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Postural Orientation During Standing in Children With Bilateral Cerebral Palsy ˚ Bartonek, PT, PhD Cecilia M. Lidbeck, PT, MSc; Elena M. Gutierrez-Farewik, PhD; Eva Brostr¨om, PT, PhD; Asa Department of Women’s and Children’s Health (Ms Lidbeck and Drs Gutierrez-Farewik, Brostrom, ¨ and Bartonek) Karolinska Institutet, Stockholm, Sweden; KTH Mechanics (Dr Gutierrez-Farewik), Royal Institute of Technology, Stockholm, Sweden.

Purpose: To investigate postural orientation and maintenance of joint position during standing in children with bilateral spastic cerebral palsy (BSCP). Methods: Standing was examined with 3-D motion analysis in 26 children with BSCP, and 19 children typically developing (TD). Two groups of children with cerebral palsy (CP) were analyzed: 15 who were able to maintain standing without support and 11 who needed support. Results: Children with CP stood with more flexion than children TD. In the CP groups, children standing without support stood more asymmetrically with less hip and knee flexion and less movement than those who required support. Conclusion: Children with CP had varying abilities to stand and maintain standing posture with or without support. Both CP groups stood with more flexion than their potential passive joint angle, more obvious in children requiring support. Investigations on how muscle strength and spatial perception influence posture remains to be explored. (Pediatr Phys Ther 2014;26:223–229) Key words: activity of daily living, cerebral palsy, child, joint range of motion, kinematics, postural balance, posture INTRODUCTION Postural control requires a continuous interaction between the individual, the task, and the environment and involves the individual’s musculoskeletal and neural systems.1 In cerebral palsy (CP), motor functions are affected by disturbances in the development of movement and posture with atypical postural and motor control due to an early damage to the immature brain.2 The motor disorder may be characterized by spasticity, hyperreflexia and cocontraction, as well as by weakness, loss of selective motor control, and deficient balance.3 The consequences of

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Correspondence: Cecilia M. Lidbeck, PT, MSc, Motoriklab Q2:07, Astrid Lindgren Children’s Hospital, Karolinska University Hospital, 171 76 Stockholm, Sweden ([email protected]). Grant support: This study was supported by The Frimurare Barnhuset Foundation and Promobilia Foundation in Stockholm, Sweden. The authors declare no conflict of interest. DOI: 10.1097/PEP.0000000000000025

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the neural features may lead to musculoskeletal deformities and deterioration of walking ability.4 A recent definition of CP includes cognition, sensation, and perception as accompanying disturbances, in addition to musculoskeletal problems.2 In children with spastic diplegia, the lack of effective anticipatory postural adjustments indicates that not only do motor and postural disorders but also perceptive impairments strongly influence motor control strategies.5 The main rehabilitation goals for children with CP are to support and facilitate each individual’s mobility. Gait in children with spastic uni- and bilateral CP with independent walking ability has been comprehensively documented. Even though standing ability has functional consequences for many daily activities, few studies describing standing ability in this patient population have been published; standing posture in children with CP has predominantly been reported in terms of postural equilibrium, which involves coordination of movement strategies to stabilize the center of body mass following self-initiated or unexpected environmental changes.6,7 In studies measuring reactive balance control during standing on a platform, larger center of pressure displacements under altered sensory conditions and a longer time to recover from perturbations were found in children with CP compared with children typically developing (TD).8 During standing on

Standing Posture in Children With CP

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a movable platform, children with CP also activated all joints simultaneously with altered joint torque patterns.9 To achieve voluntary standing, the ability for postural orientation, that is, the maintenance of posture, and the active alignment of body segments with respect to gravity, support surfaces, visual information, and internal references are required.6,7 Standing in both children TD and children with CP was observed to be affected by an inclined surface, wherein a strain to the gastrocnemius muscle resulted in a flexed body posture, with a lower threshold in children with CP.10 The effect of modifying the support area with heel lifts also showed varying results in children with bilateral spastic CP (BSCP) and children TD. Whereas children with BSCP reorganized their posture, namely with increasingly flexed ankles and knees and increased pelvic anterior tilt with increasing heel heights, the children TD only responded by changing angles at the ankle.11 Orthoses with supramalleolar design in children with spastic diplegia did not affect the mainly flexed joint position observed in barefoot standing.12 Although postural equilibrium has been extensively reported in children with CP, postural orientation has not been studied to the same extent. In clinical practice, we see children with CP with various abilities to self-align during quiet standing, but we lack reference data for comparison. The aim of this study was to investigate postural orientation, that is, body segment alignment and maintenance of joint position, during quiet standing in children with BSCP.

level I, 9 in level II, and 3 in level III. In CP group B 8 children were in GMFCS level III and 3 in level IV. Nineteen children TD (12 girls and 7 boys, median [range]: 8.9 [5.8, 12.9] years) constituted a control group. All children with CP underwent a clinical examination by the same physiotherapist. Passive joint range of motion (ROM) measurements were performed with a goniometer in the sagittal plane at the hip, knee, and ankle.13 Lower limb contractures were defined as passive ROM less than the neutral joint position. Spasticity was assessed with the modified Ashworth scale in the hip flexors, the knee flexors and extensors, and the plantar flexors.14 Prior orthopedic surgery and neurosurgery were documented as well as the use of ankle-foot orthoses (AFOs). Ethical approval by the local ethics committee, parental consent, and subject assent were obtained. Instruments All children were tested in a 3-D 8-camera motion analysis (Vicon MX40, Oxford, United Kingdom) using a full-body biomechanical model with 34 retroreflective markers. Lower body kinematics were analyzed on the basis of the Newington model15 and the upper body according to the Plug-In-Gait model (Vicon). The thorax and pelvic segments were described in the global coordinate frame and the hip, knee, and ankle joints as relative angles between distal and proximal segments. In the children who used orthoses, the markers were placed as near as possible to the anatomical joint position.

METHODS The study was designed as a cross-sectional descriptive study. Participants A consecutive series of 32 children with BSCP referred to Astrid Lindgren Children’s Hospital were invited to participate. Inclusion criteria were the ability to stand independently with or without the use of hand support with habitual shoes and orthoses for at least 30 seconds, as well as the ability to understand instructions for performing the examinations. Exclusion criteria were treatment with focal spasticity reduction during the previous 3 months or orthopedic surgery during the previous year. Six children were excluded, 3 due to dyskinetic CP and 3 due to insufficient standing ability; thus 26 children participated in the study. Children with CP were grouped according to their ability to achieve and maintain standing posture. Fifteen children (4 girls and 11 boys, median [range] age: 10.2 [5.6, 16.2] years) with the ability to achieve and maintain standing without support were designated as CP group A, and the 11 children (6 boys and 5 girls, median [range]: 10.8 [4.4, 16.8] years) who needed support were designated as CP group B. In CP group A, 3 children were classified in Gross Motor Function Classification System (GMFCS) 224

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Procedures Standing was recorded for 30 seconds while the children stood in front of a frame with a height-adjustable handrail. Children were instructed to maintain a quiet standing position; the children who required hand support to achieve and maintain standing held the handrail with a slightly flexed elbow position. All children were tested with their habitual footwear and orthoses. Video observation with 2 digital cameras was performed simultaneously from sagittal and frontal views. Data Analysis Data from the more weight-bearing limb, assessed through video observations, were used for analysis. When standing asymmetry in the children with CP was not visually apparent, and in all children TD, data from the right limb were used. All available recorded frames with complete marker data from each child’s standing trial were analyzed (median [range]: 20 [8, 20] seconds). The mean and SD sagittal plane angles from 3-D motion analysis of trunk and pelvic segments and hip, knee, and ankle joints were used to describe the children’s standing posture. Ranges of joint movements during the period of standing, defined as the differences between maximum and minimum angles, were used to describe maintenance Pediatric Physical Therapy

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of segment and joint position during the recorded time. Trunk values were not available for 2 children, 1 in each of the CP groups, due to nonacceptance of trunk markers. Sagittal plane passive joint ROM from the clinical examination in the hip, knee, and ankle was used to compare unloaded joint conditions versus joint angles during standing. Statistical Analysis Nonparametric statistical analyses were carried out using the statistical program SPSS 19.0 (Chicago, Illinois). Significant differences were determined at the α ≤ 0.05 level. Comparisons of age, weight, height, segment and joint angles and movements between the children in the 2 CP groups and the children TD were calculated with a Kruskal-Wallis test. To determine further differences, a post hoc Mann-Whitney U test was used. The test also was used for comparing joint/segment angles between standing with shoes only and standing with orthoses in CP group A. Prior surgical procedures, presence of joint contractures and spasticity, and use of AFOs were compared between the CP groups using a chi-square (χ 2 ) test. A Wilcoxon signed rank test was used to compare leg length and joint angle asymmetry during standing between the more and less weight-bearing limbs and to compare passive joint ROM with joint angles during standing in the more weightbearing limb. RESULTS Participants The Kruskal-Wallis test results indicated no differences in age, weight, or height between the children in the 2 CP groups and the children TD. No statistical differences were found in number of prior orthopedic surgeries in the more weight-bearing limb between the 2 CP groups (7 in CP group A vs 5 in CP group B, χ 2 = 0.004, P = 1.000). Achilles and/or soleus lengthenings were performed in 6 of 7 children in CP group A and in 4 of 5 children in CP group B. Combinations of 2 to 4 soft tissue procedures, in total 12, were performed in 5 children in CP group A and 8 procedures were performed in 3 children in CP group B, with lengthenings of hamstring, adductor, Achilles tendon, soleus, and/or tibialis posterior. One child in each group had undergone a femoral osteotomy. Selective dorsal rhizotomy had been performed in 1 child in each group. No statistical difference was found in number of joint contractures in the support limb between the CP groups A and B at the hip (2 vs 5, χ 2 = 3.328, P = .095) and the ankle (1 vs 2, χ 2 = 0.824, P = .556), but a difference was seen at the knee (5 vs 9, χ 2 = 6.003, P = .021). The MannWhitney test indicated that CP group A presented with less severe contractures and greater passive joint ROM than CP group B in hip extension (median [range]: 0◦ [−10, 10] vs 0◦ [−15, 0], P = .041), knee extension (0◦ [−10, 10] vs −10◦ [−30, 0], P = .001), and in ankle dorsiflexion (10◦ [−10, 20] vs 0◦ [−15, 35], P = .009). Pediatric Physical Therapy

Using the χ 2 test, no significant difference was found in the presence of spasticity between the children in CP groups A and B, in the hip flexors (3 vs 6, χ 2 = 3.346, P = .103), the knee flexors (12 vs 11, χ 2 = 2.487, P = .238), the plantar flexors (14 vs 10, χ 2 = 0.053, P = 1.000), and the Duncan Ely test (8 vs 8, χ 2 = 2.006, P = .333). Knee extensor spasticity was significantly less frequent in CP group A than in CP group B (5 vs 9, χ 2 = 6.003, P = .021). Asymmetry From video observation, asymmetric weight-bearing during standing was observed as frontal plane weight shift to 1 side in 22 children; 13 of 15 in CP group A and in 9 of 11 in CP group B. Between the 2 sides, the children in CP group A stood with significantly less knee flexion in the more weight-bearing limb (median [range]: 16.6◦ [−6.1, 46.9]) than in the less weight-bearing limb (24.1◦ [1.6, 56.3], P = .015). In CP group B no difference was found in knee flexion between the limbs (45.0◦ [27.9, 94.5] vs 46.2◦ [29.7, 91.4], P = .594). Three children in CP group A and 2 in CP group B presented with a leg length difference between 20 and 35 mm, but no statistical difference in leg length was observed in either CP group A (P = .528) or B (P = .063) using the Wilcoxon signed rank test. In the children TD, a statistical difference of 2◦ in hip flexion was found between the more and less weight-bearing limbs; however, the difference was interpreted to be of no clinical relevance. Segment and Joint Angles During Standing Segment and joint angles during standing are presented in the Table and Figure 1a. Identified differences between the groups are presented in the text. The children TD stood with significantly more extended trunks than the children in CP group A (P = .001) and CP group B (P = .002), wherein both groups stood with forward leaning trunks. No significant difference was found in trunk tilt between the children in CP group A and CP group B (P = .114). Both the children TD and the children with CP stood with anteriorly tilted pelvic positions. The children TD stood with significantly more hip extension than children in CP group A (P < .001) and CP group B (P < .001), both groups standing with increased hip flexion, significantly more in CP group B than in CP group A (P = .040). The children TD stood with hyperextended knees, significantly more than children in CP group A (P < .001) and CP group B (P < .001), both groups standing with flexed knees, significantly more in CP group B than in CP group A (P < .001). The children TD stood with the ankle joint in a nearly neutral position compared with children in CP group A, who stood with significantly more dorsiflexion (P < .001). No differences in the ankle were identified between the children TD and the children in CP group B (P = .505). No significant difference was found in the ankle between the CP groups A and B (P = .659). Standing Posture in Children With CP

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TABLE 1 Potential Passive Joint ROM in Degrees, Median [Range], in CP Group A (Without Support) and CP Group B (With Support) (Calculated With Mann-Whitney U Test)a TD n Passive ROM Hip extension Knee extension Ankle dorsiflexion Segment and joint angles during standing Trunk Pelvis Hip Knee Ankle Movement range during standing Trunk Pelvis Hip Knee Ankle

CP Group A

CP Group B

Median [Range]

n

Median [Range]

n

Median [Range]

P

NA NA NA

15 15 15

0 [−10, 10]b 0 [−10, 10]c 10 [−10, 20]d

11 11 11

0 [−15, 0]b −10 [−30, 0]c 0 [−15, 35]d

.041 .001 .009

19 19 19 19 19

−5.2 [−15.1, 6.3]e 14.6 [5.1, 24.8] 5.0 [−4.1, 15.7]b −4.5 [−15.6, 0.5]c −0.4 [−9.3, 10.0]d

14 15 15 15 15

2.0 [−6.5, 25.8]e 15.9 [−1.8, 28.7]f 18.4 [7.3, 32.4] 16.6 [−6.1, 46.9]c 12.7 [−0.4, 33.1]d

10 11 11 11 11

12.2 [−14.5, 34.0]e 12.5 [−9.5, 25.4]f 30.7 [−1.9, 54.0]b 45.0 [27.9, 94.5] 8.5 [−19.0, 57.8]d

Postural orientation during standing in children with bilateral cerebral palsy.

To investigate postural orientation and maintenance of joint position during standing in children with bilateral spastic cerebral palsy (BSCP)...
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