68 Original article
An innovative ultrasound foot scanner system for measuring the change in biomechanical properties of plantar tissue from sitting to standing Thomas Ka-Wai Nga,b, Yong-Ping Zhengc, Rachel Lai-Chu Kwana and Gladys Lai-Ying Cheinga The present study investigated the reliability of an innovative ultrasound foot scanner system in assessing the thickness and stiffness of plantar soft tissue and the comparison of stiffness and thickness in sitting and standing. Fifteen young healthy individuals were examined. The target sites on the foot sole for investigation included the heel pad, the fifth metatarsal head, the second metatarsal head, the first metatarsal head, and the pulp of the hallux. The test (day 1) and retest (day 2) were performed 1 week apart at the exact time with humidity and temperature of the assessment room under control. The thickness and stiffness of the plantar soft tissue obtained in sitting and standing positions on day 1 were used for comparison. The results showed significant test–retest reliability [intraclass correlation coefficient(3,2) > 0.90, P < 0.001] at all five sites in both sitting and standing positions. When changing from sitting to standing, the plantar soft tissue became significantly thinner (with decrease ranging from 10 to 14% at various sites) and stiffer (with increase ranging from 123 to 164% at various sites, all P < 0.05). The present innovative system is a reliable device for the measurement of the thickness
and stiffness of plantar soft tissue in either the sitting or the standing position. The change in positions from sitting to standing resulted in a significant thinning and stiffening of plantar soft tissues. This system could be a potential clinical device to monitor the biomechanical properties of plantar tissue in the elderly or in patients with diseases such as diabetes to estimate the risk of developing foot ulcer or other foot complications. International Journal of Rehabilitation Research 38:68–73 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
foot (Abouaesha et al., 2001; Cheung et al., 2005), clinicians have been keen to develop devices to assess the biomechanical properties of plantar soft tissue to predict the risk of developing foot ulcers in patients with diabetes. Several systems were adopted to assess plantar pressure using different imaging technologies such as ultrasound, computed tomography, and MRI (Gooding et al., 1986; Smith et al., 2000; Petre et al., 2008). The tissue ultrasound palpation system (TUPS) is a hand-held system with an ultrasound transducer and a load cell installed in the head of the probe for measurement of the real-time thickness of the tissue and the force required to deform the tissue. The TUPS was shown to have high reliability and validity in measuring the biomechanical properties of soft tissues in humans in terms of thickness and stiffness (Zheng and Mak, 1996; Zheng and Mak, 1999). Several studies have adopted TUPS to assess the biomechanical properties of various sites of plantar soft tissue (Zheng et al., 2000; Kwan et al., 2010). However, TUPS can only be used when the patients are in nonweight-bearing positions such as lying (in supine or prone) or half-sitting. Assessment in these positions only
The feet of humans are a complex structure for shock absorption in weight-bearing status. The prevalence of foot complications has been increasing in patients with diabetes, placing a huge burden on society (Frykberg, 1998; Wild et al., 2004; World Health Organization, 2009). The decrease in distal sensation and the increase in plantar pressure have been suggested to be the causes of diabetic foot ulcer (Edwards et al., 2008). Increase in plantar pressure could be associated with structural changes of the foot such as hammer toes or hallus valgus, which create pressure points over the sole during weight-bearing activities (Murray et al., 1996). Meanwhile, hyperglycemia in the diabetes population causes the nonenzymatic glycosylation of collagen in plantar soft tissue, which increases the collagen cross-link and stiffens the plantar tissue (Reihsner et al., 2000; Abate et al., 2010). The increase in stiffness of the plantar soft tissue may lead to a decrease in shock absorption ability during weight-bearing activities (Crawford et al., 2007). Since previous studies have found that plantar pressure is associated with the thickness and stiffness of the plantar 0342-5282 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
International Journal of Rehabilitation Research 2015, 38:68–73 Keywords: connective tissue, foot, scan, stiffness, thickness, ultrasound a
Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Physiotherapy Department, Kowloon Hospital and cInterdisciplinary Division of Biomedical Engineering, The Hong Kong Polytechnic University, Hong Kong SAR, China b
Correspondence to Gladys Lai-Ying Cheing, PhD, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, China Tel: + 852 27666738; fax: + 852 23308656; e-mail: [email protected] Received 7 September 2014 Accepted 11 October 2014
DOI: 10.1097/MRR.0000000000000097
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Biomechanical properties of plantar tissues Ng et al. 69
An innovative ultrasound foot scanner system was developed to overcome the shortcomings of TUPS. Measurements can be performed in weight-bearing positions and the speed and depth of the indentation are standardized through customized computer software. One preliminary study showed that this device is feasible for assessment of the thickness and stiffness of plantar soft tissue in humans, but its reliability and the change in the thickness and stiffness of plantar soft tissue in sitting and standing remain unknown (Zheng et al., 2012). Therefore, the objectives of the present study were to determine the reliability of this system in measuring the thickness and stiffness of the plantar soft tissue, and to compare the properties in sitting and standing positions.
Materials and methods Participants
Fifteen healthy young participants were recruited, seven men and eight women, ranging in age from 20 to 28 years. Exclusion criteria were as follows: recent foot lesions, foot deformity, peripheral neuropathy, or a history of foot surgery. Any presence of callus was recorded. Ethical approval was obtained from a local university and written informed consent was obtained from each participant before the study. Equipment
The ultrasound foot scanner system consists of a platform made of polyvinylchloride. Installed under the platform is an ultrasound transducer of 9 mm diameter and 5 MHz frequency for measurement. According to Zheng and Mak (1999), the transmission speed of the ultrasound in the soft tissue is 1540 m/s. The thickness of the soft tissue was calculated by measuring the distance between the first peak of the first echo and the first peak of the second echo presented in the control panel. These two echoes represent the ultrasound echo reflected from the skin and the soft tissue–bone interface, respectively (Fig. 1). To measure the stiffness of the plantar soft tissue, the ultrasound transducer was connected in series to a motor and a load cell that could receive a maximal force up to 50 N (Fig. 2). The motor was used to drive the transducer to deform the soft tissue perpendicular to the surface of the skin. The force used to deform the plantar soft tissue during the indentation process was recorded by the load cell. Real-time signals of the change in soft tissue thickness and the force during deformation were sent to the computer software for calculation and the force/
Fig. 1
Peak 1 128 Amplitude
provides limited information on the risk of developing foot ulcers because the common activities that lead to foot ulcers are performed in weight-bearing positions such as walking with barefeet (Boulton, 2000). Besides, the system requires skillful control of the speed and depth of the probe, which limits its feasibility in clinical practice.
Total thickness of plantar tissue
64
Peak 2
0 (b)
−64 −128
(a) 0
384
768 1152 1536 1920 2304 2688 3072 Time (10 ns/U)
Measurement of the thickness of total plantar soft tissue at the first metatarsal head in the standing position by the ultrasound foot scanner system. Wave (a) is the ultrasound echo reflected by the skin of the first metatarsal head, whereas wave (b) is the echo reflected by the soft tissue–bone interface.
displacement value was obtained by finding the slope of the line with the best fit. In the present study, the force/ displacement value was considered to be significant with the coefficient of determination of linear regression was R2 of 0.9 or more. The stiffness of the soft tissue was expressed in an effective Young’s modulus and the calculation was performed by the in-house software using the following equation: E¼
Pð1n2 Þ : 2awkða=h; nÞ
In this equation, E is the Young’s modulus, P is the force applied by the load cell, w is the indentation depth, a is the radius of the indenter, ν is the Poisson’s ratio of the tissue, h is the tissue thickness, and κ is a scaling factor that depends on both a/h and Poisson’s ratio ν (Mak et al., 1994). In this study, the Poisson’s ratio (ν) was set at 0.45 on the assumption that the soft tissue was nearly incompressible and this value has been adopted widely in previous studies when using this equation for calculation of human soft tissue (Zheng et al., 2000; Kwan et al., 2010). This equation was first used in a study carried out on articular cartilage and was later used to measure the Young’s modulus of soft tissue (Zheng et al., 2000). The driving velocity of the motor for the deformation of the plantar tissue was set at 1 mm/s and the indentation depth was 20% of the original thickness of the tissue before the indentation (Zheng and Mak, 1999). In each measurement, the probe was moved vertically up and down for three cycles to deform the plantar soft tissues three times and 400 frames of measurement were performed to determine the change in thickness. Experimental procedure
The humidity and the temperature of the assessment room were controlled during the entire study period. The test–retest reliability of the ultrasound foot scanner
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70 International Journal of Rehabilitation Research 2015, Vol 38 No 1
Fig. 2
Target site of the foot was placed directly at the top of the transducer Ultrasound transducer with 9 mm diameter
Load cell with 50 N range
Motor for the control of the indentation of the transducer
Customized software in a personal computer Ultrasound transducer Frequency 5 MHz, to record the change of thickness during deformation
Motor control Velocity: 1 mm/s Depth: 20% of the original thickness Deformation: 3 cycles of deformation
50 N range load cell Receive and calculate the load needed during deformation
Schematic diagram of the ultrasound foot scanner system measuring the thickness and stiffness of the plantar soft tissue.
system was assessed by the same assessor for all the measurement sites at the same time of the day 1 week apart. Five assessment sites on the foot were chosen, namely, the pulp of the hallux, the first metatarsal head, the second metatarsal head, the fifth metatarsal head, and the heel pad. These five sites were selected because they are the weight-bearing points on the sole during walking (Menz and Morris, 2006). The details on how to locate the measuring site on the scanner have been described in a previous study (Zheng et al., 2012). After completion of the assessment in a sitting position, the participants were assessed in the standing position. To avoid disturbing the position of the foot when transferring from sitting to standing positions, a nonslip mattress was placed on the surface of the foot scanner and a wall bar was placed nearby for the participants to grasp for balance. An electronic balance scale was installed on the platform to ensure that the distribution of weight of the participants was equal on both legs. Two trials of measurements were conducted on each testing foot site in sitting and standing positions. The mean scores of the thickness and stiffness of the plantar soft tissue were calculated for subsequent analysis. A 5 min rest was allowed between the measurements of each site. The data obtained on day 1 were used to compare the thickness and stiffness of the tissue in sitting and standing positions.
Data analysis
SPSS 17.0 (SPSS, Chicago, USA) was used to analyze the data. Intraclass correlation coefficient [ICC(3,2)] was used to analyze the test–retest reliability of the ultrasound foot scanner system. In the ICC, model 3 was used for a single rater in data collection and form 2 was chosen as the mean value of each measurement as the average of two scores. A paired t-test was used to compare the results obtained in the sitting and standing positions by the ultrasound foot scanner system on the first testing day. The level of significance was set at P-value less than 0.05. Because no significant difference was found between the data collected from the two legs, the data obtained from the two legs were averaged for subsequent analyses.
Results Test–retest reliability of the ultrasound foot scanner system
The thickness and stiffness over the big toes, the first metatarsal heads, the second metatarsal heads, the fifth metatarsal heads, and heels on day 1 and 2 are listed in Table 1. ICC indicated significant test–retest reliability of the ultrasound foot scanner system with all ICC(3,2) greater than 0.9 (all P < 0.001) at all five measurement sites taken 1 week apart.
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Biomechanical properties of plantar tissues Ng et al. 71
Thickness (mm) and stiffness (kPa) of plantar soft tissue of five measurement sites (mean ± SD) and intraclass correlation coefficient [ICC(3,2)]
Table 1
Position Thickness (mm) Sitting
Standing
Stiffness (kPa) Sitting
Standing
Site
Day 1
Day 2
ICC(3,2)
P-value
Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
9.03 ± 1.34 11.19 ± 1.05 10.64 ± 1.53 8.43 ± 1.44 15.27 ± 3.99 8.11 ± 1.20 9.79 ± 1.24 9.18 ± 1.33 7.47 ± 1.27 13.30 ± 3.65
8.94 ± 1.30 11.02 ± 1.12 10.67 ± 1.50 8.29 ± 1.46 15.23 ± 3.92 8.16 ± 1.13 9.70 ± 1.29 9.15 ± 1.22 7.44 ± 1.31 13.14 ± 3.57
0.988 0.973 0.989 0.993 0.997 0.988 0.989 0.986 0.991 0.997
< 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001**
Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
66.50 ± 33.35 73.59 ± 60.44 57.15 ± 28.81 108.38 ± 99.90 143.59 ± 46.29 150.69 ± 75.03 238.25 ± 278.34 149.48 ± 108.75 351.87 ± 440.69 379.63 ± 87.72
64.83 ± 32.35 75.83 ± 62.13 56.24 ± 27.33 111.86 ± 112.51 144.07 ± 47.32 150.33 ± 76.60 239.75 ± 280.24 146.00 ± 103.07 346.77 ± 425.69 384.07 ± 87.93
0.997 0.995 0.997 0.996 0.994 0.998 1.000 0.998 0.998 0.993
< 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001**
**P ≤ 0.001.
Mean ± SD of the thickness (mm) and stiffness (kPa) recorded in sitting and standing positions by the ultrasound foot scanner system
Table 2
Site Thickness (mm) Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Stiffness (kPa) Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
Sitting 9.03 ± 1.34 11.19 ± 1.05 10.64 ± 1.53 8.43 ± 1.44 15.27 ± 3.99 66.50 ± 33.35 73.59 ± 60.44 57.15 ± 28.81 108.38 ± 99.9 143.59 ± 46.29
Standing 8.11 ± 1.20 9.79 ± 1.24 9.18 ± 1.33 7.47 ± 1.27 13.30 ± 3.65 150.69 ± 75.03 238.25 ± 278.34 149.48 ± 108.75 351.87 ± 440.69 379.63 ± 87.72
P-value < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** 0.013* 0.001** 0.018* < 0.001**
*P < 0.05. **P ≤0.001.
Comparisons of the thickness and stiffness of the plantar soft tissue in sitting and standing positions
The thickness and stiffness of the five measuring sites over the soles in the sitting and standing positions are listed in Table 2. A paired t-test showed that when changing from sitting to standing positions, the plantar soft tissue became significantly thinner, with a decrease in thickness that ranged from 0.92 to 1.97 mm at different measurement sites (all P < 0.001). Also, the stiffness of plantar soft tissue was significantly increased in a standing position at different measurement sites, with an increase that ranged from 84.19 to 243.49 kPa, compared with the measurements recorded in a sitting position (all P < 0.05).
Discussion Foot ulceration is one of the complications among patients with diabetes. One of the risk factors of developing foot
ulceration is increase in the stiffness of plantar soft tissue (Reihsner and Menzel, 1998). In addition, the thinning of plantar soft tissue would further reduce the shock absorption ability of the foot during walking. As the morbidity, mortality, and additional medical cost are considerably increased for patients with diabetic foot ulceration (Ramsey et al., 1999), an accurate and convenient assessment tool to monitor the mechanical changes over the sole of foot for early detection of those at risk of developing foot ulceration is essential. Several devices and imaging systems have been used to assess the stiffness and thickness of plantar soft tissue. However, they either include expensive imaging techniques such as MRI or systems designed to provide indirect measurements of the plantar soft tissue during indentation (Gefen et al., 2001a, 2001b; Rome et al., 2001). These factors limit their feasibility of application in clinical settings. Ultrasound is a relatively inexpensive and safe imaging technology. The ultrasound foot scanner system used in the present study is an advanced model based on previously designed TUPS, which assesses the plantar soft tissues only in a nonweight-bearing position. The present foot scanner can reflect the plantar pressure during weight-bearing, which is clinically relevant as foot ulceration develops with weight-bearing activities. Redistribution of plantar pressure may occur when changing from a nonweight-bearing position to a weightbearing position as the foot is a flexible structure (Cowley et al., 2008). Moreover, TUPS requires the assessors to perform a manual indentation of the ultrasound probe. This process requires skillful practice and measurement errors may occur if the alignment of the probe is not perfectly perpendicular to the skin. One earlier study reported that the ultrasound foot scanner system can
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72 International Journal of Rehabilitation Research 2015, Vol 38 No 1
measure the stiffness and thickness of plantar soft tissue at different body weight loading, but the reliability of the system remains unknown (Zheng et al., 2012). Our findings indicated high test–retest reliability of using the ultrasound foot scanner system for assessment of the thickness and stiffness of plantar tissue. The ultrasound probe was fixated in the system to ensure its perpendicular alignment to the surface of the skin during each measurement. Besides, an electronic scale was built into the foot platform to ensure equal distribution of body weight on both feet; customized software was implemented to standardize the speed and depth of penetration. All these designs contributed toward the high consistency and reliability of the measurements of the thickness and stiffness of the plantar soft tissue. Besides reliability, the present study is the first to compare the change in the thickness and stiffness of the plantar soft tissue when transferring from sitting to standing positions. There was a significant thinning and stiffening of plantar tissue over the pulp of the hallux, the first metatarsal head, the second metatarsal head, the fifth metatarsal head, and the heel after the participants shifted from a sitting to a standing position. Specifically, there was a range of 10–14% decrease in the thickness of the plantar soft tissue and a range of 123–164% increase in the stiffness of the plantar soft tissue. When getting up from a sitting to a standing position, the body weight exerts a stronger force over the skin of the foot and the vertical compression force results in a horizontal squeezing of the tissue, which is commonly observed in biological soft tissue for protection from tissue breakdown (Zheng et al., 2012). Our results also showed that the stiffness of the plantar soft tissue was highest at the heel, followed by the fifth metatarsal head, the first metatarsal head, the pulp of the hallux, and the second metatarsal head. This trend was consistent in both sitting and standing positions. This reflects that the assessment in either sitting or standing provides similar useful information in prediction of the development of foot ulceration. This is the first study to note this trend and future studies can further investigate the alternation of this trend in the aging population or in patients such as those with diabetes. Our findings indicated that the weight-bearing status alters the stiffness of plantar tissue. Indeed, the change in stiffness of plantar tissue is associated with the increase of the plantar soft tissue pressure. Cheung et al. (2005) found that a five-fold increase in stiffness of plantar soft tissue would lead to an increase in the plantar pressure in the plantar soft tissue of more than 30%. Flynn et al. (1997) further showed that the plantar pressure was reduced during weight-supported walking as compared with normal walking. Vela et al. (1998) also found that an increase in body weight significantly increased the plantar pressure. This further supports the use of the
present foot scanner system in assessing the plantar soft tissue in weight-bearing positions as a functional position to estimate the risk of developing foot ulcers. Further investigation is required to explore the relationship of the change of plantar soft tissue stiffness and the plantar pressure using the present ultrasound foot scanner system. The percentage decrease in tissue thickness over the heel from sitting to standing positions was around 13%. This figure was lower than the results reported by Gefen et al. (2001a, 2001b), who found a deformation of about 40% of heel tissue thickness during heel strike while walking using an X-ray-based system. This discrepancy can be attributed to the ground reaction force exerted on the heel during walking. However, the device used by Gefen et al. (2001a, 2001b) only allows a one-dimensional lateral view of the foot, which is less accurate in measurement of the deformation of one particular point on the heel. Besides, exposure to radiation and the expenses would be a limitation for regular assessments. Plantar soft tissues over the metatarsal heads are common sites of foot ulceration. A previous study showed that toe extension produced a significant increase in stiffness on the plantar soft tissue over metatarsal heads, which would cause an increase in plantar soft tissue pressure during the push-off phase in walking (Garcia et al., 2008). Modification of the current system such as placement of a tilting system to fixate the toes in the extension position would be technically feasible to measure how toe extension changes the soft tissue stiffness and thickness over the metatarsal heads, but further investigation is required. Use of the present foot scanner system allows clinicians to investigate the biomechanical properties of the metatarsal heads in a neutral toe position for early identification of callus, which might not be obvious clinically. The ultrasound foot scanner system was designed to minimize possible measurement errors. Assessors were only required to assist the participants to adopt a proper sitting and standing posture during the measurement. Similarly, the participants were only required to maintain the posture during the measurement at each site. Therefore, the present system could potentially be used in clinical settings that use minimal manpower to produce accurate and efficient assessments with good test–retest reliability. It is important to assess the change in the biomechanical properties of plantar tissues in various weight-bearing positions because it allows early detection of the risk of developing foot complications such as diabetic ulcers. As the present study was carried out in healthy participants, further study can investigate the use of the present device to measure the thickness and stiffness of plantar soft tissue in other populations such as the elderly or in patients with diabetes.
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Biomechanical properties of plantar tissues Ng et al. 73
Conclusion
The ultrasound foot scanner system is a reliable tool for measurement of the thickness and stiffness of the plantar soft tissue in healthy individuals in either the sitting or the standing position. The plantar soft tissues become significantly thinner and stiffer when transferring from sitting to standing positions, which implies that weightbearing status may alter the plantar pressure. This system can potentially be used as a clinical device to identify the risk of development of foot ulcers or other foot complications in various disease groups such as patients with diabetes.
Acknowledgements This project was supported by the General Research Fund from the Research Grants Council in Hong Kong (PolyU 5128/08E). Conflicts of interest
There are no conflicts of interest.
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An innovative ultrasound foot scanner system for measuring the change in biomechanical properties of plantar tissue from sitting to standing Thomas Ka-Wai Nga,b, Yong-Ping Zhengc, Rachel Lai-Chu Kwana and Gladys Lai-Ying Cheinga The present study investigated the reliability of an innovative ultrasound foot scanner system in assessing the thickness and stiffness of plantar soft tissue and the comparison of stiffness and thickness in sitting and standing. Fifteen young healthy individuals were examined. The target sites on the foot sole for investigation included the heel pad, the fifth metatarsal head, the second metatarsal head, the first metatarsal head, and the pulp of the hallux. The test (day 1) and retest (day 2) were performed 1 week apart at the exact time with humidity and temperature of the assessment room under control. The thickness and stiffness of the plantar soft tissue obtained in sitting and standing positions on day 1 were used for comparison. The results showed significant test–retest reliability [intraclass correlation coefficient(3,2) > 0.90, P < 0.001] at all five sites in both sitting and standing positions. When changing from sitting to standing, the plantar soft tissue became significantly thinner (with decrease ranging from 10 to 14% at various sites) and stiffer (with increase ranging from 123 to 164% at various sites, all P < 0.05). The present innovative system is a reliable device for the measurement of the thickness
and stiffness of plantar soft tissue in either the sitting or the standing position. The change in positions from sitting to standing resulted in a significant thinning and stiffening of plantar soft tissues. This system could be a potential clinical device to monitor the biomechanical properties of plantar tissue in the elderly or in patients with diseases such as diabetes to estimate the risk of developing foot ulcer or other foot complications. International Journal of Rehabilitation Research 38:68–73 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
foot (Abouaesha et al., 2001; Cheung et al., 2005), clinicians have been keen to develop devices to assess the biomechanical properties of plantar soft tissue to predict the risk of developing foot ulcers in patients with diabetes. Several systems were adopted to assess plantar pressure using different imaging technologies such as ultrasound, computed tomography, and MRI (Gooding et al., 1986; Smith et al., 2000; Petre et al., 2008). The tissue ultrasound palpation system (TUPS) is a hand-held system with an ultrasound transducer and a load cell installed in the head of the probe for measurement of the real-time thickness of the tissue and the force required to deform the tissue. The TUPS was shown to have high reliability and validity in measuring the biomechanical properties of soft tissues in humans in terms of thickness and stiffness (Zheng and Mak, 1996; Zheng and Mak, 1999). Several studies have adopted TUPS to assess the biomechanical properties of various sites of plantar soft tissue (Zheng et al., 2000; Kwan et al., 2010). However, TUPS can only be used when the patients are in nonweight-bearing positions such as lying (in supine or prone) or half-sitting. Assessment in these positions only
The feet of humans are a complex structure for shock absorption in weight-bearing status. The prevalence of foot complications has been increasing in patients with diabetes, placing a huge burden on society (Frykberg, 1998; Wild et al., 2004; World Health Organization, 2009). The decrease in distal sensation and the increase in plantar pressure have been suggested to be the causes of diabetic foot ulcer (Edwards et al., 2008). Increase in plantar pressure could be associated with structural changes of the foot such as hammer toes or hallus valgus, which create pressure points over the sole during weight-bearing activities (Murray et al., 1996). Meanwhile, hyperglycemia in the diabetes population causes the nonenzymatic glycosylation of collagen in plantar soft tissue, which increases the collagen cross-link and stiffens the plantar tissue (Reihsner et al., 2000; Abate et al., 2010). The increase in stiffness of the plantar soft tissue may lead to a decrease in shock absorption ability during weight-bearing activities (Crawford et al., 2007). Since previous studies have found that plantar pressure is associated with the thickness and stiffness of the plantar 0342-5282 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
International Journal of Rehabilitation Research 2015, 38:68–73 Keywords: connective tissue, foot, scan, stiffness, thickness, ultrasound a
Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Physiotherapy Department, Kowloon Hospital and cInterdisciplinary Division of Biomedical Engineering, The Hong Kong Polytechnic University, Hong Kong SAR, China b
Correspondence to Gladys Lai-Ying Cheing, PhD, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, China Tel: + 852 27666738; fax: + 852 23308656; e-mail: [email protected] Received 7 September 2014 Accepted 11 October 2014
DOI: 10.1097/MRR.0000000000000097
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Biomechanical properties of plantar tissues Ng et al. 69
An innovative ultrasound foot scanner system was developed to overcome the shortcomings of TUPS. Measurements can be performed in weight-bearing positions and the speed and depth of the indentation are standardized through customized computer software. One preliminary study showed that this device is feasible for assessment of the thickness and stiffness of plantar soft tissue in humans, but its reliability and the change in the thickness and stiffness of plantar soft tissue in sitting and standing remain unknown (Zheng et al., 2012). Therefore, the objectives of the present study were to determine the reliability of this system in measuring the thickness and stiffness of the plantar soft tissue, and to compare the properties in sitting and standing positions.
Materials and methods Participants
Fifteen healthy young participants were recruited, seven men and eight women, ranging in age from 20 to 28 years. Exclusion criteria were as follows: recent foot lesions, foot deformity, peripheral neuropathy, or a history of foot surgery. Any presence of callus was recorded. Ethical approval was obtained from a local university and written informed consent was obtained from each participant before the study. Equipment
The ultrasound foot scanner system consists of a platform made of polyvinylchloride. Installed under the platform is an ultrasound transducer of 9 mm diameter and 5 MHz frequency for measurement. According to Zheng and Mak (1999), the transmission speed of the ultrasound in the soft tissue is 1540 m/s. The thickness of the soft tissue was calculated by measuring the distance between the first peak of the first echo and the first peak of the second echo presented in the control panel. These two echoes represent the ultrasound echo reflected from the skin and the soft tissue–bone interface, respectively (Fig. 1). To measure the stiffness of the plantar soft tissue, the ultrasound transducer was connected in series to a motor and a load cell that could receive a maximal force up to 50 N (Fig. 2). The motor was used to drive the transducer to deform the soft tissue perpendicular to the surface of the skin. The force used to deform the plantar soft tissue during the indentation process was recorded by the load cell. Real-time signals of the change in soft tissue thickness and the force during deformation were sent to the computer software for calculation and the force/
Fig. 1
Peak 1 128 Amplitude
provides limited information on the risk of developing foot ulcers because the common activities that lead to foot ulcers are performed in weight-bearing positions such as walking with barefeet (Boulton, 2000). Besides, the system requires skillful control of the speed and depth of the probe, which limits its feasibility in clinical practice.
Total thickness of plantar tissue
64
Peak 2
0 (b)
−64 −128
(a) 0
384
768 1152 1536 1920 2304 2688 3072 Time (10 ns/U)
Measurement of the thickness of total plantar soft tissue at the first metatarsal head in the standing position by the ultrasound foot scanner system. Wave (a) is the ultrasound echo reflected by the skin of the first metatarsal head, whereas wave (b) is the echo reflected by the soft tissue–bone interface.
displacement value was obtained by finding the slope of the line with the best fit. In the present study, the force/ displacement value was considered to be significant with the coefficient of determination of linear regression was R2 of 0.9 or more. The stiffness of the soft tissue was expressed in an effective Young’s modulus and the calculation was performed by the in-house software using the following equation: E¼
Pð1n2 Þ : 2awkða=h; nÞ
In this equation, E is the Young’s modulus, P is the force applied by the load cell, w is the indentation depth, a is the radius of the indenter, ν is the Poisson’s ratio of the tissue, h is the tissue thickness, and κ is a scaling factor that depends on both a/h and Poisson’s ratio ν (Mak et al., 1994). In this study, the Poisson’s ratio (ν) was set at 0.45 on the assumption that the soft tissue was nearly incompressible and this value has been adopted widely in previous studies when using this equation for calculation of human soft tissue (Zheng et al., 2000; Kwan et al., 2010). This equation was first used in a study carried out on articular cartilage and was later used to measure the Young’s modulus of soft tissue (Zheng et al., 2000). The driving velocity of the motor for the deformation of the plantar tissue was set at 1 mm/s and the indentation depth was 20% of the original thickness of the tissue before the indentation (Zheng and Mak, 1999). In each measurement, the probe was moved vertically up and down for three cycles to deform the plantar soft tissues three times and 400 frames of measurement were performed to determine the change in thickness. Experimental procedure
The humidity and the temperature of the assessment room were controlled during the entire study period. The test–retest reliability of the ultrasound foot scanner
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70 International Journal of Rehabilitation Research 2015, Vol 38 No 1
Fig. 2
Target site of the foot was placed directly at the top of the transducer Ultrasound transducer with 9 mm diameter
Load cell with 50 N range
Motor for the control of the indentation of the transducer
Customized software in a personal computer Ultrasound transducer Frequency 5 MHz, to record the change of thickness during deformation
Motor control Velocity: 1 mm/s Depth: 20% of the original thickness Deformation: 3 cycles of deformation
50 N range load cell Receive and calculate the load needed during deformation
Schematic diagram of the ultrasound foot scanner system measuring the thickness and stiffness of the plantar soft tissue.
system was assessed by the same assessor for all the measurement sites at the same time of the day 1 week apart. Five assessment sites on the foot were chosen, namely, the pulp of the hallux, the first metatarsal head, the second metatarsal head, the fifth metatarsal head, and the heel pad. These five sites were selected because they are the weight-bearing points on the sole during walking (Menz and Morris, 2006). The details on how to locate the measuring site on the scanner have been described in a previous study (Zheng et al., 2012). After completion of the assessment in a sitting position, the participants were assessed in the standing position. To avoid disturbing the position of the foot when transferring from sitting to standing positions, a nonslip mattress was placed on the surface of the foot scanner and a wall bar was placed nearby for the participants to grasp for balance. An electronic balance scale was installed on the platform to ensure that the distribution of weight of the participants was equal on both legs. Two trials of measurements were conducted on each testing foot site in sitting and standing positions. The mean scores of the thickness and stiffness of the plantar soft tissue were calculated for subsequent analysis. A 5 min rest was allowed between the measurements of each site. The data obtained on day 1 were used to compare the thickness and stiffness of the tissue in sitting and standing positions.
Data analysis
SPSS 17.0 (SPSS, Chicago, USA) was used to analyze the data. Intraclass correlation coefficient [ICC(3,2)] was used to analyze the test–retest reliability of the ultrasound foot scanner system. In the ICC, model 3 was used for a single rater in data collection and form 2 was chosen as the mean value of each measurement as the average of two scores. A paired t-test was used to compare the results obtained in the sitting and standing positions by the ultrasound foot scanner system on the first testing day. The level of significance was set at P-value less than 0.05. Because no significant difference was found between the data collected from the two legs, the data obtained from the two legs were averaged for subsequent analyses.
Results Test–retest reliability of the ultrasound foot scanner system
The thickness and stiffness over the big toes, the first metatarsal heads, the second metatarsal heads, the fifth metatarsal heads, and heels on day 1 and 2 are listed in Table 1. ICC indicated significant test–retest reliability of the ultrasound foot scanner system with all ICC(3,2) greater than 0.9 (all P < 0.001) at all five measurement sites taken 1 week apart.
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Biomechanical properties of plantar tissues Ng et al. 71
Thickness (mm) and stiffness (kPa) of plantar soft tissue of five measurement sites (mean ± SD) and intraclass correlation coefficient [ICC(3,2)]
Table 1
Position Thickness (mm) Sitting
Standing
Stiffness (kPa) Sitting
Standing
Site
Day 1
Day 2
ICC(3,2)
P-value
Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
9.03 ± 1.34 11.19 ± 1.05 10.64 ± 1.53 8.43 ± 1.44 15.27 ± 3.99 8.11 ± 1.20 9.79 ± 1.24 9.18 ± 1.33 7.47 ± 1.27 13.30 ± 3.65
8.94 ± 1.30 11.02 ± 1.12 10.67 ± 1.50 8.29 ± 1.46 15.23 ± 3.92 8.16 ± 1.13 9.70 ± 1.29 9.15 ± 1.22 7.44 ± 1.31 13.14 ± 3.57
0.988 0.973 0.989 0.993 0.997 0.988 0.989 0.986 0.991 0.997
< 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001**
Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
66.50 ± 33.35 73.59 ± 60.44 57.15 ± 28.81 108.38 ± 99.90 143.59 ± 46.29 150.69 ± 75.03 238.25 ± 278.34 149.48 ± 108.75 351.87 ± 440.69 379.63 ± 87.72
64.83 ± 32.35 75.83 ± 62.13 56.24 ± 27.33 111.86 ± 112.51 144.07 ± 47.32 150.33 ± 76.60 239.75 ± 280.24 146.00 ± 103.07 346.77 ± 425.69 384.07 ± 87.93
0.997 0.995 0.997 0.996 0.994 0.998 1.000 0.998 0.998 0.993
< 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001**
**P ≤ 0.001.
Mean ± SD of the thickness (mm) and stiffness (kPa) recorded in sitting and standing positions by the ultrasound foot scanner system
Table 2
Site Thickness (mm) Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel Stiffness (kPa) Hallux First metatarsal head Second metatarsal head Fifth metatarsal head Heel
Sitting 9.03 ± 1.34 11.19 ± 1.05 10.64 ± 1.53 8.43 ± 1.44 15.27 ± 3.99 66.50 ± 33.35 73.59 ± 60.44 57.15 ± 28.81 108.38 ± 99.9 143.59 ± 46.29
Standing 8.11 ± 1.20 9.79 ± 1.24 9.18 ± 1.33 7.47 ± 1.27 13.30 ± 3.65 150.69 ± 75.03 238.25 ± 278.34 149.48 ± 108.75 351.87 ± 440.69 379.63 ± 87.72
P-value < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** < 0.001** 0.013* 0.001** 0.018* < 0.001**
*P < 0.05. **P ≤0.001.
Comparisons of the thickness and stiffness of the plantar soft tissue in sitting and standing positions
The thickness and stiffness of the five measuring sites over the soles in the sitting and standing positions are listed in Table 2. A paired t-test showed that when changing from sitting to standing positions, the plantar soft tissue became significantly thinner, with a decrease in thickness that ranged from 0.92 to 1.97 mm at different measurement sites (all P < 0.001). Also, the stiffness of plantar soft tissue was significantly increased in a standing position at different measurement sites, with an increase that ranged from 84.19 to 243.49 kPa, compared with the measurements recorded in a sitting position (all P < 0.05).
Discussion Foot ulceration is one of the complications among patients with diabetes. One of the risk factors of developing foot
ulceration is increase in the stiffness of plantar soft tissue (Reihsner and Menzel, 1998). In addition, the thinning of plantar soft tissue would further reduce the shock absorption ability of the foot during walking. As the morbidity, mortality, and additional medical cost are considerably increased for patients with diabetic foot ulceration (Ramsey et al., 1999), an accurate and convenient assessment tool to monitor the mechanical changes over the sole of foot for early detection of those at risk of developing foot ulceration is essential. Several devices and imaging systems have been used to assess the stiffness and thickness of plantar soft tissue. However, they either include expensive imaging techniques such as MRI or systems designed to provide indirect measurements of the plantar soft tissue during indentation (Gefen et al., 2001a, 2001b; Rome et al., 2001). These factors limit their feasibility of application in clinical settings. Ultrasound is a relatively inexpensive and safe imaging technology. The ultrasound foot scanner system used in the present study is an advanced model based on previously designed TUPS, which assesses the plantar soft tissues only in a nonweight-bearing position. The present foot scanner can reflect the plantar pressure during weight-bearing, which is clinically relevant as foot ulceration develops with weight-bearing activities. Redistribution of plantar pressure may occur when changing from a nonweight-bearing position to a weightbearing position as the foot is a flexible structure (Cowley et al., 2008). Moreover, TUPS requires the assessors to perform a manual indentation of the ultrasound probe. This process requires skillful practice and measurement errors may occur if the alignment of the probe is not perfectly perpendicular to the skin. One earlier study reported that the ultrasound foot scanner system can
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72 International Journal of Rehabilitation Research 2015, Vol 38 No 1
measure the stiffness and thickness of plantar soft tissue at different body weight loading, but the reliability of the system remains unknown (Zheng et al., 2012). Our findings indicated high test–retest reliability of using the ultrasound foot scanner system for assessment of the thickness and stiffness of plantar tissue. The ultrasound probe was fixated in the system to ensure its perpendicular alignment to the surface of the skin during each measurement. Besides, an electronic scale was built into the foot platform to ensure equal distribution of body weight on both feet; customized software was implemented to standardize the speed and depth of penetration. All these designs contributed toward the high consistency and reliability of the measurements of the thickness and stiffness of the plantar soft tissue. Besides reliability, the present study is the first to compare the change in the thickness and stiffness of the plantar soft tissue when transferring from sitting to standing positions. There was a significant thinning and stiffening of plantar tissue over the pulp of the hallux, the first metatarsal head, the second metatarsal head, the fifth metatarsal head, and the heel after the participants shifted from a sitting to a standing position. Specifically, there was a range of 10–14% decrease in the thickness of the plantar soft tissue and a range of 123–164% increase in the stiffness of the plantar soft tissue. When getting up from a sitting to a standing position, the body weight exerts a stronger force over the skin of the foot and the vertical compression force results in a horizontal squeezing of the tissue, which is commonly observed in biological soft tissue for protection from tissue breakdown (Zheng et al., 2012). Our results also showed that the stiffness of the plantar soft tissue was highest at the heel, followed by the fifth metatarsal head, the first metatarsal head, the pulp of the hallux, and the second metatarsal head. This trend was consistent in both sitting and standing positions. This reflects that the assessment in either sitting or standing provides similar useful information in prediction of the development of foot ulceration. This is the first study to note this trend and future studies can further investigate the alternation of this trend in the aging population or in patients such as those with diabetes. Our findings indicated that the weight-bearing status alters the stiffness of plantar tissue. Indeed, the change in stiffness of plantar tissue is associated with the increase of the plantar soft tissue pressure. Cheung et al. (2005) found that a five-fold increase in stiffness of plantar soft tissue would lead to an increase in the plantar pressure in the plantar soft tissue of more than 30%. Flynn et al. (1997) further showed that the plantar pressure was reduced during weight-supported walking as compared with normal walking. Vela et al. (1998) also found that an increase in body weight significantly increased the plantar pressure. This further supports the use of the
present foot scanner system in assessing the plantar soft tissue in weight-bearing positions as a functional position to estimate the risk of developing foot ulcers. Further investigation is required to explore the relationship of the change of plantar soft tissue stiffness and the plantar pressure using the present ultrasound foot scanner system. The percentage decrease in tissue thickness over the heel from sitting to standing positions was around 13%. This figure was lower than the results reported by Gefen et al. (2001a, 2001b), who found a deformation of about 40% of heel tissue thickness during heel strike while walking using an X-ray-based system. This discrepancy can be attributed to the ground reaction force exerted on the heel during walking. However, the device used by Gefen et al. (2001a, 2001b) only allows a one-dimensional lateral view of the foot, which is less accurate in measurement of the deformation of one particular point on the heel. Besides, exposure to radiation and the expenses would be a limitation for regular assessments. Plantar soft tissues over the metatarsal heads are common sites of foot ulceration. A previous study showed that toe extension produced a significant increase in stiffness on the plantar soft tissue over metatarsal heads, which would cause an increase in plantar soft tissue pressure during the push-off phase in walking (Garcia et al., 2008). Modification of the current system such as placement of a tilting system to fixate the toes in the extension position would be technically feasible to measure how toe extension changes the soft tissue stiffness and thickness over the metatarsal heads, but further investigation is required. Use of the present foot scanner system allows clinicians to investigate the biomechanical properties of the metatarsal heads in a neutral toe position for early identification of callus, which might not be obvious clinically. The ultrasound foot scanner system was designed to minimize possible measurement errors. Assessors were only required to assist the participants to adopt a proper sitting and standing posture during the measurement. Similarly, the participants were only required to maintain the posture during the measurement at each site. Therefore, the present system could potentially be used in clinical settings that use minimal manpower to produce accurate and efficient assessments with good test–retest reliability. It is important to assess the change in the biomechanical properties of plantar tissues in various weight-bearing positions because it allows early detection of the risk of developing foot complications such as diabetic ulcers. As the present study was carried out in healthy participants, further study can investigate the use of the present device to measure the thickness and stiffness of plantar soft tissue in other populations such as the elderly or in patients with diabetes.
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Biomechanical properties of plantar tissues Ng et al. 73
Conclusion
The ultrasound foot scanner system is a reliable tool for measurement of the thickness and stiffness of the plantar soft tissue in healthy individuals in either the sitting or the standing position. The plantar soft tissues become significantly thinner and stiffer when transferring from sitting to standing positions, which implies that weightbearing status may alter the plantar pressure. This system can potentially be used as a clinical device to identify the risk of development of foot ulcers or other foot complications in various disease groups such as patients with diabetes.
Acknowledgements This project was supported by the General Research Fund from the Research Grants Council in Hong Kong (PolyU 5128/08E). Conflicts of interest
There are no conflicts of interest.
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