Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

Ye Ma; Yali Liang; Xiaodong Kang; Ming Shao; Lilja Siemelink; Yanxin Zhang

doi:10.1155/2019/8049156

Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

Ma, Ye;Liang, Yali;Kang, Xiaodong;Shao, Ming;Siemelink, Lilja;Zhang, Yanxin 2019-08-19 00:00:00 Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 8049156, 9 pages https://doi.org/10.1155/2019/8049156 Research Article Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment 1 2 2 2 3 4 Ye Ma , Yali Liang, Xiaodong Kang, Ming Shao, Lilja Siemelink, and Yanxin Zhang The Research Academy of Grand Health, Faculty of Sport Science, Ningbo University, Ningbo, China Bayi Rehabilitation Center, Chengdu, Sichuan, China Motekforce Link, Netherlands Department of Exercise Sciences, The University of Auckland, New Zealand Correspondence should be addressed to Ye Ma; maye@nbu.edu.cn Received 21 December 2018; Revised 23 May 2019; Accepted 3 June 2019; Published 19 August 2019 Academic Editor: Jan Harm Koolstra Copyright © 2019 Ye Ma et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. To investigate gait characteristics in children with spastic cerebral palsy during inclined treadmill walking under a virtual reality environment. Methods. Ten spastic cerebral palsy (CP) children and ten typically developing (TD) children were asked to walk at their comfortable speed on a treadmill at a ground level and 10 inclined. Three-dimensional kinematic data and ground reaction force data were captured in a computer-assisted rehabilitation environment system. Kinetic parameters and dynamic balance parameters were calculated using a standard biomechanical approach. Results. During uphill walking, both groups decreased walking speed and stride length and increased peak pelvis tilt, ankle dorsiﬂexion, and hip ﬂexion. Compared with TD children, CP children had decreased walking speed and stride length, decreased peak hip abduction moment, increased stance phase percentage, increased peak ankle dorsiﬂexion and knee ﬂexion, and increased peak hip extension moment. The peak trunk rotation angle, ankle angle at initial contact, and stride length showed a signiﬁcant group ∗ walking condition interaction eﬀect. Conclusions. CP children showed similar adjustments for most gait parameters during uphill walking as TD children. With a lower walking speed, CP children could maintain similar dynamic balance as TD children. Uphill walking magniﬁes the existing abnormal gait patterns of the cerebral palsy children. We suggest that during a treadmill training with an inclination, the walking speed should be carefully controlled in the case of improving peak joint loading too much. feasible method for CP children and can improve walking 1. Introduction speed and general gross motor skills. Willerslev-Olsen et al. Cerebral palsy (CP) is a neurological disorder that results [9] investigated the eﬀect of inclined treadmill training on CP from defects or damages of the immature brain [1, 2]. Prob- children. Their study suggests that inclined intensive gait lems caused by CP, such as muscle tightness, weakness, or training increases beta and gamma oscillatory drive to ankle spasticity, could impede musculoskeletal development and dorsiﬂexor motor neurons and therefore improves toe lift thus result in abnormal gait patterns [3]. and heel strike in CP children. Improving walking ability is one of the major concerns The biomechanical studies including kinematics, kinet- in therapeutic interventions for children with CP. Tread- ics, and dynamic balance analysis are helpful for gaining mill walking has been widely used in the rehabilitation insight into the neural control strategies, understanding the abnormal gait patterns thoroughly, and designing eﬀec- of CP children to provide repetitive training of the whole gait cycle [4–7]. A systematic literature review evaluated tive therapeutic interventions for CP patients. Kinematics is the eﬀectiveness of treadmill training for CP children [8]. used to quantify the abnormalities of gait patterns [10–12]. The review suggested that treadmill training is a safe and Kinetics provides an indication of the causes of the gait 2 Applied Bionics and Biomechanics Table 1: Characteristics of participants. Age Height Weight Patient Gender Aﬀected side GFMCS level Gait type (year) (cm) (kg) S1 7 Male 125 30 L, R II Mild crouch S2 7 Female 114 20 L, R I Mild crouch S3 6 Female 131 27 L, R I Crouch S4 8 Female 125 22.5 L, R I Mild crouch S5 6 Male 117 21 L, R I Mild crouch S6 7 Male 122 22.5 L, R II Mild crouch S7 11 Male 145 37 L, R II Apparent equines S8 10 Male 140 36 L, R II Apparent equines S9 12 Female 146 32 L, R I Crouch S10 11 Male 127 30 L, R II Apparent equines Abbreviations: GMFCS = Gross Motor Function Classiﬁcation System; L = left; R = right. abnormalities and the underlying muscle function pathology and ten TD children (age: 7 9±1 4 years old; height: [10]. Healthy people can adapt to uphill walking by increas- 132 5 ± 11 cm; weight: 26 8±6 3kg) were included. The ing hip, knee, and ankle dorsiﬂexion and thus maintaining characteristics of the CP participants are presented in an upright posture [13]. This adaptation can be used as a Table 1. There are no signiﬁcant diﬀerences in age targeted training of a group of muscles (ankle dorsiﬂexor, (p =0 478), height (p =0 494), or weight (p =0 255) between knee extensor, and hip extensor). However, CP children the two groups. might have diﬃculties in adjusting to inclined walking due The inclusion criteria for CP children are as follows: (1) to impaired postural control or dynamic balance. diagnosed with diplegic CP, (2) 6-12 years old, (3) ranked Biomechanical studies are limited for inclined treadmill I-II in the Gross Motor Function Classiﬁcation System gait training on CP children. Several studies investigated (GFMCS), (4) capable of understanding and executing the biomechanical characteristics and gait adaptation strate- instructions, (5) independent walkers without assistance for gies of CP children for walking on an inclined ramp or tread- more than six minutes, and (6) with no botulinum toxin in mill [13–16]. These studies report that CP children adapt the lower extremities or surgery during the preceding six to inclined walking with similar gait adjustment strategies months. The exclusion criteria for both CP and TD children as the typically developing (TD) children but use greater are the absence of (1) severe heart and lung diseases and (2) postural adaptations. visual or auditory system disorders. The ethical approval To the best of our knowledge, there is a lack of thorough was obtained from the Sichuan Bayi Rehabilitation Center’s understanding of abnormal gait patterns for children with ethics committee (Sichuan, China). Children’s parents signed spastic CP during inclined treadmill walking using three- the consent forms for participation. dimensional (3D) gait analysis including kinematics, kinetics, and dynamic balance analysis. Only kinematic data is 2.2. Instrumentation. Three-dimensional (3D) joint kinemat- reported in most of the aforementioned studies [14, 15]. ics and ground reaction force (GRF) were collected using a The use of two-dimensional (2D) motion cameras [15] also computer-assisted rehabilitation environment (CAREN) sys- loses considerable measurement accuracy for this data. tem. The CAREN system is an immersive virtual environ- This study is aimed at comprehensively investigating ment system consisting of a 3D motion capture system with gait adjustment strategies of CP children in level treadmill twelve high-speed infrared cameras (Vicon, Oxford Metrics, and uphill treadmill walking under a virtual reality envi- UK), a split-belt force plate instrumented treadmill ronment (a default setting for a computer-assisted rehabil- (ADAL3DM-F-COP-Mz, Tecmachine, France) atop a six itation environment (CAREN) system; Motekforce Link, the degree-of-freedom motion base platform, and a cylindrical Netherlands). The study quantiﬁed spatial-temporal parame- projection system. A safety harness and side rails are placed ters, 3D kinematics, 3D kinetics, and dynamic balance of the to ensure the safety and comfort of the user (see Figure 1). CP children by using the state-of-the-art motion capture tech- The Vicon motion capture system recorded kinematic data niques. We hypothesized that (1) CP children used similar gait at a sampling frequency of 100 Hz. The force plate data were adjustment strategies as their TD peers during inclined walk- recorded with a sampling frequency of 1000 Hz. The visual ing and (2) the CP group would have signiﬁcantly lower scene is usually synchronized with the movement of the postural stability due to impaired postural control. platform or the motion of the patient. The CAREN system is employed in this study due to the following concerns: (1) the CAREN system can perform 3D 2. Methods movement for a full body in real time, which provides imme- 2.1. Study Design and Subjects. Ten spastic CP children (age: diate feedback to both the therapist and patient [17]; (2) the 8 5±2 3 years old; height: 131 ± 13 cm; weight: 28 ± 6 9kg) CAREN system can conduct inclined walking experiment Applied Bionics and Biomechanics 3 (a virtual walkway) projected on a cylindrical screen. The data were recorded for one minute during level treadmill walking. Subsequently, the platform was tilted at ten degrees uphill. Uphill walking data were recorded for one minute as well. 2.4. Data Processing. The study used a commercial software system, named the human body model (HBM) [26], embedded in the D-ﬂow of the CAREN system [25], to calculate kinematics and kinetics. For the kinematic data and the GRF, the cutoﬀ frequency of the low-pass ﬁlter was set to 6 Hz. Figure 1: The CAREN system used for this study. The HBM solves the inverse kinematics problem using a nonlinear least squares problem (1). The inverse dynamic and collect kinematic and kinetic information simulta- solution is to ﬁnd an optimal pose Q that best ﬁts the maker neously; (3) the virtual environment is reproducible and as data. In equation (1), r Q is the 3D position of a marker i close to a natural environment as possible [18, 19]; (4) the and r is the marker coordinates measured by the i,meas CAREN system is proved to be an eﬀective tool for rehabili- motion capture system. tation (such as gait training [17, 20], prosthetic adjustment [21], balance training [22, 23], and cognitive rehabilitation [24]) and biomechanics research [25–27]. Q = arg min 〠 r Q − r 1 Q i i,meas i=1 2.3. Experimental Protocol. The motor functioning informa- tion (described by the GMFCS ranking) for CP and the The HBM solves the inverse dynamic problem using the classiﬁcation of CP subtypes were obtained from each CP typical multibody equation of motion (2). child’s medical record. The participants were fully instructed before the measurements. Each participant started with a τ =MQ Q +cQ, Q + G + E, 2 familiarization of three minutes on the treadmill at zero and a ten-degree inclined slope (uphill), respectively. The familiarization ﬁnished until the participant adapted to the where τ is the unknown joint moments and forces, M Q is walking conditions with a comfortable walking speed for the human body mass matrix, c is the centrifugal and Coriolis each condition. loading, G is the gravity, and E represents the external force. After changing clothes and shoes, 25 retroreﬂective The center of pressure (COP) position was measured by markers were placed on the participant’s anatomical land- the instrumented treadmill. The center of mass (COM) posi- marks following the deﬁnition of the whole body human body tion was calculated based on measured kinematic data using th model (HBM) [26]. The markers are placed on the 10 tho- a standard procedure as described by Winter, which deter- racic vertebra, navel, sternum, anterior superior iliac spine, mined the whole body COM based on the COM from indi- posterior superior iliac spine, greater trochanter, lateral epi- vidual body segment [28]. COP-COM separation in both condyle of knee, lateral malleolus, posterior calcanei, the tip the anterior-posterior (AP) and medial-lateral (ML) direc- of big toe, lateral ﬁfth metatarsal heads, acromion, lateral epi- tions, the distance between COM and COP in the AP and condyle and medial epicondyle of the elbow, lateral wrist, ML directions, was calculated to represent the dynamic th medial wrist, xiphoid process, the 7 cervical vertebra, top balance during gait [29]. To cater both the left footed of the head, right side of the head, and left side of the head. and right footed trials, the COP-COM separation in the Local segment coordinate systems were set up for the ML direction is made positive for all trails. These positive torso, pelvis, thigh, shank, and foot segments based on values reﬂect the distance of the feet which were being recorded markers’ positions, which are listed in Table 2 placed on either side of the COM in the ML direction. (see more details from [26]). The average COP-COM separation in the AP and ML For each sampling time frame, the coordinates of each directions is normalized to each participant’s leg length segment with respect to its proximal segment were trans- to allow for a comparison between subjects. Assuming that formed by a sequence of three rotations delineated by three both legs have equal lengths, leg length was calculated as Euler angles following the ﬂexion/extension, adduction/ab- the distance between the left hip joint center and left ankle duction, and internal/external order. joint center during the static trial. For safety considerations, the participants wore a har- ness which was fastened to a metal frame using a safety 2.5. Statistical Analysis. Spatial-temporal, kinematic, kinetic line throughout the experiment. Every participant was data, and dynamic balance parameters were analyzed. Low asked to perform a static trial to locate the positions of reliability and large errors have been reported for the hip the anatomical landmarks and the locations of the joint and knee transverse plane angles and knee frontal plane centers. Then, each participant walked at their comfortable angles recorded by 3D motion capture systems [30]. These speed without handrail support in the virtual environment parameters were not included in this study. 4 Applied Bionics and Biomechanics Table 2: Segment coordination systems. Segment Deﬁnition of the segment coordination system Origin Midpoint between hip joint centers X Unit vector of cross product between the Z-axis and the vector from right hip joint center to left hip joint center Pelvis Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector parallel to the line from S1/L5 to the midpoint between left and right shoulder joint centers Origin Thoracolumbar joint center Unit vector perpendicular to the plane formed by the Z-axis and the vector from right shoulder joint center to left shoulder joint center Torso Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector parallel to the line from S1/L5 to the midpoint between left and right shoulder joint centers Origin Hip joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Thigh Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from knee joint center to hip joint center Origin Knee joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Shank Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from ankle joint center to knee joint center Origin Subtalar joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Foot Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from toe joint center to subtalar joint center Eight gait cycles from each participant under each walk- compared to level treadmill walking (p <0 01, η =0 557), ing condition were selected for the analysis. The Shapiro– with a signiﬁcant group ∗ walking condition interaction Wilk test was performed to test the normality of the data. eﬀect (p <0 01, η =0 298). A two-way mixed-design analysis of variance (ANOVA) (group ∗ walking condition) was used to analyze the spa- 3.2. Joint Kinematics and Dynamic Balance. As shown in tial-temporal, kinematic, and dynamic balance parameters Table 3, CP and TD children increase peak pelvic anterior using SPSS 22.0. For kinetic parameters (joint moments), a 2 tilt when walking uphill (p <0 01, η =0 842). CP and TD two-way ANCOVA (group ∗ walking condition) with speed children have less peak pelvic posterior tilt (p <0 01, η = as a covariate was used. A statistically signiﬁcant diﬀerence 0 843), peak pelvis oblique (p <0 01, η =0 423), and less was accepted as p <0 05. The eta squared (η ) is used as peak trunk extension (p =0 026, η =0 245) when walking the measure of the eﬀect size. The η of 0.01, 0.06, and uphill (p <0 01, η =0 843). Kinematic data shows signiﬁ- 0.14 means the small eﬀect, moderate eﬀect, and large eﬀect, cant diﬀerences for peak hip abduction during the swing respectively [31]. phase (p =0 026, η =0 309), peak hip ﬂexion (p <0 01, η =0 752) during the swing phase, and decreased peak hip extension during the stance phase (p <0 01, η = 3. Results 0 478) during uphill walking in both groups. Compared 3.1. Spatial Temporal Parameters. As shown in Table 3, a to level treadmill walking, uphill walking has a signiﬁ- signiﬁcant diﬀerence is identiﬁed in walking speed between cantly smaller distance between COM and COP in the 2 2 CP and TD children (p <0 01, η =0 749). Both groups anterior-posterior (AP) direction (p <0 01, η =0 190). decreased walking speed during uphill walking (p <0 01, CP children walk with a lower peak knee ﬂexion angle 2 2 η =0 737). The interaction eﬀect of the walking speed during the swing phase than TD children (p <0 01, η = (group ∗ walking condition) does not reach a statistical signif- 0 439). Both groups ﬂex the knee more when walking uphill icance. The stride lengths of the CP children are shorter than (p <0 01, η =0 539). There is a signiﬁcant group ∗ walking 2 2 those of the TD children (p <0 01, η =0 516). Both groups condition interaction eﬀect (p <0 01, η =0 238). At initial decreased stride length signiﬁcantly during uphill walking contact, CP has more knee ﬂexion than TD (p <0 01, η = (p <0 01, η =0 581). There is a signiﬁcant diﬀerence in the 0 614). Both groups increase peak knee ﬂexion during interaction eﬀect (p <0 01, η =0 388) of the stride length. the load responding phase when walking uphill (p <0 01, The CP children show a signiﬁcantly longer stance phase η =0 825). compared to the TD children (p <0 01, η =0 523). Both There is no signiﬁcant group ∗ walking condition interac- groups increase stance percentage during uphill walking tion eﬀect in peak ankle dorsiﬂexion. Both groups increased Applied Bionics and Biomechanics 5 Table 3: Descriptive statistics for key gait variables of CP and TD children under two walking conditions (level and uphill treadmill walking) and results of two-way ANOVA for diﬀerences in the group (CP or TD children), walking condition, and group ∗ walking condition interaction. Level Uphill (+10 degree) p value of ANOVA Parameters CP TD CP TD Walking Group Interaction Mean SD Mean SD Mean SD Mean SD condition Speed (m/s) 0.42 0.16 0.64 0.06 0.32 0.14 0.58 0.07 <0.01 <0.01 0.494 Stride length (m) 0.52 0.19 0.68 0.12 0.39 0.16 0.65 0.14 0.003 <0.01 0.001 Step width (m) 0.09 0.02 0.12 0.04 0.09 0.03 0.11 0.04 0.05 0.135 0.199 Stance phase (%) 71.12 4.23 66.2 0.92 73.95 3.5 67.49 1.07 <0.01 <0.01 0.063 Peak trunk ﬂexion ( ) 8.12 4.07 6.01 1.85 7.21 4.32 4.56 3.1 0.069 0.228 0.779 Peak trunk extension ( ) -2.7 2.75 -0.16 1.38 1.06 4.48 0.62 3.85 0.375 0.026 0.132 Peak trunk rotation ( ) 4.84 8.90 4.96 6.67 2.86 8.53 9.21 5.23 0.493 0.224 0.017 Peak trunk lateral ﬂexion ( ) -2.30 6.92 6.36 2.50 8.28 6.01 4.50 3.66 0.226 0.241 0.47 Peak pelvic anterior tilt ( ) 12.46 5.2 12.93 4.35 26.07 6.94 26.3 7.38 0.88 <0.01 0.865 Peak pelvic posterior tilt ( ) 7.34 4.49 8.9 4.48 21.01 7.13 21.9 7.7 0.593 <0.01 0.682 Peak pelvic oblique ( ) -2.88 7.28 -2.53 3.29 -5.86 7.55 -5.47 4.30 0.95 <0.01 0.941 Peak hip ﬂexion ( ) 39.81 9.32 38.91 7.33 49.65 11.4 52.5 10.26 0.786 <0.01 0.292 Peak hip extension ( ) 6.62 7.62 3.36 6.61 11.28 7.26 7.16 8.36 0.182 <0.01 0.684 Peak hip abduction ( ) 9.98 10.18 9.85 3.77 8.47 9.36 6.33 2.96 0.816 0.026 0.28 Peak hip adduction ( ) 2.74 16.79 4.62 4.99 1.30 11.20 5.18 5.03 0.581 0.761 0.459 Peak knee ﬂexion during LR ( ) 27.15 6.43 20.54 9.95 44.63 6.7 34.66 10.09 <0.01 <0.01 0.333 Peak knee ﬂexion ( ) 60.74 8.11 65.63 11.18 60.58 7.72 67.06 5.44 0.044 0.546 0.454 Peak knee extension ( ) 12.75 6.9 4.23 4.8 14.61 7.24 10.49 6.57 <0.01 <0.01 0.063 Mean SD Mean SD Mean SD Mean SD Peak ankle dorsiﬂexion ( ) 17.55 6.53 11.86 3.59 24.18 5.81 18.64 4.3 <0.01 <0.01 0.932 Peak ankle plantarﬂexion ( ) -5.58 7.62 -14.27 6.14 2.73 7.36 -9.57 6.64 <0.01 <0.01 0.174 Knee ﬂexion at IC ( ) 23.49 7.86 6.93 6.01 43.88 6.21 26.74 13.21 <0.01 <0.01 0.878 Ankle sagittal angle at IC ( ) -1.14 8.18 -5.43 4.6 11.31 7.05 1.46 5.82 <0.01 <0.01 0.004 Peak hip extension moment (N m/kg) 0.54 0.18 0.36 0.09 0.79 0.19 0.55 0.15 <0.01 <0.01 0.395 Peak hip ﬂexion moment (N m/kg) -0.17 0.07 -0.16 0.07 -0.10 0.05 -0.08 0.04 0.398 <0.01 0.852 Peak hip abduction moment (N m/kg) 0.44 0.21 0.62 0.12 0.39 0.14 0.54 0.09 0.018 0.113 0.596 Peak knee abduction moment (N m/kg) 0.11 0.05 0.10 0.05 0.12 0.06 0.15 0.08 0.898 0.066 0.179 Peak knee adduction moment (N m/kg) 0.11 0.11 0.12 0.11 0.11 0.13 0.12 0.11 0.737 0.78 0.962 First peak knee extension moment (N m/kg) 0.14 0.16 0.15 0.08 0.09 0.12 0.23 0.15 0.032 0.657 0.057 Peak knee ﬂexion moment (N m/kg) -0.24 0.14 -0.22 0.19 -0.24 0.15 -0.25 0.11 0.908 0.423 0.584 First knee peak ﬂexion moment (N m/kg) -0.23 0.15 -0.19 0.11 -0.23 0.16 -0.24 0.13 0.82 0.368 0.392 Peak ankle plantarﬂexion moment (N m/kg) 0.76 0.26 0.99 0.19 0.74 0.16 0.91 0.21 <0.01 0.255 0.545 Peak ankle dorsiﬂexion moment (N m/kg) -0.05 0.06 -0.09 0.05 -0.02 0.01 -0.06 0.03 <0.01 0.01 0.996 COM-COP anterior distance (m) 0.12 0.05 0.14 0.05 0.03 0.04 0.06 0.05 0.077 <0.01 0.838 COM-COP posterior distance (m) 0.09 0.08 0.22 0.19 0.14 0.14 0.27 0.13 0.088 0.092 0.764 COM-COP medial distance (m) 0.15 0.04 0.15 0.02 0.16 0.04 0.14 0.02 0.696 0.628 0.555 COM-COP lateral distance (m) -0.09 0.04 -0.04 0.04 -0.08 0.07 -0.03 0.03 0.07 0.32 0.624 Abbreviations: LR = load responding; IC = initial contact; CP = cerebral palsy; TD = typically developing. peak ankle dorsiﬂexion during the stance phase when than TD at the initial contact. Signiﬁcant diﬀerences of walking uphill (p <0 01, η =0 721). CP children show the ankle dorsiﬂexion at the initial contact are identiﬁed in decreased peak plantarﬂexion compared to TD children the main eﬀect for the group (p <0 01, η =0 362), walking 2 2 during the swing phase (p <0 01, η =0 656). Both CP condition (p <0 01, η =0 863), and the interaction eﬀect and TD decrease their peak plantar ﬂexion during the (group ∗ walking condition)(p <0 01, η =0 357). The peak stance phase and swing phase when walking uphill trunk rotation angle shows a signiﬁcant group ∗ walking 2 2 condition interaction eﬀect (p =0 017, η =0 470). (p <0 01, η =0 598). CP has higher ankle dorsiﬂexion 6 Applied Bionics and Biomechanics Hip angle Knee angle Ankle angle 80 30 −10 0 0 −20 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 Gait cycle (%) Gait cycle (%) Gait cycle (%) Hip moment Knee moment Ankle moment 0.8 0.4 0.6 0.2 0.5 0.4 0.2 −0.2 −0.2 −0.4 −0.5 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 Gait cycle (%) Gait cycle (%) Gait cycle (%) Figure 2: Mean joint angles and joint moments for CP and TD during level ground walking and uphill walking (solid black line: TD level walking; dashed black line: TD uphill walking; solid red line: CP level walking; dashed red line: CP uphill walking). 3.3. Joint Kinetics. As shown in Table 3, both CP and TD process of balance [32] and there is no signiﬁcantly diﬀerent children decrease hip peak ﬂexion moment during the stance COP displacement between the subjects who participate in phase when walking uphill (p <0 01, η =0 817). CP children the virtual environment and those who do not [33]. Walking characters including temporal-spatial parameters and kine- have greater peak hip extension moment than TD children matics in treadmill walking using CAREN system and over (p <0 01, η =0 565) during the stance phase. The main ground walking have no signiﬁcant diﬀerence. Visual pertur- eﬀect for the walking condition also shows that peak hip bations are not involved in our experiment design. Thus, the extension moments during the stance phase increased when gait characteristics are comparable with other studies, which walking uphill (p <0 01, η =0 638). Peak knee ﬂexion do not use a virtual environment. moment and extension moment during the stance phase do Our results reveal that CP children had signiﬁcant gait not show signiﬁcantly main eﬀects in the group and walking changes in several spatial-temporal, kinematics, and kinetics condition. CP children have lower peak ankle dorsiﬂexion parameters when walking uphill. The changed gait character- moment in the stance phase than TD children (p <0 01, istics include decreased walking speed and stride length and η =0 623). Lower peak ankle dorsiﬂexion moments in increased peak pelvis tilt, peak ankle dorsiﬂexion (during the stance phase are found both in CP and in TD children the stance phase), hip ﬂexion, and knee ﬂexion (during the during uphill walking compared to level ground walking stance phase). Decreased peak hip abduction in the swing (p <0 01, η =0 416). CP children have reduced peak ankle phase and increased peak pelvis oblique angles are also plantarﬂexion moments in the stance phase compared to TD 2 observed. In general, CP children show similar gait adjust- children (p <0 05, η =0 480). Signiﬁcant between-group dif- ments as TD children during uphill walking. ferences are observed for peak hip abduction moment in the This gait adjustment strategy agrees with the results from stance phase (p =0 018, η =0 340). previous studies [34] using healthy participants, which shows that healthy adults walking on a slope increased hip ﬂexion, knee ﬂexion, and ankle dorsiﬂexion to increase toe clearance. 4. Discussion However, it is noted that, during level treadmill walking, children with CP had a pathological gait pattern with The study is aimed at investigating gait characteristics during inclined treadmill walking under a computer-assisted rehabil- greater knee ﬂexion and ankle dorsiﬂexion during the stance itation environment (CAREN) system in children with CP. phase compared with TD children (see Figure 2). Uphill The CAREN system, which is employed in our study, is walking requires more knee ﬂexion and ankle dorsiﬂexion appropriate for cognitive and physical rehabilitation training during the stance phase and increased the severity of the pathological gait. or assessment owing to its ability of creating realistic envi- ronments and collecting multisensory research data. Studies The ankle angle at the initial contact (IC) showed a signif- on postural control training in the CAREN system show that icant group ∗ walking condition interaction eﬀect. The inter- a single training session is enough to trigger an adaptation action eﬀect means that slope walking inﬂuenced ankle Flex-Ext (N m/kg) Ext-Flex (degree) Flex-Ext (N m/kg) Ext-Flex (degree) Dor-Plan (N m/kg) Plan-Dor (degree) Applied Bionics and Biomechanics 7 th dorsiﬂexion at the IC more in CP than in TD children and e walking speed should be carefully controlled so that peak inﬂuenced knee extension less in CP than in TD children. joint loading will not increase too much. Using a partial The diﬀerence may be due to spasticity of muscles, limiting weight support system during treadmill training may reduce the range of motion in the CP group and the adaptation abil- some joint load for patients. ity of CP and TD children for the diﬀerent walking condi- Studies on single measures of the overall gait pathology tions. Besides, uphill walking requires a signiﬁcant eﬀort to such as the Gait Deviation Index (GDI) [37], Gait Proﬁle propel the body upwards. Previous research shows that com- Score (GPS), and Movement Analysis Proﬁle (MAP) [38] have pared with level treadmill walking condition, the peak hip shown their eﬀectiveness in clinical scenarios. Such outcome extension moment, peak knee extension moment, and peak measures could assess the overall severity of walking or eval- ankle plantar ﬂexion moment are signiﬁcantly higher when uate the overall performance of an intervention the patient walking uphill at the same speed [13]. Our results show that received to improve gait ability. A further study is needed there are no signiﬁcant diﬀerences in peak knee extension to investigate the overall gait pathology for the CP children moment and peak ankle plantar ﬂexion joint moment for during inclined walking under a virtual reality environment the two walking conditions. This ﬁnding may be caused by using an index like the GPS or MAP. the slower walking speed for uphill walking, which can be The study has a small sample size, with ten participants in explained as a strategy to reduce joint loading [13]. each group. The CP group also does not distinguish between In the frontal plane, a signiﬁcant between-group diﬀer- crouch gaits with apparent equines. These issues aﬀect statis- ence is observed for hip abduction moment. This is under tical power to a certain extent. Studies with a larger sample expectation as TD children have wider steps, which results size are required to testify these results and to investigate in a larger moment arm of the ground reaction forces. We the relationship between pathological gait patterns, gait func- ﬁnd that the uphill walking also results in greater pelvic obli- tions, GFMCS, spasticity, muscle force, and dynamic balance que angles and decreased hip abduction angles compared to during inclined walking or other diﬀerent environments in level treadmill walking, which may be a strategy to maintain daily life. balance in the medial-lateral (ML) direction as these changes will move the COM more close to the COP in the ML direc- 5. Conclusion tion. In addition, the trunk rotation angle shows a signiﬁcant CP children showed similar adjustments in their gait during group ∗ walking condition interaction eﬀect. This means that uphill treadmill walking under a virtual reality environment uphill walking inﬂuenced trunk rotation more in TD than in as TD children. CP children could maintain similar dynamic CP. Further research is expected to investigate the contribut- balance with a lower walking speed when walking uphill. ing factors for trunk motion strategies during slope walking. Uphill walking magniﬁes the existing abnormal gait patterns Compared to level treadmill walking, uphill walking has a of the CP children. During a treadmill training with an incli- signiﬁcantly less COM-COP distance in the anterior direc- nation, the walking speed should be carefully controlled in tion. The signiﬁcant diﬀerence may be caused by the smaller the case of improving peak joint loading too much. inclination angle during uphill walking conditions [35]. No between-group diﬀerence is identiﬁed for the COP-COM Data Availability distance in the lateral direction. These results are a bit sur- prising given that children with CP are reported to have The data that support the ﬁndings of this study are available larger displacements of the COP and COM in the medial- on request from the corresponding author, Ye Ma. The data lateral direction [29]. This may also be aﬀected by the are not publicly available yet due to the underdevelopment COM velocity in the ML direction. of the system and the ethics of the project. To the best of the authors’ knowledge, this is the ﬁrst time a comprehensive 3D kinematics and kinetics as well as the Conflicts of Interest dynamic stability analysis (except for some angles in the transverse planes) performed for CP children during slope The authors declare that they have no conﬂicts of interest. walking under a virtual reality environment. Our ﬁndings have some clinical implications. As evident Authors’ Contributions from Figure 2, CP children need to generate extra ankle plan- tar ﬂexion moment during the early stance phase with a Ye Ma and Yanxin Zhang contributed to the conception and crouched posture (excessive ankle dorsiﬂexion and knee ﬂex- design, as well as the drafting of the article. Yali Liang, Xiao- ion). This ﬁnding agrees with Hösl et al. [16], who observes dong Kang, and Lilja Siemelink are responsible for the data the increased activation of the calf muscles for CP children processing and drafting. Yanxin Zhang and Ming Shao are during the early stance phase. A biomechanical study shows responsible for the overall content and are the guarantors. that the peak knee joint force could be greater than six times the body-weight for severe crouch gait [35]. Crouched gait Acknowledgments also could cause joint pain and decrease walking ability [36]. 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Publisher: Hindawi Publishing Corporation
Copyright: Copyright © 2019 Ye Ma et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ISSN: 1176-2322
eISSN: 1754-2103
DOI: 10.1155/2019/8049156
Publisher site: See Article on Publisher Site

Abstract

Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 8049156, 9 pages https://doi.org/10.1155/2019/8049156 Research Article Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment 1 2 2 2 3 4 Ye Ma , Yali Liang, Xiaodong Kang, Ming Shao, Lilja Siemelink, and Yanxin Zhang The Research Academy of Grand Health, Faculty of Sport Science, Ningbo University, Ningbo, China Bayi Rehabilitation Center, Chengdu, Sichuan, China Motekforce Link, Netherlands Department of Exercise Sciences, The University of Auckland, New Zealand Correspondence should be addressed to Ye Ma; maye@nbu.edu.cn Received 21 December 2018; Revised 23 May 2019; Accepted 3 June 2019; Published 19 August 2019 Academic Editor: Jan Harm Koolstra Copyright © 2019 Ye Ma et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. To investigate gait characteristics in children with spastic cerebral palsy during inclined treadmill walking under a virtual reality environment. Methods. Ten spastic cerebral palsy (CP) children and ten typically developing (TD) children were asked to walk at their comfortable speed on a treadmill at a ground level and 10 inclined. Three-dimensional kinematic data and ground reaction force data were captured in a computer-assisted rehabilitation environment system. Kinetic parameters and dynamic balance parameters were calculated using a standard biomechanical approach. Results. During uphill walking, both groups decreased walking speed and stride length and increased peak pelvis tilt, ankle dorsiﬂexion, and hip ﬂexion. Compared with TD children, CP children had decreased walking speed and stride length, decreased peak hip abduction moment, increased stance phase percentage, increased peak ankle dorsiﬂexion and knee ﬂexion, and increased peak hip extension moment. The peak trunk rotation angle, ankle angle at initial contact, and stride length showed a signiﬁcant group ∗ walking condition interaction eﬀect. Conclusions. CP children showed similar adjustments for most gait parameters during uphill walking as TD children. With a lower walking speed, CP children could maintain similar dynamic balance as TD children. Uphill walking magniﬁes the existing abnormal gait patterns of the cerebral palsy children. We suggest that during a treadmill training with an inclination, the walking speed should be carefully controlled in the case of improving peak joint loading too much. feasible method for CP children and can improve walking 1. Introduction speed and general gross motor skills. Willerslev-Olsen et al. Cerebral palsy (CP) is a neurological disorder that results [9] investigated the eﬀect of inclined treadmill training on CP from defects or damages of the immature brain [1, 2]. Prob- children. Their study suggests that inclined intensive gait lems caused by CP, such as muscle tightness, weakness, or training increases beta and gamma oscillatory drive to ankle spasticity, could impede musculoskeletal development and dorsiﬂexor motor neurons and therefore improves toe lift thus result in abnormal gait patterns [3]. and heel strike in CP children. Improving walking ability is one of the major concerns The biomechanical studies including kinematics, kinet- in therapeutic interventions for children with CP. Tread- ics, and dynamic balance analysis are helpful for gaining mill walking has been widely used in the rehabilitation insight into the neural control strategies, understanding the abnormal gait patterns thoroughly, and designing eﬀec- of CP children to provide repetitive training of the whole gait cycle [4–7]. A systematic literature review evaluated tive therapeutic interventions for CP patients. Kinematics is the eﬀectiveness of treadmill training for CP children [8]. used to quantify the abnormalities of gait patterns [10–12]. The review suggested that treadmill training is a safe and Kinetics provides an indication of the causes of the gait 2 Applied Bionics and Biomechanics Table 1: Characteristics of participants. Age Height Weight Patient Gender Aﬀected side GFMCS level Gait type (year) (cm) (kg) S1 7 Male 125 30 L, R II Mild crouch S2 7 Female 114 20 L, R I Mild crouch S3 6 Female 131 27 L, R I Crouch S4 8 Female 125 22.5 L, R I Mild crouch S5 6 Male 117 21 L, R I Mild crouch S6 7 Male 122 22.5 L, R II Mild crouch S7 11 Male 145 37 L, R II Apparent equines S8 10 Male 140 36 L, R II Apparent equines S9 12 Female 146 32 L, R I Crouch S10 11 Male 127 30 L, R II Apparent equines Abbreviations: GMFCS = Gross Motor Function Classiﬁcation System; L = left; R = right. abnormalities and the underlying muscle function pathology and ten TD children (age: 7 9±1 4 years old; height: [10]. Healthy people can adapt to uphill walking by increas- 132 5 ± 11 cm; weight: 26 8±6 3kg) were included. The ing hip, knee, and ankle dorsiﬂexion and thus maintaining characteristics of the CP participants are presented in an upright posture [13]. This adaptation can be used as a Table 1. There are no signiﬁcant diﬀerences in age targeted training of a group of muscles (ankle dorsiﬂexor, (p =0 478), height (p =0 494), or weight (p =0 255) between knee extensor, and hip extensor). However, CP children the two groups. might have diﬃculties in adjusting to inclined walking due The inclusion criteria for CP children are as follows: (1) to impaired postural control or dynamic balance. diagnosed with diplegic CP, (2) 6-12 years old, (3) ranked Biomechanical studies are limited for inclined treadmill I-II in the Gross Motor Function Classiﬁcation System gait training on CP children. Several studies investigated (GFMCS), (4) capable of understanding and executing the biomechanical characteristics and gait adaptation strate- instructions, (5) independent walkers without assistance for gies of CP children for walking on an inclined ramp or tread- more than six minutes, and (6) with no botulinum toxin in mill [13–16]. These studies report that CP children adapt the lower extremities or surgery during the preceding six to inclined walking with similar gait adjustment strategies months. The exclusion criteria for both CP and TD children as the typically developing (TD) children but use greater are the absence of (1) severe heart and lung diseases and (2) postural adaptations. visual or auditory system disorders. The ethical approval To the best of our knowledge, there is a lack of thorough was obtained from the Sichuan Bayi Rehabilitation Center’s understanding of abnormal gait patterns for children with ethics committee (Sichuan, China). Children’s parents signed spastic CP during inclined treadmill walking using three- the consent forms for participation. dimensional (3D) gait analysis including kinematics, kinetics, and dynamic balance analysis. Only kinematic data is 2.2. Instrumentation. Three-dimensional (3D) joint kinemat- reported in most of the aforementioned studies [14, 15]. ics and ground reaction force (GRF) were collected using a The use of two-dimensional (2D) motion cameras [15] also computer-assisted rehabilitation environment (CAREN) sys- loses considerable measurement accuracy for this data. tem. The CAREN system is an immersive virtual environ- This study is aimed at comprehensively investigating ment system consisting of a 3D motion capture system with gait adjustment strategies of CP children in level treadmill twelve high-speed infrared cameras (Vicon, Oxford Metrics, and uphill treadmill walking under a virtual reality envi- UK), a split-belt force plate instrumented treadmill ronment (a default setting for a computer-assisted rehabil- (ADAL3DM-F-COP-Mz, Tecmachine, France) atop a six itation environment (CAREN) system; Motekforce Link, the degree-of-freedom motion base platform, and a cylindrical Netherlands). The study quantiﬁed spatial-temporal parame- projection system. A safety harness and side rails are placed ters, 3D kinematics, 3D kinetics, and dynamic balance of the to ensure the safety and comfort of the user (see Figure 1). CP children by using the state-of-the-art motion capture tech- The Vicon motion capture system recorded kinematic data niques. We hypothesized that (1) CP children used similar gait at a sampling frequency of 100 Hz. The force plate data were adjustment strategies as their TD peers during inclined walk- recorded with a sampling frequency of 1000 Hz. The visual ing and (2) the CP group would have signiﬁcantly lower scene is usually synchronized with the movement of the postural stability due to impaired postural control. platform or the motion of the patient. The CAREN system is employed in this study due to the following concerns: (1) the CAREN system can perform 3D 2. Methods movement for a full body in real time, which provides imme- 2.1. Study Design and Subjects. Ten spastic CP children (age: diate feedback to both the therapist and patient [17]; (2) the 8 5±2 3 years old; height: 131 ± 13 cm; weight: 28 ± 6 9kg) CAREN system can conduct inclined walking experiment Applied Bionics and Biomechanics 3 (a virtual walkway) projected on a cylindrical screen. The data were recorded for one minute during level treadmill walking. Subsequently, the platform was tilted at ten degrees uphill. Uphill walking data were recorded for one minute as well. 2.4. Data Processing. The study used a commercial software system, named the human body model (HBM) [26], embedded in the D-ﬂow of the CAREN system [25], to calculate kinematics and kinetics. For the kinematic data and the GRF, the cutoﬀ frequency of the low-pass ﬁlter was set to 6 Hz. Figure 1: The CAREN system used for this study. The HBM solves the inverse kinematics problem using a nonlinear least squares problem (1). The inverse dynamic and collect kinematic and kinetic information simulta- solution is to ﬁnd an optimal pose Q that best ﬁts the maker neously; (3) the virtual environment is reproducible and as data. In equation (1), r Q is the 3D position of a marker i close to a natural environment as possible [18, 19]; (4) the and r is the marker coordinates measured by the i,meas CAREN system is proved to be an eﬀective tool for rehabili- motion capture system. tation (such as gait training [17, 20], prosthetic adjustment [21], balance training [22, 23], and cognitive rehabilitation [24]) and biomechanics research [25–27]. Q = arg min 〠 r Q − r 1 Q i i,meas i=1 2.3. Experimental Protocol. The motor functioning informa- tion (described by the GMFCS ranking) for CP and the The HBM solves the inverse dynamic problem using the classiﬁcation of CP subtypes were obtained from each CP typical multibody equation of motion (2). child’s medical record. The participants were fully instructed before the measurements. Each participant started with a τ =MQ Q +cQ, Q + G + E, 2 familiarization of three minutes on the treadmill at zero and a ten-degree inclined slope (uphill), respectively. The familiarization ﬁnished until the participant adapted to the where τ is the unknown joint moments and forces, M Q is walking conditions with a comfortable walking speed for the human body mass matrix, c is the centrifugal and Coriolis each condition. loading, G is the gravity, and E represents the external force. After changing clothes and shoes, 25 retroreﬂective The center of pressure (COP) position was measured by markers were placed on the participant’s anatomical land- the instrumented treadmill. The center of mass (COM) posi- marks following the deﬁnition of the whole body human body tion was calculated based on measured kinematic data using th model (HBM) [26]. The markers are placed on the 10 tho- a standard procedure as described by Winter, which deter- racic vertebra, navel, sternum, anterior superior iliac spine, mined the whole body COM based on the COM from indi- posterior superior iliac spine, greater trochanter, lateral epi- vidual body segment [28]. COP-COM separation in both condyle of knee, lateral malleolus, posterior calcanei, the tip the anterior-posterior (AP) and medial-lateral (ML) direc- of big toe, lateral ﬁfth metatarsal heads, acromion, lateral epi- tions, the distance between COM and COP in the AP and condyle and medial epicondyle of the elbow, lateral wrist, ML directions, was calculated to represent the dynamic th medial wrist, xiphoid process, the 7 cervical vertebra, top balance during gait [29]. To cater both the left footed of the head, right side of the head, and left side of the head. and right footed trials, the COP-COM separation in the Local segment coordinate systems were set up for the ML direction is made positive for all trails. These positive torso, pelvis, thigh, shank, and foot segments based on values reﬂect the distance of the feet which were being recorded markers’ positions, which are listed in Table 2 placed on either side of the COM in the ML direction. (see more details from [26]). The average COP-COM separation in the AP and ML For each sampling time frame, the coordinates of each directions is normalized to each participant’s leg length segment with respect to its proximal segment were trans- to allow for a comparison between subjects. Assuming that formed by a sequence of three rotations delineated by three both legs have equal lengths, leg length was calculated as Euler angles following the ﬂexion/extension, adduction/ab- the distance between the left hip joint center and left ankle duction, and internal/external order. joint center during the static trial. For safety considerations, the participants wore a har- ness which was fastened to a metal frame using a safety 2.5. Statistical Analysis. Spatial-temporal, kinematic, kinetic line throughout the experiment. Every participant was data, and dynamic balance parameters were analyzed. Low asked to perform a static trial to locate the positions of reliability and large errors have been reported for the hip the anatomical landmarks and the locations of the joint and knee transverse plane angles and knee frontal plane centers. Then, each participant walked at their comfortable angles recorded by 3D motion capture systems [30]. These speed without handrail support in the virtual environment parameters were not included in this study. 4 Applied Bionics and Biomechanics Table 2: Segment coordination systems. Segment Deﬁnition of the segment coordination system Origin Midpoint between hip joint centers X Unit vector of cross product between the Z-axis and the vector from right hip joint center to left hip joint center Pelvis Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector parallel to the line from S1/L5 to the midpoint between left and right shoulder joint centers Origin Thoracolumbar joint center Unit vector perpendicular to the plane formed by the Z-axis and the vector from right shoulder joint center to left shoulder joint center Torso Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector parallel to the line from S1/L5 to the midpoint between left and right shoulder joint centers Origin Hip joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Thigh Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from knee joint center to hip joint center Origin Knee joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Shank Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from ankle joint center to knee joint center Origin Subtalar joint center X Unit vector perpendicular to the Z-axis lies in the global sagittal plane and points anteriorly Foot Y Unit vector deﬁned by the X-axis and Y-axis to create a right-hand coordinate system Z Unit vector from toe joint center to subtalar joint center Eight gait cycles from each participant under each walk- compared to level treadmill walking (p <0 01, η =0 557), ing condition were selected for the analysis. The Shapiro– with a signiﬁcant group ∗ walking condition interaction Wilk test was performed to test the normality of the data. eﬀect (p <0 01, η =0 298). A two-way mixed-design analysis of variance (ANOVA) (group ∗ walking condition) was used to analyze the spa- 3.2. Joint Kinematics and Dynamic Balance. As shown in tial-temporal, kinematic, and dynamic balance parameters Table 3, CP and TD children increase peak pelvic anterior using SPSS 22.0. For kinetic parameters (joint moments), a 2 tilt when walking uphill (p <0 01, η =0 842). CP and TD two-way ANCOVA (group ∗ walking condition) with speed children have less peak pelvic posterior tilt (p <0 01, η = as a covariate was used. A statistically signiﬁcant diﬀerence 0 843), peak pelvis oblique (p <0 01, η =0 423), and less was accepted as p <0 05. The eta squared (η ) is used as peak trunk extension (p =0 026, η =0 245) when walking the measure of the eﬀect size. The η of 0.01, 0.06, and uphill (p <0 01, η =0 843). Kinematic data shows signiﬁ- 0.14 means the small eﬀect, moderate eﬀect, and large eﬀect, cant diﬀerences for peak hip abduction during the swing respectively [31]. phase (p =0 026, η =0 309), peak hip ﬂexion (p <0 01, η =0 752) during the swing phase, and decreased peak hip extension during the stance phase (p <0 01, η = 3. Results 0 478) during uphill walking in both groups. Compared 3.1. Spatial Temporal Parameters. As shown in Table 3, a to level treadmill walking, uphill walking has a signiﬁ- signiﬁcant diﬀerence is identiﬁed in walking speed between cantly smaller distance between COM and COP in the 2 2 CP and TD children (p <0 01, η =0 749). Both groups anterior-posterior (AP) direction (p <0 01, η =0 190). decreased walking speed during uphill walking (p <0 01, CP children walk with a lower peak knee ﬂexion angle 2 2 η =0 737). The interaction eﬀect of the walking speed during the swing phase than TD children (p <0 01, η = (group ∗ walking condition) does not reach a statistical signif- 0 439). Both groups ﬂex the knee more when walking uphill icance. The stride lengths of the CP children are shorter than (p <0 01, η =0 539). There is a signiﬁcant group ∗ walking 2 2 those of the TD children (p <0 01, η =0 516). Both groups condition interaction eﬀect (p <0 01, η =0 238). At initial decreased stride length signiﬁcantly during uphill walking contact, CP has more knee ﬂexion than TD (p <0 01, η = (p <0 01, η =0 581). There is a signiﬁcant diﬀerence in the 0 614). Both groups increase peak knee ﬂexion during interaction eﬀect (p <0 01, η =0 388) of the stride length. the load responding phase when walking uphill (p <0 01, The CP children show a signiﬁcantly longer stance phase η =0 825). compared to the TD children (p <0 01, η =0 523). Both There is no signiﬁcant group ∗ walking condition interac- groups increase stance percentage during uphill walking tion eﬀect in peak ankle dorsiﬂexion. Both groups increased Applied Bionics and Biomechanics 5 Table 3: Descriptive statistics for key gait variables of CP and TD children under two walking conditions (level and uphill treadmill walking) and results of two-way ANOVA for diﬀerences in the group (CP or TD children), walking condition, and group ∗ walking condition interaction. Level Uphill (+10 degree) p value of ANOVA Parameters CP TD CP TD Walking Group Interaction Mean SD Mean SD Mean SD Mean SD condition Speed (m/s) 0.42 0.16 0.64 0.06 0.32 0.14 0.58 0.07 <0.01 <0.01 0.494 Stride length (m) 0.52 0.19 0.68 0.12 0.39 0.16 0.65 0.14 0.003 <0.01 0.001 Step width (m) 0.09 0.02 0.12 0.04 0.09 0.03 0.11 0.04 0.05 0.135 0.199 Stance phase (%) 71.12 4.23 66.2 0.92 73.95 3.5 67.49 1.07 <0.01 <0.01 0.063 Peak trunk ﬂexion ( ) 8.12 4.07 6.01 1.85 7.21 4.32 4.56 3.1 0.069 0.228 0.779 Peak trunk extension ( ) -2.7 2.75 -0.16 1.38 1.06 4.48 0.62 3.85 0.375 0.026 0.132 Peak trunk rotation ( ) 4.84 8.90 4.96 6.67 2.86 8.53 9.21 5.23 0.493 0.224 0.017 Peak trunk lateral ﬂexion ( ) -2.30 6.92 6.36 2.50 8.28 6.01 4.50 3.66 0.226 0.241 0.47 Peak pelvic anterior tilt ( ) 12.46 5.2 12.93 4.35 26.07 6.94 26.3 7.38 0.88 <0.01 0.865 Peak pelvic posterior tilt ( ) 7.34 4.49 8.9 4.48 21.01 7.13 21.9 7.7 0.593 <0.01 0.682 Peak pelvic oblique ( ) -2.88 7.28 -2.53 3.29 -5.86 7.55 -5.47 4.30 0.95 <0.01 0.941 Peak hip ﬂexion ( ) 39.81 9.32 38.91 7.33 49.65 11.4 52.5 10.26 0.786 <0.01 0.292 Peak hip extension ( ) 6.62 7.62 3.36 6.61 11.28 7.26 7.16 8.36 0.182 <0.01 0.684 Peak hip abduction ( ) 9.98 10.18 9.85 3.77 8.47 9.36 6.33 2.96 0.816 0.026 0.28 Peak hip adduction ( ) 2.74 16.79 4.62 4.99 1.30 11.20 5.18 5.03 0.581 0.761 0.459 Peak knee ﬂexion during LR ( ) 27.15 6.43 20.54 9.95 44.63 6.7 34.66 10.09 <0.01 <0.01 0.333 Peak knee ﬂexion ( ) 60.74 8.11 65.63 11.18 60.58 7.72 67.06 5.44 0.044 0.546 0.454 Peak knee extension ( ) 12.75 6.9 4.23 4.8 14.61 7.24 10.49 6.57 <0.01 <0.01 0.063 Mean SD Mean SD Mean SD Mean SD Peak ankle dorsiﬂexion ( ) 17.55 6.53 11.86 3.59 24.18 5.81 18.64 4.3 <0.01 <0.01 0.932 Peak ankle plantarﬂexion ( ) -5.58 7.62 -14.27 6.14 2.73 7.36 -9.57 6.64 <0.01 <0.01 0.174 Knee ﬂexion at IC ( ) 23.49 7.86 6.93 6.01 43.88 6.21 26.74 13.21 <0.01 <0.01 0.878 Ankle sagittal angle at IC ( ) -1.14 8.18 -5.43 4.6 11.31 7.05 1.46 5.82 <0.01 <0.01 0.004 Peak hip extension moment (N m/kg) 0.54 0.18 0.36 0.09 0.79 0.19 0.55 0.15 <0.01 <0.01 0.395 Peak hip ﬂexion moment (N m/kg) -0.17 0.07 -0.16 0.07 -0.10 0.05 -0.08 0.04 0.398 <0.01 0.852 Peak hip abduction moment (N m/kg) 0.44 0.21 0.62 0.12 0.39 0.14 0.54 0.09 0.018 0.113 0.596 Peak knee abduction moment (N m/kg) 0.11 0.05 0.10 0.05 0.12 0.06 0.15 0.08 0.898 0.066 0.179 Peak knee adduction moment (N m/kg) 0.11 0.11 0.12 0.11 0.11 0.13 0.12 0.11 0.737 0.78 0.962 First peak knee extension moment (N m/kg) 0.14 0.16 0.15 0.08 0.09 0.12 0.23 0.15 0.032 0.657 0.057 Peak knee ﬂexion moment (N m/kg) -0.24 0.14 -0.22 0.19 -0.24 0.15 -0.25 0.11 0.908 0.423 0.584 First knee peak ﬂexion moment (N m/kg) -0.23 0.15 -0.19 0.11 -0.23 0.16 -0.24 0.13 0.82 0.368 0.392 Peak ankle plantarﬂexion moment (N m/kg) 0.76 0.26 0.99 0.19 0.74 0.16 0.91 0.21 <0.01 0.255 0.545 Peak ankle dorsiﬂexion moment (N m/kg) -0.05 0.06 -0.09 0.05 -0.02 0.01 -0.06 0.03 <0.01 0.01 0.996 COM-COP anterior distance (m) 0.12 0.05 0.14 0.05 0.03 0.04 0.06 0.05 0.077 <0.01 0.838 COM-COP posterior distance (m) 0.09 0.08 0.22 0.19 0.14 0.14 0.27 0.13 0.088 0.092 0.764 COM-COP medial distance (m) 0.15 0.04 0.15 0.02 0.16 0.04 0.14 0.02 0.696 0.628 0.555 COM-COP lateral distance (m) -0.09 0.04 -0.04 0.04 -0.08 0.07 -0.03 0.03 0.07 0.32 0.624 Abbreviations: LR = load responding; IC = initial contact; CP = cerebral palsy; TD = typically developing. peak ankle dorsiﬂexion during the stance phase when than TD at the initial contact. Signiﬁcant diﬀerences of walking uphill (p <0 01, η =0 721). CP children show the ankle dorsiﬂexion at the initial contact are identiﬁed in decreased peak plantarﬂexion compared to TD children the main eﬀect for the group (p <0 01, η =0 362), walking 2 2 during the swing phase (p <0 01, η =0 656). Both CP condition (p <0 01, η =0 863), and the interaction eﬀect and TD decrease their peak plantar ﬂexion during the (group ∗ walking condition)(p <0 01, η =0 357). The peak stance phase and swing phase when walking uphill trunk rotation angle shows a signiﬁcant group ∗ walking 2 2 condition interaction eﬀect (p =0 017, η =0 470). (p <0 01, η =0 598). CP has higher ankle dorsiﬂexion 6 Applied Bionics and Biomechanics Hip angle Knee angle Ankle angle 80 30 −10 0 0 −20 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 Gait cycle (%) Gait cycle (%) Gait cycle (%) Hip moment Knee moment Ankle moment 0.8 0.4 0.6 0.2 0.5 0.4 0.2 −0.2 −0.2 −0.4 −0.5 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 Gait cycle (%) Gait cycle (%) Gait cycle (%) Figure 2: Mean joint angles and joint moments for CP and TD during level ground walking and uphill walking (solid black line: TD level walking; dashed black line: TD uphill walking; solid red line: CP level walking; dashed red line: CP uphill walking). 3.3. Joint Kinetics. As shown in Table 3, both CP and TD process of balance [32] and there is no signiﬁcantly diﬀerent children decrease hip peak ﬂexion moment during the stance COP displacement between the subjects who participate in phase when walking uphill (p <0 01, η =0 817). CP children the virtual environment and those who do not [33]. Walking characters including temporal-spatial parameters and kine- have greater peak hip extension moment than TD children matics in treadmill walking using CAREN system and over (p <0 01, η =0 565) during the stance phase. The main ground walking have no signiﬁcant diﬀerence. Visual pertur- eﬀect for the walking condition also shows that peak hip bations are not involved in our experiment design. Thus, the extension moments during the stance phase increased when gait characteristics are comparable with other studies, which walking uphill (p <0 01, η =0 638). Peak knee ﬂexion do not use a virtual environment. moment and extension moment during the stance phase do Our results reveal that CP children had signiﬁcant gait not show signiﬁcantly main eﬀects in the group and walking changes in several spatial-temporal, kinematics, and kinetics condition. CP children have lower peak ankle dorsiﬂexion parameters when walking uphill. The changed gait character- moment in the stance phase than TD children (p <0 01, istics include decreased walking speed and stride length and η =0 623). Lower peak ankle dorsiﬂexion moments in increased peak pelvis tilt, peak ankle dorsiﬂexion (during the stance phase are found both in CP and in TD children the stance phase), hip ﬂexion, and knee ﬂexion (during the during uphill walking compared to level ground walking stance phase). Decreased peak hip abduction in the swing (p <0 01, η =0 416). CP children have reduced peak ankle phase and increased peak pelvis oblique angles are also plantarﬂexion moments in the stance phase compared to TD 2 observed. In general, CP children show similar gait adjust- children (p <0 05, η =0 480). Signiﬁcant between-group dif- ments as TD children during uphill walking. ferences are observed for peak hip abduction moment in the This gait adjustment strategy agrees with the results from stance phase (p =0 018, η =0 340). previous studies [34] using healthy participants, which shows that healthy adults walking on a slope increased hip ﬂexion, knee ﬂexion, and ankle dorsiﬂexion to increase toe clearance. 4. Discussion However, it is noted that, during level treadmill walking, children with CP had a pathological gait pattern with The study is aimed at investigating gait characteristics during inclined treadmill walking under a computer-assisted rehabil- greater knee ﬂexion and ankle dorsiﬂexion during the stance itation environment (CAREN) system in children with CP. phase compared with TD children (see Figure 2). Uphill The CAREN system, which is employed in our study, is walking requires more knee ﬂexion and ankle dorsiﬂexion appropriate for cognitive and physical rehabilitation training during the stance phase and increased the severity of the pathological gait. or assessment owing to its ability of creating realistic envi- ronments and collecting multisensory research data. Studies The ankle angle at the initial contact (IC) showed a signif- on postural control training in the CAREN system show that icant group ∗ walking condition interaction eﬀect. The inter- a single training session is enough to trigger an adaptation action eﬀect means that slope walking inﬂuenced ankle Flex-Ext (N m/kg) Ext-Flex (degree) Flex-Ext (N m/kg) Ext-Flex (degree) Dor-Plan (N m/kg) Plan-Dor (degree) Applied Bionics and Biomechanics 7 th dorsiﬂexion at the IC more in CP than in TD children and e walking speed should be carefully controlled so that peak inﬂuenced knee extension less in CP than in TD children. joint loading will not increase too much. Using a partial The diﬀerence may be due to spasticity of muscles, limiting weight support system during treadmill training may reduce the range of motion in the CP group and the adaptation abil- some joint load for patients. ity of CP and TD children for the diﬀerent walking condi- Studies on single measures of the overall gait pathology tions. Besides, uphill walking requires a signiﬁcant eﬀort to such as the Gait Deviation Index (GDI) [37], Gait Proﬁle propel the body upwards. Previous research shows that com- Score (GPS), and Movement Analysis Proﬁle (MAP) [38] have pared with level treadmill walking condition, the peak hip shown their eﬀectiveness in clinical scenarios. Such outcome extension moment, peak knee extension moment, and peak measures could assess the overall severity of walking or eval- ankle plantar ﬂexion moment are signiﬁcantly higher when uate the overall performance of an intervention the patient walking uphill at the same speed [13]. Our results show that received to improve gait ability. A further study is needed there are no signiﬁcant diﬀerences in peak knee extension to investigate the overall gait pathology for the CP children moment and peak ankle plantar ﬂexion joint moment for during inclined walking under a virtual reality environment the two walking conditions. This ﬁnding may be caused by using an index like the GPS or MAP. the slower walking speed for uphill walking, which can be The study has a small sample size, with ten participants in explained as a strategy to reduce joint loading [13]. each group. The CP group also does not distinguish between In the frontal plane, a signiﬁcant between-group diﬀer- crouch gaits with apparent equines. These issues aﬀect statis- ence is observed for hip abduction moment. This is under tical power to a certain extent. Studies with a larger sample expectation as TD children have wider steps, which results size are required to testify these results and to investigate in a larger moment arm of the ground reaction forces. We the relationship between pathological gait patterns, gait func- ﬁnd that the uphill walking also results in greater pelvic obli- tions, GFMCS, spasticity, muscle force, and dynamic balance que angles and decreased hip abduction angles compared to during inclined walking or other diﬀerent environments in level treadmill walking, which may be a strategy to maintain daily life. balance in the medial-lateral (ML) direction as these changes will move the COM more close to the COP in the ML direc- 5. Conclusion tion. In addition, the trunk rotation angle shows a signiﬁcant CP children showed similar adjustments in their gait during group ∗ walking condition interaction eﬀect. This means that uphill treadmill walking under a virtual reality environment uphill walking inﬂuenced trunk rotation more in TD than in as TD children. CP children could maintain similar dynamic CP. Further research is expected to investigate the contribut- balance with a lower walking speed when walking uphill. ing factors for trunk motion strategies during slope walking. Uphill walking magniﬁes the existing abnormal gait patterns Compared to level treadmill walking, uphill walking has a of the CP children. During a treadmill training with an incli- signiﬁcantly less COM-COP distance in the anterior direc- nation, the walking speed should be carefully controlled in tion. The signiﬁcant diﬀerence may be caused by the smaller the case of improving peak joint loading too much. inclination angle during uphill walking conditions [35]. No between-group diﬀerence is identiﬁed for the COP-COM Data Availability distance in the lateral direction. These results are a bit sur- prising given that children with CP are reported to have The data that support the ﬁndings of this study are available larger displacements of the COP and COM in the medial- on request from the corresponding author, Ye Ma. The data lateral direction [29]. This may also be aﬀected by the are not publicly available yet due to the underdevelopment COM velocity in the ML direction. of the system and the ethics of the project. To the best of the authors’ knowledge, this is the ﬁrst time a comprehensive 3D kinematics and kinetics as well as the Conflicts of Interest dynamic stability analysis (except for some angles in the transverse planes) performed for CP children during slope The authors declare that they have no conﬂicts of interest. walking under a virtual reality environment. Our ﬁndings have some clinical implications. As evident Authors’ Contributions from Figure 2, CP children need to generate extra ankle plan- tar ﬂexion moment during the early stance phase with a Ye Ma and Yanxin Zhang contributed to the conception and crouched posture (excessive ankle dorsiﬂexion and knee ﬂex- design, as well as the drafting of the article. Yali Liang, Xiao- ion). This ﬁnding agrees with Hösl et al. [16], who observes dong Kang, and Lilja Siemelink are responsible for the data the increased activation of the calf muscles for CP children processing and drafting. Yanxin Zhang and Ming Shao are during the early stance phase. A biomechanical study shows responsible for the overall content and are the guarantors. that the peak knee joint force could be greater than six times the body-weight for severe crouch gait [35]. Crouched gait Acknowledgments also could cause joint pain and decrease walking ability [36]. 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Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

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Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

Gait Characteristics of Children with Spastic Cerebral Palsy during Inclined Treadmill Walking under a Virtual Reality Environment

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