Literature DB >> 36225329

Effect of robot-assisted gait training on the biomechanical properties of burn scars: a single-blind, randomized controlled trial.

Yoon Soo Cho1, So Young Joo1, Cheong Hoon Seo1.   

Abstract

Background: Robot-assisted gait training (RAGT) is more effective in the range of motion (ROM) and isometric strength in patients with burns than conventional training. However, concerns have been raised about whether RAGT might negatively affect the scars of patients with burns. Therefore, we investigated the effects of RAGT-induced mechanical load on the biomechanical properties of burn scars.
Methods: This was a single-blind, randomized clinical trial conducted on inpatients admitted to the Department of Rehabilitation Medicine between September 2020 and August 2021. RAGT was conducted for 30 min per day, five days a week for 12 weeks and the control group received conventional gait training for 12 weeks. The pre-training ROM of lower extremity joints was evaluated and the levels of melanin, erythema, trans-epidermal water loss, scar distensibility and elasticity were assessed before training and at 4 and 12 weeks after training. Finally, 19 patients in the gait assistance robot (GAR) group and 20 patients in the control group completed the 12-week trial and all evaluations.
Results: There were no significant differences in the epidemiologic characteristics, pre-training ROM of joints and pre-training biomechanical properties of the burn scar between the groups (p > 0.05 for all). None of the patients experienced skin abrasion around the burn scar where the fastening belts were applied or musculoskeletal or cardiovascular adverse events during the training. Scar thickness significantly increased in both groups (p = 0.037 and p = 0.019) and scar distensibility significantly decreased in the control group (p = 0.011) during the training. Hysteresis was significantly decreased in the GAR group during the training (p = 0.038). The GAR and control groups showed significant difference in the change in the values of hysteresis between pre-training and 12 weeks after training (p = 0.441 and p = 0.049). Conclusions: RAGT significantly decreased hysteresis in hypertrophic burn scars and did not cause a significant decrease in skin distensibility. Moreover, no skin complications around the burn scars were detected during RAGT. Trial registration: This study registered on the Clinical Research Information Service (KCT0005204).
© The Author(s) 2022. Published by Oxford University Press.

Entities:  

Keywords:  Burn; Burn rehabilitation; Hysteresis; Robot-assisted gait training; Scar biomechanical properties

Year:  2022        PMID: 36225329      PMCID: PMC9547496          DOI: 10.1093/burnst/tkac026

Source DB:  PubMed          Journal:  Burns Trauma        ISSN: 2321-3868


This study clarified the effect of robot-assisted gait training on biomechanical properties of burn scars. Robot-assisted gait training had no negative effects on burn scars. Robot-assisted gait training decreased hysteresis on burn scars.

Background

The primary goals of burn rehabilitation medicine are preventing the formation of burn scar contracture, improving the limited range of motion (ROM) of joints and limiting functional restrictions [1]. In particular, scar contracture of the lower extremities can lead to pain during walking and limited ROM of the hip, knee and ankle joints, which can result in gait disturbance [2,3]. Appropriate and sufficient rehabilitation therapy following burn injury can decrease hypertrophic scar formation and delay the progression of scar contracture in burn survivors [1,4]. Conventional rehabilitation therapy for patients with burns with scar contracture of the lower extremities includes passive joint ROM training with disconnected movements, gait training using walking aids and manual therapy by a physical therapist [5]. The latest trends in rehabilitation therapy emphasize the motor learning theory, which states that motor skills can be learned through intensive, repetitive training mimicking the patient’s motion [6]. Task-specific training based on the motor learning theory is reportedly more effective than conventional rehabilitation therapy [7]. Accordingly, intensive, repetitive training of normal gait motion has been applied by experienced physical therapists and, more recently, by gait assistance robots (GARs) for patients with gait disturbance. GARs are pre-programmed to induce lower extremity movements following normal physiological gait patterns and assist gait training by therapists. Therefore, it can improve the repeatability of gait kinematics and can thereby reduce the time and physical labour requirements of therapists [3,8-11]. In our previous studies, we showed that robot-assisted gait training (RAGT) in patients with burns increased isometric strength and ROM of the lower extremities more significantly than does conventional training [3,11]. However, concerns exist regarding the potential negative effects of RAGT on the scars of patients with burns despite the absence of skin complications during our study. To our knowledge, no studies have demonstrated or published the effects of RAGT-induced mechanical load on the biomechanical properties of burn scars despite the expansion of robotic technologies in the field of burn rehabilitation medicine. Furthermore, applying mechanical loads to re-epithelializing wounds of mouse skin stimulated the formation of hypertrophic scars by reducing cellular apoptosis [12], and mechanical stretching enhanced hypertrophy and hyperplasia in the pulmonary artery [13]. Skin safety studies for RAGT are needed to revitalize the use of GAR in rehabilitation therapy for patients with burns. Therefore, GAR was applied to the rehabilitation therapy of patients with burns with limited ROM in the lower extremities to investigate the effects of RAGT on the scar biomechanical properties.

Methods

Study population and ethics statement

This was a single-blind, randomized clinical trial conducted between September 2020 and August 2021. A total of 46 patients admitted to the burn centre in the Department of Rehabilitation Medicine were recruited. The inclusion criteria were (1) adult (19 years or older) patients with burn scar contracture in the lower extremities, (2) sufficient cognitive function to control the robot, (3) no neuromuscular diseases, which could be associated with weakness in the lower extremities. and (4) written informed consent provided for trial inclusion. Six of them were excluded for the following reasons: (1) duration of <2 months from burn injury to the evaluation because of a high risk of skin abrasion during RAGT in our previous pilot study (n = 3); (2) weight of ≥100 kg or height of <150 cm or ≥185 cm due to exceeding the constraints of the robot (n = 1); (3) bleeding tendency in the scar area (n = 1); and (4) history of fibula fracture (n = 1) [3,11]. Flow chart of patient enrollment and participation

Randomization and blinding

The remaining 40 burn patients were enrolled and numbers were assigned according to the order of admission of 40 patients with scar contracture in the lower extremities. Then a computer program was used to randomly divide them into the GAR group for RAGT (n = 20) and the control group for conventional gait training (n = 20) (Figure 1). An experienced physical therapist, who was not involved in the rehabilitation training, measured the ROMs of the joints in the lower extremities. A research assistant, who was not involved in the rehabilitation training, performed a skin test for the scar biomechanical properties. The present study and study protocol were approved by the Institutional Review Board (HG2020-006) and registered on the Clinical Research Information Service (KCT0005204). All patients voluntarily participated in the study after providing written informed consent.
Figure 1.

Flow chart of patient enrollment and participation

RAGT

The ROM of the joints in the lower extremities was evaluated to test pre-training homogeneity before training. Flexion and extension ROM in the hip, knee and ankle joints were evaluated using a portable goniometer following a standardized technique by an experienced physical therapist, who was not involved in the rehabilitation training [14]. The GAR group received gait training using the SUBAR® (CRETEM Co. Ltd, Anyang-si, South Korea) (Figure 2). The SUBAR® consists of an exoskeleton that supports the legs and an operating device that assists gait. The robot provides force to the patient for walking. The leg exoskeleton was adjusted for each patient based on hip-to-knee and knee-to-foot length measurements that were taken prior to RAGT. Both lower limbs were placed into the exoskeleton and the thighs and legs were firmly fixed with the fastening belts. The gait speed and knee ROM were gradually adjusted according to improvements in joint motion and gait function. The setup could be operated directly by the patient or be controlled remotely by the physical therapist for the safety of the patient. The RAGT consisted of stepping in place, forward gait and backward gait. The training was conducted for 30 min per day, 5 days a week for 12 weeks. The control group received conventional gait training, including ROM and strengthening exercise training in the sitting or standing position, weight-bearing training on the side with leg weakness and balance training to facilitate normal gait pattern.
Figure 2.

Burn patient undergoing robot-assisted gait training using the SUBAR®

Burn patient undergoing robot-assisted gait training using the SUBAR® A skin test was conducted on the burn scars of eligible patients before training and at 4 and 12 weeks after training. (a) Patient with the initial burn injury, (b) Mexameter® for measuring the levels of melanin and erythema, (c) Tewameter® for measuring trans-epidermal water loss and (d) Cutometer® for measuring scar distensibility and elasticity

Assessment of the scar biomechanical properties

A skin test was conducted by a research assistant in an independent and blinded fashion before training and at 4 and 12 weeks after training (Figure 3). To ensure consistency of the scar location, a translucent linear low-density polyethylene film, Cleanwrap® (CLEANWRAP Co., Ltd, Gimhae-si, South Korea), was applied to the measurement site. For identification of the region to be measured, remarkable landmarks and a circle with a 3-cm diameter were drawn on the film as in previous studies [15,16]. The levels of melanin and erythema were evaluated using a Mexameter MX18® (Courage-Khazaka Electronics GmbH, Cologne, Germany), with a higher value representing a darker and redder scar. Trans-epidermal water loss, which represents skin barrier function, was investigated using a Tewameter® (Courage-Khazaka Electronics GmbH, Cologne, Germany). Relative humidity was maintained at 40–50% and room temperature at 20–25°C during skin assessment [17]. Scar distensibility and elasticity were assessed using a Cutometer SEM 5801® (Courage-Khazaka Electronic GmbH, Cologne, Germany). The skin was pulled upwards by negative pressure for 5 s, followed by 3 s of relaxation. A skin deformation curve was obtained from three measurement cycles (Figure 4). Relative R-parameters, such as R1, Uf–Ua; R2, Ua/Uf; R5, Ur/Ue; R6, Uv/Ue; R7, Ur/Uf; and R9, R3–R0, could be derived from Ua, Ue, Uf = R0, Ur and Uv, which are absolute parameters [18]. Absolute parameters are less reliable in hypertrophic scars since these are dependent on the skin thickness. Relative parameters can be used to compare different anatomical sites because these are independent of the skin thickness [19]. Therefore, four parameters, R0, R2, R6 and R9, were selected to compare the biomechanical properties of the burn scars [19-21]. Final distensibility (R0 = Uf) is the length of skin displaced from the initial location by negative pressure. Gross elasticity (R2 = Ua/Uf) is the capacity that the skin exhibits to return to its initial location. Viscoelasticity (R6 = Uv/Ue) is the potency against an interstitial fluid shift, which is higher in firmer skin. Hysteresis (R9 = H) is the difference in the skin distension between the first and last suction, which indicates tiring effects [21]. Scar thickness was measured using an E-CUBE 7® ultrasound machine (Alpinion Medical Systems Co., Ltd, Anyang-si, Korea).
Figure 3.

A skin test was conducted on the burn scars of eligible patients before training and at 4 and 12 weeks after training. (a) Patient with the initial burn injury, (b) Mexameter® for measuring the levels of melanin and erythema, (c) Tewameter® for measuring trans-epidermal water loss and (d) Cutometer® for measuring scar distensibility and elasticity

Figure 4.

Skin deformation assessments. Four parameters, namely, final distensibility (R0 = Uf), gross elasticity (R2 = Ua/Uf), viscoelasticity (R6 = Uv/Ue) and hysteresis (R9 = H), were used to investigate the effect of robot-assisted gait training on burn scars

Primary outcome measures

The primary outcome measures to compare the biomechanical properties of the burn scars were R0, R2, R6 and R9 parameters, and scar thickness before RAG training and at 4 and 12 weeks after training. Skin deformation assessments. Four parameters, namely, final distensibility (R0 = Uf), gross elasticity (R2 = Ua/Uf), viscoelasticity (R6 = Uv/Ue) and hysteresis (R9 = H), were used to investigate the effect of robot-assisted gait training on burn scars

Secondary outcome measures

Secondary outcome measure was the presence or absence of skin complication around the burn scars during RAGT. Patient demographics Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile) for continuous variables or as numbers (%) for categorical variables. GAR gait assistance robot, TBSA total body surface area aFisher’s exact test bMann–Whitney U test cIndependent t-test Pre-training scar biomechanical properties and pre-training joint range of motion Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, AU arbitrary unit, TEWL trans-epidermal water loss, ROM range of motion aIndependent t-test bMann–Whitney U test

Statistical analyses

All statistical analyses were performed using SPSS version 21 (IBM Corp., Armonk, NY, USA), with p < 0.05 considered statistically significant. To estimate the sample size with sufficient statistical power, GPower (version 3.1.9.7, Franz Faul, Universität Kiel, Germany), which is a freely-available statistical software package, was used (effective size f of 0.25; alpha level of 0.05; statistical power of 80%) [22]. A total of 40 patients were included with a dropout rate of 10%. The intention-to-treat analysis was conducted at the same time to avoid the bias caused by the elimination of randomization. Numerical data are presented as mean ± standard deviation or median (interquartile range) and categorical data as a number (%). The Shapiro–Wilk test was used for the assumption of normality. To evaluate the pre-training homogeneity between the GAR and control groups, the independent t- and Mann–Whitney U tests for numeric data and Fisher’s exact test for categorical data were used. The effect of RAGT-induced mechanical load on the biomechanical properties of burn scars throughout the training regimen was analyzed using one-way repeated-measures analysis of variance and the Friedman test. The independent t- and Mann–Whitney U tests were used for intergroup comparisons of the change in the values of the scar biomechanical properties between pre-training and 4 and 12 weeks after training. Melanin, erythema and trans-epidermal water loss throughout the training regimen Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, AU arbitrary unit, TEWL trans-epidermal water loss aOne way repeated-measures analysis of variance bFriedman test Comparison of skin biomechanical properties throughout the training regimen Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot aOne way repeated-measures analysis of variance bFriedman test Comparison of change values in skin biomechanical properties between pre-training and 4 and 12 weeks after training Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, wks weeks aIndependent t-test bMann–Whitney U test

Results

A total of 40 patients with burns who satisfied the inclusion criteria were enrolled in the study, 39 of whom completed all assessments. All of the 40 patients were included in the statistical analysis following the intention-to-treat analytic strategy. There were no significant differences in the mean age, height, weight, burned area percent of total body surface area, duration since burn injury or type of burn between the GAR and control groups (p > 0.05 for all). Scar sites were not significantly different between the groups (p = 0.841) (Table 1). The pre-training biomechanical properties of the burn scars and pre-training ROM of joints were not significantly different between the groups (p > 0.05 for all) (Table 2). None of the patients experienced skin abrasion around the burn scar when the fastening belts were applied or musculoskeletal or cardiovascular adverse events, such as dizziness or changes in blood pressure, during training.
Table 1

Patient demographics

GAR group Control group P value
Male : female, n (%)17(85) : 3(15)16(80) : 4(20)1.000a
Age (years)54.1 ± 9.555.1 ± 12.30.550b
Height (cm)170.7 ± 5.5172.9 ± 5.00.196c
Weight (kg)68.1 ± 9.969.4 ± 7.20.645c
Percent of TBSA (%)29.1 ± 15.225.0 ± 17.00.343b
Duration since burn injury (days)76 (63.5, 109.0)70 (63.3, 114.0)0.634b
Types of burn, n (%)1.000a
 Flame burn12 (60)11 (55.0)
 Scalding burn5 (25)4 (20.0)
 Contact burn1 (5)2 (10.0)
 Electrical burn2 (10)3 (15.0)
Scar site for evaluation, n (%)0.841a
 Thigh4 (20)3 (15.0)
 Knee8 (40)10 (50.0)
 Leg8 (40)7 (35.0)

Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile) for continuous variables or as numbers (%) for categorical variables. GAR gait assistance robot, TBSA total body surface area

aFisher’s exact test

bMann–Whitney U test

cIndependent t-test

Table 2

Pre-training scar biomechanical properties and pre-training joint range of motion

GAR group (n = 20) Control group (n = 20) P value
Biomechanical property
 Melanin (AU)164.7 ± 42.6198.8 ± 77.00.093a
 Erythema (AU)472.6 ± 82.9455.5 ± 88.00.530a
 TEWL (g/h/m2)13.9 (12.1, 17.2)15.7 (10.1, 17.8)0.794b
 Final distensibility (R0 = Uf)0.58 (0.37, 1.54)0.78 (0.33, 1.20)0.963b
 Gross elasticity (R2 = Ua/Uf)0.64 (0.08, 0.74)0.61 (0.02, 0.73)0.449b
 Viscoelasticity (R6 = Uv/Ue)0.30 (0.02, 0.43)0.34 (0.01, 0.47)0.931b
 Hysteresis (R9 = H)0.063 (0.034, 0.130)0.065 (0.025, 0.125)0.815b
 Thickness (mm)1.89 ± 0.461.91 ± 0.510.922a
ROM of joint (degree)
 Hip flexion100 (98.5, 100.0)100 (100.0, 100.0)0.231b
 Hip extension14.8 ± 9.819.2 ± 8.50.141a
 Knee flexion109.9 ± 17.7116.6 ± 13.20.179a
 Knee extension−0.5 (−8.0, 0.0)0 (−0.5, 0.0)0.606b
 Ankle dorsiflexion19 (14.0, 20.0)20 (15.0, 20.0)0.470b
 Ankle plantarflexion40 (20.0, 40.0)36.5 (20.3, 40.0)0.696b

Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, AU arbitrary unit, TEWL trans-epidermal water loss, ROM range of motion

aIndependent t-test

bMann–Whitney U test

Table 3 shows the mean or median values of melanin, erythema and trans-epidermal water loss between the GAR and control groups before training and at 4 and 12 weeks after training. The levels of melanin, erythema and trans-epidermal water loss were not significantly different in both groups throughout the training regimen (p > 0.05 for all).
Table 3

Melanin, erythema and trans-epidermal water loss throughout the training regimen

Variable Pre-training At 4 weeks At 12 weeks P value
Melanin (AU)GAR (n = 19)163.9 ± 43.6174.8 ± 43.7192.4 ± 63.90.097a
Control (n = 20)198.8 ± 77.0185.9 ± 74.6191.9 ± 68.80.786a
Erythema (AU)GAR (n = 19)473.6 ± 85.0498.3 ± 80.1486.0 ± 77.50.570a
Control (n = 20)455.5 ± 88.0465.8 ± 87.1447.9 ± 89.20.567a
TEWL (g/h/m2)GAR (n = 19)13.9 (12.1, 17.2)15.9 (12.8, 18.8)13.6 (12.3, 16.7)0.766b
Control (n = 20)15.7 (10.1, 17.8)15.2 (12.8, 17.9)15.2 (12.2, 16.6)0.947b

Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, AU arbitrary unit, TEWL trans-epidermal water loss

aOne way repeated-measures analysis of variance

bFriedman test

Scar thickness significantly increased in the GAR and control groups during the 12 weeks of training (p = 0.037 and p = 0.019, respectively). Final distensibility (R0) was not significantly different in the GAR group during training (p = 0.455) and significantly decreased in the control group during training (p = 0.011). There were no significant differences in the gross elasticity (R2) and viscoelasticity (R6) in both groups throughout the training regimen (p = 0.873 and p = 0.633, and p = 0.559 and p = 0.539, respectively). Hysteresis (R9) was significantly reduced in the GAR group during the training (p = 0.038) and was not significantly different in the control group (p = 0.804) (Table 4).
Table 4

Comparison of skin biomechanical properties throughout the training regimen

Variable Pre-training At 4 weeks At 12 weeks P value
Thickness (mm)GAR (n = 19)1.86 ± 0.462.02 ± 0.502.11 ± 0.580.037a
Control (n = 20)1.91 ± 0.512.02 ± 0.502.23 ± 0.630.019a
Final distensibility (R0 = Uf)GAR (n = 19)0.54 (0.36, 1.74)0.65 (0.40, 0.97)0.68 (0.39, 0.86)0.455b
Control (n = 20)0.78 (0.33, 1.18)0.65 (0.31, 1.11)0.37 (0.23, 0.74)0.011b
Gross elasticity (R2 = Ua/Uf)GAR (n = 19)0.67 (0.03, 0.74)0.74 (0.06, 0.80)0.75 (0.11, 1.87)0.873b
Control (n = 20)0.61 (0.02, 0.73)0.58 (0.09, 0.82)0.52 (0.08, 0.80)0.633b
Viscoelasticity (R6 = Uv/Ue)GAR (n = 19)0.29 (0.01, 0.43)0.31 (0.03, 0.49)0.37 (0.02, 0.46)0.559b
Control (n = 20)0.34 (0.01, 0.47)0.10 (0.03, 0.39)0.21 (0.03, 0.38)0.539b
Hysteresis (R9 = H)GAR (n = 19)0.059 (0.033, 0.133)0.059 (0.032, 0.122)0.048 (0.022, 0.109)0.038b
Control (n = 20)0.065 (0.025, 0.125)0.097 (0.031, 0.110)0.101 (0.046, 0.13100.804b

Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot

aOne way repeated-measures analysis of variance

bFriedman test

The GAR and control groups showed significant difference in the change in the values of hysteresis (R9) between pre-training and 12 weeks after training (p = 0.441 and p = 0.049, respectively). Changes in values for scar thickness, distensibility (R0), gross elasticity (R2) and viscoelasticity (R6) were not significantly different between pre-training and 4 and 12 weeks after training (p > 0.05 for all) (Table 5).
Table 5

Comparison of change values in skin biomechanical properties between pre-training and 4 and 12 weeks after training

GAR group Control group P value
Thickness (mm)Pre ~4 wks0.15 ± 0.300.12 ± 0.170.700a
Pre ~12 wks0.12 ± 0.760.32 ± 0.550.337a
Final distensibilityPre ~4 wks−0.00 (−0.09, 0.00)−0.04 (−0.37, 0.15)0.297b
(R0 = Uf)Pre ~12 wks−0.13 (−0.67, 0.33)−0.28 (−0.41, −0.01)0.351b
Gross elasticityPre ~4 wks0.00 (−0.01, 0.12)0.03 (−0.01, 0.24)0.820b
(R2 = Ua/Uf)Pre ~12 wks0.00 (−0.13, 0.23)0.01 (−0.28, 0.14)0.989b
ViscoelasticityPre ~4 wks0.00 (−0.11, 0.07)−0.01 (−0.31, 0.02)0.653b
(R6 = Uv/Ue)Pre ~12 wks0.00 (−0.12, 0.08)−0.01 (−0.33, 0.15)0.569b
HysteresisPre ~4 wks0.003 (−0.019, 0.029)−0.003 (−0.035, 0.032)0.441b
(R9 = H)Pre ~12 wks−0.005 (−0.040, 0.005)0.010 (−0.005, 0.043)0.049b

Data are presented as mean ± standard deviation or median (25% percentile, 75% percentile). GAR gait assistance robot, wks weeks

aIndependent t-test

bMann–Whitney U test

Discussion

To the best of our knowledge, this is the first study to demonstrate the effects of RAGT-induced mechanical load on burn scars of the lower extremity. In our pilot study, three patients experienced skin abrasion on the burn scars when the fasten belt was applied at <2 months after injury. Therefore, we conducted RAGT at >2 months post-burn after the scars had become stable, and no patients experienced skin abrasion. Interestingly, RAGT-induced mechanical load significantly decreased the hysteresis of burn scars. Low hysteresis means less dissipation of energy during repetitive skin distension and relaxation [23] and indicates improvement in the tiring effect of skin [20]. Hypertrophic scars generally grow quickly from 3 to 6 months and can regress slightly after this period [24]. Since most of the burns in patients in this study were in the proliferative phase, both the GAR and control groups exhibited hypertrophic changes, with collagen and proteoglycan overproduction in the scars, and demonstrated a similar significant increase in scar thickness during training. Furthermore, no significant difference in scar thickness change was noted between the two groups. Aarabi et al reported that artificial mechanical loading in the early proliferative phase of wound healing induced hypertrophic scars by inhibiting apoptosis [12]. They applied mechanical stress earlier than in the GAR group and perpendicular to the craniocaudal axis. However, RAGT was conducted at >2 months after the burn injury and RAGT-induced mechanical load was applied parallel to the craniocaudal axis. These differences in the applied time and direction of mechanical stress could account for the inconsistencies with the findings of the previous study. Therefore, similar hypertrophic scar formation in the GAR and control groups is likely owing to chronic inflammation, cytokines, growth factors and macrophages associated with pathologic scar formation. Collagen is the main component of the dermis (70–80% of the dry skin weight) that affects skin elasticity, and a proteoglycan-rich matrix is needed to maintain skin viscosity [25]. The overall viscoelasticity of the skin depends mainly on the connective tissue structure of the dermis and subcutaneous tissue, with minimal contribution from the epidermis [26]. The orientation, density, alignment and interconnections of collagen bundles also influence skin elasticity [27]. Stromal collagen is typically composed of type I and type III collagen. Type I collagen fibres are thick and show minimal distensible activity when mechanical load is applied. Type III collagen bundles are thin and pliable and are enriched in the dermis, vasculature, internal organs and fine reticular fibres [28]. Hypertrophic scars demonstrated a low type I/III collagen ratio because they increased the expression of type III collagen and decreased the expression of type I collagen [29]. However, the predominant type III collagen bundles in hypertrophic scars are oriented parallel to the epithelial surface [30], compared to those in the normal dermis in which collagen bundles have a basket-weave pattern that permits tissue strength and flexibility [31]. Therefore, the parallel arrangement of the collagen bundles can make the scar less flexible and malleable [28] and decrease the distensibility in the scars, resulting from abnormal collagen patterns [30]. The skin distensibility of the burn scar significantly decreased in the control group during conventional training and this finding is consistent with those in previous studies [28,30]. However, the GAR group showed no significant change in skin distensibility during RAGT. Repetitive stretching of the human muscle–tendon units reduced peak passive tension and stiffness, and increased the utilization of elastic strain energy [32]. Therefore, improvement of the skin distensibility in the GAR group could be attributed to periodic and repetitive stretching exercises by the RAGT. A force results in a certain change. Hysteresis refers to persistence of a condition or state even after the force is removed [33]. Hysteresis is represented in Figure S1 (see online supplementary material) by the area surrounded by the two curves that indicate the loading and unloading stages. When energy absorption and consumption are repeated during loading and unloading, more energy is absorbed at loading stress than at relaxation [34]. Hysteresis is also defined as the difference in energy changes in the tissue during loading and unloading in a stress–strain relationship [23], in which strain represents the ratio of altered to original tissue length [34]. The GAR group showed a decrease of hysteresis in hypertrophic burn scars after RAGT. Repetitive stretching significantly decreased hysteresis and stiffness of tendon structure [32]. Therefore, the reduced hysteresis in the hypertrophic scar of the GAR group could be attributed to periodic and repetitive stretching by RAGT. Elastin is present in the dermis in small amounts (<1% of the dry skin weight) [35] and is involved in the initial elastic deformation of the stress–strain curve, as shown in Figure S1 [34]. Elastin, in particular, enables the collagen network to return to its original shape after stress removal [35]. Initial change of loading is mostly influenced by elastin fibres and after the initial stage, collagen fibres dominate deformation [36]. Elastin turnover is rare in healthy adult tissues because its half-life is ~70 years [37]. After stretching the scar tissue with a skin-stretching device, the alignment of the collagen bundle was more parallel than that of the nonstretched scars; however, the thickness and space of the collagen bundle were not significantly different between the stretched and nonstretched scars [38]. Additionally, the stretched scars showed no significant difference in the quantity of elastic fibres compared with the nonstretched scars [38]. Therefore, the change in the scar biomechanical properties after RAGT could probably be explained by the realignment of the collagen bundle and interconnection of the connective tissue rather than any change in the elastin fibre. The small sample size in this study may be a limitation on generalizing the results. Future in vitro and in vivo studies are warranted to demonstrate the mechanism of the effect of RAGT on the scar biomechanical properties and the distribution of collagen and elastin in scars after RAGT. RAGT could reduce personnel costs involved in manual assistance training [39]. Although the cost of rehabilitative therapy may not be uniform in each country, owing to the difference in the medical insurance systems, there is no difference in the cost between conventional training by a physical therapist and RAGT in South Korea. Since RAGT can reduce the time and labour required of a therapist for one patient, the cost and labour efficiencies are high [40,41]. Compared to the conventional training group, there was a better improvement in the isometric strength of the ankle and ROM of the knee and ankle in patients with burns after RAGT [2]. This study has the potential to clarify that RAGT does not negatively affect burn scars. Furthermore, it is expected to contribute to the active use of GAR in rehabilitation therapy for patients with burn injuries on the lower extremity.

Conclusions

In this study, RAGT significantly reduced hysteresis in hypertrophic burn scars and did not cause a significant decrease in skin distensibility, unlike in the control group. Furthermore, no skin complications were detected around the burn scars where the fastening belts were applied during RAGT.

Abbreviations

GAR: Gait assistance robot; RAGT: Robot-assisted gait training; ROM: Range of motion. Click here for additional data file.
  37 in total

Review 1.  Burn rehabilitation: an overview.

Authors:  Peter C Esselman
Journal:  Arch Phys Med Rehabil       Date:  2007-12       Impact factor: 3.966

2.  Adaptation of the dermal collagen structure of human skin and scar tissue in response to stretch: an experimental study.

Authors:  Pauline D Verhaegen; Hennie J Schouten; Wikky Tigchelaar-Gutter; Jan van Marle; Cornelis J van Noorden; Esther Middelkoop; Paul P van Zuijlen
Journal:  Wound Repair Regen       Date:  2012-08-10       Impact factor: 3.617

3.  Mechanical properties of skin in Ehlers-Danlos syndrome, types I, II, and III.

Authors:  F Henry; V Goffin; C Piérard-Franchimont; G E Piérard
Journal:  Pediatr Dermatol       Date:  1996 Nov-Dec       Impact factor: 1.588

4.  Burn Patient Acuity Demographics, Scar Contractures, and Rehabilitation Treatment Time Related to Patient Outcomes: The ACT Study.

Authors:  Reg Richard; Alexis R Santos-Lozada
Journal:  J Burn Care Res       Date:  2017 Jul/Aug       Impact factor: 1.845

5.  Quantitative measurement of hypertrophic scar: intrarater reliability, sensitivity, and specificity.

Authors:  Bernadette Nedelec; José A Correa; Grazyna Rachelska; Alexis Armour; Léo LaSalle
Journal:  J Burn Care Res       Date:  2008 May-Jun       Impact factor: 1.845

6.  Robot-assisted gait training versus treadmill training in patients with Parkinson's disease: a kinematic evaluation with gait profile score.

Authors:  M Galli; V Cimolin; M F De Pandis; D Le Pera; I Sova; G Albertini; F Stocchi; M Franceschini
Journal:  Funct Neurol       Date:  2016 Jul-Sep

7.  Longitudinal burn scar quantification.

Authors:  Bernadette Nedelec; José A Correa; Ana de Oliveira; Leo LaSalle; Isabelle Perrault
Journal:  Burns       Date:  2014-04-02       Impact factor: 2.744

8.  Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis.

Authors:  Shahram Aarabi; Kirit A Bhatt; Yubin Shi; Josemaria Paterno; Edward I Chang; Shang A Loh; Jeffrey W Holmes; Michael T Longaker; Herman Yee; Geoffrey C Gurtner
Journal:  FASEB J       Date:  2007-05-15       Impact factor: 5.191

9.  Improvement of walking ability during postoperative rehabilitation with the hybrid assistive limb after total knee arthroplasty: A randomized controlled study.

Authors:  Yohei Tanaka; Hiroyuki Oka; Shuichi Nakayama; Takaaki Ueno; Ko Matsudaira; Toshiki Miura; Kiyokazu Tanaka; Sakae Tanaka
Journal:  SAGE Open Med       Date:  2017-06-08

Review 10.  The molecular basis of hypertrophic scars.

Authors:  Zhensen Zhu; Jie Ding; Edward E Tredget
Journal:  Burns Trauma       Date:  2016-01-21
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