- Email: [email protected]
New extensometer to measure in vivo uniaxial mechanical properties of human skin
ARTICLE IN PRESS
Journal of Biomechanics 41 (2008) 931–936 www.elsevier.com/locate/jbiomech www.JBiomech.com
New extensometer to measure in vivo uniaxial mechanical properties of human skin K.H. Lima,b,, C.M. Chewb, P.C.Y. Chenb, S. Jeyapalinac, H.N. Hoc, J.K. Rappelc, B.H. Limc a
Digital Medicine Laboratory, National University Hospital, Singapore 119260, Singapore Department of Mechanical Engineering, National University of Singapore, Singapore 119260, Singapore c Department of Orthopaedic Surgery, National University of Singapore, Singapore 119260, Singapore
b
Accepted 9 January 2008
Abstract Biomechanical properties of skin are important for clinical decision making as well as clinical intervention. Measuring these properties in vivo is critical for estimating dimensional behaviour of skin flap or graft after harvest. However, existing methodologies and devices often suffer from lack of standardisation and unwanted peripheral force contribution due to the deformation of surrounding tissues during measurement. This naturally leads to measurement inaccuracies and lack of reproducibility. In order to improve the measurement accuracy, a new portable extensometer, which measures the non-invasive in vivo biomechanical properties of skin, has been designed and constructed. This design incorporates three pads that attach to the skin, including a C-shaped pad to shield the force sensor from peripheral forces. Such design produces data that are significantly closer to in vitro measurements. The results have been verified by finite element analysis, and experiments on rubber sheets and pig skins. This device can be used to obtain biomechanical properties of skin that will aid doctors in measuring skin elasticity and surgical planning, especially in skin flap surgery. r 2008 Elsevier Ltd. All rights reserved. Keywords: Skin measurement device; Extensometer; Biomechanical properties; Skin flap; In vivo
1. Introduction Skin flap and graft transplants are common in reconstructive surgery, where surgeons transfer a healthy skin flap from a donor site to a wound site. Skin is subjected to pre-tension on a human body (Cox, 1941; Langer, 1978) and thus when a piece of skin is harvested from a donor site, it is known to undergo deformation. The amount of deformation is known to be highly sensitive to the patientspecific skin structure and internal tension, and this varies with age, health, location and BMI index. In practice, often inaccurate size skin flaps are harvested due to the lack of quantitative tools, poor understanding of the biomechanical behaviour of the skin and inexperience of the surgeon. This usually leads to further complications during surgery Corresponding author at: Digital Medicine Laboratory, National University Hospital, Singapore 119260, Singapore. Tel.: +65 68 742 137; fax: +65 67 791 459. E-mail address: [email protected] (K.H. Lim).
0021-9290/$ - see front matter r 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2008.01.004
and unnecessary trauma to the patient. Therefore, in order to assist surgeons during the critical stage of skin flap planning and to reliably predict the deformation of skin flap, there is a need to develop an appropriate measurement method that will consistently predict the biomechanical property of skin. Skin is a complex structure and is classified as a nonlinear viscoelastic material. It comprises three main layers, namely the epidermis, dermis and subcutaneous (fat) layers. The latter two layers contain a network of blood vessels (Fawcett, 1986). The entire flap sits above the muscle surface, separated by a thin layer of fascia; is particularly dense in the scalp, the back of the neck and the palms of the hands, where it serves to anchor the skin firmly to underlying tissues. In other areas of the body, such as the dorsal or volar skin regions, it is loose and the skin may be moved freely. Skin also shows directionally dependent mechanical properties and it is reported to be stiffer along the Langer’s lines compared with across the Langer’s lines (Alexander and Cook, 1977; Cox, 1941;
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Daly, 1982; Langer, 1978; Reihsner et al., 1995; Stark, 1977). The biomechanical properties of skin have been measured by both in vivo and in vitro methods. The simplest method is the in vitro tensile testing, where the applied stress and resultant strain are measured under a carefully controlled environment and thus the material constants can be determined accurately; here, the stress field in the test material is uniform. In vivo test on the other hand, is challenging as explained earlier and therefore the results are descriptive and suffer from lack of reproducibility. Berardesca and Elsner conducted comprehensive literature reviews on current skin measurement devices (Berardesca et al., 1995; Elsner et al., 2002). Their studies revealed that all the in vivo non-invasive devices are capable of determining a qualitative measure of the mechanical properties, but the measured result differs from in vitro measurements significantly. Thus, this research work was undertaken to develop a new device to address this problem. Current commercial skin measurement devices measures skin properties by applying deformation forces in various manner. One set of devices, such as the cutometer, produces multi-axial loading on skin and thus is not capable of identifying directional differences. In contrast, uniaxial extensometers can be used to ascertain directional differences in material properties. A uniaxial extensometer works by applying displacements to the skin using two extensible pads/tabs/legs that are attached to the skin using double-sided tape. The force needed for deformation is measured by a load cell as the skin deforms (Evans and Siesennop, 1967; Baker et al., 1988; Gunner et al., 1979a, b; Larrabee, 1986; Manschot and Brakkee, 1986; Vescovo, 1998). In order to study the directionally dependent in vivo biomechanical properties of skin, a custom made extensometer was designed and built during this investigation.
F’
F
A
B
F’ Fig. 1. Stretching of surrounding skin contributes to peripheral forces F0 ; where A and B represent the two pads of a typical extensometer; the force is measured by a load cell at B.
F´
F B
A
C
F´ Fig. 2. Pad arrangement showing how the pad C is positioned to shield the load cell (at pad B) from peripheral forces; pads B and C move as a single unit during operation.
isolate the force in the test direction, thus yielding results that are closer to an actual in vitro measurement.
2. Methods 2.1. Description of new extensometer design 2.1.1. Design concept In a typical extensometer design, two pads that are attached to the skin surface using adhesive deform the skin during a measurement. Using such instruments to achieve an actual force–displacement profile of the area of skin between the pads is not possible. When extension is applied to the skin, not only the skin tissue between the pads deforms, but also the surrounding tissue too. This inevitability contributes to the overall force detected by the force sensor on the device. Therefore, as pictorially represented by Fig. 1, the measured force also includes force contributed from directions other than the test direction. The dotted lines are simplified tensor line representations of tensile forces during skin stretch. In order to improve the uniaxial measurement, a new extensometer was devised and the arrangement of the pads is shown in Fig. 2. Here, a third pad (a C-shaped shield pad) partially envelopes Pad B which contains the load cell, thus effectively shielding out the peripheral forces F0 during measurement. Pad C achieves this by moving together with pad B, thus isolating the skin region between B and C so that the skin tension there remains constant as the skin at other parts stretches during measurement. In this way, the load cell is mostly subjected to experience the uniaxial force F between A and B. This arrangement was shown to effectively
2.1.2. Constructed extensometer A schematic diagram of the constructed device is shown in Fig. 3(a). This device, developed to conduct tests at a user-defined extension rate, consists of the three pads A, B and C mounted along a carriage. During measurement, the extensometer is attached to the skin at the pads using double-sided adhesive tape. Pad A is fixed to the carriage body while B and C are free to slide on the carriage. The load cell, which has a flat profile, is attached to the pad B for force measurement and the pad C is used to shield the peripheral forces during the stretching from being detected by the load cell. Fig. 3(b) shows the pad dimensions used. Pads B and C (attached together as a single unit) are connected via a lead screw to a servomotor, which actuates the pads along the carriage. The displacement of the pads is logged from the servomotor encoder and the force is measured by the load cell, which has a resolution of 2 mN. Pads B–C have a maximum velocity of 0.6 mm/s. A computer, connected to the servomotor, motor controller and driver, strain gauge amplifier and data acquisition card, is used to automatically control the movement of the pads and to log measurement data. 2.1.3. Articulated arm Fig. 4 shows the articulated arm that is designed to hold the device onto the skin. Using the articulated arm to hold the device during measurement is part of the standardisation protocol that is intended to eliminate
ARTICLE IN PRESS K.H. Lim et al. / Journal of Biomechanics 41 (2008) 931–936
D
A B
C
G
E F
30
10
10 36
A
12
36
B
10
C
* All dimensions in mm
Fig. 3. (a) Schematic drawing of extensometer showing: A—fixed pad, B—pad (attached to the load cell and is movable along the carriage), C— C-shaped shield pad (moves simultaneously with pad B), D—load cell, E—lead screw, F—carriage and G-servo motor. (b) Pad dimensions.
Articulated arm
Device slides freely
Linear slide, H
Extensometer Fig. 4. Photograph of shield pad extensometer mounted on an articulated arm with a linear slide attachment. handling inconsistency and variations in contact pressure of the device on the skin. This arm has six degrees of freedom and thus enables the device to be easily placed in any position. It also has sufficient stiffness so that pad A remains stationary relative to the underlying skin tissue during measurement, and the only movement occurs at pads B and C. In order to standardise the device placement, a low friction vertical linear slide is used at the mount attachment so that the device always presses onto the skin with its own weight (2.45 N).
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2.2.2. In vitro measurements: rubber strip Using a universal tensometer (Instron, model no. 5440), the typical force–extension measurements of the rubber (Therabands) strips were obtained. In order to avoid the premature failure at the gripper/pads, a dumbbell-shaped specimen of test size 25 (L) 12 (W) mm was stretched at a pre-defined speed of 0.6 mm/min and the resultant force extension data was recorded. This procedure was repeated three times. 2.2.3. In vivo measurements: rubber sheet The force-elongation experiments using the extensometer were conducted on large Therabands sheets (both yellow and grey) using both the traditional two-pad and the proposed shield pad arrangement. The experimental settings were the same as what were used in the earlier measurements on the rubber strips. The measurements were performed at the centre of square sheets (120 mm 120 mm), which were attached by double-sided tape onto a fixed frame (on all four sides) to emulate skin covering a human body. The articulated arm was used to hold the extensometer over the sheet, so that the position of pad A was fixed relative to the frame. Since the rubber edges were constrained by the frame, the rubber surrounding the pads was stretched as the pads moved. This set of experiments were compared with the in vitro measurements described earlier to evaluate how effective the shield pad is in removing peripheral forces during stretching. 2.2.4. In vivo measurements: pig skin All handling and experimentation involving animals were done in a humane, ethical manner (animal ethical clearance number: 006/06; clearing authority: Institution of Animal Care and Use Committee, National University of Singapore). The pigs were humanely killed at the animal facility (according to the ethics regulations) and the hair at the planned test sites was shaved-off. In vivo extensometer measurements using both the two-pad and shield pad arrangements were carried out on abdomen, upper thigh and upper shoulder skin surfaces. The measurements were performed in the compressive mode, where the pads move towards each other instead of moving apart. The reasons for compressive mode measurement are discussed in the discussion section. Experimental sites were preconditioned by two successive loading–unloading cycles, and the data from the third cycle was taken as the actual measurement; it was observed that data points converged after the second cycle. Such preconditioning is necessary to obtain consistent and reproducible data, as explained by Fung (1996). Unlike the rubber experiments, pig skin was not harvested in order to obtain the in vitro measurements to compare against the in vivo ones. Instead, an island of skin area was isolated from the surrounding tissue (refer to Fig. 5) and in vivo compressive mode measurements were taken there. Isolating the skin area removes peripheral forces during
Extensometer
2.2. Mechanical testing 2.2.1. Materials Two rubber sheets (Therabands) with different stiffness were purchased from a hospital pharmacy. These two grades of Therabands (yellow and grey) have average stiffness values of 0.8 and 2.9 MPa at 50% strain, respectively. The yellow Therabands has stiffness values closer to that of elastic deformation region of skin. Two piglets (6 months old; genus: Sus; species: Duroc & Yorkshire) were supplied by the Singapore National University Hospital’s animal holding unit. Commercial doublesided tape (3 M) was purchased from a local supplier and used to attach the extensometer pads to the skin.
Extensometer pads
Fascia-muscle layer (skin flap removed)
Skin island under measurement
Fig. 5. Picture showing surrounding skin flap around the pads removed down to the fascia to remove influence of peripheral forces during measurement.
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measurement, thus emulating an in vitro setting. It is important that the skin remained attached to the body (via the fascia) because this was the state that the earlier in vivo measurements were taken. Thus, this ensured minimum variations at the underlying skin section among the three different measurement configurations. Furthermore, it should be noted that the test dimensions of the skin involved in all three configurations were similar, hence enabling effective comparison.
2.3. Finite element analysis A finite element simulation was also used to determine the effectiveness of the shield pad arrangement. A simulation representing the in vivo rubber stretching experiment (Section 2.2.3) was studied by the software Ansys 8.0 (Ansys, Inc.). These results will be compared with those simulated in an in vitro setting. For this simulation, the material was classified as a pure, incompressible elastic shell, with Young’s modulus of 0.8 MPa. This value was selected because it is of the same order of magnitude as skin stiffness.
3. Results Finite element method was employed to simulate the effectiveness of the proposed shield pad arrangement. The simulated results for measurement representing in vivo twopad and shield pad arrangements are given in Fig. 6(a) and (b), respectively. In the shield pad arrangement, the load cell that is located on pad B is protected from the generated compressive forces and the peripheral forces due to the deformation of surrounding materials. Therefore, the force experienced by the load cell will have minimal contribution from the forces of the surrounding tissues. Table 1 compares simulated results of stress in different settings when a strain of 0.42 is applied. In simulation, the average stress on all the nodes surrounding the pad labelled B is assumed to be stress that is experienced by the load cell and thus calculated. The percentage error of simulated stress values compared with the in vitro value was computed. It can be clearly seen that in vivo shield pad arrangement produces result that is much closer to the in vitro result. It was observed during the initial experiments that contact pressure of the device on the skin marginally
influenced the obtained reading. For verification, the contact pressure was varied by placing weights (2 N) on the top of the device before measurement, and the produced data was found to differ by about 10%; greater the pressure, larger the difference. Owing to this sensitivity, an articulated arm with a vertical slide attachment was used to hold the extensometer onto the body so that the device rests on the skin with its own weight, as seen in Fig. 4. Two sets of experiments were conducted to test the effectiveness of the shield pad on constrained rubber sheets and pig skins. Hysteresis data of the rubber sheets are shown in Figs. 7 and 8. Both yellow and grey Therabands produced the same trend, where it can be seen that the shield-pad data are significantly closer to the in vitro data, but the data from the traditional two-pad diverge significantly from the in vitro data. The results from the in vivo pig experiment have the same outcome, where the shield pad data are significantly closer to the data in which the skin sides are removed (‘‘in vitro’’ setting emulated). The typical results are given in Fig. 9. 4. Discussion Data measured in an in vitro setting may be considered as the true biomechanical uniaxial properties of the skin because the stress field in the test material is uniform. Since the shield pad has been shown in different experiments to produce results that were close to the in vitro measurements, it is deemed that this new design is capable of Table 1 FEM simulated stress at a strain of 0.42, and percentage difference of in vivo stress values compared with the in vitro value Method of simulation
Stress (MPa) at 0.42 strain
Difference (%)
In vitro arrangement Shield pad arrangement Traditional two-pad arrangement
0.34 0.39 0.66
– 13.7 91.0
Fig. 6. Finite element modelling of material that is constrained on a 120 mm 120 mm frame, undergoing an extension test by extensometer: (a) traditional two-pad arrangement and (b) shield pad arrangement. Shades represent stresses along the principle (horizontal) direction of testing.
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3 In-vivo 2-pad arrangement
0.08
In-vivo shield-pad arrangement
2.5
Force / Width (N / mm)
In-vitro measurement
Force (N)
2 1.5 1
0.07 0.06 0.05
In-vivo 2-pad arrangement In-vivo shield-pad arrangement In-vivo (skin sides separated)
0.04 0.03 0.02 0.01
0.5
0 0.0
0 2
4 6 Displacement (mm)
8
Fig. 7. Force–extension data of rubber (yellow Therabands) showing the curves obtained by in vivo two-pad, in vivo shield pads and in vitro tensile testing.
7 In-vivo 2-pad arrangement
6
In-vivo shield-pad arrangement In-vitro measurement
Force (N)
5 4
2 1 0 2
4 6 Displacement (mm)
8
10
Fig. 8. Force–extension data of rubber (grey Therabands) showing the curves obtained by in vivo two-pad, in vivo shield pads and in vitro tensile testing.
measuring the true properties effectively. It can also be observed that the differences between the shield-pad result and in vitro result is greater for the grey than yellow Therabands. This is expected because the grey Therabands is stiffer than the yellow one and so the magnitude of the peripheral forces, which cannot be completely removed by the shield pad, is higher. It should be noted that the experiments were carried out in the extensive mode for rubber sheets and in the compressive mode for pig skin. In the extensive mode, the pads moved apart at the loading cycle, and then moved back together at the subsequent unloading cycle; compressive mode is the reverse. The compressive mode measurement is conducted for skin because the skin at rest on the body is already in a stretched state with internal tension. Therefore, the biomechanical properties will be measured for the skin from the initial pre-tensioned state, to a relaxed tension-free state, and then to a wrinkled/compressed state. Since the purpose of this research is to eventually estimate the skin deformation upon harvest (where the skin is
4.0 6.0 Displacement (mm)
8.0
0.05 In-vivo 2-pad arrangement In-vivo shield-pad arrangement In-vivo (skin sides separated)
0.04 0.03 0.02 0.01 0 0.0
3
0
2.0
10
Force / Width (N / mm)
0
2.0
4.0 6.0 Displacement (mm)
8.0
Fig. 9. Force–displacement data from pig (a) belly region (b) shoulder region, showing the curves obtained by in vivo two-pad, in vivo shield pads and in vivo two-pad of isolated Skin Island. Note that for the plots’ vertical axes, the force is normalised against the width of the load cell pad because the pad widths used for the three experiments differ slightly.
tension free), it is therefore more relevant to measure in the compressive mode. In fact, a method has been proposed to use the mechanical behaviour in the compressive direction to estimate flap deformation upon harvest (Lim et al., 2006). When calculating the stress involved during measurement, the width of the skin tested must be known. In an in vitro measurement, the width of the skin tested is simply the width of the sample itself since the stress field is uniform. Manschot had suggested that in an in vivo extensometer measurement (using the traditional two-pad extensometer), the effective width of the skin can be approximated by the width of the pads itself (Manschot and Brakkee, 1986). However, this cannot be the case since the adjoining skin around the pads is inevitably deformed during measurement, which can also be clearly seen in the simulated FEM images. In the experiments conducted with the new device, it is evident that the in vivo measurements showed significant closeness with the in vitro measurements (in which the width of the samples tested were the same as the width of pad B). Thus, it can be concluded that in the new device, the effective width of the skin measured in vivo can be approximated by the width of the pad itself, thus enabling the stress involved during measurement to be calculated directly and conveniently.
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It was found that contact pressure of the device on the skin should be standardised during measurement. As the forces measured were small, the load cell used was very sensitive such that forces from directions other than the measurement axis may be registered marginally. Since downward pressure created vertical forces which would affect the reading, this variable should be kept constant by standardising the contact pressure. The design solution currently employed was to use a vertical slide attachment at the articulated arm so that the extensometer always pressed onto the skin with 2.45 N (i.e. its own weight). However, this design has the disadvantage that measurements must be done with the device at a horizontal position. For future improvement, a pressure transducer can replace the slide attachment to ensure a constant pressure. Ideally, the extensometer should just sit on the skin surface with zero pressure. Rodrigues reported that the literature reviews of the in vivo measurement of Young’s modulus of elasticity of skin produced results that vary by four orders of magnitude (Rodrigues, 2001). For devices of different measurement principles, e.g. suction and traction, the results may inevitably differ due to dissimilar methods of load application and force measurement. However, for devices of the same principle, one reason for the inconsistency may be the lack of standardisation. While there is currently no internationally adopted standard, this issue must be recognised when conducting measurement on skin. Therefore, a standardising protocol was used in this study, which included standardising the pad dimensions, initial distance between the pads, strain rate, device contact pressure, the means of holding the device during measurement, skin preconditioning and controlled environment. This protocol, coupled with the new shield pad design, would ensure that the results obtained are consistent, reproducible and more accurate. 5. Conclusion It can be concluded that by eliminating the peripheral forces during an in vivo skin measurement, one can obtain considerably reliable biomechanical properties of skin that are significantly closer to the actual in vitro properties. Thus, an extensometer with an additional third pad, shielding the pad containing the force sensor, was proposed. Experimental results indicated such arrangement was effective. Finally, it can be summarised that a measurement standardisation protocol that consisted of the device design and measurement parameters should be used. Compared with a traditional design of two-pad arrangement, this new system is standardised to obtain accurate, reliable and consistent results. Conflict of Interest There is no conflict of interest associated with this publication and there has been no significant financial
support for this work that could have influenced its outcome. Acknowledgements Authors wish to thank the Biomedical Research Council (A*STAR) of Singapore for the financial support and also wish to express gratitude to NUS and NUH staff members, who have contributed their time and ideas to this project. References Alexander, H., Cook, T.H., 1977. Accounting for natural tension in the mechanical testing of human skin. Journal of Investigative Dermatology 69, 310–314. Baker, M.R., Bader, D.L., Hopewell, J.W., 1988. An apparatus for testing the mechanical properties of skin in vivo: its application to the assessment of normal and irradiated pigskin. Bioengineering of Skin 4, 87–103. Berardesca, E., Elsner, P., Wilhelm, K., Maibach, H. (Eds.), 1995. Bioengineering of the Skin: Methods and Instrumentation. CRC Press, Boca Raton, London, New York. Cox, H.T., 1941. The cleavage lines of the skin. British Journal of Surgery 29, 234–240. Daly, C.H., 1982. Biomechanical properties of dermis. Journal of Investigative Dermatology 79, 17–20. Elsner, P., Berardesca, E., Wilhelm, K., Maibach, H., 2002. In: Bioengineering of the Skin. CRC Press, Boca Raton, London, New York, Washington, DC (Chapters 5–14). Evans, J.H., Siesennop, W.W., Controlled quasi-static testing of human skin in vivo. In: Digest of the Seventh International Conference on Medical and Biological Engineering, Stockholm, 1967. Fawcett, D.W. (Ed.), 1986. A Textbook of Histology, 11th ed. W.B Saunders Company, Philadelphia. Fung, Y.C. (Ed.), 1996. Biomechanics: Mechanical Properties of Living Tissues. Springer, New York. Gunner, C.W., Hutton, W.C., Burlin, T.E., 1979a. The mechanical properties of skin in vivo—a portable hand held extensometer. British Journal of Dermatology 100, 161–163. Gunner, C.W., Hutton, W.C., Burlin, T.E., 1979b. An apparatus for measuring the recoil characteristics of human skin in vivo. Medical and Biological Engineering and Computing 17, 142–144. Langer, K., 1978. On the anatomy and physiology of the skin I. The cleavability of the cutis. British Journal of Plastic Surgery 31, 3–8. Larrabee Jr., W.F., 1986. A finite element model of skin deformation. An experimental model of skin deformation. Laryngoscope 96, 406–412. Lim, K.H., Ho, H.N., Chew, C.M., Chen, C.Y., Jeyapalina, S., Teo, C.L., Lim, B.H., 2006. Non-invasive in vivo measurement of skin flap shrinkage. In: Proceedings of the XVth International Conference of Mechanics in Medicine and Biology. Nanyang Technological University, Singapore. Manschot, J.F.M., Brakkee, A.J.M., 1986. The measurement and modeling of the mechanical properties of human skin in vivo, 1. The measurement. Journal of Biomechanics 19, 511–515. Reihsner, R., Baloghi, B., Menzel, E.J., 1995. Two-dimensional elastic properties of human skin in terms of an incremental model at the in vivo configuration. Medical Engineering and Physics 17, 304–313. Rodrigues, L., 2001. Part 2 EEMCO Guidance to the in vivo assessment of tensile functional properties of the skin part 2: instrumentation and test modes. Journal of Pharmacological and Biophysiological Research 14, 52–67. Stark, H.L., 1977. Directional variations in the extensibility of human skin. British Journal of Plastic Surgery 30, 105–114. Vescovo, P., 1998. Validation de methods de measure des mod modules d’e´lasticite´ de la peau humaine. Diploˆme d’Etudes Approfondies, Universite´ de Franche-Comte´.
Journal of Biomechanics 41 (2008) 931–936 www.elsevier.com/locate/jbiomech www.JBiomech.com
New extensometer to measure in vivo uniaxial mechanical properties of human skin K.H. Lima,b,, C.M. Chewb, P.C.Y. Chenb, S. Jeyapalinac, H.N. Hoc, J.K. Rappelc, B.H. Limc a
Digital Medicine Laboratory, National University Hospital, Singapore 119260, Singapore Department of Mechanical Engineering, National University of Singapore, Singapore 119260, Singapore c Department of Orthopaedic Surgery, National University of Singapore, Singapore 119260, Singapore
b
Accepted 9 January 2008
Abstract Biomechanical properties of skin are important for clinical decision making as well as clinical intervention. Measuring these properties in vivo is critical for estimating dimensional behaviour of skin flap or graft after harvest. However, existing methodologies and devices often suffer from lack of standardisation and unwanted peripheral force contribution due to the deformation of surrounding tissues during measurement. This naturally leads to measurement inaccuracies and lack of reproducibility. In order to improve the measurement accuracy, a new portable extensometer, which measures the non-invasive in vivo biomechanical properties of skin, has been designed and constructed. This design incorporates three pads that attach to the skin, including a C-shaped pad to shield the force sensor from peripheral forces. Such design produces data that are significantly closer to in vitro measurements. The results have been verified by finite element analysis, and experiments on rubber sheets and pig skins. This device can be used to obtain biomechanical properties of skin that will aid doctors in measuring skin elasticity and surgical planning, especially in skin flap surgery. r 2008 Elsevier Ltd. All rights reserved. Keywords: Skin measurement device; Extensometer; Biomechanical properties; Skin flap; In vivo
1. Introduction Skin flap and graft transplants are common in reconstructive surgery, where surgeons transfer a healthy skin flap from a donor site to a wound site. Skin is subjected to pre-tension on a human body (Cox, 1941; Langer, 1978) and thus when a piece of skin is harvested from a donor site, it is known to undergo deformation. The amount of deformation is known to be highly sensitive to the patientspecific skin structure and internal tension, and this varies with age, health, location and BMI index. In practice, often inaccurate size skin flaps are harvested due to the lack of quantitative tools, poor understanding of the biomechanical behaviour of the skin and inexperience of the surgeon. This usually leads to further complications during surgery Corresponding author at: Digital Medicine Laboratory, National University Hospital, Singapore 119260, Singapore. Tel.: +65 68 742 137; fax: +65 67 791 459. E-mail address: [email protected] (K.H. Lim).
0021-9290/$ - see front matter r 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2008.01.004
and unnecessary trauma to the patient. Therefore, in order to assist surgeons during the critical stage of skin flap planning and to reliably predict the deformation of skin flap, there is a need to develop an appropriate measurement method that will consistently predict the biomechanical property of skin. Skin is a complex structure and is classified as a nonlinear viscoelastic material. It comprises three main layers, namely the epidermis, dermis and subcutaneous (fat) layers. The latter two layers contain a network of blood vessels (Fawcett, 1986). The entire flap sits above the muscle surface, separated by a thin layer of fascia; is particularly dense in the scalp, the back of the neck and the palms of the hands, where it serves to anchor the skin firmly to underlying tissues. In other areas of the body, such as the dorsal or volar skin regions, it is loose and the skin may be moved freely. Skin also shows directionally dependent mechanical properties and it is reported to be stiffer along the Langer’s lines compared with across the Langer’s lines (Alexander and Cook, 1977; Cox, 1941;
ARTICLE IN PRESS 932
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Daly, 1982; Langer, 1978; Reihsner et al., 1995; Stark, 1977). The biomechanical properties of skin have been measured by both in vivo and in vitro methods. The simplest method is the in vitro tensile testing, where the applied stress and resultant strain are measured under a carefully controlled environment and thus the material constants can be determined accurately; here, the stress field in the test material is uniform. In vivo test on the other hand, is challenging as explained earlier and therefore the results are descriptive and suffer from lack of reproducibility. Berardesca and Elsner conducted comprehensive literature reviews on current skin measurement devices (Berardesca et al., 1995; Elsner et al., 2002). Their studies revealed that all the in vivo non-invasive devices are capable of determining a qualitative measure of the mechanical properties, but the measured result differs from in vitro measurements significantly. Thus, this research work was undertaken to develop a new device to address this problem. Current commercial skin measurement devices measures skin properties by applying deformation forces in various manner. One set of devices, such as the cutometer, produces multi-axial loading on skin and thus is not capable of identifying directional differences. In contrast, uniaxial extensometers can be used to ascertain directional differences in material properties. A uniaxial extensometer works by applying displacements to the skin using two extensible pads/tabs/legs that are attached to the skin using double-sided tape. The force needed for deformation is measured by a load cell as the skin deforms (Evans and Siesennop, 1967; Baker et al., 1988; Gunner et al., 1979a, b; Larrabee, 1986; Manschot and Brakkee, 1986; Vescovo, 1998). In order to study the directionally dependent in vivo biomechanical properties of skin, a custom made extensometer was designed and built during this investigation.
F’
F
A
B
F’ Fig. 1. Stretching of surrounding skin contributes to peripheral forces F0 ; where A and B represent the two pads of a typical extensometer; the force is measured by a load cell at B.
F´
F B
A
C
F´ Fig. 2. Pad arrangement showing how the pad C is positioned to shield the load cell (at pad B) from peripheral forces; pads B and C move as a single unit during operation.
isolate the force in the test direction, thus yielding results that are closer to an actual in vitro measurement.
2. Methods 2.1. Description of new extensometer design 2.1.1. Design concept In a typical extensometer design, two pads that are attached to the skin surface using adhesive deform the skin during a measurement. Using such instruments to achieve an actual force–displacement profile of the area of skin between the pads is not possible. When extension is applied to the skin, not only the skin tissue between the pads deforms, but also the surrounding tissue too. This inevitability contributes to the overall force detected by the force sensor on the device. Therefore, as pictorially represented by Fig. 1, the measured force also includes force contributed from directions other than the test direction. The dotted lines are simplified tensor line representations of tensile forces during skin stretch. In order to improve the uniaxial measurement, a new extensometer was devised and the arrangement of the pads is shown in Fig. 2. Here, a third pad (a C-shaped shield pad) partially envelopes Pad B which contains the load cell, thus effectively shielding out the peripheral forces F0 during measurement. Pad C achieves this by moving together with pad B, thus isolating the skin region between B and C so that the skin tension there remains constant as the skin at other parts stretches during measurement. In this way, the load cell is mostly subjected to experience the uniaxial force F between A and B. This arrangement was shown to effectively
2.1.2. Constructed extensometer A schematic diagram of the constructed device is shown in Fig. 3(a). This device, developed to conduct tests at a user-defined extension rate, consists of the three pads A, B and C mounted along a carriage. During measurement, the extensometer is attached to the skin at the pads using double-sided adhesive tape. Pad A is fixed to the carriage body while B and C are free to slide on the carriage. The load cell, which has a flat profile, is attached to the pad B for force measurement and the pad C is used to shield the peripheral forces during the stretching from being detected by the load cell. Fig. 3(b) shows the pad dimensions used. Pads B and C (attached together as a single unit) are connected via a lead screw to a servomotor, which actuates the pads along the carriage. The displacement of the pads is logged from the servomotor encoder and the force is measured by the load cell, which has a resolution of 2 mN. Pads B–C have a maximum velocity of 0.6 mm/s. A computer, connected to the servomotor, motor controller and driver, strain gauge amplifier and data acquisition card, is used to automatically control the movement of the pads and to log measurement data. 2.1.3. Articulated arm Fig. 4 shows the articulated arm that is designed to hold the device onto the skin. Using the articulated arm to hold the device during measurement is part of the standardisation protocol that is intended to eliminate
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D
A B
C
G
E F
30
10
10 36
A
12
36
B
10
C
* All dimensions in mm
Fig. 3. (a) Schematic drawing of extensometer showing: A—fixed pad, B—pad (attached to the load cell and is movable along the carriage), C— C-shaped shield pad (moves simultaneously with pad B), D—load cell, E—lead screw, F—carriage and G-servo motor. (b) Pad dimensions.
Articulated arm
Device slides freely
Linear slide, H
Extensometer Fig. 4. Photograph of shield pad extensometer mounted on an articulated arm with a linear slide attachment. handling inconsistency and variations in contact pressure of the device on the skin. This arm has six degrees of freedom and thus enables the device to be easily placed in any position. It also has sufficient stiffness so that pad A remains stationary relative to the underlying skin tissue during measurement, and the only movement occurs at pads B and C. In order to standardise the device placement, a low friction vertical linear slide is used at the mount attachment so that the device always presses onto the skin with its own weight (2.45 N).
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2.2.2. In vitro measurements: rubber strip Using a universal tensometer (Instron, model no. 5440), the typical force–extension measurements of the rubber (Therabands) strips were obtained. In order to avoid the premature failure at the gripper/pads, a dumbbell-shaped specimen of test size 25 (L) 12 (W) mm was stretched at a pre-defined speed of 0.6 mm/min and the resultant force extension data was recorded. This procedure was repeated three times. 2.2.3. In vivo measurements: rubber sheet The force-elongation experiments using the extensometer were conducted on large Therabands sheets (both yellow and grey) using both the traditional two-pad and the proposed shield pad arrangement. The experimental settings were the same as what were used in the earlier measurements on the rubber strips. The measurements were performed at the centre of square sheets (120 mm 120 mm), which were attached by double-sided tape onto a fixed frame (on all four sides) to emulate skin covering a human body. The articulated arm was used to hold the extensometer over the sheet, so that the position of pad A was fixed relative to the frame. Since the rubber edges were constrained by the frame, the rubber surrounding the pads was stretched as the pads moved. This set of experiments were compared with the in vitro measurements described earlier to evaluate how effective the shield pad is in removing peripheral forces during stretching. 2.2.4. In vivo measurements: pig skin All handling and experimentation involving animals were done in a humane, ethical manner (animal ethical clearance number: 006/06; clearing authority: Institution of Animal Care and Use Committee, National University of Singapore). The pigs were humanely killed at the animal facility (according to the ethics regulations) and the hair at the planned test sites was shaved-off. In vivo extensometer measurements using both the two-pad and shield pad arrangements were carried out on abdomen, upper thigh and upper shoulder skin surfaces. The measurements were performed in the compressive mode, where the pads move towards each other instead of moving apart. The reasons for compressive mode measurement are discussed in the discussion section. Experimental sites were preconditioned by two successive loading–unloading cycles, and the data from the third cycle was taken as the actual measurement; it was observed that data points converged after the second cycle. Such preconditioning is necessary to obtain consistent and reproducible data, as explained by Fung (1996). Unlike the rubber experiments, pig skin was not harvested in order to obtain the in vitro measurements to compare against the in vivo ones. Instead, an island of skin area was isolated from the surrounding tissue (refer to Fig. 5) and in vivo compressive mode measurements were taken there. Isolating the skin area removes peripheral forces during
Extensometer
2.2. Mechanical testing 2.2.1. Materials Two rubber sheets (Therabands) with different stiffness were purchased from a hospital pharmacy. These two grades of Therabands (yellow and grey) have average stiffness values of 0.8 and 2.9 MPa at 50% strain, respectively. The yellow Therabands has stiffness values closer to that of elastic deformation region of skin. Two piglets (6 months old; genus: Sus; species: Duroc & Yorkshire) were supplied by the Singapore National University Hospital’s animal holding unit. Commercial doublesided tape (3 M) was purchased from a local supplier and used to attach the extensometer pads to the skin.
Extensometer pads
Fascia-muscle layer (skin flap removed)
Skin island under measurement
Fig. 5. Picture showing surrounding skin flap around the pads removed down to the fascia to remove influence of peripheral forces during measurement.
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measurement, thus emulating an in vitro setting. It is important that the skin remained attached to the body (via the fascia) because this was the state that the earlier in vivo measurements were taken. Thus, this ensured minimum variations at the underlying skin section among the three different measurement configurations. Furthermore, it should be noted that the test dimensions of the skin involved in all three configurations were similar, hence enabling effective comparison.
2.3. Finite element analysis A finite element simulation was also used to determine the effectiveness of the shield pad arrangement. A simulation representing the in vivo rubber stretching experiment (Section 2.2.3) was studied by the software Ansys 8.0 (Ansys, Inc.). These results will be compared with those simulated in an in vitro setting. For this simulation, the material was classified as a pure, incompressible elastic shell, with Young’s modulus of 0.8 MPa. This value was selected because it is of the same order of magnitude as skin stiffness.
3. Results Finite element method was employed to simulate the effectiveness of the proposed shield pad arrangement. The simulated results for measurement representing in vivo twopad and shield pad arrangements are given in Fig. 6(a) and (b), respectively. In the shield pad arrangement, the load cell that is located on pad B is protected from the generated compressive forces and the peripheral forces due to the deformation of surrounding materials. Therefore, the force experienced by the load cell will have minimal contribution from the forces of the surrounding tissues. Table 1 compares simulated results of stress in different settings when a strain of 0.42 is applied. In simulation, the average stress on all the nodes surrounding the pad labelled B is assumed to be stress that is experienced by the load cell and thus calculated. The percentage error of simulated stress values compared with the in vitro value was computed. It can be clearly seen that in vivo shield pad arrangement produces result that is much closer to the in vitro result. It was observed during the initial experiments that contact pressure of the device on the skin marginally
influenced the obtained reading. For verification, the contact pressure was varied by placing weights (2 N) on the top of the device before measurement, and the produced data was found to differ by about 10%; greater the pressure, larger the difference. Owing to this sensitivity, an articulated arm with a vertical slide attachment was used to hold the extensometer onto the body so that the device rests on the skin with its own weight, as seen in Fig. 4. Two sets of experiments were conducted to test the effectiveness of the shield pad on constrained rubber sheets and pig skins. Hysteresis data of the rubber sheets are shown in Figs. 7 and 8. Both yellow and grey Therabands produced the same trend, where it can be seen that the shield-pad data are significantly closer to the in vitro data, but the data from the traditional two-pad diverge significantly from the in vitro data. The results from the in vivo pig experiment have the same outcome, where the shield pad data are significantly closer to the data in which the skin sides are removed (‘‘in vitro’’ setting emulated). The typical results are given in Fig. 9. 4. Discussion Data measured in an in vitro setting may be considered as the true biomechanical uniaxial properties of the skin because the stress field in the test material is uniform. Since the shield pad has been shown in different experiments to produce results that were close to the in vitro measurements, it is deemed that this new design is capable of Table 1 FEM simulated stress at a strain of 0.42, and percentage difference of in vivo stress values compared with the in vitro value Method of simulation
Stress (MPa) at 0.42 strain
Difference (%)
In vitro arrangement Shield pad arrangement Traditional two-pad arrangement
0.34 0.39 0.66
– 13.7 91.0
Fig. 6. Finite element modelling of material that is constrained on a 120 mm 120 mm frame, undergoing an extension test by extensometer: (a) traditional two-pad arrangement and (b) shield pad arrangement. Shades represent stresses along the principle (horizontal) direction of testing.
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In-vivo shield-pad arrangement
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Force / Width (N / mm)
In-vitro measurement
Force (N)
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In-vivo 2-pad arrangement In-vivo shield-pad arrangement In-vivo (skin sides separated)
0.04 0.03 0.02 0.01
0.5
0 0.0
0 2
4 6 Displacement (mm)
8
Fig. 7. Force–extension data of rubber (yellow Therabands) showing the curves obtained by in vivo two-pad, in vivo shield pads and in vitro tensile testing.
7 In-vivo 2-pad arrangement
6
In-vivo shield-pad arrangement In-vitro measurement
Force (N)
5 4
2 1 0 2
4 6 Displacement (mm)
8
10
Fig. 8. Force–extension data of rubber (grey Therabands) showing the curves obtained by in vivo two-pad, in vivo shield pads and in vitro tensile testing.
measuring the true properties effectively. It can also be observed that the differences between the shield-pad result and in vitro result is greater for the grey than yellow Therabands. This is expected because the grey Therabands is stiffer than the yellow one and so the magnitude of the peripheral forces, which cannot be completely removed by the shield pad, is higher. It should be noted that the experiments were carried out in the extensive mode for rubber sheets and in the compressive mode for pig skin. In the extensive mode, the pads moved apart at the loading cycle, and then moved back together at the subsequent unloading cycle; compressive mode is the reverse. The compressive mode measurement is conducted for skin because the skin at rest on the body is already in a stretched state with internal tension. Therefore, the biomechanical properties will be measured for the skin from the initial pre-tensioned state, to a relaxed tension-free state, and then to a wrinkled/compressed state. Since the purpose of this research is to eventually estimate the skin deformation upon harvest (where the skin is
4.0 6.0 Displacement (mm)
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Force / Width (N / mm)
0
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Fig. 9. Force–displacement data from pig (a) belly region (b) shoulder region, showing the curves obtained by in vivo two-pad, in vivo shield pads and in vivo two-pad of isolated Skin Island. Note that for the plots’ vertical axes, the force is normalised against the width of the load cell pad because the pad widths used for the three experiments differ slightly.
tension free), it is therefore more relevant to measure in the compressive mode. In fact, a method has been proposed to use the mechanical behaviour in the compressive direction to estimate flap deformation upon harvest (Lim et al., 2006). When calculating the stress involved during measurement, the width of the skin tested must be known. In an in vitro measurement, the width of the skin tested is simply the width of the sample itself since the stress field is uniform. Manschot had suggested that in an in vivo extensometer measurement (using the traditional two-pad extensometer), the effective width of the skin can be approximated by the width of the pads itself (Manschot and Brakkee, 1986). However, this cannot be the case since the adjoining skin around the pads is inevitably deformed during measurement, which can also be clearly seen in the simulated FEM images. In the experiments conducted with the new device, it is evident that the in vivo measurements showed significant closeness with the in vitro measurements (in which the width of the samples tested were the same as the width of pad B). Thus, it can be concluded that in the new device, the effective width of the skin measured in vivo can be approximated by the width of the pad itself, thus enabling the stress involved during measurement to be calculated directly and conveniently.
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It was found that contact pressure of the device on the skin should be standardised during measurement. As the forces measured were small, the load cell used was very sensitive such that forces from directions other than the measurement axis may be registered marginally. Since downward pressure created vertical forces which would affect the reading, this variable should be kept constant by standardising the contact pressure. The design solution currently employed was to use a vertical slide attachment at the articulated arm so that the extensometer always pressed onto the skin with 2.45 N (i.e. its own weight). However, this design has the disadvantage that measurements must be done with the device at a horizontal position. For future improvement, a pressure transducer can replace the slide attachment to ensure a constant pressure. Ideally, the extensometer should just sit on the skin surface with zero pressure. Rodrigues reported that the literature reviews of the in vivo measurement of Young’s modulus of elasticity of skin produced results that vary by four orders of magnitude (Rodrigues, 2001). For devices of different measurement principles, e.g. suction and traction, the results may inevitably differ due to dissimilar methods of load application and force measurement. However, for devices of the same principle, one reason for the inconsistency may be the lack of standardisation. While there is currently no internationally adopted standard, this issue must be recognised when conducting measurement on skin. Therefore, a standardising protocol was used in this study, which included standardising the pad dimensions, initial distance between the pads, strain rate, device contact pressure, the means of holding the device during measurement, skin preconditioning and controlled environment. This protocol, coupled with the new shield pad design, would ensure that the results obtained are consistent, reproducible and more accurate. 5. Conclusion It can be concluded that by eliminating the peripheral forces during an in vivo skin measurement, one can obtain considerably reliable biomechanical properties of skin that are significantly closer to the actual in vitro properties. Thus, an extensometer with an additional third pad, shielding the pad containing the force sensor, was proposed. Experimental results indicated such arrangement was effective. Finally, it can be summarised that a measurement standardisation protocol that consisted of the device design and measurement parameters should be used. Compared with a traditional design of two-pad arrangement, this new system is standardised to obtain accurate, reliable and consistent results. Conflict of Interest There is no conflict of interest associated with this publication and there has been no significant financial
support for this work that could have influenced its outcome. Acknowledgements Authors wish to thank the Biomedical Research Council (A*STAR) of Singapore for the financial support and also wish to express gratitude to NUS and NUH staff members, who have contributed their time and ideas to this project. References Alexander, H., Cook, T.H., 1977. Accounting for natural tension in the mechanical testing of human skin. Journal of Investigative Dermatology 69, 310–314. Baker, M.R., Bader, D.L., Hopewell, J.W., 1988. An apparatus for testing the mechanical properties of skin in vivo: its application to the assessment of normal and irradiated pigskin. Bioengineering of Skin 4, 87–103. Berardesca, E., Elsner, P., Wilhelm, K., Maibach, H. (Eds.), 1995. Bioengineering of the Skin: Methods and Instrumentation. CRC Press, Boca Raton, London, New York. Cox, H.T., 1941. The cleavage lines of the skin. British Journal of Surgery 29, 234–240. Daly, C.H., 1982. Biomechanical properties of dermis. Journal of Investigative Dermatology 79, 17–20. Elsner, P., Berardesca, E., Wilhelm, K., Maibach, H., 2002. In: Bioengineering of the Skin. CRC Press, Boca Raton, London, New York, Washington, DC (Chapters 5–14). Evans, J.H., Siesennop, W.W., Controlled quasi-static testing of human skin in vivo. In: Digest of the Seventh International Conference on Medical and Biological Engineering, Stockholm, 1967. Fawcett, D.W. (Ed.), 1986. A Textbook of Histology, 11th ed. W.B Saunders Company, Philadelphia. Fung, Y.C. (Ed.), 1996. Biomechanics: Mechanical Properties of Living Tissues. Springer, New York. Gunner, C.W., Hutton, W.C., Burlin, T.E., 1979a. The mechanical properties of skin in vivo—a portable hand held extensometer. British Journal of Dermatology 100, 161–163. Gunner, C.W., Hutton, W.C., Burlin, T.E., 1979b. An apparatus for measuring the recoil characteristics of human skin in vivo. Medical and Biological Engineering and Computing 17, 142–144. Langer, K., 1978. On the anatomy and physiology of the skin I. The cleavability of the cutis. British Journal of Plastic Surgery 31, 3–8. Larrabee Jr., W.F., 1986. A finite element model of skin deformation. An experimental model of skin deformation. Laryngoscope 96, 406–412. Lim, K.H., Ho, H.N., Chew, C.M., Chen, C.Y., Jeyapalina, S., Teo, C.L., Lim, B.H., 2006. Non-invasive in vivo measurement of skin flap shrinkage. In: Proceedings of the XVth International Conference of Mechanics in Medicine and Biology. Nanyang Technological University, Singapore. Manschot, J.F.M., Brakkee, A.J.M., 1986. The measurement and modeling of the mechanical properties of human skin in vivo, 1. The measurement. Journal of Biomechanics 19, 511–515. Reihsner, R., Baloghi, B., Menzel, E.J., 1995. Two-dimensional elastic properties of human skin in terms of an incremental model at the in vivo configuration. Medical Engineering and Physics 17, 304–313. Rodrigues, L., 2001. Part 2 EEMCO Guidance to the in vivo assessment of tensile functional properties of the skin part 2: instrumentation and test modes. Journal of Pharmacological and Biophysiological Research 14, 52–67. Stark, H.L., 1977. Directional variations in the extensibility of human skin. British Journal of Plastic Surgery 30, 105–114. Vescovo, P., 1998. Validation de methods de measure des mod modules d’e´lasticite´ de la peau humaine. Diploˆme d’Etudes Approfondies, Universite´ de Franche-Comte´.