finland (grant 218038), and Oy LabVision Technologies Ltd (Lappeenranta, Finland). Furthermore, the strategic funding of the University of Eastern Finland was used. The funding sources were not involved in conducting this research or in preparing this manuscript. CSC – IT Center for Science, Finland, is acknowledged for computational resources and Delfin Technologies Oy Ltd (Kuopio, Finland) for technical support.

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Address: J. Iivarinen Department of Applied Physics University of Eastern Finland Yliopistonranta 1F 70211 Kuopio Finland Tel: +358 407007121 Fax: +358 17162585 e-mail: jarkko.iivarinen@uef.fi

Experimental and numerical analysis of soft tissue stiffness measurement using manual indentation device--significance of indentation geometry and soft tissue thickness.

Indentation techniques haves been applied to measure stiffness of human soft tissues. Tissue properties and geometry of the indentation instrument con...
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