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Asymmetry in children with unilateral cerebral palsy during sit-to-stand movement: Cross-sectional, repeated-measures and comparative study
Journal Pre-proof Asymmetry in children with unilateral cerebral palsy during sitto-stand movement: Cross-sectional, repeated-measures and comparative study
Adriana Neves dos Santos, Gisele Moreira Pena, Evelyn Maria Guilherme, Nelci Adriana Cicuto Ferreira Rocha PII:
S0268-0033(19)30281-5
DOI:
https://doi.org/10.1016/j.clinbiomech.2019.11.007
Reference:
JCLB 4899
To appear in:
Clinical Biomechanics
Received date:
17 April 2019
Accepted date:
12 November 2019
Please cite this article as: A.N. dos Santos, G.M. Pena, E.M. Guilherme, et al., Asymmetry in children with unilateral cerebral palsy during sit-to-stand movement: Cross-sectional, repeated-measures and comparative study, Clinical Biomechanics (2019), https://doi.org/ 10.1016/j.clinbiomech.2019.11.007
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© 2019 Published by Elsevier.
Journal Pre-proof Title: Asymmetry in children with Unilateral Cerebral Palsy during sit-to-stand movement: cross-sectional, repeated-measures and comparative study
Author’s names: Adriana Neves dos Santosa,b,*, Gisele Moreira Penaa, Evelyn Maria Guilhermea,
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Nelci Adriana Cicuto Ferreira Rochaa
Department of Physiotherapy, Universidade Federal de São Carlos, Rod.
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Affiliation:
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Washington Luis, km 235, 13565-905, São Carlos-SP, Brazil. Department of Health Science, Universidade Federal de Santa Catarina, Rod.
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Governador Jorge Lacerda, nº 3201 - Km 35,4, 88905-355, Araranguá-SC, Brazil.
* CorrespondingAuthor:
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Name: Adriana Neves dos Santos e-mail: [email protected] Address: Rod. Governador Jorge Lacerda, nº 3201 - Km 35,4, 88905-355, Araranguá SC, Brazil
Abstract word count: 248 Manuscript word count: 2600
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Journal Pre-proof ABSTRACT
Background: We aimed to compare motor strategies adopted by children with unilateral Cerebral Palsy and typically developing children during the performance of sit-to-stand. Methods: Eleven children with unilateral cerebral palsy and 20 typically developing children were evaluated. Kinematic and kinetic analysis of the sit-to-stand movement was performed. Three seat heights were evaluated: neutral (90° of hip-knee-ankle
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flexion), elevated to 120% of the neutral height, and lowered to 80% of the neutral
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height. As outcome variables, we considered sit-to-stand duration (temporal); initial,
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final and maximal sagittal angles and range of motion of trunk, pelvis, hip, knee, and
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ankle (kinematics); the peak of vertical ground reaction force (kinetics), and asymmetric index. Effect size is represented by η2p. Findings: We found that for the lowered seat,
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all groups presented increased flexion of lower limbs and trunk to initiate sit-to-stand
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(p≤0.012; η2p=0.41-0.84), increased peak flexion of trunk, hip and knee (p≤0.01; η2p=0.39-0.88), increased range of motion of knee and trunk (p≤0.01; η2p=0.45-0.85)
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and the duration of sit-to-stand (p≤0.05 η2p=0.23-0.56). Children with unilateral cerebral palsy presented increased posterior pelvic tilt (p≤0.01) and decreased hip flexion of both lower limbs (p≤0.01) for all seat heights and moved their non-affected limb backward in the lowered seat (p≤0.01). Asymmetry was observed for the final and the maximal angles of the ankle in neutral and lowered seats in unilateral cerebral palsy (asymmetry index = 3.3-5.8 %). Interpretation: The lowered seat height led to adaptive motor strategies in children with unilateral cerebral palsy, which should be considered in clinical practice.
Keywords: standing up; functionality; motor control; kinematics; kinetics.
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Journal Pre-proof 1. Introduction Recent motor control theories establish that the interaction between multiple internal systems of one individual, the characteristics of the task, and the environment influence motor activities1, such as Sit to Stand (STS). The STS is commonly performed in daily routine and is a prerequisite for other functional activities2. Intrinsic factors, such as body weight and age, and extrinsic factors, such as seat height and feet position, influence the strategies used to perform STS3; 4; 5.
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One intrinsic factor that modifies STS is the presence of motor deficits, as is the
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case of children with Cerebral Palsy (CP). More functional children with CP took a
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longer time to perform the STS when compared to typically developing children6; 7.
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More dependent children with CP increased pelvic tilt, decreased the peak of knee moment, and extended abruptly the knee during STS8. One extrinsic factor that has been
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studied during the assessment of STS is seat height9. A lowered seat height increased
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trunk flexion and peak flexion of the knee for typically developing children and children with CP10;11. One study found that body sway decreased in the elevated seat in children
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with Unilateral CP (UCP)12.
A lowered seat height increases asymmetry in individuals with hemiparesis. Studies have found lower limb asymmetry during gait in children with UCP 17; 18. The asymmetric weight-bearing distribution between lower limbs could optimize function in children with CP19. However, asymmetry does not provide optimal biomechanical stability20. Also, asymmetric weight-bearing could decrease muscle strength, minimize joint compression, and reduce sensory awareness of the affected limb21. One study found that children with UCP decreased vertical ground reaction force on the affected side during STS, implying that body weight was shifted to the sound side8.
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Journal Pre-proof We did not find studies that evaluated the effects of seat height on the asymmetry of the lower limbs during STS in children with UCP. The knowledge about task conditions that could lead to increased asymmetry and the presence of learned nonuse in children with UCP is important as a preventive measure. Therefore, we aimed to compare motor strategies adopted by children with UCP during the performance of STS in three seats, as well as between children with UCP and typically developing children. We hypothesized that lowered seats would increase time to perform STS,
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modify kinematic variables, and increase peak vertical ground reaction force. Also,
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children with UCP would present lower limb asymmetry, especially on the lowered
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seat.
2. Method
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We used a repeated-measure design and comparative study. The ethics
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committee of the Federal University of São Carlos approved the study (CAAE 05060912.5.0000.5504) and agreed with the Declaration of Helsinki and resolution
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466/2012 from the National Health Council. Children received parental consent and received a child-appropriate letter with information about the study. We recruited a convenience sample of two groups: children with UCP and typically developing children. Participants were recruited from the rehabilitation clinic of the Federal University of São Carlos and care facilities, between July of 2013 and January of 2015, and regular schools. Table 1 demonstrates the inclusion and exclusion criteria. We evaluated eleven children with UCP (age: mean=8.0 years, standard deviation = 1.7 years), seven boys and four girls, classified as level I (6) and II (5) according to the Gross Motor Function Classification System. Twenty typically developing children (age: mean=9.3 years, standard deviation = 2.9 years), nine boys
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Journal Pre-proof and 11 girls, also participated in the study (Figure 1). There were no differences between groups regarding age, height, weight, and gender (p>0.05). Kinematic data were obtained from motion analysis system Qualisys Pro-Reflex - MCU 240 (QUALISYS MEDICAL AB, 411 12 Gothenburg, Sweden), with six cameras and acquisition rate of 240 Hz. The software Qualisys Track Manager 1.9.215 was used to track markers coordinates. Kinetic data were obtained from two force plates (Bertec400, EMG System – Brazil), at an acquisition rate of 1000 Hz (Figure 2A).
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We attached twenty-seven non-colinear passive markers with the child standing
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with feet parallel and hip-width apart on the following anatomical landmarks: acromion,
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sternum, spinous process of 7th cervical and 5th lumbar vertebrae, iliac crest, posterior
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superior iliac spine, prominence of the greater trochanter, lateral and medial epicondyle of the femur, lateral and medial malleolus, 1st and 5th metatarsal bone, tip of big toe
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and heel bone of both sides. We also attached six clusters: one at the spinous process of
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the ninth thoracic, one at the first lumbar vertebrae, one at the lateral side of the thigh of each limb, and one at the lateral side of the shank of each limb25; 26. The same examiner
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attached the markers across participants. The child seated on a bench with adjustable height. Children should: a) be without shoes or ankle-foot orthosis, b) position each foot on a force plate, c) position feet with shoulder-width apart, d) cross their arms over the chest, f) do not use their arms to push off the chair, g) seat over gluteal and the upper thighs regions (Figure 2B). We allowed the child to move the feet backward or forward, except if their feet moved outside the force plate. The child performed the STS movement at a self-selected speed7. The child performed five trials of STS from three-seat heights, randomly selected by drawing lots: neutral (90° of the knee and ankle flexion), elevated (120% of
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Journal Pre-proof neutral height) and lowered (80% of neutral)27 (Figure 2B). We selected only three trials where: a) all markers could be tracked, b) the child did not resort to postural control strategies, such as taking a step forward or to the side. Each trial and each seat height were respectively set apart by 30 seconds and five minutes. We recorded, with a digital camera positioned laterally to the child, each trial to observe foot position (Figure 2A). Kinematic data were processed using Visual 3D (Version 3.9; C-motion Inc., USA). Joint coordinate system definitions recommended by the International Society of
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Biomechanics was used to calculate the Cardan Angles (rotation sequence: sagittal,
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frontal, transverse)29 relative to the static standing trial (child standing for ten seconds).
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We computed joint angles during all STS movements. We considered only the angles
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related to flexion and extension (sagittal plane). We applied a 4th-order Butterworth zero-lag filter, cut-off frequency of 4 Hz, to filter kinematic data. By convention,
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positive kinematic values represented trunk, hip, knee and ankle flexion, and anterior
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pelvic tilt. A custom program in Matlab (version 7.0.1, The MathWorks Inc., Natick, USA) was used to determine initial, final, maximal angles, range of motion and STS
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duration. Data from three attempts for each seat height, each joint, each lower limb, and each angle was averaged. Definitions are: a) Initial angle: anterior displacement of the marker placed on the spinous process of 7th cervical vertebrae greater than 2 standard deviations from STS beginning. b) Final angle: anterior displacement of the marker placed on the spinous
process of 7th cervical vertebrae less than 1 standard deviation from the acquisition of standing posture and maximal hip and knee extension. c) Maximal angle: the peak of anterior pelvic tilt; trunk, hip and knee flexion
and ankle dorsiflexion.
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Journal Pre-proof d) Range of motion: the difference between the final and initial angles7; 8.
Kinetic data were processed and filtered (4th order Butterworth filter, with a low pass frequency of 5 Hz) on Matlab. We normalized data by each participants’ body weight. As a kinetic variable, we used the peak vertical ground reaction force. Asymmetry index (AI) was defined as: 100% × (Vnon-preferred − Vpreferred)/(Vnon-preferred + Vpreferred). V represented angles of the hip, knee, and ankle in the sagittal plane and peak vertical force. The magnitude of AI represented the
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degree of asymmetry. The sign of AI represented the direction. The positive index
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indicated a large angle or peak vertical force for non-preferred limb. We classified a
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variable as asymmetric when it fell outside the associated reference range of the healthy
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group, defined as mean ± 2SD of a particular asymmetry index31. The independent variables were seat height (neutral, elevated and lowered),
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group (UCP and typically developing children), and lower limb (preferred and non-
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preferred lower limb). The dominant lower limb of typically developing children and the non-paretic lower limb of children with UCP was the preferred limb. The dominant
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limb was determined by asking which leg the child would use to kick a ball as far as possible28. The dependent variables were temporal (duration of STS), kinematic (initial, final and maximal angles, and range of motion) and kinetic variables (vertical ground reaction force).
Variables presented a normal distribution, analyzed by the Shapiro-Wilk test. The independent T-test verified the differences between groups for the variables duration, and pelvis and trunk angles. The one-way ANOVA compared the hip, the knee, and the ankle angles, and the peak ground reaction vertical force of the preferred limb of typically developing children with both lower limbs of children with UCP. We used a Tukey post hoc test. The repeated ANOVA test compared seat heights. We used
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Journal Pre-proof SPSS software (version 17.0) to run statistical analysis, with a significance level equal to 0.05.
3. Results
3.1.Comparison Between seats height For both groups, the lowered seat increased: a) the initial angle of both hips and
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knees, b) the trunk flexion represented by increased peak flexion of the trunk and hip,
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c) the peak of the knees, d) the range of motion of the hips, e) the peak vertical ground
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reaction force. For children with UCP, the lowered seat also increased: a) the duration
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of STS, b) the range of motion of both knees and the trunk. For typically developing children, the lowered bench also increased: a) the peak angle of the ankle, b) the range
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motion of the ankle (Figure 3 and Table 2).
3.2.Comparison between groups and lower limbs
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Children with UCP increased pelvic posterior tilt and decreased flexion of both hips for initial, peak, and final angles when compared with typically developing children. As seat height was reduced, children with UCP took a longer time to perform STS, decreased peak of the trunk, increased the peak of both knees, and increased the plantar flexion of the non-preferred lower limb during STS and at the end of the movement. We did not find differences between lower limbs for the peak of vertical force (Figure 3 and Table 3).
3.3.Asymmetry Index
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Journal Pre-proof Children with UCP presented asymmetry for the final and the maximal angles of the ankle in neutral and lowered seats, compared with the non-preferred lower limb (Table 4).
4. Discussion
Our results confirmed our first hypothesis since the lowered seat increased the duration of STS, the trunk flexion and the maximal angle of the knee, and the peak of
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the vertical ground reaction force. The results agreed with previous studies with
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children with CP10; 11. The lowered seat increases task demand requiring an increased
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joint moment of the knee to stand up. When the child increases trunk flexion, the body
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vector line approximates to the knee joint. This strategy facilitates the forward motion of the body and reduces the effort required from knee extensors to stand up32; 33.
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Our second hypothesis was also confirmed since children with UCP adopted an
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adaptive motor strategy to perform STS, especially in the lowered seat, in comparison with typically developing children. The first difference between groups was an
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increased posterior pelvic tilt and a decreased hip flexion on both lower limbs of children with UCP during the entire performance of STS. Studies have found that children with CP usually acquire sitting position with posterior pelvic tilt34; 35. The second difference between groups was that even though children with UCP were able to increase trunk flexion when seat height was reduced, the trunk peak flexion was always inferior to the typically developing children. Children with UCP, therefore, presented limited ability to move the trunk forward when compared to typically developing children. Studies have associated an increased posterior pelvic tilt with decreased pelvic mobility, limited performance of functional activities, and limited forward movement of the body36.
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Journal Pre-proof The third difference between groups was that children with UCP moved their preferred lower limb backward before standing up from the lowered seat. The adoption of this strategy could be explained by the limitation to increase anterior pelvic tilt and, as a consequence, to move the body forward, similar to typically developing children. Children with UCP, therefore, would require a higher joint moment of the knee in the lowered seat32;
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. Children with UCP, however, present knee extensor weakness,
especially in the affected limb7. The lower limb that moves backward is responsible for
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weight-bearing and knee extensor torque3. Moving the preferred limb backward,
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therefore, is an adaptative strategy that allows children with UCP to use their stronger
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lower limb to stand up. Similar results have been found in individuals with stroke21; 38.
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The fourth difference between groups was the inability of the non-preferred limb of children with UCP to increase peak flexion of the ankle. We found that children with
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UCP maintained their non-preferred limb in plantar flexion during most of the STS
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trials. One study also found maintained plantar flexion in children with CP10. Our third hypothesis was also confirmed since we found an asymmetry of the
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peak angle of the knee (neutral seat), and of the maximal and the final angles of the ankle (neutral and the lowered seat), in children with UCP. The asymmetries that we found could be associated with the strategy to move the preferred limb backward. We did not find an asymmetry for the peak of vertical ground reaction force between the preferred and the non-preferred lower limbs of children with UCP., which could be explained by the small sample size.
Limitations The main limitation of our study is the small sample size. Also, we used nonprobabilistic recruitment that could affect generalizability and external validity. We also
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Journal Pre-proof evaluated only children with CP with minimal motor impairment since they were able to perform STS independently. Therefore, our results can be generalized only for this population. Another methodological limitation is the analysis of the relative angles instead of the angles of joints in all movement planes. We restricted foot placement in cases when the children moved their feet backward and placed them outside the force plate, which could modify the motor strategies used to perform STS. Since foot placement
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was restricted, some children may have artificially performed STS, changing motor
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strategies and body alignment.
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The fact that we considered the average of only three repetitions is also a
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limitation of the study. Even though we assessed five repetitions for each child, we had to exclude some repetitions because children moved their feet outside force plate or
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at the moment they stood up.
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because the system could not track all markers or because children gave a step forward
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Clinical implications
Our results demonstrated that even children with CP with less compromised function modified their motor strategies to perform STS movement when task demand increased. The knowledge of the motor strategies most used is important to guide clinical approaches. We verified that children with UCP when compared to typically developing children, during the performance of STS from the lowered seat, presented: a) limited active pelvic and trunk mobility, b) movement of the preferred limb backward, c) compromised ability to increase ankle dorsiflexion, d) increased total duration, e) asymmetry of the ankle. These results show that the environment and the task demands
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Journal Pre-proof modify the performance of STS. The implementation of a lowered seat in daily routine or at the clinical setting should be carefully analyzed. Rehabilitation strategies to improve pelvic and trunk mobility, weight-bearing at the non-preferred lower limb, and active movement of the ankle seems to be important to facilitate STS when the demand of the task increases, as is the case of the lowered seat.
Acknowledgments
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We would like to thank the staff of the LADI Laboratory –UFSCar, Livia
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Pessarelli and Mariana Martins dos Santos, for their assistance with data collection.
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Funding
This work was supported by the Fundação de Amparo à Pesquisa do Estado de
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cerebral palsy. Indian J Orthop, v. 44, n. 2, p. 148-58, Apr 2010. ISSN 1998-3727. Disponível em: < https://www.ncbi.nlm.nih.gov/pubmed/20419001 >. 36
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VAN DER HEIDE, J. C. et al. Development of postural adjustments during
ro
reaching in sitting children. Exp Brain Res, v. 151, n. 1, p. 32-45, Jul 2003. ISSN
-p
0014-4819. Disponível em: < https://www.ncbi.nlm.nih.gov/pubmed/12740725 >. 37
re
KWONG, P. W. et al. Foot placement and arm position affect the five times sit-
to-stand test time of individuals with chronic stroke. Biomed Res Int, v. 2014, p.
38
lP
636530, 2014.
na
LECOURS, J. et al. Interactions between foot placement, trunk frontal position,
weight-bearing and knee moment asymmetry at seat-off during rising from a chair in
Jo ur
healthy controls and persons with hemiparesis. J Rehabil Med, v. 40, n. 3, p. 200-7, Mar 2008. ISSN 1650-1977 (Print) 1650-1977. 39
HAN, J.; KIM, Y.; KIM, K. Effects of foot position of the nonparetic side during
sit-to-stand training on postural balance in patients with stroke. J Phys Ther Sci, v. 27, n.
8,
p.
2625-7,
Aug
2015.
ISSN
0915-5287.
Disponível
em:
<
https://www.ncbi.nlm.nih.gov/pubmed/26356809 >. 40
CAMARGOS, A. C.; RODRIGUES-DE-PAULA-GOULART, F.; TEIXEIRA-
SALMELA, L. F. The effects of foot position on the performance of the sit-to-stand movement with chronic stroke subjects. Arch Phys Med Rehabil, v. 90, n. 2, p. 314-9, Feb 2009. ISSN 0003-9993.
17
Journal Pre-proof 41
KIM, K.; KIM, Y. M.; KANG, D. Y. Repetitive sit-to-stand training with the
step-foot position on the non-paretic side, and its effects on the balance and foot pressure of chronic stroke subjects. J Phys Ther Sci, v. 27, n. 8, p. 2621-4, Aug 2015. ISSN 0915-5287. Disponível em: < https://www.ncbi.nlm.nih.gov/pubmed/26357448 >. 42
ROCHA ADE, S.; KNABBEN, R. J.; MICHAELSEN, S. M. Non-paretic lower
limb constraint with a step decreases the asymmetry of vertical forces during sit-tostand at two seat heights in subjects with hemiparesis. Gait Posture, v. 32, n. 4, p. 457-
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na
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re
-p
ro
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63, Oct 2010. ISSN 0966-6362.
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Table 1 – Exclusion criteria for typically developing children and children with UCP. Criteria Typically developing children Absence of current lower limb injury, neurological or systemic conditions, aged from 6 to 12 years Inclusion Height and weight not in accordance with the expected percentile for age Exclusion Children with Unilateral cerebral Palsy Children with CP, aged between 6 and 12 years Inclusion
Ability to perform STS without support in three-seat height Inability to follow simple commands Muscle contracture in hamstrings, gastrocnemius or hip flexors
l a
Deformity in the lower limbs, such as fixed hip or knee flexion, which could compromise STS
n r u
Exclusion
Orthopedic surgery in the lower limbs in the previous 12 months Botulinum toxin injection in the lower limbs previous in the previous 6 months Height and weight not in accordance with the expected percentile for age a
o J
First assessment, by the researchers
f o
o r p
e
r P
How it was assessed
Stadiometer and digital scalea Diagnosed by a doctor
First assessment, by the researchers Conversation between the therapist and the child Hamstrings: Straight Leg Raise Testb Gastrocnemius: manual test Hip flexors: Modified Thomas Testb Exclusion: negative tests During manual test as described for muscle shortening. Exclusion: any fixed restriction Interview with the caregivers Interview with the caregivers Stadiometer and digital scalea
FILHO, V. C. et al. [Anthropometric indices among schoolchildren from a municipality in Southern Brazil: a descriptive analysis using the LMS method]. Rev Paul Pediatr, v. 32, n. 4, p. 333-41, Dec 2014.
b
MÉLO, T. R.; GUIMARÃES, A. T. B.; ISRAEL, V. L. Repeatability and comparison of clinical tests in children with spastic diplegia and with typical development. Fisioterapia e Movimento, v. 28, n. 1, p. 13 - 22, 2015.
19
Journal Pre-proof Table 2 – Statistics data for comparisons between seats height for duration (seconds); angles of trunk, pelvis, hip, knee and ankle (º), and peak vertical force (N/V/Kg) during sit to stand movement. Comparasions
p
Mean difference
95% CI mean difference
Lowered > Elevated
p≤0.01
0.9
0.5 / 1.3
Repeated ANOVA
Healthy
Maximal
Trunk
maximal
Lowered > Neutral
p=0.03
0.5
0.1 / 1.0
Lowered > Elevated
p≤0.01
9.8
5.7 / 13.9
Lowered > Neutral
p≤0.02
7.0
4.6 / 9.4
Lowered > Elevated
p≤0.01
1.1
6.6 / 15.6
Lowered > Neutral
p=0.039
2.9
0.2 / 5.6
F=19.57; p≤0.01; η2p=0.5
F=22.36; p≤0.01; η2p=0.7
UCP
F=22.36; p≤0.01; η2p=0.7
UCP
F=6.68; p=0.006; η2p=0.4
Neutral > Elevated
p=0.002
8.2
3.9 / 12.4
Lowered > Elevated
p≤0.01
11.1
6.6 / 15.6
Lowered > Neutral
P=0.039
2.9
0.2 / 5.6
Neutral > Elevated
P=0.002
8.2
3.9 / 12.4
Lowered > Elevated
p=0.19
4.9
1.0 / 8.7
Neutral > Elevated
p≤0.01
4.8
2.7 / 6.3
Lowered > Elevated
p≤0.01
16.8
12.9 / 20.6
Lowered > Neutral
p≤0.01
7.5
4.7 / 10.3
Neutral > Elevated
p≤0.01
9.3
6.1 / 12.4
Lowered > Elevated
p≤0.01
10.8
7.4 / 14.2
Lowered > Neutral
p≤0.01
4.6
2.6 / 6.5
Neutral > Elevated
p≤0.01
6.2
3.6 / 8.9
Lowered > Elevated
p≤0.01
14.2
10.9 / 17.5
Lowered > Neutral
p≤0.01
4.6
2.9 / 6.3
Neutral > Elevated
p=0.002
9.6
6.2 / 12.9
Lowered > Elevated
p≤0.01
17.6
14.4 / 20.8
Lowered > Neutral
p≤0.01
9.1
6.3 / 11.8
Neutral > Elevated
p≤0.01
8.5
5.4 / 11.6
Lowered > Elevated
p≤0.01
16.5
9.7 / 23.2
Neutral > Elevated
p=0.003
2.9
4.8 / 17.8
Lowered > Elevated
p=0.001
17.1
8.3 / 25.8
Lowered > Neutral
p=0.012
9.3
2.5 / 16.0
Neutral > Elevated
p=0.001
7.8
4.3 / 11.2
Lowered > Elevated
p≤0.01
22.6
17.6 / 27.5
Lowered > Neutral
p=0.001
14.3
8.0 / 20.6
Neutral > Elevated
p=0.013
8.3
2.2 / 14.3
Lowered > Elevated
p≤0.01
10.8
7.4 / 14.2
Lowered > Neutral
p≤0.01
4.6
2.6 / 6.5
Neutral > Elevated
p≤0.01
6.22
3.6 / 8.9
Lowered > Elevated
p≤0.01
30.1
21.0 / 38.4
Lowered > Neutral
p≤0.01
18.0
13.1 / 22.9
Neutral > Elevated
p=0.002
12.1
6.0 / 18.1
Lowered > Elevated
p≤0.01
15.6
5.2 / 26.0
Neutral > Elevated
p≤0.01
6.7
1.9 / 11.4
-p
Pelvis
Range of motion
UCP
F=12.83; p≤0.01; η2p=0.6
of
UCP
ro
Duration
Healthy
Hip
Range of motion
UCP
F=76.07; p≤0.01; η2p=0.8
UCP
F=15.05; p=0.003; η2p=0.6
UCP
Healthy
Maximal Knee
re
Healthy
Healthy
Initial
F=36.01; p≤0.01; η2p=0.7 F=22.36; p≤0.01; η2p=0.7
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Maximal
F=59.06; p≤0.01; η2p=0.8
lP
Healthy
na
Initial
UCP
Range of motion Healthy
F=16.15; p=0.001; η2p=0.6
F=41.53; p≤0.01; η2p=0.8
F=64.01; p≤0.01; η2p=0.9
F=56.34; p≤0.01; η2p=0.9 F=8.23; p=0.09; η2p=0.4
20
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UCP Healthy Healthy
23.1
17.8 / 28.4
Lowered > Neutral
p=0.001
15.1
8.6 / 21.6
Neutral > Elevated
p=0.007
8.0
2.9 / 13.1
Lowered > Elevated
p=0.002
6.6
3.0 / 10.1
Lowered > Neutral Lowered > Elevated
p=0.041 p≤0.01
4.7 0.9
0.2 / 9.2 0.8 / 01.0
Neutral > Elevated
p≤0.01
1.0
0.8 / 1.1
Lowered > Elevated
p≤0.01
1.0
0.9 / 1.1
Neutral > Elevated
p≤0.01
1.0
0.9 / 1.1
F=45.68; p≤0.01; η2p=0.8 F=6.48; p=0.007; η2p=0.4 F=453.30; p≤0.01; η2p=0.9
F=267.58; p≤0.01; η2p=1.0
na
lP
re
-p
ro
of
UCP
p≤0.01
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Ankle Maximal Peak vertical force
Lowered > Elevated
21
Journal Pre-proof Table 3 – Statistics data for comparisons between Unilateral Cerebral Palsy (UCP) and typically developing children for duration (seconds); and angles of trunk, pelvis, hip, knee and ankle (º) during sit to stand movement.
Independent T-Teste
Comparasions
Mean difference
95% CI mean difference
t=2.61; p=0.023
UCP > Healthy
0.3
-0.1 / 0.7
Duration Lowered t=1.45; p=0.174 t=-3.34; p=0.002 Elevated t=-2.64; p=0.013 Trunk Maximal Lowered
UCP > Healthy
0.6
0.1 / 1.1
Elevated t=-5.09; p≤0.01 Neutral t=-6.55; p≤0.01
Neutral
UCP < Healthy
-20.4
-27.3 / -13.4
Lowered t=-6.00; p≤0.01
UCP < Healthy
-22.0
-28.9 / -15.1
Elevated t=-6.62; p≤0.01 Neutral t=-4.37; p≤0.01
UCP < Healthy
-22.2
-29.0 / -15.3
UCP < Healthy
-17.5
-25.4 / -9.5
UCP < Healthy
-18.5
-27.1 / -9.9
UCP < Healthy
-21.1
-27.4 / -14.7
UCP < Healthy
-22.2
-29.1 / -15.3
UCP < Healthy
-20.9
-27.6 / -14.1
-19.3
-29.8 / -8.8
-18.7
-29.2 / -8.2
-13.0
-21.2 / -4.9
-12.4
-20.6 / -4.3
-14.8
-26.0 / -3.6
-13.8
-24.9 / -2.6
-14.7
-25.9 / -3.4
-13.6
-24.9 / -2.4
-19.3
-29.8 / -8.8
-18.68
-29.2 / -8.2
-13.02
-21.2 / -4.9
-12.42
-20.6 / -4.3
-19.2
-30.1 / -8.4
-19.2
-30.0 / -8.4
-16.1
-26.9 / -5.3
-16.1
-26.9 / -5.2
ro
of
UCP < Healthy
re
Final
Lowered t=-6.31; p≤0.01
F=11.23; p≤0.01
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Elevated
na
lP
ANOVA
Neutral
Initial
Hip
-16.5 / -3.9 -21.0 / -2.6 -25.2 / -10.6
Elevated t=-6.76; p≤0.01 Neutral t=-6.59; p≤0.01 Pelvis
-10.2 -11.8 -17.9
Maximal Lowered t=-4.42; p≤0.01
UCP < Healthy
-p
Initial
UCP < Healthy
Lowered
Maximal Elevated
F=7.53; p≤0.01
F=15.04; p≤0.01
F=19.57; p≤0.01
Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy
22
Journal Pre-proof
F=12.56; p≤0.01
F=8.26; p≤0.01
Lowered
Maximal Lowered Knee
Final
Lowered
Neutral Maximal Lowered Neutral
Ankle
Final
F=4.61; p=0.006;
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Final
na
lP
Neutral
re
-p
Elevated
F=19.57; p≤0.01
Lowered
F=7.31; p≤0.0 F=3.74; p=0.016
F=3.47; p=0.022 F=5.20; p=0.003 F=3.74; p=0.016
F=4.27; p=0.009
-13.8
-23.9 / -3.7
-13.0
-23.1 / -2.9
-13.8
-23.8 / -3.7
-12.9
-23.1 / -2.9
-14.2
-25.6 / -2.8
-12.8
-24.2 / -1.4
-16.7
-27.7 / -5.7
-14.7
-25.7 / -3.7
-13.6
-24.6 / -2.6
-11.7
-22.7 / -0.7
-16.1
-26.8 / -5.4
-12.4
-22.9 / -1.9
-16.0
-26.7 / -5.4
-12.4
-22.8 / -1.9
-12.1
-23.6 / -0.6
-10.1
-21.7 / 1.3
-12.1
-23.6 / -0.6
-10.1
-21.6 / 1.4
14.0
3.3 / 24.8
11.3
0.6 / 22.1
-10.5
-20.6 / -0.4
-8.5
-15.3 / -1.8
-6.7
-12.6 / -0.7
-7.0
-12.9 / -1.2
-9.9
-18.2 / -1.5
-12.6
-21.4 / -3.8
-8.4
-16.2 / -0.7
of
Lowered
F=19.57; p≤0.01
ro
Neutral
Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP > Non-Prefered Healthy Prefered UCP > NonPrefered Healthy Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered Healthy
23
Journal Pre-proof Table 4 – Asymmetry index (%) of hip, knee and ankle during STS movement from elevated, lowered and neutral seats, in typically developing children and children with unilateral Cerebral Palsy (UCP). HIP
KNEE
DP Typical UCP Typical Typical Elevated
-0.6
UCP
ANKLE DP DP Typical Typical UCP Typical
*8.6
4.2
-1.6
1.6
6.0
-0.9
1.6
2.9
-0.9
0.8
4.1
-2.3
2.3
5.3
-1.3
2.9
2.6
-1.1
-0.8
3.6
-2.5
2.5
3.6
-1.2
1.5
2.1
Elevated
0.0
2.8
3.8
-0.5
0.5
4.6
0.1
3.4
3.2
Neutral
-0.5
0.4
3.1
-2.0
2.0
4.5
-0.6
*4.7
1.5
Maximal Lowered
-0.7
-2.8
3.1
-2.8
2.8
4.0
-1.1
*4.7
1.9
Elevated
7.8
-8.7
53.4
15.8
26.5
Neutral
46.0
68.6
-8.28
Lowered
23.8
8.2 249.1
262.8
24.2
Elevated
-1.6
3.8
7.3
Range of Neutral Motion Lowered
-1.1
3.1
5.6
-1.5
3.9
5.4
Elevated
-4.2
5.2
11.2
-0.1
*3.3
1.4
*364.4
22.57
-0.6
*4.7
1.0
-24.2
37.1
-0.5
*5.8
1.5
-p
ro
-15.8
-1.3
1.3
6.3
6.5
36.6
35.9
-1.3
1.3
6.2
10.1
10.7
19.8
2.6
3.9
6.9
24.4
18.4
re
Final
of
Neutral Lowered
Initial
-2.6
Jo ur
na
lP
5. -2.0 17.2 Vertical Neutral -6.3 -2.4 44.6 Force Lowered * Asymmetric index superior to mean ± 2 standard deviation of typically developing children.
24
Journal Pre-proof Figure Legends:
Figure 1 - Flowchart of selection and inclusion of children.
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Figure 2 – Kinematic curves of the trunk, pelvis and preferred lower limb of a typically developing child, and the preferred and non-preferred lower limbs of a child with Unilateral Cerebral Palsy, during sit to stand movement. The figures refer to sagittal plane, where negative values represent extension and positive values represent flexion for trunk and lower limbs. For pelvis, negative values represent posterior tilt and positive values anterior tilt. Joints: Ankle (pink), Knee (green), Hip (red), Trunk (blue) and Pelvis (black). a: Unilateral Cerebral Palsy = preferred limb. b: Unilateral Cerebral Palsy = non-preferred lower limb
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na
lP
re
-p
ro
Figure 3- Study set up.
25
Journal Pre-proof CRediT Author Statement
Adriana
Neves
dos
Santos:
Investigation;
Methodology;
Project
administration; Software; Visualization; Roles/Writing – original draft; Writing – review & editing
Gisele Moreira Pena: Investigation; Roles/Writing – original draft; Writing –
ro
of
review & editing
-p
Evelyn Maria Guilherme: Investigation; Roles/Writing – original draft;
re
Writing – review & editing
Jo ur
na
review & editing; Resources
lP
Nelci Adriana Cicuto Ferreira Rocha: Investigation; Methodology; Writing –
26
Journal Pre-proof Highlights
na
lP
re
-p
ro
of
Lowered seat leads to lower limb asymmetry in unilateral cerebral palsy. Pelvic mobility is compromised in cerebral palsy, especially in a lowered seat. Ankle asymmetry is increased in the lowered seat. Sit-to-stand movement is influenced by extrinsic factors such as seat height.
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27
Figure 1
Figure 2
Figure 3
Adriana Neves dos Santos, Gisele Moreira Pena, Evelyn Maria Guilherme, Nelci Adriana Cicuto Ferreira Rocha PII:
S0268-0033(19)30281-5
DOI:
https://doi.org/10.1016/j.clinbiomech.2019.11.007
Reference:
JCLB 4899
To appear in:
Clinical Biomechanics
Received date:
17 April 2019
Accepted date:
12 November 2019
Please cite this article as: A.N. dos Santos, G.M. Pena, E.M. Guilherme, et al., Asymmetry in children with unilateral cerebral palsy during sit-to-stand movement: Cross-sectional, repeated-measures and comparative study, Clinical Biomechanics (2019), https://doi.org/ 10.1016/j.clinbiomech.2019.11.007
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© 2019 Published by Elsevier.
Journal Pre-proof Title: Asymmetry in children with Unilateral Cerebral Palsy during sit-to-stand movement: cross-sectional, repeated-measures and comparative study
Author’s names: Adriana Neves dos Santosa,b,*, Gisele Moreira Penaa, Evelyn Maria Guilhermea,
of
Nelci Adriana Cicuto Ferreira Rochaa
Department of Physiotherapy, Universidade Federal de São Carlos, Rod.
-p
a
ro
Affiliation:
b
re
Washington Luis, km 235, 13565-905, São Carlos-SP, Brazil. Department of Health Science, Universidade Federal de Santa Catarina, Rod.
na
lP
Governador Jorge Lacerda, nº 3201 - Km 35,4, 88905-355, Araranguá-SC, Brazil.
* CorrespondingAuthor:
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Name: Adriana Neves dos Santos e-mail: [email protected] Address: Rod. Governador Jorge Lacerda, nº 3201 - Km 35,4, 88905-355, Araranguá SC, Brazil
Abstract word count: 248 Manuscript word count: 2600
1
Journal Pre-proof ABSTRACT
Background: We aimed to compare motor strategies adopted by children with unilateral Cerebral Palsy and typically developing children during the performance of sit-to-stand. Methods: Eleven children with unilateral cerebral palsy and 20 typically developing children were evaluated. Kinematic and kinetic analysis of the sit-to-stand movement was performed. Three seat heights were evaluated: neutral (90° of hip-knee-ankle
of
flexion), elevated to 120% of the neutral height, and lowered to 80% of the neutral
ro
height. As outcome variables, we considered sit-to-stand duration (temporal); initial,
-p
final and maximal sagittal angles and range of motion of trunk, pelvis, hip, knee, and
re
ankle (kinematics); the peak of vertical ground reaction force (kinetics), and asymmetric index. Effect size is represented by η2p. Findings: We found that for the lowered seat,
lP
all groups presented increased flexion of lower limbs and trunk to initiate sit-to-stand
na
(p≤0.012; η2p=0.41-0.84), increased peak flexion of trunk, hip and knee (p≤0.01; η2p=0.39-0.88), increased range of motion of knee and trunk (p≤0.01; η2p=0.45-0.85)
Jo ur
and the duration of sit-to-stand (p≤0.05 η2p=0.23-0.56). Children with unilateral cerebral palsy presented increased posterior pelvic tilt (p≤0.01) and decreased hip flexion of both lower limbs (p≤0.01) for all seat heights and moved their non-affected limb backward in the lowered seat (p≤0.01). Asymmetry was observed for the final and the maximal angles of the ankle in neutral and lowered seats in unilateral cerebral palsy (asymmetry index = 3.3-5.8 %). Interpretation: The lowered seat height led to adaptive motor strategies in children with unilateral cerebral palsy, which should be considered in clinical practice.
Keywords: standing up; functionality; motor control; kinematics; kinetics.
2
Journal Pre-proof 1. Introduction Recent motor control theories establish that the interaction between multiple internal systems of one individual, the characteristics of the task, and the environment influence motor activities1, such as Sit to Stand (STS). The STS is commonly performed in daily routine and is a prerequisite for other functional activities2. Intrinsic factors, such as body weight and age, and extrinsic factors, such as seat height and feet position, influence the strategies used to perform STS3; 4; 5.
of
One intrinsic factor that modifies STS is the presence of motor deficits, as is the
ro
case of children with Cerebral Palsy (CP). More functional children with CP took a
-p
longer time to perform the STS when compared to typically developing children6; 7.
re
More dependent children with CP increased pelvic tilt, decreased the peak of knee moment, and extended abruptly the knee during STS8. One extrinsic factor that has been
lP
studied during the assessment of STS is seat height9. A lowered seat height increased
na
trunk flexion and peak flexion of the knee for typically developing children and children with CP10;11. One study found that body sway decreased in the elevated seat in children
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with Unilateral CP (UCP)12.
A lowered seat height increases asymmetry in individuals with hemiparesis. Studies have found lower limb asymmetry during gait in children with UCP 17; 18. The asymmetric weight-bearing distribution between lower limbs could optimize function in children with CP19. However, asymmetry does not provide optimal biomechanical stability20. Also, asymmetric weight-bearing could decrease muscle strength, minimize joint compression, and reduce sensory awareness of the affected limb21. One study found that children with UCP decreased vertical ground reaction force on the affected side during STS, implying that body weight was shifted to the sound side8.
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Journal Pre-proof We did not find studies that evaluated the effects of seat height on the asymmetry of the lower limbs during STS in children with UCP. The knowledge about task conditions that could lead to increased asymmetry and the presence of learned nonuse in children with UCP is important as a preventive measure. Therefore, we aimed to compare motor strategies adopted by children with UCP during the performance of STS in three seats, as well as between children with UCP and typically developing children. We hypothesized that lowered seats would increase time to perform STS,
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modify kinematic variables, and increase peak vertical ground reaction force. Also,
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children with UCP would present lower limb asymmetry, especially on the lowered
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seat.
2. Method
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We used a repeated-measure design and comparative study. The ethics
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committee of the Federal University of São Carlos approved the study (CAAE 05060912.5.0000.5504) and agreed with the Declaration of Helsinki and resolution
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466/2012 from the National Health Council. Children received parental consent and received a child-appropriate letter with information about the study. We recruited a convenience sample of two groups: children with UCP and typically developing children. Participants were recruited from the rehabilitation clinic of the Federal University of São Carlos and care facilities, between July of 2013 and January of 2015, and regular schools. Table 1 demonstrates the inclusion and exclusion criteria. We evaluated eleven children with UCP (age: mean=8.0 years, standard deviation = 1.7 years), seven boys and four girls, classified as level I (6) and II (5) according to the Gross Motor Function Classification System. Twenty typically developing children (age: mean=9.3 years, standard deviation = 2.9 years), nine boys
4
Journal Pre-proof and 11 girls, also participated in the study (Figure 1). There were no differences between groups regarding age, height, weight, and gender (p>0.05). Kinematic data were obtained from motion analysis system Qualisys Pro-Reflex - MCU 240 (QUALISYS MEDICAL AB, 411 12 Gothenburg, Sweden), with six cameras and acquisition rate of 240 Hz. The software Qualisys Track Manager 1.9.215 was used to track markers coordinates. Kinetic data were obtained from two force plates (Bertec400, EMG System – Brazil), at an acquisition rate of 1000 Hz (Figure 2A).
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We attached twenty-seven non-colinear passive markers with the child standing
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with feet parallel and hip-width apart on the following anatomical landmarks: acromion,
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sternum, spinous process of 7th cervical and 5th lumbar vertebrae, iliac crest, posterior
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superior iliac spine, prominence of the greater trochanter, lateral and medial epicondyle of the femur, lateral and medial malleolus, 1st and 5th metatarsal bone, tip of big toe
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and heel bone of both sides. We also attached six clusters: one at the spinous process of
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the ninth thoracic, one at the first lumbar vertebrae, one at the lateral side of the thigh of each limb, and one at the lateral side of the shank of each limb25; 26. The same examiner
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attached the markers across participants. The child seated on a bench with adjustable height. Children should: a) be without shoes or ankle-foot orthosis, b) position each foot on a force plate, c) position feet with shoulder-width apart, d) cross their arms over the chest, f) do not use their arms to push off the chair, g) seat over gluteal and the upper thighs regions (Figure 2B). We allowed the child to move the feet backward or forward, except if their feet moved outside the force plate. The child performed the STS movement at a self-selected speed7. The child performed five trials of STS from three-seat heights, randomly selected by drawing lots: neutral (90° of the knee and ankle flexion), elevated (120% of
5
Journal Pre-proof neutral height) and lowered (80% of neutral)27 (Figure 2B). We selected only three trials where: a) all markers could be tracked, b) the child did not resort to postural control strategies, such as taking a step forward or to the side. Each trial and each seat height were respectively set apart by 30 seconds and five minutes. We recorded, with a digital camera positioned laterally to the child, each trial to observe foot position (Figure 2A). Kinematic data were processed using Visual 3D (Version 3.9; C-motion Inc., USA). Joint coordinate system definitions recommended by the International Society of
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Biomechanics was used to calculate the Cardan Angles (rotation sequence: sagittal,
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frontal, transverse)29 relative to the static standing trial (child standing for ten seconds).
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We computed joint angles during all STS movements. We considered only the angles
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related to flexion and extension (sagittal plane). We applied a 4th-order Butterworth zero-lag filter, cut-off frequency of 4 Hz, to filter kinematic data. By convention,
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positive kinematic values represented trunk, hip, knee and ankle flexion, and anterior
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pelvic tilt. A custom program in Matlab (version 7.0.1, The MathWorks Inc., Natick, USA) was used to determine initial, final, maximal angles, range of motion and STS
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duration. Data from three attempts for each seat height, each joint, each lower limb, and each angle was averaged. Definitions are: a) Initial angle: anterior displacement of the marker placed on the spinous process of 7th cervical vertebrae greater than 2 standard deviations from STS beginning. b) Final angle: anterior displacement of the marker placed on the spinous
process of 7th cervical vertebrae less than 1 standard deviation from the acquisition of standing posture and maximal hip and knee extension. c) Maximal angle: the peak of anterior pelvic tilt; trunk, hip and knee flexion
and ankle dorsiflexion.
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Journal Pre-proof d) Range of motion: the difference between the final and initial angles7; 8.
Kinetic data were processed and filtered (4th order Butterworth filter, with a low pass frequency of 5 Hz) on Matlab. We normalized data by each participants’ body weight. As a kinetic variable, we used the peak vertical ground reaction force. Asymmetry index (AI) was defined as: 100% × (Vnon-preferred − Vpreferred)/(Vnon-preferred + Vpreferred). V represented angles of the hip, knee, and ankle in the sagittal plane and peak vertical force. The magnitude of AI represented the
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degree of asymmetry. The sign of AI represented the direction. The positive index
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indicated a large angle or peak vertical force for non-preferred limb. We classified a
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variable as asymmetric when it fell outside the associated reference range of the healthy
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group, defined as mean ± 2SD of a particular asymmetry index31. The independent variables were seat height (neutral, elevated and lowered),
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group (UCP and typically developing children), and lower limb (preferred and non-
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preferred lower limb). The dominant lower limb of typically developing children and the non-paretic lower limb of children with UCP was the preferred limb. The dominant
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limb was determined by asking which leg the child would use to kick a ball as far as possible28. The dependent variables were temporal (duration of STS), kinematic (initial, final and maximal angles, and range of motion) and kinetic variables (vertical ground reaction force).
Variables presented a normal distribution, analyzed by the Shapiro-Wilk test. The independent T-test verified the differences between groups for the variables duration, and pelvis and trunk angles. The one-way ANOVA compared the hip, the knee, and the ankle angles, and the peak ground reaction vertical force of the preferred limb of typically developing children with both lower limbs of children with UCP. We used a Tukey post hoc test. The repeated ANOVA test compared seat heights. We used
7
Journal Pre-proof SPSS software (version 17.0) to run statistical analysis, with a significance level equal to 0.05.
3. Results
3.1.Comparison Between seats height For both groups, the lowered seat increased: a) the initial angle of both hips and
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knees, b) the trunk flexion represented by increased peak flexion of the trunk and hip,
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c) the peak of the knees, d) the range of motion of the hips, e) the peak vertical ground
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reaction force. For children with UCP, the lowered seat also increased: a) the duration
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of STS, b) the range of motion of both knees and the trunk. For typically developing children, the lowered bench also increased: a) the peak angle of the ankle, b) the range
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motion of the ankle (Figure 3 and Table 2).
3.2.Comparison between groups and lower limbs
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Children with UCP increased pelvic posterior tilt and decreased flexion of both hips for initial, peak, and final angles when compared with typically developing children. As seat height was reduced, children with UCP took a longer time to perform STS, decreased peak of the trunk, increased the peak of both knees, and increased the plantar flexion of the non-preferred lower limb during STS and at the end of the movement. We did not find differences between lower limbs for the peak of vertical force (Figure 3 and Table 3).
3.3.Asymmetry Index
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Journal Pre-proof Children with UCP presented asymmetry for the final and the maximal angles of the ankle in neutral and lowered seats, compared with the non-preferred lower limb (Table 4).
4. Discussion
Our results confirmed our first hypothesis since the lowered seat increased the duration of STS, the trunk flexion and the maximal angle of the knee, and the peak of
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the vertical ground reaction force. The results agreed with previous studies with
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children with CP10; 11. The lowered seat increases task demand requiring an increased
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joint moment of the knee to stand up. When the child increases trunk flexion, the body
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vector line approximates to the knee joint. This strategy facilitates the forward motion of the body and reduces the effort required from knee extensors to stand up32; 33.
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Our second hypothesis was also confirmed since children with UCP adopted an
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adaptive motor strategy to perform STS, especially in the lowered seat, in comparison with typically developing children. The first difference between groups was an
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increased posterior pelvic tilt and a decreased hip flexion on both lower limbs of children with UCP during the entire performance of STS. Studies have found that children with CP usually acquire sitting position with posterior pelvic tilt34; 35. The second difference between groups was that even though children with UCP were able to increase trunk flexion when seat height was reduced, the trunk peak flexion was always inferior to the typically developing children. Children with UCP, therefore, presented limited ability to move the trunk forward when compared to typically developing children. Studies have associated an increased posterior pelvic tilt with decreased pelvic mobility, limited performance of functional activities, and limited forward movement of the body36.
9
Journal Pre-proof The third difference between groups was that children with UCP moved their preferred lower limb backward before standing up from the lowered seat. The adoption of this strategy could be explained by the limitation to increase anterior pelvic tilt and, as a consequence, to move the body forward, similar to typically developing children. Children with UCP, therefore, would require a higher joint moment of the knee in the lowered seat32;
33
. Children with UCP, however, present knee extensor weakness,
especially in the affected limb7. The lower limb that moves backward is responsible for
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weight-bearing and knee extensor torque3. Moving the preferred limb backward,
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therefore, is an adaptative strategy that allows children with UCP to use their stronger
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lower limb to stand up. Similar results have been found in individuals with stroke21; 38.
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The fourth difference between groups was the inability of the non-preferred limb of children with UCP to increase peak flexion of the ankle. We found that children with
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UCP maintained their non-preferred limb in plantar flexion during most of the STS
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trials. One study also found maintained plantar flexion in children with CP10. Our third hypothesis was also confirmed since we found an asymmetry of the
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peak angle of the knee (neutral seat), and of the maximal and the final angles of the ankle (neutral and the lowered seat), in children with UCP. The asymmetries that we found could be associated with the strategy to move the preferred limb backward. We did not find an asymmetry for the peak of vertical ground reaction force between the preferred and the non-preferred lower limbs of children with UCP., which could be explained by the small sample size.
Limitations The main limitation of our study is the small sample size. Also, we used nonprobabilistic recruitment that could affect generalizability and external validity. We also
10
Journal Pre-proof evaluated only children with CP with minimal motor impairment since they were able to perform STS independently. Therefore, our results can be generalized only for this population. Another methodological limitation is the analysis of the relative angles instead of the angles of joints in all movement planes. We restricted foot placement in cases when the children moved their feet backward and placed them outside the force plate, which could modify the motor strategies used to perform STS. Since foot placement
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was restricted, some children may have artificially performed STS, changing motor
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strategies and body alignment.
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The fact that we considered the average of only three repetitions is also a
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limitation of the study. Even though we assessed five repetitions for each child, we had to exclude some repetitions because children moved their feet outside force plate or
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at the moment they stood up.
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because the system could not track all markers or because children gave a step forward
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Clinical implications
Our results demonstrated that even children with CP with less compromised function modified their motor strategies to perform STS movement when task demand increased. The knowledge of the motor strategies most used is important to guide clinical approaches. We verified that children with UCP when compared to typically developing children, during the performance of STS from the lowered seat, presented: a) limited active pelvic and trunk mobility, b) movement of the preferred limb backward, c) compromised ability to increase ankle dorsiflexion, d) increased total duration, e) asymmetry of the ankle. These results show that the environment and the task demands
11
Journal Pre-proof modify the performance of STS. The implementation of a lowered seat in daily routine or at the clinical setting should be carefully analyzed. Rehabilitation strategies to improve pelvic and trunk mobility, weight-bearing at the non-preferred lower limb, and active movement of the ankle seems to be important to facilitate STS when the demand of the task increases, as is the case of the lowered seat.
Acknowledgments
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We would like to thank the staff of the LADI Laboratory –UFSCar, Livia
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Pessarelli and Mariana Martins dos Santos, for their assistance with data collection.
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Funding
This work was supported by the Fundação de Amparo à Pesquisa do Estado de
1
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Table 1 – Exclusion criteria for typically developing children and children with UCP. Criteria Typically developing children Absence of current lower limb injury, neurological or systemic conditions, aged from 6 to 12 years Inclusion Height and weight not in accordance with the expected percentile for age Exclusion Children with Unilateral cerebral Palsy Children with CP, aged between 6 and 12 years Inclusion
Ability to perform STS without support in three-seat height Inability to follow simple commands Muscle contracture in hamstrings, gastrocnemius or hip flexors
l a
Deformity in the lower limbs, such as fixed hip or knee flexion, which could compromise STS
n r u
Exclusion
Orthopedic surgery in the lower limbs in the previous 12 months Botulinum toxin injection in the lower limbs previous in the previous 6 months Height and weight not in accordance with the expected percentile for age a
o J
First assessment, by the researchers
f o
o r p
e
r P
How it was assessed
Stadiometer and digital scalea Diagnosed by a doctor
First assessment, by the researchers Conversation between the therapist and the child Hamstrings: Straight Leg Raise Testb Gastrocnemius: manual test Hip flexors: Modified Thomas Testb Exclusion: negative tests During manual test as described for muscle shortening. Exclusion: any fixed restriction Interview with the caregivers Interview with the caregivers Stadiometer and digital scalea
FILHO, V. C. et al. [Anthropometric indices among schoolchildren from a municipality in Southern Brazil: a descriptive analysis using the LMS method]. Rev Paul Pediatr, v. 32, n. 4, p. 333-41, Dec 2014.
b
MÉLO, T. R.; GUIMARÃES, A. T. B.; ISRAEL, V. L. Repeatability and comparison of clinical tests in children with spastic diplegia and with typical development. Fisioterapia e Movimento, v. 28, n. 1, p. 13 - 22, 2015.
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Journal Pre-proof Table 2 – Statistics data for comparisons between seats height for duration (seconds); angles of trunk, pelvis, hip, knee and ankle (º), and peak vertical force (N/V/Kg) during sit to stand movement. Comparasions
p
Mean difference
95% CI mean difference
Lowered > Elevated
p≤0.01
0.9
0.5 / 1.3
Repeated ANOVA
Healthy
Maximal
Trunk
maximal
Lowered > Neutral
p=0.03
0.5
0.1 / 1.0
Lowered > Elevated
p≤0.01
9.8
5.7 / 13.9
Lowered > Neutral
p≤0.02
7.0
4.6 / 9.4
Lowered > Elevated
p≤0.01
1.1
6.6 / 15.6
Lowered > Neutral
p=0.039
2.9
0.2 / 5.6
F=19.57; p≤0.01; η2p=0.5
F=22.36; p≤0.01; η2p=0.7
UCP
F=22.36; p≤0.01; η2p=0.7
UCP
F=6.68; p=0.006; η2p=0.4
Neutral > Elevated
p=0.002
8.2
3.9 / 12.4
Lowered > Elevated
p≤0.01
11.1
6.6 / 15.6
Lowered > Neutral
P=0.039
2.9
0.2 / 5.6
Neutral > Elevated
P=0.002
8.2
3.9 / 12.4
Lowered > Elevated
p=0.19
4.9
1.0 / 8.7
Neutral > Elevated
p≤0.01
4.8
2.7 / 6.3
Lowered > Elevated
p≤0.01
16.8
12.9 / 20.6
Lowered > Neutral
p≤0.01
7.5
4.7 / 10.3
Neutral > Elevated
p≤0.01
9.3
6.1 / 12.4
Lowered > Elevated
p≤0.01
10.8
7.4 / 14.2
Lowered > Neutral
p≤0.01
4.6
2.6 / 6.5
Neutral > Elevated
p≤0.01
6.2
3.6 / 8.9
Lowered > Elevated
p≤0.01
14.2
10.9 / 17.5
Lowered > Neutral
p≤0.01
4.6
2.9 / 6.3
Neutral > Elevated
p=0.002
9.6
6.2 / 12.9
Lowered > Elevated
p≤0.01
17.6
14.4 / 20.8
Lowered > Neutral
p≤0.01
9.1
6.3 / 11.8
Neutral > Elevated
p≤0.01
8.5
5.4 / 11.6
Lowered > Elevated
p≤0.01
16.5
9.7 / 23.2
Neutral > Elevated
p=0.003
2.9
4.8 / 17.8
Lowered > Elevated
p=0.001
17.1
8.3 / 25.8
Lowered > Neutral
p=0.012
9.3
2.5 / 16.0
Neutral > Elevated
p=0.001
7.8
4.3 / 11.2
Lowered > Elevated
p≤0.01
22.6
17.6 / 27.5
Lowered > Neutral
p=0.001
14.3
8.0 / 20.6
Neutral > Elevated
p=0.013
8.3
2.2 / 14.3
Lowered > Elevated
p≤0.01
10.8
7.4 / 14.2
Lowered > Neutral
p≤0.01
4.6
2.6 / 6.5
Neutral > Elevated
p≤0.01
6.22
3.6 / 8.9
Lowered > Elevated
p≤0.01
30.1
21.0 / 38.4
Lowered > Neutral
p≤0.01
18.0
13.1 / 22.9
Neutral > Elevated
p=0.002
12.1
6.0 / 18.1
Lowered > Elevated
p≤0.01
15.6
5.2 / 26.0
Neutral > Elevated
p≤0.01
6.7
1.9 / 11.4
-p
Pelvis
Range of motion
UCP
F=12.83; p≤0.01; η2p=0.6
of
UCP
ro
Duration
Healthy
Hip
Range of motion
UCP
F=76.07; p≤0.01; η2p=0.8
UCP
F=15.05; p=0.003; η2p=0.6
UCP
Healthy
Maximal Knee
re
Healthy
Healthy
Initial
F=36.01; p≤0.01; η2p=0.7 F=22.36; p≤0.01; η2p=0.7
Jo ur
Maximal
F=59.06; p≤0.01; η2p=0.8
lP
Healthy
na
Initial
UCP
Range of motion Healthy
F=16.15; p=0.001; η2p=0.6
F=41.53; p≤0.01; η2p=0.8
F=64.01; p≤0.01; η2p=0.9
F=56.34; p≤0.01; η2p=0.9 F=8.23; p=0.09; η2p=0.4
20
Journal Pre-proof
UCP Healthy Healthy
23.1
17.8 / 28.4
Lowered > Neutral
p=0.001
15.1
8.6 / 21.6
Neutral > Elevated
p=0.007
8.0
2.9 / 13.1
Lowered > Elevated
p=0.002
6.6
3.0 / 10.1
Lowered > Neutral Lowered > Elevated
p=0.041 p≤0.01
4.7 0.9
0.2 / 9.2 0.8 / 01.0
Neutral > Elevated
p≤0.01
1.0
0.8 / 1.1
Lowered > Elevated
p≤0.01
1.0
0.9 / 1.1
Neutral > Elevated
p≤0.01
1.0
0.9 / 1.1
F=45.68; p≤0.01; η2p=0.8 F=6.48; p=0.007; η2p=0.4 F=453.30; p≤0.01; η2p=0.9
F=267.58; p≤0.01; η2p=1.0
na
lP
re
-p
ro
of
UCP
p≤0.01
Jo ur
Ankle Maximal Peak vertical force
Lowered > Elevated
21
Journal Pre-proof Table 3 – Statistics data for comparisons between Unilateral Cerebral Palsy (UCP) and typically developing children for duration (seconds); and angles of trunk, pelvis, hip, knee and ankle (º) during sit to stand movement.
Independent T-Teste
Comparasions
Mean difference
95% CI mean difference
t=2.61; p=0.023
UCP > Healthy
0.3
-0.1 / 0.7
Duration Lowered t=1.45; p=0.174 t=-3.34; p=0.002 Elevated t=-2.64; p=0.013 Trunk Maximal Lowered
UCP > Healthy
0.6
0.1 / 1.1
Elevated t=-5.09; p≤0.01 Neutral t=-6.55; p≤0.01
Neutral
UCP < Healthy
-20.4
-27.3 / -13.4
Lowered t=-6.00; p≤0.01
UCP < Healthy
-22.0
-28.9 / -15.1
Elevated t=-6.62; p≤0.01 Neutral t=-4.37; p≤0.01
UCP < Healthy
-22.2
-29.0 / -15.3
UCP < Healthy
-17.5
-25.4 / -9.5
UCP < Healthy
-18.5
-27.1 / -9.9
UCP < Healthy
-21.1
-27.4 / -14.7
UCP < Healthy
-22.2
-29.1 / -15.3
UCP < Healthy
-20.9
-27.6 / -14.1
-19.3
-29.8 / -8.8
-18.7
-29.2 / -8.2
-13.0
-21.2 / -4.9
-12.4
-20.6 / -4.3
-14.8
-26.0 / -3.6
-13.8
-24.9 / -2.6
-14.7
-25.9 / -3.4
-13.6
-24.9 / -2.4
-19.3
-29.8 / -8.8
-18.68
-29.2 / -8.2
-13.02
-21.2 / -4.9
-12.42
-20.6 / -4.3
-19.2
-30.1 / -8.4
-19.2
-30.0 / -8.4
-16.1
-26.9 / -5.3
-16.1
-26.9 / -5.2
ro
of
UCP < Healthy
re
Final
Lowered t=-6.31; p≤0.01
F=11.23; p≤0.01
Jo ur
Elevated
na
lP
ANOVA
Neutral
Initial
Hip
-16.5 / -3.9 -21.0 / -2.6 -25.2 / -10.6
Elevated t=-6.76; p≤0.01 Neutral t=-6.59; p≤0.01 Pelvis
-10.2 -11.8 -17.9
Maximal Lowered t=-4.42; p≤0.01
UCP < Healthy
-p
Initial
UCP < Healthy
Lowered
Maximal Elevated
F=7.53; p≤0.01
F=15.04; p≤0.01
F=19.57; p≤0.01
Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy
22
Journal Pre-proof
F=12.56; p≤0.01
F=8.26; p≤0.01
Lowered
Maximal Lowered Knee
Final
Lowered
Neutral Maximal Lowered Neutral
Ankle
Final
F=4.61; p=0.006;
Jo ur
Final
na
lP
Neutral
re
-p
Elevated
F=19.57; p≤0.01
Lowered
F=7.31; p≤0.0 F=3.74; p=0.016
F=3.47; p=0.022 F=5.20; p=0.003 F=3.74; p=0.016
F=4.27; p=0.009
-13.8
-23.9 / -3.7
-13.0
-23.1 / -2.9
-13.8
-23.8 / -3.7
-12.9
-23.1 / -2.9
-14.2
-25.6 / -2.8
-12.8
-24.2 / -1.4
-16.7
-27.7 / -5.7
-14.7
-25.7 / -3.7
-13.6
-24.6 / -2.6
-11.7
-22.7 / -0.7
-16.1
-26.8 / -5.4
-12.4
-22.9 / -1.9
-16.0
-26.7 / -5.4
-12.4
-22.8 / -1.9
-12.1
-23.6 / -0.6
-10.1
-21.7 / 1.3
-12.1
-23.6 / -0.6
-10.1
-21.6 / 1.4
14.0
3.3 / 24.8
11.3
0.6 / 22.1
-10.5
-20.6 / -0.4
-8.5
-15.3 / -1.8
-6.7
-12.6 / -0.7
-7.0
-12.9 / -1.2
-9.9
-18.2 / -1.5
-12.6
-21.4 / -3.8
-8.4
-16.2 / -0.7
of
Lowered
F=19.57; p≤0.01
ro
Neutral
Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Non-Prefered Healthy Prefered UCP < Prefered Healthy Prefered UCP < NonPrefered Healthy Non-prefered UCP > Non-Prefered Healthy Prefered UCP > NonPrefered Healthy Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered Healthy Non-prefered UCP < Prefered Healthy Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered UCP Non-prefered UCP < Prefered Healthy
23
Journal Pre-proof Table 4 – Asymmetry index (%) of hip, knee and ankle during STS movement from elevated, lowered and neutral seats, in typically developing children and children with unilateral Cerebral Palsy (UCP). HIP
KNEE
DP Typical UCP Typical Typical Elevated
-0.6
UCP
ANKLE DP DP Typical Typical UCP Typical
*8.6
4.2
-1.6
1.6
6.0
-0.9
1.6
2.9
-0.9
0.8
4.1
-2.3
2.3
5.3
-1.3
2.9
2.6
-1.1
-0.8
3.6
-2.5
2.5
3.6
-1.2
1.5
2.1
Elevated
0.0
2.8
3.8
-0.5
0.5
4.6
0.1
3.4
3.2
Neutral
-0.5
0.4
3.1
-2.0
2.0
4.5
-0.6
*4.7
1.5
Maximal Lowered
-0.7
-2.8
3.1
-2.8
2.8
4.0
-1.1
*4.7
1.9
Elevated
7.8
-8.7
53.4
15.8
26.5
Neutral
46.0
68.6
-8.28
Lowered
23.8
8.2 249.1
262.8
24.2
Elevated
-1.6
3.8
7.3
Range of Neutral Motion Lowered
-1.1
3.1
5.6
-1.5
3.9
5.4
Elevated
-4.2
5.2
11.2
-0.1
*3.3
1.4
*364.4
22.57
-0.6
*4.7
1.0
-24.2
37.1
-0.5
*5.8
1.5
-p
ro
-15.8
-1.3
1.3
6.3
6.5
36.6
35.9
-1.3
1.3
6.2
10.1
10.7
19.8
2.6
3.9
6.9
24.4
18.4
re
Final
of
Neutral Lowered
Initial
-2.6
Jo ur
na
lP
5. -2.0 17.2 Vertical Neutral -6.3 -2.4 44.6 Force Lowered * Asymmetric index superior to mean ± 2 standard deviation of typically developing children.
24
Journal Pre-proof Figure Legends:
Figure 1 - Flowchart of selection and inclusion of children.
of
Figure 2 – Kinematic curves of the trunk, pelvis and preferred lower limb of a typically developing child, and the preferred and non-preferred lower limbs of a child with Unilateral Cerebral Palsy, during sit to stand movement. The figures refer to sagittal plane, where negative values represent extension and positive values represent flexion for trunk and lower limbs. For pelvis, negative values represent posterior tilt and positive values anterior tilt. Joints: Ankle (pink), Knee (green), Hip (red), Trunk (blue) and Pelvis (black). a: Unilateral Cerebral Palsy = preferred limb. b: Unilateral Cerebral Palsy = non-preferred lower limb
Jo ur
na
lP
re
-p
ro
Figure 3- Study set up.
25
Journal Pre-proof CRediT Author Statement
Adriana
Neves
dos
Santos:
Investigation;
Methodology;
Project
administration; Software; Visualization; Roles/Writing – original draft; Writing – review & editing
Gisele Moreira Pena: Investigation; Roles/Writing – original draft; Writing –
ro
of
review & editing
-p
Evelyn Maria Guilherme: Investigation; Roles/Writing – original draft;
re
Writing – review & editing
Jo ur
na
review & editing; Resources
lP
Nelci Adriana Cicuto Ferreira Rocha: Investigation; Methodology; Writing –
26
Journal Pre-proof Highlights
na
lP
re
-p
ro
of
Lowered seat leads to lower limb asymmetry in unilateral cerebral palsy. Pelvic mobility is compromised in cerebral palsy, especially in a lowered seat. Ankle asymmetry is increased in the lowered seat. Sit-to-stand movement is influenced by extrinsic factors such as seat height.
Jo ur
27
Figure 1
Figure 2
Figure 3