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Walking on uneven ground: How do patients with unilateral cerebral palsy adapt?
Clinical Biomechanics 74 (2020) 8–13
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Walking on uneven ground: How do patients with unilateral cerebral palsy adapt? Jacqueline Romkesa, Marie Fresliera, Erich Rutza,b, Katrin Bracht-Schweizera, a b
T
⁎
Laboratory for Movement Analysis, University of Basle Children's Hospital Basel (UKBB), Switzerland Neuro-Orthopaedic Unit, University of Basle Children's Hospital Basel (UKBB), Switzerland
A R T I C LE I N FO
A B S T R A C T
Keywords: Unilateral cerebral palsy Gait analysis Uneven ground Gait adaptations
Background: Children with cerebral palsy experience movement disorders that influence gait stability. It is likely that gait stability further decreases when walking on uneven compared to even ground. Therefore, the aim of this study was to investigate gait on uneven ground in children with unilateral cerebral palsy. Methods: Twenty children with unilateral cerebral palsy and twenty typically developing children performed a three-dimensional gait analysis when walking on even and uneven ground. Spatio-temporal parameters, fullbody joint kinematics and centre of mass displacements were compared. Findings: On uneven versus even ground, both groups showed decreased cadence, increased stance phase and double support time, increased toe clearance height, and increased knee and hip flexion during swing phase. Whereas only the typically developing children walked slower and had increased dorsiflexion and external foot progression during stance phase, only the patients showed increased stride width, increased elbow flexion (affected and non-affected side), and kept the centre of mass more medial when standing on the affected leg. Interpretation: Patients and healthy children use similar adaptation mechanisms when walking on uneven ground. Both groups increased the toe clearance height by increasing knee and hip flexion during swing. However, whereas patients enlarge their base of support by increasing stride width, healthy children do so by increasing their external foot progression angle. Furthermore, patients seem to feel more insecure and hold their arms in a position to prepare for falls on uneven ground. They also do not compensate with their non-affected side for their affected side on uneven ground.
1. Introduction According to Rosenbaum et al. (2007) cerebral palsy (CP) “describes a group of permanent disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing fetal or infant brain.” In patients with unilateral CP (uni-CP) the arm and leg primarily of one body side are involved. In these patients, toe-walking is the most common kinematic deviation (64%), followed by stiff knee gait (56%), in-toeing (54%) and excessive hip flexion (48%) (Wren et al., 2005). The gait deviations can lead to gait instability (Bruijn et al., 2013), loss of harmony, and tripping or falling (Iosa et al., 2012; Wren et al., 2005). Other factors influencing the loss of gait stability in patients with CP include sensory impairment, deficient equilibrium reactions (Gage, 1991), loss of selective muscle control, increased upper body motion (Galli et al., 2012; Schweizer et al., 2014) and centre of mass (CoM)
sway (Hsue et al., 2009). It is likely that gait instability further increases when walking on uneven terrain, such as forest soil or on cobble stone pavement. Unlike patients, healthy subjects have a variety of adaptation mechanisms to adjust their movement patterns when walking on different surfaces. One of these mechanisms is to lower the CoM by increasing knee and hip flexion and ankle dorsiflexion (Gates et al., 2012) when stepping from a flat surface onto a soft (MacLellan and Patla, 2006), slippery (Marigold and Patla, 2002), or destabilising loose rock (Gates et al., 2012) surface. MacLellan and Patla (2006) reported that dynamic stability on a soft foamy surface can be maintained by enlarging the base of support by increasing step width and step length. These changes in spatio-temporal parameters were, however, not supported by Gates et al. (2012) when walking on a loose rocky surface compared to flat ground. Other adaptation mechanisms that are mentioned in the literature to adjust walking on uneven or irregular ground are the
⁎ Corresponding author at: Children's University Hospital Basel (UKBB), Laboratory for Movement Analysis, c/o University of Basel, Spitalstrasse 33, Postfach, 4031 Basel, Switzerland. E-mail address: [email protected] (K. Bracht-Schweizer).
https://doi.org/10.1016/j.clinbiomech.2020.02.001 Received 10 December 2018; Accepted 6 February 2020 0268-0033/ © 2020 Elsevier Ltd. All rights reserved.
Clinical Biomechanics 74 (2020) 8–13
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inclusion criteria for both groups were age between 8 and 18 years and a body mass index below 85th percentile (WHO Body Mass Index-forage standards). Children younger than 8 years were excluded to ensure that the children were able to stay concentrated for the entire measurement session, which took around 2 h. The patients with uni-CP should have a level I or II on the Gross Motor Function Classification System (GMFCS) (Palisano et al., 1997) and be able to walk without assistance or assistive devices. The vast majority of children with uniCP generally falls into this category. Exclusion criteria for this group were: Botulinum toxin type A injections within six months prior to the measurements, surgery within one year prior to the measurements, Baclofen or selective dorsal rhizotomy. These treatments may influence the gait performance considerably. Patients with ataxia, dystonia and reduced vision despite wearing glasses were also excluded, since these factors only exist in a minor group of children and do not represent the group as a whole. Exclusion criteria for the TD group were: any neurological or orthopaedic impairment, major lower limb surgery and a leg length discrepancy > 1% body height. The study was approved by the local ethical committee and all subject signed an informed consent.
increase of step time and step width variability, the change in stance phase duration, and an increased foot height (Böhm et al., 2014; Finlay and Beringer, 2007; Gates et al., 2012; MacLellan and Patla, 2006; Schulz, 2011; Thies et al., 2005). Based on the literature, we expect that children with uni-CP have limited abilities to adapt their walking pattern to more challenging surfaces, such as uneven ground. To date, only few studies have explored walking on uneven ground in patients with CP. Böhm et al. (2014) studied the spatio-temporal parameters and joint kinematics in patients with diplegic CP and stiff knee gait when walking on uneven ground. They found that patients and healthy subjects similarly adapted walking speed, step length, and cadence when walking on uneven ground, but only the patients increased step width. Although the patients walked with reduced knee flexion during swing phase on even ground (stiff-knee gait) compared to healthy subjects, the patients were able to adapt to uneven ground with increased knee flexion during swing similar to the healthy subjects (Böhm et al., 2014). Based on these results the authors rejected the hypothesis that the spasticity of the rectus femoris muscle in patients with CP limits toe-clearance. Malone et al. (2015) reported that the maximum distance between the CoM and centre of pressure was lower in patients with CP when walking on uneven ground compared to healthy controls. Malone et al. (2015) further reported adaptations to uneven ground including reduced hip extension and ankle movement in the sagittal and coronal planes in the control subjects, but not in the patients with CP. However, this study included a mix of patients with uni- and bilateral CP, which may have influenced the results. Up till now, no study has investigated the gait adaptations in uni-CP patients on uneven ground. As opposed to patients with bilateral CP, uni-CP patients have a non-affected body side, which they could, theoretically use to compensate for the impaired side. Limitations when walking on uneven ground may have profound effects on the patients' ability to participate in outdoor activities with their healthy peers (Malone et al., 2015). Therefore, to gain knowledge on the adaptive possibilities is of high clinical relevance to improve therapy and training concepts in uni-CP. The research question for this study was: Do children with uni-CP experience more difficulties than typically developing (TD) children when walking on uneven ground compared to even ground? Our hypotheses were that: 1) Uni-CP patients use different adaptation mechanisms to uneven ground compared to TD children regarding the spatio-temporal parameters and the three dimensional whole body kinematics, 2) The non-affected side of uni-CP patients compensates for the affected side on uneven ground by showing greater adaptation mechanisms than the affected side, and 3) Uni-CP patients have limited adaptation mechanisms compared to TD children when walking on uneven ground.
2.2. Experimental protocol The subjects performed two testing conditions, namely walking on even and uneven ground, during a single measurement session. The uneven ground was a 6 m long by 1 m wide walkway, consisting of 24 floor panels (50 × 50 × 4–8 cm, Terrasensa, Hübner GmbH, Kassel, Germany). The surface is a relief system made from polyurethane which is comfortable to walk on and shock absorbing. The two walking conditions were performed barefoot at a comfortable self-selected walking speed and the order of the conditions was randomised among the subjects. The subjects were allowed one practice trial on the uneven ground for familiarisation, before performing 7 trials that were recorded. The even ground condition was performed directly underneath the uneven walkway, resulting in a 3–5 min resting period for the subjects between the conditions while placing or removing the uneven walkway. Full-body kinematic data were collected at 150 Hz with a 12-camera Vicon Motion Capture system (Vicon Inc., Oxford, UK) using the Plugin-Gait marker-set (9 mm in diameter) and model (lower body: Kadaba et al. (1990), upper body and whole body CoM: Gutierrez et al. (2003)). A knee alignment device was applied in a static trial to define the knee flexion axis (Motion Lab Systems Inc., Los Angeles, USA). The same static trial was used for both walking conditions. For each walking condition, data collection continued until seven error-free-trials were recorded. Errors that occurred in disregarded trials included disappearing markers (gaps in any marker trajectory), the subject stopping/accelerating/decelerating/stumbling, or unforeseen data collection errors.
2. Methods 2.3. Data analysis 2.1. Subjects The Nexus software (Version 2.5, Vicon Inc., Oxford, UK) was used for data collection and post-processing of the raw kinematic data. First, the gait cycles were determined by visually defining gait events (foot
Between November 2017 and October 2018, 20 children diagnosed with spastic uni-CP and 20 TD children participated (Table 1). The
Table 1 Group details. Uni-CP: children with unilateral cerebral palsy, TD: typically developing children, GMFCS: Gross Motor Function Classification System, M: male, F: female, R: right, L: left, NA: not applicable. Group
Parameter N
Uni-CP TD
20 20
Gender
Age (years)
Height (m)
Weight (kg)
Affected side
GMFCS
M/F
Mean [range]
Mean [SD]
Mean [SD]
R/L
Level I/II
13 M/7 F 10 M/10 F
10.8 [8.3–17.7] 11.4 [7.6–16.7]
1.42 [0.15] 1.47 [0.18]
33.2 [10.3] 37.3 [12.0]
13 R, 7 L NA
18 I, 2 II NA
9
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Table 2 ANOVA and post hoc test results for the spatio-temporal parameters. Comparison between groups (typically developing children, unilateral cerebral palsy nonaffected and affected side) and surface conditions (even, uneven) are shown. The non-dimensional mean and standard deviations [SD] are given for all spatiotemporal parameters, except for foot off (in % gait cycle) and toe clearance height (in mm). Paired student t-tests results are given for the difference between even and uneven ground for each group. Significant results with P < 0.007 are highlighted in bold. Mixed-factor model ANOVA
Typically developing children
Unilateral cerebral palsy patients Non-affected side
Affected side
Group
Floor
Interaction
Even
Uneven
t-test
Even
Uneven
t-test
Even
Uneven
t-test
P
P
P
Mean [SD]
Mean [SD]
P
Mean [SD]
Mean [SD]
P
Mean [SD]
Mean [SD]
P
Walking speed
0.019
< 0.001
0.400
0.41 [0.05]
0.38 [0.06]
0.020
0.41 [0.05]
0.39 [0.05]
0.024
0.362
< 0.001
0.309
< 0.001
0.375 < 0.001
0.113 0.096
Foot off (% gait cycle) Double support time
< 0.001
< 0.001
0.881
0.001
< 0.001
1.000
Toe clearance (mm)
0.776
< 0.001
0.007
58.80 [2.24] 0.64 [0.15] 94.4 [10.5]
61.01 [1.74] 0.87 [0.14] 133.7 [11.8]
0.51 [0.04] 0.77 [0.07] 0.16 [0.05] 64.21 [1.91] 1.02 [0.19] 135.2 [10.6]
0.55 [0.04] 0.75 [0.06] 0.13 [0.03] 59.39 [2.18] 0.81 [0.19] 86.0 [15.0]
0.51 [0.04] 0.73 [0.10] 0.16 [0.05] 61.58 [1.74] 1.03 [0.18] 136.9 [14.7]
< 0.001
0.028 0.059
0.55 [0.04] 0.75 [0.06] 0.13 [0.03] 62.33 [2.09] 0.80 [0.19] 90.6 [12.2]
< 0.001
Step length Stride width
0.41 [0.06] 0.52 [0.05] 0.79 [0.09] 0.13 [0.04]
< 0.001
Cadence
0.46 [0.05] 0.57 [0.04] 0.81 [0.08] 0.12 [0.03]
0.095 0.164 < 0.001 < 0.001 < 0.001
strike, toe-off). Then marker trajectories were filtered to reduce noise, such as skin movements (Nexus build-in Woltring filter with mean square error set to 10 mm2 as filter parameter). Finally, the spatiotemporal gait parameters (e.g. walking speed, step length, etc.), lower and upper body joint angles, and CoM were calculated. The kinematic data were time-normalised to a gait cycle, i.e. the time between two consecutive foot strikes of the same leg were equal to 100 data points, by self-written Matlab codes (Matlab software, Version R2017b, The MathWorks Inc., Natick (MA), USA). For the TD children data were analysed for the left body side and for the children with uni-CP for both sides, i.e. affected and non-affected side. If possible two gait cycles were extracted from trials 1 to 5 (=10 gait cycles). Trials 6 and 7 were used as back-ups in case the quality of any of the trials 1 to 5 was not sufficient (e.g. had gaps in the marker trajectory). For each parameter, the average across 10 gait cycles per body side was calculated for each subject. Spatio-temporal parameters (walking speed, cadence, step length, stride width and double support time) were transformed to non-dimensional units to correct for differences in leg length (measured from the anterior superior iliac spine to the medial malleolus) between subjects (Hof, 1996). Foot-off is given in percentage of gait cycle. Furthermore, toe clearance height, defined as the maximum distance of the toe marker above the floor during swing phase, was calculated as in Böhm et al. (2014). Stride width was calculated as the medio-lateral distance of the ankle joint centres during double support. The data of the CoM displacement were calculated in respect to the ankle joint centre of the corresponding side of the gait cycle, i.e. the position of the ipsilateral ankle joint centre was subtracted from the CoM data. Then, the whole body CoM relative to the ankle joint was normalised to body height (CoM_rel) (Broström et al., 2007; Lulic Jurcevic et al., 2010).
0.232 0.002 0.006 < 0.001 < 0.001
0.315 0.002 < 0.001 < 0.001 < 0.001
anterior-posterior directions. For each of the seven spatio-temporal parameter, a two-factor mixed model ANOVA with factor group (TD, uni-CP non-affected side, uni-CP affected side) as between factor and surface condition (even, uneven ground) as within factor was calculated (Trujillo-Ortiz et al., 2004). Subsequently, post hoc paired t-tests were performed to further analyse significant differences between ground surfaces. As we conducted seven two-factor mixed model ANOVAs (one for each spatio-temporal parameter), the significance level was adjusted for multiple testing on seven parameters according to Bonferroni to P < 0.05/7 = 0.007. The full-body joint kinematics and CoM_rel displacements were compared with one-dimensional Statistical Parametric Mapping (SPM: spm1d-package, http://www.spm1d.org/index.html, function “spm1d.stats.ttest_paired”). Three comparisons were calculated: 1) even versus uneven ground for the non-affected side of the uni-CP group, 2) even versus uneven ground for the affected side and 3) even versus uneven ground for the TD group. The alpha-level for the SPM statistics was set to 0.05. A threshold of 5° deviation of the mean for the joint kinematics was set to define the clinical relevance. Differences of < 5° deviation were considered as clinically irrelevant. All datasets were complete, with 19 degrees-of-freedom. All statistic calculations were conducted in the Matlab software (Version R2017b, The MathWorks Inc., Natick (MA), USA).
3. Results 3.1. Spatio-temporal parameters Table 2 shows the results for the spatio-temporal parameters. For both groups the cadence was reduced on uneven ground (TD: 9%, uniCP affected side: 6% and non-affected side: 7%) compared to even ground but no adaptations in step length were observed. This resulted in a 10% significantly slower walking speed on uneven ground in the TD group, but not for the uni-CP group. Also for both groups the foot-off occurred later in the gait cycle on uneven ground (TD: 4%, uni-CP affected side: 4%, non-affected side: 3%) and the double support time was prolonged (TD: 35%, uni-CP both sides: 28%). Toe clearance height was the only spatio-temporal parameter with a significant interaction. However, toe clearance height was for both groups significantly higher when walking on uneven ground compared to even ground (TD: 42%, uni-CP affected side: 59%, non-affected side: 49%).
2.4. Parameters of interest and statistics The seven spatio-temporal parameters of interest were: walking speed, cadence, step length, stride width, double support time, foot-off and toe clearance height. The full-body joint kinematic angles included: the pelvis and hip for all three planes, knee flexion, ankle plantarflexion, foot progression, thorax for all three planes, shoulder flexion, shoulder abduction and elbow flexion. Furthermore, we were interested in the CoM_rel displacements for the mediolateral, vertical and 10
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Fig. 1. Hip and knee flexion angles when walking on even versus uneven ground. Joint angles (degrees, means and one standard deviation) are plotted on the y-axis normalised to a gait cycle (x-axis) for typically developing children and patients with unilateral cerebral palsy (non-affected and affected side). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping.
Only the uni-CP group took significantly wider strides on uneven ground compared to even ground (affected side: 25%, unaffected side: 24%). 3.2. Kinematic deviations In the following section, only the joint kinematic results with the clinical relevance (i.e. maximum deviation of the mean of 5° or more) are reported. In the supplementary material, the figures (Fig. 1s, Fig. 2s and Fig. 3s) of all joint angles can be found. Both uni-CP and TD showed increased hip and knee flexion during swing phase when walking on uneven versus even ground (Fig. 1). UniCP significantly increased hip flexion during swing phase on the nonaffected leg to a maximum difference of 7.9° (70–100% gait cycle, P < 0.001) and on the affected leg to 6.2° (68–100% gait cycle, P < 0.001), and the TD children to 6.8° (70–100% gait cycle, P < 0.001). Knee flexion increased on uneven ground during swing phase to 8.9° (69–100% gait cycle, P < 0.001) on the affected leg of uni-CP patients, 10.5° (71–100% gait cycle, P < 0.001) on the nonaffected leg of uni-CP patients and 10.2° (68–100% gait cycle, P < 0.001) in TD children. Only the TD group showed increased dorsiflexion during stance phase on uneven ground to a maximum difference of 5.0° (2–19% gait cycle, P < 0.001; 57–62% gait cycle, P = 0.007, Fig. 2). The TD group also showed an increased external foot progression angle up to 6.8° in stance phase (43–65% gait cycle, P = 0.001). The uni-CP patients showed increased elbow flexion on uneven ground to 6.8° (18–33% gait cycle, P = 0.014) on the affected side and to 6.9° (12–44% gait cycle, P < 0.001) on the non-affected side (Fig. 3). The uni-CP patients also kept the CoM_rel 1.5% more medial when standing on the affected leg (1–40% gait cycle, P < 0.001) (Fig. 3).
Fig. 2. Foot and ankle kinematics of typically developing children when walking on even versus uneven ground. Joint angles (degrees, means and one standard deviation) are plotted on the yaxis normalised to a gait cycle (x-axis). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping.
between even and uneven ground in patients with uni-CP and in TD children. As no significant interactions in the spatio-temporal parameters were found except for toe clearance height, we conclude that uni-CP patients and TD children use similar adaptations when walking on uneven ground (hypothesis 1). Patients and TD children both increase their toe clearance height on uneven ground, to prevent stumbling. The significant interaction for this parameter indicates that patients increase their toe clearance height more than TD children, especially on the affected side. The higher toe clearance is achieved in both groups by using the same adaptation mechanism of increasing hip and knee flexion during swing phase. These results are in line with Böhm et al.
4. Discussion The objective of this study was to explore the gait deviations 11
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Fig. 3. Elbow flexion and centre of mass relative displacement of unilateral cerebral palsy patients when walking on even versus uneven ground. Means and one standard deviation of the joint angles (degrees) and relative centre of mass displacement (%-body height) are plotted normalised to a gait cycle (x-axis). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping. Swing phase of the centre of mass is left blank, because the centre of mass is given relative to the ankle joint centre (CoM_rel).
(2014), who also found increased hip and knee flexion in swing phase in TD children and patients with bilateral spastic CP. Additionally, they detected an increased ankle dorsiflexion in swing phase in TD children of 3.4°. We also found significantly increased dorsiflexion in TD children and the non-affected side of uni-CP patients. However, maximum difference between the flooring conditions (< 3°) were considered clinically irrelevant. Similar to Böhm et al. (2014) we also did not discover other strategies to secure foot clearance on uneven ground, such as circumduction (increased hip abduction during swing) or pelvic hike (increased pelvic obliquity in swing) in uni-CP or TD children (see Supplementary data). Malone et al. (2016) reported a higher toe clearance in patients with CP (diplegic and hemiplegic) when crossing an obstacle compared to control subjects. So did Böhm et al. (2014), who found that the effect of surface condition (even and uneven ground) on toe clearance was greater in patients with bilateral spastic CP with stiff-knee gait than in TD children. Our results show a similar trend. Uni-CP increased their toe clearance on the affected side on uneven ground more than TD. Therefore, we also found an indication for a lack of selectivity that prevented children with CP from finetuning the most efficient multi-joint pattern to ensure toe clearance. We can only speculate about the reasons for the increased dorsiflexion in TD children during stance. It could be a mechanism to lower the CoM to gain more stability. Another possible explanation could be that this is a mechanism to stiffen the ankle joint in medio-lateral direction, as in dorsiflexion the calcaneus is better locked within the mortise of the fibular and tibia (Netter and Böttcher, 2001; Sarrafian, 1993). However, the increased dorsiflexion could also result from the uneven ground itself, meaning that the forefoot may have been placed on an elevated part of the floor. With an initial heel contact, the heel is then positioned below the level of the forefoot resulting in dorsiflexion. This mechanism could be either an intended foot placement of the TD group or a random result of the uneven ground. Apart from the foot, uni-CP patients used barely any different adaptation mechanisms to uneven ground than the TD children used (hypothesis 1). However, it seems that uni-CP feel less secure on uneven than on even ground. During mid stance, when stability is lowest due to single support, they increase their elbow flexion to keep their arms in a position to better absorb a possible fall (e.g. guardian position). This pre-cautious arm position on uneven ground may be a sign of feeling insecure, e.g. feeling a loss of balance control. TD children seem to feel subjectively more stable on the uneven ground, as they show a less altered arm position. Their maximum increase in elbow flexion was 4°, hence below a clinically relevant difference. In the kinematic parameters, we saw similar adaptations in uni-CP for the non-affected and the affected side. Therefore, we conclude, that the non-affected side does not seem to compensate for the affected side on uneven ground (hypothesis 2).
Our results demonstrated that uni-CP patients are limited, to some extent, in their adaptation mechanisms to uneven ground compared to TD children (hypothesis 3). In general, CP patients are known for increased internal rotations of the leg and/or foot (Wren et al., 2005) and therefore have limited external rotation abilities (O'Sullivan et al., 2006). This is probably the reason why uni-CP patients did not show the same adaptation as TD children on uneven ground at the level of the foot. TD children increase their external foot progression angle on uneven ground and consequently increase their base of support. As uni-CP patients cannot increase their external foot progression as TD children do, they need to keep their CoM_rel more medially to stay in balance on uneven ground. Patients seem to achieve a wider base of support by increasing their stride width on uneven ground, thereby increasing medio-lateral stability. A limitation of this study is that uni-CP patients were rather mildly affected, with 18 patients being classified as GMFCS level I and only two patients with GMFCS level II. Possibly, more severely impaired patients would show more and greater deviations from the TD group when walking on uneven ground. As the ability to walk on uneven ground has profound effects on the patients' ability to participate in outdoor activities with their healthy peers (Malone et al., 2015), it would be interesting to investigate to what extend patients with CP can be trained to walk on uneven ground.
5. Conclusion The rather mildly affected uni-CP patients in this study behaved similar to the TD children when walking on uneven ground in most of the parameters investigated. The major deviations between the patient group and the TD group were the different mechanisms to increase the base of support and the position of the arms. The increased toe clearance on uneven ground on the affected side of uni-CP indicates a lack of selectivity that prevented children with CP from fine-tuning the most efficient multi-joint pattern to ensure toe clearance. While uni-CP patients enlarge their base of support by increasing the stride width, TD children enlarge their base of support by increasing their external foot progression angle. Uni-CP patients seemed less stable on uneven ground and held their arms in a more “guardian position”. Furthermore, patients do not compensate with their non-affected side for their affected side on uneven ground.
Funding This work was financially supported by the University of Basel, Switzerland, Research Fund. 12
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Declaration of competing interest
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None. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.clinbiomech.2020.02.001. References Böhm, H., Hösl, M., Schwameder, H., Döderlein, L., 2014. Stiff-knee gait in cerebral palsy: how do patients adapt to uneven ground? Gait Posture 39, 1028–1033. https://doi. org/10.1016/j.gaitpost.2014.01.001. Broström, E., Örtqvist, M., Haglund-Akerlind, Y., Hagelberg, S., Gutierrez-Farewik, E., 2007. Trunk and center of mass movements during gait in children with juvenile idiopathic arthritis. Hum. Mov. Sci. 26, 296–305. Bruijn, S.M., Millard, M., van Gestel, L., Meyns, P., Jonkers, I., Desloovere, K., 2013. Gait stability in children with cerebral palsy. Res. Dev. Disabil. 34, 1689–1699. https:// doi.org/10.1016/j.ridd.2013.02.011. Finlay, O., Beringer, T., 2007. Effects of floor coverings on measurement of gait and plantar pressure. Physiotherapy 93, 144–150. https://doi.org/10.1016/j.physio. 2006.11.014. Gage, J.R., 1991. Gait Analysis in Cerebral Palsy. Mac Keith Press, London. Galli, M., Cimolin, V., Crivellini, M., Romkes, J., Albertini, G., Brunner, R., 2012. Quantification of upper limb motion during gait in children with hemiplegic cerebral palsy. J. Dev. Phys. Disabil. 24, 1–8. Gates, D.H., Wilken, J.M., Scott, S.J., Sinitski, E.H., Dingwell, J.B., 2012. Kinematic strategies for walking across a destabilizing rock surface. Gait Posture 35, 36–42. https://doi.org/10.1016/j.gaitpost.2011.08.001. Gutierrez, E.M., Bartonek, A., Haglund-Akerlind, Y., Saraste, H., 2003. Characteristic gait kinematics in persons with lumbosacral myelomeningocele. Gait Posture 18, 170–177. https://doi.org/10.1016/s0966-6362(03)00011-0. Hof, A.L., 1996. Scaling gait data to body size. Gait Posture 4, 222–223. Hsue, B.-J., Miller, F., Su, F.-C., 2009. The dynamic balance of the children with cerebral palsy and typical developing during gait. Part I: spatial relationship between COM and COP trajectories. Gait Posture 29, 465–470. https://doi.org/10.1016/j.gaitpost. 2008.11.007. Iosa, M., Marro, T., Paolucci, S., Morelli, D., 2012. Stability and harmony of gait in children with cerebral palsy. Res. Dev. Disabil. 33, 129–135. https://doi.org/10. 1016/J.RIDD.2011.08.031. Kadaba, M.P., Ramakrishnan, H.K., Wootten, M.E., 1990. Measurement of lower extremity kinematics during level walking. J. Orthop. Res. 8, 383–392. https://doi.org/
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Walking on uneven ground: How do patients with unilateral cerebral palsy adapt? Jacqueline Romkesa, Marie Fresliera, Erich Rutza,b, Katrin Bracht-Schweizera, a b
T
⁎
Laboratory for Movement Analysis, University of Basle Children's Hospital Basel (UKBB), Switzerland Neuro-Orthopaedic Unit, University of Basle Children's Hospital Basel (UKBB), Switzerland
A R T I C LE I N FO
A B S T R A C T
Keywords: Unilateral cerebral palsy Gait analysis Uneven ground Gait adaptations
Background: Children with cerebral palsy experience movement disorders that influence gait stability. It is likely that gait stability further decreases when walking on uneven compared to even ground. Therefore, the aim of this study was to investigate gait on uneven ground in children with unilateral cerebral palsy. Methods: Twenty children with unilateral cerebral palsy and twenty typically developing children performed a three-dimensional gait analysis when walking on even and uneven ground. Spatio-temporal parameters, fullbody joint kinematics and centre of mass displacements were compared. Findings: On uneven versus even ground, both groups showed decreased cadence, increased stance phase and double support time, increased toe clearance height, and increased knee and hip flexion during swing phase. Whereas only the typically developing children walked slower and had increased dorsiflexion and external foot progression during stance phase, only the patients showed increased stride width, increased elbow flexion (affected and non-affected side), and kept the centre of mass more medial when standing on the affected leg. Interpretation: Patients and healthy children use similar adaptation mechanisms when walking on uneven ground. Both groups increased the toe clearance height by increasing knee and hip flexion during swing. However, whereas patients enlarge their base of support by increasing stride width, healthy children do so by increasing their external foot progression angle. Furthermore, patients seem to feel more insecure and hold their arms in a position to prepare for falls on uneven ground. They also do not compensate with their non-affected side for their affected side on uneven ground.
1. Introduction According to Rosenbaum et al. (2007) cerebral palsy (CP) “describes a group of permanent disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing fetal or infant brain.” In patients with unilateral CP (uni-CP) the arm and leg primarily of one body side are involved. In these patients, toe-walking is the most common kinematic deviation (64%), followed by stiff knee gait (56%), in-toeing (54%) and excessive hip flexion (48%) (Wren et al., 2005). The gait deviations can lead to gait instability (Bruijn et al., 2013), loss of harmony, and tripping or falling (Iosa et al., 2012; Wren et al., 2005). Other factors influencing the loss of gait stability in patients with CP include sensory impairment, deficient equilibrium reactions (Gage, 1991), loss of selective muscle control, increased upper body motion (Galli et al., 2012; Schweizer et al., 2014) and centre of mass (CoM)
sway (Hsue et al., 2009). It is likely that gait instability further increases when walking on uneven terrain, such as forest soil or on cobble stone pavement. Unlike patients, healthy subjects have a variety of adaptation mechanisms to adjust their movement patterns when walking on different surfaces. One of these mechanisms is to lower the CoM by increasing knee and hip flexion and ankle dorsiflexion (Gates et al., 2012) when stepping from a flat surface onto a soft (MacLellan and Patla, 2006), slippery (Marigold and Patla, 2002), or destabilising loose rock (Gates et al., 2012) surface. MacLellan and Patla (2006) reported that dynamic stability on a soft foamy surface can be maintained by enlarging the base of support by increasing step width and step length. These changes in spatio-temporal parameters were, however, not supported by Gates et al. (2012) when walking on a loose rocky surface compared to flat ground. Other adaptation mechanisms that are mentioned in the literature to adjust walking on uneven or irregular ground are the
⁎ Corresponding author at: Children's University Hospital Basel (UKBB), Laboratory for Movement Analysis, c/o University of Basel, Spitalstrasse 33, Postfach, 4031 Basel, Switzerland. E-mail address: [email protected] (K. Bracht-Schweizer).
https://doi.org/10.1016/j.clinbiomech.2020.02.001 Received 10 December 2018; Accepted 6 February 2020 0268-0033/ © 2020 Elsevier Ltd. All rights reserved.
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inclusion criteria for both groups were age between 8 and 18 years and a body mass index below 85th percentile (WHO Body Mass Index-forage standards). Children younger than 8 years were excluded to ensure that the children were able to stay concentrated for the entire measurement session, which took around 2 h. The patients with uni-CP should have a level I or II on the Gross Motor Function Classification System (GMFCS) (Palisano et al., 1997) and be able to walk without assistance or assistive devices. The vast majority of children with uniCP generally falls into this category. Exclusion criteria for this group were: Botulinum toxin type A injections within six months prior to the measurements, surgery within one year prior to the measurements, Baclofen or selective dorsal rhizotomy. These treatments may influence the gait performance considerably. Patients with ataxia, dystonia and reduced vision despite wearing glasses were also excluded, since these factors only exist in a minor group of children and do not represent the group as a whole. Exclusion criteria for the TD group were: any neurological or orthopaedic impairment, major lower limb surgery and a leg length discrepancy > 1% body height. The study was approved by the local ethical committee and all subject signed an informed consent.
increase of step time and step width variability, the change in stance phase duration, and an increased foot height (Böhm et al., 2014; Finlay and Beringer, 2007; Gates et al., 2012; MacLellan and Patla, 2006; Schulz, 2011; Thies et al., 2005). Based on the literature, we expect that children with uni-CP have limited abilities to adapt their walking pattern to more challenging surfaces, such as uneven ground. To date, only few studies have explored walking on uneven ground in patients with CP. Böhm et al. (2014) studied the spatio-temporal parameters and joint kinematics in patients with diplegic CP and stiff knee gait when walking on uneven ground. They found that patients and healthy subjects similarly adapted walking speed, step length, and cadence when walking on uneven ground, but only the patients increased step width. Although the patients walked with reduced knee flexion during swing phase on even ground (stiff-knee gait) compared to healthy subjects, the patients were able to adapt to uneven ground with increased knee flexion during swing similar to the healthy subjects (Böhm et al., 2014). Based on these results the authors rejected the hypothesis that the spasticity of the rectus femoris muscle in patients with CP limits toe-clearance. Malone et al. (2015) reported that the maximum distance between the CoM and centre of pressure was lower in patients with CP when walking on uneven ground compared to healthy controls. Malone et al. (2015) further reported adaptations to uneven ground including reduced hip extension and ankle movement in the sagittal and coronal planes in the control subjects, but not in the patients with CP. However, this study included a mix of patients with uni- and bilateral CP, which may have influenced the results. Up till now, no study has investigated the gait adaptations in uni-CP patients on uneven ground. As opposed to patients with bilateral CP, uni-CP patients have a non-affected body side, which they could, theoretically use to compensate for the impaired side. Limitations when walking on uneven ground may have profound effects on the patients' ability to participate in outdoor activities with their healthy peers (Malone et al., 2015). Therefore, to gain knowledge on the adaptive possibilities is of high clinical relevance to improve therapy and training concepts in uni-CP. The research question for this study was: Do children with uni-CP experience more difficulties than typically developing (TD) children when walking on uneven ground compared to even ground? Our hypotheses were that: 1) Uni-CP patients use different adaptation mechanisms to uneven ground compared to TD children regarding the spatio-temporal parameters and the three dimensional whole body kinematics, 2) The non-affected side of uni-CP patients compensates for the affected side on uneven ground by showing greater adaptation mechanisms than the affected side, and 3) Uni-CP patients have limited adaptation mechanisms compared to TD children when walking on uneven ground.
2.2. Experimental protocol The subjects performed two testing conditions, namely walking on even and uneven ground, during a single measurement session. The uneven ground was a 6 m long by 1 m wide walkway, consisting of 24 floor panels (50 × 50 × 4–8 cm, Terrasensa, Hübner GmbH, Kassel, Germany). The surface is a relief system made from polyurethane which is comfortable to walk on and shock absorbing. The two walking conditions were performed barefoot at a comfortable self-selected walking speed and the order of the conditions was randomised among the subjects. The subjects were allowed one practice trial on the uneven ground for familiarisation, before performing 7 trials that were recorded. The even ground condition was performed directly underneath the uneven walkway, resulting in a 3–5 min resting period for the subjects between the conditions while placing or removing the uneven walkway. Full-body kinematic data were collected at 150 Hz with a 12-camera Vicon Motion Capture system (Vicon Inc., Oxford, UK) using the Plugin-Gait marker-set (9 mm in diameter) and model (lower body: Kadaba et al. (1990), upper body and whole body CoM: Gutierrez et al. (2003)). A knee alignment device was applied in a static trial to define the knee flexion axis (Motion Lab Systems Inc., Los Angeles, USA). The same static trial was used for both walking conditions. For each walking condition, data collection continued until seven error-free-trials were recorded. Errors that occurred in disregarded trials included disappearing markers (gaps in any marker trajectory), the subject stopping/accelerating/decelerating/stumbling, or unforeseen data collection errors.
2. Methods 2.3. Data analysis 2.1. Subjects The Nexus software (Version 2.5, Vicon Inc., Oxford, UK) was used for data collection and post-processing of the raw kinematic data. First, the gait cycles were determined by visually defining gait events (foot
Between November 2017 and October 2018, 20 children diagnosed with spastic uni-CP and 20 TD children participated (Table 1). The
Table 1 Group details. Uni-CP: children with unilateral cerebral palsy, TD: typically developing children, GMFCS: Gross Motor Function Classification System, M: male, F: female, R: right, L: left, NA: not applicable. Group
Parameter N
Uni-CP TD
20 20
Gender
Age (years)
Height (m)
Weight (kg)
Affected side
GMFCS
M/F
Mean [range]
Mean [SD]
Mean [SD]
R/L
Level I/II
13 M/7 F 10 M/10 F
10.8 [8.3–17.7] 11.4 [7.6–16.7]
1.42 [0.15] 1.47 [0.18]
33.2 [10.3] 37.3 [12.0]
13 R, 7 L NA
18 I, 2 II NA
9
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Table 2 ANOVA and post hoc test results for the spatio-temporal parameters. Comparison between groups (typically developing children, unilateral cerebral palsy nonaffected and affected side) and surface conditions (even, uneven) are shown. The non-dimensional mean and standard deviations [SD] are given for all spatiotemporal parameters, except for foot off (in % gait cycle) and toe clearance height (in mm). Paired student t-tests results are given for the difference between even and uneven ground for each group. Significant results with P < 0.007 are highlighted in bold. Mixed-factor model ANOVA
Typically developing children
Unilateral cerebral palsy patients Non-affected side
Affected side
Group
Floor
Interaction
Even
Uneven
t-test
Even
Uneven
t-test
Even
Uneven
t-test
P
P
P
Mean [SD]
Mean [SD]
P
Mean [SD]
Mean [SD]
P
Mean [SD]
Mean [SD]
P
Walking speed
0.019
< 0.001
0.400
0.41 [0.05]
0.38 [0.06]
0.020
0.41 [0.05]
0.39 [0.05]
0.024
0.362
< 0.001
0.309
< 0.001
0.375 < 0.001
0.113 0.096
Foot off (% gait cycle) Double support time
< 0.001
< 0.001
0.881
0.001
< 0.001
1.000
Toe clearance (mm)
0.776
< 0.001
0.007
58.80 [2.24] 0.64 [0.15] 94.4 [10.5]
61.01 [1.74] 0.87 [0.14] 133.7 [11.8]
0.51 [0.04] 0.77 [0.07] 0.16 [0.05] 64.21 [1.91] 1.02 [0.19] 135.2 [10.6]
0.55 [0.04] 0.75 [0.06] 0.13 [0.03] 59.39 [2.18] 0.81 [0.19] 86.0 [15.0]
0.51 [0.04] 0.73 [0.10] 0.16 [0.05] 61.58 [1.74] 1.03 [0.18] 136.9 [14.7]
< 0.001
0.028 0.059
0.55 [0.04] 0.75 [0.06] 0.13 [0.03] 62.33 [2.09] 0.80 [0.19] 90.6 [12.2]
< 0.001
Step length Stride width
0.41 [0.06] 0.52 [0.05] 0.79 [0.09] 0.13 [0.04]
< 0.001
Cadence
0.46 [0.05] 0.57 [0.04] 0.81 [0.08] 0.12 [0.03]
0.095 0.164 < 0.001 < 0.001 < 0.001
strike, toe-off). Then marker trajectories were filtered to reduce noise, such as skin movements (Nexus build-in Woltring filter with mean square error set to 10 mm2 as filter parameter). Finally, the spatiotemporal gait parameters (e.g. walking speed, step length, etc.), lower and upper body joint angles, and CoM were calculated. The kinematic data were time-normalised to a gait cycle, i.e. the time between two consecutive foot strikes of the same leg were equal to 100 data points, by self-written Matlab codes (Matlab software, Version R2017b, The MathWorks Inc., Natick (MA), USA). For the TD children data were analysed for the left body side and for the children with uni-CP for both sides, i.e. affected and non-affected side. If possible two gait cycles were extracted from trials 1 to 5 (=10 gait cycles). Trials 6 and 7 were used as back-ups in case the quality of any of the trials 1 to 5 was not sufficient (e.g. had gaps in the marker trajectory). For each parameter, the average across 10 gait cycles per body side was calculated for each subject. Spatio-temporal parameters (walking speed, cadence, step length, stride width and double support time) were transformed to non-dimensional units to correct for differences in leg length (measured from the anterior superior iliac spine to the medial malleolus) between subjects (Hof, 1996). Foot-off is given in percentage of gait cycle. Furthermore, toe clearance height, defined as the maximum distance of the toe marker above the floor during swing phase, was calculated as in Böhm et al. (2014). Stride width was calculated as the medio-lateral distance of the ankle joint centres during double support. The data of the CoM displacement were calculated in respect to the ankle joint centre of the corresponding side of the gait cycle, i.e. the position of the ipsilateral ankle joint centre was subtracted from the CoM data. Then, the whole body CoM relative to the ankle joint was normalised to body height (CoM_rel) (Broström et al., 2007; Lulic Jurcevic et al., 2010).
0.232 0.002 0.006 < 0.001 < 0.001
0.315 0.002 < 0.001 < 0.001 < 0.001
anterior-posterior directions. For each of the seven spatio-temporal parameter, a two-factor mixed model ANOVA with factor group (TD, uni-CP non-affected side, uni-CP affected side) as between factor and surface condition (even, uneven ground) as within factor was calculated (Trujillo-Ortiz et al., 2004). Subsequently, post hoc paired t-tests were performed to further analyse significant differences between ground surfaces. As we conducted seven two-factor mixed model ANOVAs (one for each spatio-temporal parameter), the significance level was adjusted for multiple testing on seven parameters according to Bonferroni to P < 0.05/7 = 0.007. The full-body joint kinematics and CoM_rel displacements were compared with one-dimensional Statistical Parametric Mapping (SPM: spm1d-package, http://www.spm1d.org/index.html, function “spm1d.stats.ttest_paired”). Three comparisons were calculated: 1) even versus uneven ground for the non-affected side of the uni-CP group, 2) even versus uneven ground for the affected side and 3) even versus uneven ground for the TD group. The alpha-level for the SPM statistics was set to 0.05. A threshold of 5° deviation of the mean for the joint kinematics was set to define the clinical relevance. Differences of < 5° deviation were considered as clinically irrelevant. All datasets were complete, with 19 degrees-of-freedom. All statistic calculations were conducted in the Matlab software (Version R2017b, The MathWorks Inc., Natick (MA), USA).
3. Results 3.1. Spatio-temporal parameters Table 2 shows the results for the spatio-temporal parameters. For both groups the cadence was reduced on uneven ground (TD: 9%, uniCP affected side: 6% and non-affected side: 7%) compared to even ground but no adaptations in step length were observed. This resulted in a 10% significantly slower walking speed on uneven ground in the TD group, but not for the uni-CP group. Also for both groups the foot-off occurred later in the gait cycle on uneven ground (TD: 4%, uni-CP affected side: 4%, non-affected side: 3%) and the double support time was prolonged (TD: 35%, uni-CP both sides: 28%). Toe clearance height was the only spatio-temporal parameter with a significant interaction. However, toe clearance height was for both groups significantly higher when walking on uneven ground compared to even ground (TD: 42%, uni-CP affected side: 59%, non-affected side: 49%).
2.4. Parameters of interest and statistics The seven spatio-temporal parameters of interest were: walking speed, cadence, step length, stride width, double support time, foot-off and toe clearance height. The full-body joint kinematic angles included: the pelvis and hip for all three planes, knee flexion, ankle plantarflexion, foot progression, thorax for all three planes, shoulder flexion, shoulder abduction and elbow flexion. Furthermore, we were interested in the CoM_rel displacements for the mediolateral, vertical and 10
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Fig. 1. Hip and knee flexion angles when walking on even versus uneven ground. Joint angles (degrees, means and one standard deviation) are plotted on the y-axis normalised to a gait cycle (x-axis) for typically developing children and patients with unilateral cerebral palsy (non-affected and affected side). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping.
Only the uni-CP group took significantly wider strides on uneven ground compared to even ground (affected side: 25%, unaffected side: 24%). 3.2. Kinematic deviations In the following section, only the joint kinematic results with the clinical relevance (i.e. maximum deviation of the mean of 5° or more) are reported. In the supplementary material, the figures (Fig. 1s, Fig. 2s and Fig. 3s) of all joint angles can be found. Both uni-CP and TD showed increased hip and knee flexion during swing phase when walking on uneven versus even ground (Fig. 1). UniCP significantly increased hip flexion during swing phase on the nonaffected leg to a maximum difference of 7.9° (70–100% gait cycle, P < 0.001) and on the affected leg to 6.2° (68–100% gait cycle, P < 0.001), and the TD children to 6.8° (70–100% gait cycle, P < 0.001). Knee flexion increased on uneven ground during swing phase to 8.9° (69–100% gait cycle, P < 0.001) on the affected leg of uni-CP patients, 10.5° (71–100% gait cycle, P < 0.001) on the nonaffected leg of uni-CP patients and 10.2° (68–100% gait cycle, P < 0.001) in TD children. Only the TD group showed increased dorsiflexion during stance phase on uneven ground to a maximum difference of 5.0° (2–19% gait cycle, P < 0.001; 57–62% gait cycle, P = 0.007, Fig. 2). The TD group also showed an increased external foot progression angle up to 6.8° in stance phase (43–65% gait cycle, P = 0.001). The uni-CP patients showed increased elbow flexion on uneven ground to 6.8° (18–33% gait cycle, P = 0.014) on the affected side and to 6.9° (12–44% gait cycle, P < 0.001) on the non-affected side (Fig. 3). The uni-CP patients also kept the CoM_rel 1.5% more medial when standing on the affected leg (1–40% gait cycle, P < 0.001) (Fig. 3).
Fig. 2. Foot and ankle kinematics of typically developing children when walking on even versus uneven ground. Joint angles (degrees, means and one standard deviation) are plotted on the yaxis normalised to a gait cycle (x-axis). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping.
between even and uneven ground in patients with uni-CP and in TD children. As no significant interactions in the spatio-temporal parameters were found except for toe clearance height, we conclude that uni-CP patients and TD children use similar adaptations when walking on uneven ground (hypothesis 1). Patients and TD children both increase their toe clearance height on uneven ground, to prevent stumbling. The significant interaction for this parameter indicates that patients increase their toe clearance height more than TD children, especially on the affected side. The higher toe clearance is achieved in both groups by using the same adaptation mechanism of increasing hip and knee flexion during swing phase. These results are in line with Böhm et al.
4. Discussion The objective of this study was to explore the gait deviations 11
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Fig. 3. Elbow flexion and centre of mass relative displacement of unilateral cerebral palsy patients when walking on even versus uneven ground. Means and one standard deviation of the joint angles (degrees) and relative centre of mass displacement (%-body height) are plotted normalised to a gait cycle (x-axis). Continuous grey line = even ground, dashed black line = uneven ground. The vertical lines, at around 60% of the gait cycle, display the foot-off. The grey shaded rectangle areas define the phase in the gait cycle during which there is a statistically significant difference according to one-dimensional Statistical Parametric Mapping. Swing phase of the centre of mass is left blank, because the centre of mass is given relative to the ankle joint centre (CoM_rel).
(2014), who also found increased hip and knee flexion in swing phase in TD children and patients with bilateral spastic CP. Additionally, they detected an increased ankle dorsiflexion in swing phase in TD children of 3.4°. We also found significantly increased dorsiflexion in TD children and the non-affected side of uni-CP patients. However, maximum difference between the flooring conditions (< 3°) were considered clinically irrelevant. Similar to Böhm et al. (2014) we also did not discover other strategies to secure foot clearance on uneven ground, such as circumduction (increased hip abduction during swing) or pelvic hike (increased pelvic obliquity in swing) in uni-CP or TD children (see Supplementary data). Malone et al. (2016) reported a higher toe clearance in patients with CP (diplegic and hemiplegic) when crossing an obstacle compared to control subjects. So did Böhm et al. (2014), who found that the effect of surface condition (even and uneven ground) on toe clearance was greater in patients with bilateral spastic CP with stiff-knee gait than in TD children. Our results show a similar trend. Uni-CP increased their toe clearance on the affected side on uneven ground more than TD. Therefore, we also found an indication for a lack of selectivity that prevented children with CP from finetuning the most efficient multi-joint pattern to ensure toe clearance. We can only speculate about the reasons for the increased dorsiflexion in TD children during stance. It could be a mechanism to lower the CoM to gain more stability. Another possible explanation could be that this is a mechanism to stiffen the ankle joint in medio-lateral direction, as in dorsiflexion the calcaneus is better locked within the mortise of the fibular and tibia (Netter and Böttcher, 2001; Sarrafian, 1993). However, the increased dorsiflexion could also result from the uneven ground itself, meaning that the forefoot may have been placed on an elevated part of the floor. With an initial heel contact, the heel is then positioned below the level of the forefoot resulting in dorsiflexion. This mechanism could be either an intended foot placement of the TD group or a random result of the uneven ground. Apart from the foot, uni-CP patients used barely any different adaptation mechanisms to uneven ground than the TD children used (hypothesis 1). However, it seems that uni-CP feel less secure on uneven than on even ground. During mid stance, when stability is lowest due to single support, they increase their elbow flexion to keep their arms in a position to better absorb a possible fall (e.g. guardian position). This pre-cautious arm position on uneven ground may be a sign of feeling insecure, e.g. feeling a loss of balance control. TD children seem to feel subjectively more stable on the uneven ground, as they show a less altered arm position. Their maximum increase in elbow flexion was 4°, hence below a clinically relevant difference. In the kinematic parameters, we saw similar adaptations in uni-CP for the non-affected and the affected side. Therefore, we conclude, that the non-affected side does not seem to compensate for the affected side on uneven ground (hypothesis 2).
Our results demonstrated that uni-CP patients are limited, to some extent, in their adaptation mechanisms to uneven ground compared to TD children (hypothesis 3). In general, CP patients are known for increased internal rotations of the leg and/or foot (Wren et al., 2005) and therefore have limited external rotation abilities (O'Sullivan et al., 2006). This is probably the reason why uni-CP patients did not show the same adaptation as TD children on uneven ground at the level of the foot. TD children increase their external foot progression angle on uneven ground and consequently increase their base of support. As uni-CP patients cannot increase their external foot progression as TD children do, they need to keep their CoM_rel more medially to stay in balance on uneven ground. Patients seem to achieve a wider base of support by increasing their stride width on uneven ground, thereby increasing medio-lateral stability. A limitation of this study is that uni-CP patients were rather mildly affected, with 18 patients being classified as GMFCS level I and only two patients with GMFCS level II. Possibly, more severely impaired patients would show more and greater deviations from the TD group when walking on uneven ground. As the ability to walk on uneven ground has profound effects on the patients' ability to participate in outdoor activities with their healthy peers (Malone et al., 2015), it would be interesting to investigate to what extend patients with CP can be trained to walk on uneven ground.
5. Conclusion The rather mildly affected uni-CP patients in this study behaved similar to the TD children when walking on uneven ground in most of the parameters investigated. The major deviations between the patient group and the TD group were the different mechanisms to increase the base of support and the position of the arms. The increased toe clearance on uneven ground on the affected side of uni-CP indicates a lack of selectivity that prevented children with CP from fine-tuning the most efficient multi-joint pattern to ensure toe clearance. While uni-CP patients enlarge their base of support by increasing the stride width, TD children enlarge their base of support by increasing their external foot progression angle. Uni-CP patients seemed less stable on uneven ground and held their arms in a more “guardian position”. Furthermore, patients do not compensate with their non-affected side for their affected side on uneven ground.
Funding This work was financially supported by the University of Basel, Switzerland, Research Fund. 12
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Declaration of competing interest
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