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Rheumatology Advance Access originally published online on April 25, 2008
Rheumatology 2008 47(7):1018-1024; doi:10.1093/rheumatology/ken145
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© 2008 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Quantification of hardness, elasticity and viscosity of the skin of patients with systemic sclerosis using a novel sensing device (Vesmeter): a proposal for a new outcome measurement procedure

Y. Kuwahara1, Y. Shima1, D. Shirayama2, M. Kawai1, K. Hagihara1, T. Hirano1, J. Arimitsu1, A. Ogata1, T. Tanaka1 and I. Kawase1

1Department of Respiratory Medicine, Allergy and Rheumatic Diseases, Osaka University Graduate School of Medicine, Osaka, and 2WaveCyber Co. Ltd., Saitama, Japan.

Correspondence to: Y. Shima, Department of Respiratory Medicine, Allergy and Rheumatic Diseases, Osaka University Graduate School of Medicine, 2-2 Yamada-oka, Suita city, Osaka, 565-0871, Japan. E-mail: ryanjin{at}imed3.med.osaka-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Supplementary data
 Acknowledgements
 References
 
Objectives. No objective method to measure skin involvement in SSc has been established. We developed a novel method using a computer-linked device to simultaneously quantify physical properties of the skin such as hardness, elasticity and viscosity.

Methods. Skin hardness was calculated by measuring the depth of an indenter pressed onto the skin. The Voigt model was used to calculate skin elasticity, viscosity, visco–elastic ratio and relaxation time by analysing the waveform of skin surface behaviour. The results were compared with the modified Rodnan skin score (mRSS) obtained at 17 sites on the bodies of 20 SSc patients and 20 healthy controls. A functional assessment questionnaire was administered to determine how skin hardness represents a patient's disability. We also examined intra- and inter-observer variability to determine the reliability of this method.

Results. The crude hardness obtained with this device correlated well with the standard hardness specified by the American Society for Testing and Materials (ASTM, r = 0.957). A close relationship between hardness and total mRSS was also observed (r = 0.832). Skin elasticity correlated positively, and relaxation time negatively with mRSS. Functional disability correlated more closely with skin hardness (r = 0.643) than with mRSS (r = 0.517). Intra- and inter-observer variabilities were 7.63 and 19.76%, respectively, which were lower than those reported for mRSS.

Conclusions. Increases in hardness and elasticity as well as shortening of relaxation time constitute objective characteristics of skin involvement in SSc. The system devised by us proved to be able to assess skin abnormalities of SSc with high reliability.

KEY WORDS: Systemic sclerosis, Scleroderma, Skin hardness, Skin elasticity, Skin viscosity, Visco–elastic ratio, Relaxation time, Skin score, Sensing device, Computer-assisted device


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Supplementary data
 Acknowledgements
 References
 
Skin involvement is a major problem for patients with SSc because it affects the quality of life and prognosis of the disease [1, 2]. It has also been demonstrated that improvement in skin thickening is associated with improved survival rate [3]. Therefore, an objective and reliable method to measure the degree of skin involvement is essential for the evaluation of a novel therapy for SSc. The severity and extent of skin involvement in SSc is generally assessed by using the modified Rodnan skin score (mRSS) in which the dermal thickening is classified into four grades by pinching the skin with the fingers [4, 5]. The overall degree of skin involvement is evaluated as the modified Rodnan total skin score (mRTSS) by adding up the mRSS of 17 sites of the body. The validity of mRSS as a semi-quantitative method and of mRTSS as an outcome measure has been supported by findings of a series of studies [6–9]. This method has the following advantages: (i) It takes a short time; (ii) It requires no special equipment; and (iii) It is painless. Skin scoring, however, entails two problems. First, small but important changes within the same skin score will be neglected. Second, appropriate training and technical skills are necessary for accurate assessment of skin thickness with mRSS, and even appropriately trained examiners find it difficult to accurately score borderline severities.

To date, several methods for the objective assessment of skin involvement in SSc have been proposed, including imaging with ultrasound [10, 11], X-ray [12, 13] or magnetic resonance [14], suction cup [15], elastometer [16] and durometer [17, 18]. Almost all of these have certain drawbacks, however. Imaging using X-ray or magnetic resonance needs large-scale expensive equipment. It has been reported that the 17-point dermal ultrasound scoring system is a reliable measure of skin thickness in SSc patients [10], but this method requires a certain level of technical skill and considerable time for an entire body. Skin involvement of uneven surfaces such as dorsal hands and fingers is difficult to measure using a suction cup or elastometer, and it may take more than half an hour to examine an entire body with these methods. A durometer is small and easy to use, and represents a promising approach for daily clinical use. In a recent study, Kissin et al. [18] demonstrated the high validity and reliability of durometer-measured skin hardness in SSc patients. However, the durometer is originally intended for industrial materials such as rubbers and plastic polymers. The hardness of the specimen is measured based on the extent of the depression produced by the indenter when the resilient force of the specimen becomes equal to the pressure load produced by the specific inner spring. The strength of the spring and the shape of the indenter used in durometers depend on the hardness of the target. It may therefore be difficult to accurately measure the various body sites with a single durometer. Moreover, durometer measurements will vary more if the pressure or speed of the indenter onto the specimen is not constant. Some kind of instructions is therefore needed to maintain consistency of measurement among the observers.

Human skin is viscoelastic having the properties of both viscosity and elasticity. Viscosity is related to delayed recovery from deformation. It functions as a buffer that counteracts velocity of the external force resulting in a delay of movement. Oil and honey are examples of highly viscous materials. Elasticity is related to rebounding and quick recovery from deformation. It produces a force proportional to the extent of deformation. Spring and rubber are examples of highly elastic objects. It is not clear, however, how these physical properties change in the skin of SSc patients.

We therefore developed a new computer-linked sensing device named Vesmeter, and investigated the hardness, elasticity and viscosity of the skin of SSc patients. Based on the results of these measurements, we propose a novel system for the objective and practical assessment of skin involvement in SSc patients. In this system, skin hardness is represented as a relative value (z-score) compared with the average value for healthy controls so that skin abnormalities can be assessed for different sites of the body. The degree of overall skin involvement is then evaluated by adding up the z-scores for 17 sites of the body. The reproducibility and accuracy of this method were investigated by analysing intra- and inter-observer variability.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Supplementary data
 Acknowledgements
 References
 
Sensing device
The device is shown in Fig. 1A. The probe, with the configuration shown in Fig. 1B, has a built-in position sensor, which is connected to the computer. When the probe is placed at a right angle on the skin, the indenter is depressed onto the skin at a constant speed by means of electromagnetic power, and the path of the indenter is constantly traced by the position sensor. The hardness of an object can then be expressed as the area of the depression divided by the pressure of the indenter. The stress relaxation behaviour of viscoelastic materials can be analysed by using the Voigt model that consists of two components, a purely viscous dashpot and a purely elastic spring connected in parallel. We calculated elasticity (G), viscosity ({eta}), visco–elastic ratio (VER) and the relaxation time ({tau}) by analysing the waveform of the stress relaxation behaviours of the skin with a computer. VER is related to the superiority of the viscous element over the elastic element. The relaxation time is related to the time taken by the deformed material to return to its original state. Theoretical information about calculation method of these properties is presented in supplementary document (see supplementary data available at Rheumatology Online).


Figure 1
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  		FIG. 1. Photograph (A) and configuration (B) of the probe. The results of the measurements are displayed on the computer screen connected to the probe. The numbers in (B) indicate the following components: 1, recognition mark; 2, position sensor; 3, indenter; 4, measurement head; 5, electromagnetic coil; 6, permanent magnet; 7, power switch.

 
Before we used this device for the human skin, accuracy of the measurements was examined by using test samples made with polyurethane or silicon gel of a known hardness, elasticity and viscosity. The measurements thus obtained were compared with those of the standards of the American Society for Testing and Materials (ASTM) for hardness and of the International Organization for Standardization (ISO) for elasticity and viscosity. The range of the samples measured fully covered the range of human skin from normal to extremely hard.

Patients and controls
Skin hardness and other physical properties were evaluated in 20 patients with SSc (10 diffuse and 10 limited cutaneous types) and 20 healthy control subjects. Either group consisted of three male and 17 female subjects. Mean age ± S.D. of SSc patients and control subjects were 52.3 ± 11.8 and 52.3 ± 11.5, respectively. Mean mRTSS ± S.D. of the patients was 19.7 ± 10.6 (range 8–40). All patients met the criteria of the American College of Rheumatology for the classification of SSc [19]. To know the effect of ageing and obesity, the associations between skin hardness and age and between skin hardness and BMI were examined for control subjects. Informed consent was obtained from all subjects. Official approval for this study was also obtained from the local ethics committee.

Elasticity, viscosity, VER and the relaxation time of the skin were all measured simultaneously at the bilateral dorsal hands because a wide variety of skin involvement was observed at this site. Measurements of skin hardness were then performed at 17 sites of the body corresponding to those used for the assessment with mRSS. The sites comprised the third finger pads at the base phalanx, the dorsal hands between the second and the third metacarpal bones, the dorsal forearms between the radius and the cubitus at one-third of the forearm from the distal end, the dorsal upper arms 6 cm from the elbow, the dorsal feet between the first and the second metatarsal bones, the middle pretibia 2 cm outside the centre top, thighs 6 cm from the upper end of patella, the face 2 cm below the right or left cheek bone, the chest at the third intercostal space at the right or left sternal border and the abdomen 4 cm to the right or left of the navel. The measurements at the extremities were performed bilaterally and all the measurements were done with the subject in the supine position. Sites with a hard structure such as bone or tendon just below the skin were avoided. For each measurement, the probe was placed at a right angle on the skin. The measurements were repeated five times at each site, and the average of the five values was used. Measurements were performed under environmental conditions of 20.8–28.6°C temperature and 25.2–52.1% humidity. For the patient group, skin involvement was also assessed with the mRSS at 17 sites by a single examiner (Y.K.) who had been trained in Scleroderma Study Conference in Japan. Measurement of mRSS was made only once for each subject.

The z-score hardness and the total z-score hardness
To compare skin abnormalities at the various sites, it was necessary to standardize the measurement values because the original skin hardness as well as thickness varies among the different sites of the body. Every crude value was converted to a z-score by subtracting the mean value and dividing the result by the SD for that site in normal controls. That is, the z-score represents the standardized degree of deviation from the average of normal controls. The sum of the z-scores for all 17 body sites was defined as the total z-score hardness and was used for the assessment of the severity and extent of overall skin involvement for the entire body.

Correlation of skin hardness with functional disability
In order to establish whether skin hardness determined with our system correlates with the activities of daily living, a functional assessment questionnaire was self-administered by SSc patients. The version modified specifically for SSc by Silman et al. [20] was used for this assessment because its validity and reliability have been demonstrated for patients with various degrees of severity of SSc. Replies for each item were scored as follows: score 0—able to perform in normal manner; 1—can manage with some change in manner; 2—can only manage with difficulty; 3—impossible to perform. Overall functional disability was assessed as the total score for 11 items.

Intra- and inter-observer variability
Intra-observer variability (reproducibility) was assessed by examining the coefficients of variation [CV = (S.D./mean)100] of five consecutive measurements for each site by a single examiner. The average CV for the 20 patients was calculated for each body site.

Inter-observer variability (accuracy) was estimated in terms of CV of hardness measured by seven different examiners in a single patient. The average of five consecutive measurements at each site was adopted as the value for that site. The examiners were not provided with any specific information except the measurement positions and did not receive any preparatory training or instructions on how to perform the measurements. A subject who had relatively severe skin involvement of the diffuse cutaneous type (mRTSS = 37) was selected. All measurements were performed within 7 days during which no particular change was observed in the severity of skin involvement.

During the course of the study, no access to previous results was allowed.

Statistical analysis
The unpaired Student's t-test was used to compare the hardness z-scores for the patient and the control groups. The Pearson correlation coefficient (r) was employed for correlation analysis. P-values <0.05 were considered statistically significant for all analyses. P-values were not calculated if the quantity of data was statistically insufficient. All analyses were performed with the statistical software package StatMate III for Windows (ATMS Co. Ltd., Tokyo, Japan).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Supplementary data
 Acknowledgements
 References
 
Correlation with standards in test materials
As shown in Fig. 2, the measurement values obtained with our device closely correlated with the standards for hardness (r = 0.957, P < 0.0001, n = 23; polyurethane samples), elasticity (r = 0.963, P < 0.0001, n = 9; silicon gel samples) and viscosity (r = 0.920, P = 0.0004, n = 9; silicon gel samples). This proves that our device can accurately measure homogeneous objects with various degrees of hardness, elasticity and viscosity corresponding to the range of values for these three parameters of human skin.


Figure 2
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  		FIG. 2. Correlation between crude measurement readings and standards in test materials. A: hardness; B: elasticity; C: viscosity. Crude measurement values determined with our device correlated well with those of standards. Homogeneous polyurethane samples with various degrees of hardness and silicon gel samples with various degrees of elasticity and viscosity were used to represent the full range of human skin.

 
Elasticity, viscosity, VER and relaxation time of the skin
Correlations of skin elasticity, viscosity, VER and the relaxation time with mRSS and skin hardness for SSc patients and control subjects are shown in Fig. 3. Figure 3A shows that there was a significant association between elasticity and mRSS, but not between viscosity and mRSS and between VER and mRSS. The relaxation time was negatively associated with mRSS. As shown in Fig. 3B, elasticity closely correlated with hardness (r = 0.967), whereas viscosity and VER showed weakly positive and negative correlation (r = 0.278 and r = –0.349, respectively) with hardness. There was a close and negative correlation between the relaxation time and hardness (r = –0.827).


Figure 3
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  		FIG. 3. Correlation of various physical properties with skin score (A) and skin hardness (B). Horizontal axis in (A) indicates the mRSS. Skin scores 0, 1, 2 and 3 were obtained for 42, 18, 12 and 8 measurement sites, respectively. Horizontal axis in (B) indicates crude value of skin hardness. Symbols cross, open triangle, open square and open circle represent skin scores 0 (n = 42), 1 (n = 22), 2 (n = 8) and 3 (n = 8), respectively. Measurements were performed at the bilateral dorsal hands of 20 SSc patients and 20 control subjects.

 
Hardness of the skin
Figure 4A and B show the association between the total z-score hardness and age and between the total z-score hardness and BMI, respectively. No significant association was observed between total z-score hardness and either age (r = 0.403, P = 0.0783) or BMI (r = 0.435, P = 0.0551). Figure 4C shows crude skin hardness for each of the body sites in control subjects. There is wide variation in crude hardness values especially on the dorsal fingers.


Figure 4
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  		FIG. 4. Skin hardness in normal control subjects. (A) Association between total z-score hardness and age. (B) Association between total z-score hardness and BMI. (C) Crude hardness at each body site. Small white circles indicate crude hardness readings (n = 40 at the fingers, hands, forearms, upper arms, femora, lower legs and feet; n = 20 at the face, chest and abdomen). Large black circles indicate the means ± S.D. of crude hardness readings.

 
The z-scores for hardness determined by mRSS for all body sites of SSc patients are plotted in Figure 5A. Mean z-scores for hardness of the skin for mRSS 0 (459 measurement sites), 1 (110), 2 (48) and 3 (63) were 0.015, 0.604, 1.779 and 2.956, respectively. All differences among those values were statistically significant (P < 0.05). However, the values showed a wide distribution, especially in the group with skin score 3. The mean z-score hardness by body site is shown in Fig. 5B. Especially for the hands and forearms where skin involvement is more common in SSc, significant differences were found between the mean z-scores. As shown in Fig. 5C, the total z-score hardness closely correlated with mRTSS (r = 0.832, P < 0.0001).


Figure 5
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  		FIG. 5. Relationship between z-score hardness and skin score. The z-score hardness is the standardized degree of deviation from the average of normal controls. (A) Values of z-score hardness for all subjects are plotted regardless of the measurement site. Numbers in parentheses below the skin scores indicate the total number of sites measured. (B) Relationships between z-score hardness and skin score were calculated for each body site. Bars correspond to skin scores 0, 1, 2 and 3 from the left. Numbers below the bars indicate number of measurements. Numbers for fingers, hands, forearms, upper arms, femora, lower legs and feet are the sum of the measurements for the right and the left sides. *P < 0.05, **P < 0.01, ***P < 0.001. (C) Relationship between total z-score hardness and mRTSS. Total z-score hardness shows the sum of z-scores at 17 body sites.

 
Functional disability
Correlations of functional disability score with the total z-score hardness and mRTSS are shown in Fig. 6. Functional disability score correlated more closely with the total z-score hardness by our device (r = 0.643, P = 0.0021) than with mRTSS (r = 0.517, P = 0.0193).


Figure 6
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  		FIG. 6. Correlation of total z-score hardness (A) and mRTSS (B) with functional disability score. Total z-score hardness obtained with our system correlated more strongly with functional disability score than did mRTSS.

 
Intra- and inter-observer variability
Intra- and inter-observer variability (coefficients of variation) is shown in Table 1. Intra-observer variability ranged from 6.05% to 10.32% for 10 different body sites, and the average was 7.63%. Inter-observer variability ranged from 15.65% to 23.96% with an average of 19.76%.


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  		TABLE 1. Intra- and inter-observer variability

 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Supplementary data
 Acknowledgements
 References
 
Compared with previous methods, our skin assessment system has several advantages: (i) Not only skin hardness but also skin elasticity, viscosity, VER and the relaxation time can be measured at the same time; (ii) Each measurement can be completed in a few seconds; (iii) No particular training or large-scale equipment is needed; (iv) Skin hardness obtained with our system correlates well with the skin score; (v) The overall severity of skin involvement can be assessed by adding up the hardness z-scores for the 17 body sites; (vi) The total z-score hardness correlates well with functional disability; (vii) Reproducibility and accuracy have been validated. Previous research has shown that intra- and inter-observer variabilities of mRTSS were estimated to be 12 and 25%, respectively, for appropriately trained observers [7]. On the other hand, intra- and inter-observer variabilities of regional measurements in our system were as low as 6.05–10.32% and 15.65–23.96%, respectively, even though the observers had received no special instructions or training. We showed in Fig. 2 that Vesmeter can accurately measure hardness, elasticity and viscosity using test materials. On the other hand, no standards exist for visco–elastic ratio and relaxation time; however, these values by Vesmeter appear to be also accurate because these parameters are automatically calculated with viscosity and elasticity. Our system may therefore be considered useful for obtaining reliable and objective outcome measurements, especially in multicentered clinical trials.

Our study showed that skin hardness and elasticity correlate positively and the relaxation time of viscoelastic behaviour negatively with mRSS. On the other hand, no significant correlation was found between skin viscosity and mRSS. As shown in Fig. 5A, the higher grades of skin score were characterized by widespread scattering. Ten of the 63 plots with a skin score 3 showed hardness z-score lower than the average for skin score 0. These findings suggest that the skin score is based on multiple factors including rebounding power generated by the deformed skin against the external force and speed of return to the original state. Extremely high correlation was detected between skin hardness and skin elasticity. This suggests that dermal thickening with dense collagen fibres results in an increase in skin elasticity as well as in skin hardness. Skin involvement in SSc may therefore be assessed in terms of skin elasticity.

Figure 5A shows that the hardness z-scores for skin score 0 are concentrated between –2 and 2, whereas those for skin score 3 varied from –2 to 10. Our additional analysis revealed that there were nine cases in total with an mRSS score of 3 with negative z-score hardness (see supplementary Table S1 available as supplementary data at Rheumatology Online). In seven of the nine cases, this phenomenon was observed in the results for the fingers, and four of them were males. These cases had relatively severe skin disease (total skin score ranged from 10 to 37, with an average of 24.7). The findings suggest that the Vesmeter may sometimes underestimate the severity of skin disease, particularly on the fingers, which is probably due to the positional characteristics of fingers such as the effect of the phalanx and the differences in skin properties between sexes. With our method, measurements at positions where there are hard structures such as bones and tendons just below the skin should be avoided because the hardness values are affected by those structures. For the dorsal hands, the area between two adjacent metacarpal bones is a suitable target. Similarly, the intercostal spaces should be selected for the chest. Although we can measure skin hardness throughout the body with our system, it is necessary to decide the measurement positions beforehand for comparison with previous results or between patients. As shown in Fig. 5B, the differences within 1.0 between z-scores were not statistically significant at most sites. We could not determine whether this is due to the insufficiency of data or to the potential limitations of the device. As seen in Fig. 5B, the reverse phenomenon of skin hardness and skin score was seen in the fingers (mRSS 2), in the femora (mRSS 1) and in the feet (mRSS 2). All three male patients were included in these estimations. It suggests that differences between sexes may affect skin hardness or skin score.

The standardization procedure we adopted uses the z-scores so that skin hardness of different regions can be quantified based on a single standard because the original skin hardness varies among different regions. Furthermore, we can calculate the degree of total skin involvement in one patient based on the total z-score hardness, the sum of the z-scores at 17 body sites. Both z-score hardness and total z-score hardness have no upper limit so that the skin disease can be evaluated correctly even in extremely severe cases.

The results of this study showed no significant association between skin hardness (total z-score hardness) and either age or BMI. Sex difference in skin hardness could not be clarified in this study because the data for male subjects was insufficient. Additional investigations such as a longitudinal study will be needed to clarify the changes in skin properties due to ageing and obesity. Further study will also be required to examine sex difference in skin properties for normal control subjects.

This study also demonstrated that the total z-score hardness correlates more positively with functional disability score than does mRTSS. This suggests that the total z-score hardness is useful for the assessment of daily living activities of patients with SSc. For our study we used the modified version of the functional disability score which comprises 11 items specific for SSc: nine items related to upper limb function and two items to muscle weakness. Although this assessment instrument has been validated previously [20], it should also be investigated in further studies to determine whether the total z-score hardness correlates with other functional indices such as the classical HAQ-disability index, the scleroderma-visual analogue scales and the UK Scleroderma Functional Score.

Rodnan et al. [4] demonstrated that skin score correlated with the weight of a skin punch biopsy. We have not yet obtained the information on comparing physical properties measured with our device to the weight or other direct findings of skin biopsy. Further investigation will be needed to find out whether the physical properties of the skin represent any histological characteristic.

Our system can be widely used for all skin diseases in which skin hardness is affected during the clinical course. It can detect small changes in skin hardness so that it may be useful for the assessment of skin condition in various diseases including morphoea, keratoderma, atopic dermatitis, dermatomyositis, diffuse psoriasis and ichthyosis.

In conclusion, we have developed a novel and reliable system for the quantification of skin hardness of patients with SSc, and we first analysed physical properties of SSc patients’ skin including elasticity, viscosity, VER and relaxation time. This system showed a useful assessment of skin involvement in SSc and will possibly provide objective evaluation for outcome measurements especially in clinical trials.


   Supplementary data
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Supplementary data
Acknowledgements
 References
 
Supplementary data are available at Rheumatology Online.


   Acknowledgements
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Supplementary data
 Acknowledgements
References
 
We would like to thank Mr Masahiro Sekine, Senior Researcher in Biotechnology Division, Northern Laboratory, Saitama Industrial Technology Center for obtaining data of elasticity and viscosity in silicon gel models, and Dr Shinya Morita, Dr Ayumu Hirata, Dr Norihiko Sugita and Dr Tomoki Yamadori for performing the measurements of skin properties. We are also grateful to the patients and volunteers who participated in this study.

Formula

Disclosure statement: The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Supplementary data
 Acknowledgements
 References
 

  1. Clements PJ, Lachenbruch PA, Ng SC, Simmons M, Sterz M, Furst DE. Skin score. A semiquantitative measure of cutaneous involvement that improves prediction of prognosis in systemic sclerosis. Arthritis Rheum (1990) 33:1256–63.[ISI][Medline]
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Submitted 19 September 2007; revised version accepted 18 March 2008.
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