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ORIGINAL ARTICLE
E1 follow-up vessel injury (n=1) The training protocol consisted of 7 exercises involving the
unattended
• Parents argued
hip, knee, and ankle extensors and flexors. If children suc-
Drop outs ceeded in overcoming the resistance against gravity, elastic
that the testing • Discontinued the
protocol was too intervention due to bands were used to increase resistance.a Two sets of 5 repeti-
stressful (n=1) unplanned tions were performed for each exercise with a low velocity to
obligations (n=2) permit movement control and eccentric activation of the mus-
cles. A more detailed description of the training protocol con-
Analyzed (n=20) Analyzed (n=19) Group tent is available from the authors (D Patikas et al, unpublished
• Missing kinetic data • Missing kinetic data comparison data, 2006).
during
Analysis
(n=11): not free wal- (n=4): not free walker The training sessions started 3 to 4 weeks after surgery.
ker during E0 or E1 during E0 or E1 E0 - E1 After hospital discharge, children in the strength-training group
were trained for 40.3⫾0.4 additional weeks, until E1. Each
session lasted approximately 30 to 45 minutes and was per-
Analyzed (n=22, CG: n=9 , SG: n=13)
E0 - E1 - E2 formed on average 3.2⫾0.3 times a week.
• Missing kinetic data (n=8, SG: n=4, CG: n=4): not comparison
free walker during E0 or E1 or E2 Gait Analysis
A 3-dimensional gait analysis was performed using the Helen
Fig 1. Flow diagram of the randomization procedure. Hayes marker set.23 Data were captured with a 9-camera
3-dimensional motion analysis systemb using reflective mark- Table 1: Results of the Statistical Analysis for the MAS, GMFM,
ers (diameter, 14mm) applied on the skin. The children were V̇O2, and EEI for the 2 Groups Before and 1 Year After Surgery
asked to walk over a 9-m line at self-selected speeds. Kinetic 95% Confidence Interval for Differences
data were captured using 2 forceplatesc and only in case a Between
patient required no external body support during walking. Measures CG–SG* E1–E0†
The heart rate, breathing frequency, and oxygen consump- NOTE. Significant differences are in boldface.
tion (V̇O2) were measured online.d Patients walked twice for 5 Abbreviations: CG, control group; SG, strength-training group.
minutes around a 25-m–long pathway (8⫺12 rounds for each *Univariate ANCOVA with the E0 measurement as covariate.
†
One-way ANOVA for repeated measurements (E0 and E1).
5-min walk, depending on walking speed). After each 5-minute
walk, children rested while sitting for 2 to 5 minutes, until the
resting heart rate was reached. The resting V̇O2 was subtracted
from the V̇O2 during walking and this value was normalized to did not change significantly between the E0 and E1 measure-
the body mass and distance that each patient walked. Further- ments or between groups. The EEI increased significantly at
more, the Energy Expenditure Index (EEI) was calculated E1, and this change was not group dependent.
using the following formula: Gait Parameters
EEI⫽
walking velocity
冉
HRwalking⫺HRrest heart beats ⁄ min
m ⁄ min
冊 One year after the surgery (E1), the spatiotemporal param-
eters of both groups deviated more from the healthy children as
compared with the preoperative measurements (E0) (fig 2).
This fact, combined with the increased EEI at E1, led us to
where HRwalking and HRrest are mean heart rates in beats per
decide to measure as many children as possible 2 years after the
minute during walking and at rest, respectively.25 The strong
operation. Because we observed no significant differences be-
linear relation between oxygen uptake and heart rate in differ-
tween the groups in the spatiotemporal, kinematic, and kinetic
ent velocities supports the use of the EEI as a walking efficiency
parameters (table 2), the 2 groups were merged to calculate the
indicator.25-27
differences between E0, E1, and E2. Walking speed, duration
Data and Statistical Analysis of the stance phase, and stride duration improved significantly
during the time period between E1 and E2.
Means and SDs of the averages from both sides were cal- The normalcy index was significantly reduced at E1, and a
culated for all dependent variables. The spatiotemporal, kine- further decrease followed at E2 (fig 3). The control group had
matic and kinetic parameters and the normalcy index28 were a higher normalcy index before the surgery (see table 2). When
processed with tools developed in Matlab.e To eliminate the we adjusted the preoperative differences between the groups,
effect of differences between the groups before surgery, a we observed no significant difference in the normalcy index
univariate analysis of covariance (ANCOVA) was assessed for between the groups.
each dependent variable to determine the differences between Concerning the hip joint, 59% of the examined lower ex-
the groups at E1, using as a covariate the E0 measurement. tremities did not reach full hip extension at E0, and this deficit
One-way analysis of variance (ANOVA) for repeated measure- was retained after the operation for both groups. Preopera-
ments was used to determine changes between E0, E1, and E2. tively, the minimum knee flexion angle at terminal swing was
The significance level was set at .05, and the 95% confidence increased for both groups with respect to the normative values.
interval of the difference between the compared groups or One year postsurgery, both groups had a significant decrease in
measurements was calculated. All statistical analyses were the knee flexion angle, approaching the normative values. This
performed using SPSS.f decrease remained significant at E2, despite the observed in-
crease between E1 and E2. The ankle joint during the stance-
RESULTS swing transition period was in the equinus position, with the
control group having a higher plantarflexion angle at E0. The
Clinical Data, GMFM, and Walking Efficiency increased plantarflexion preoperatively was drastically reversed at
No difference between the groups was observed in the spas- E1 for both groups and tended to increase toward the normative
ticity level at E0 and E1, as measured with the MAS (table 1). values at E2.
However, a significant decrease in spasticity between E1 and Concerning the kinetic data (fig 4), it was possible to capture
E0 was observed for both groups. data from 9 control-group and 15 strength-training– group chil-
The GMFM score of section D (related to standing) im- dren at E0 and E1 and from 14 children at E0, E1, and E2 (see
proved significantly at E1, and no difference between the also fig 1). The power absorption at the hip joint was decreased
groups was observed when E0 intergroup differences were at E0 and increased gradually toward the normative values at
taken into account. E1 and E2 for both groups. We observed no significant differ-
From the 13 control-group and 16 strength-training– group ence between the groups or the examinations for the maximum
children who performed the walking efficiency test, the V̇O2 knee power absorption during the loading response. Concern-
Fig 2. (A—D) Spatiotemporal parameters for the control (CG) and strength-training (SG) groups, before (E0), 1 year after (E1), and 2 years
after (E2) the surgery. The normative values with SD are represented by the continuous horizontal line and the grey zone (nⴝ29). NOTE.
Values are mean ⴞ SD. *Significant differences between the measurements for the merged group (CGⴙSG) that were examined at E0, E1,
and E2.
ing the ankle joint kinetics, we observed an improvement only though joint ROM was restored at E1, it took almost 2 years to
between E1 and E2. There was a trend to decrease between E0 restore the preoperative power when walking. Furthermore, our
and E1, whereas the changes in moment and power of the ankle study showed that 1 year after the surgery the EEI increased.
joint were not group dependent. Consequently, an interval longer than 1 year postsurgery is re-
quired to describe the long-term outcome of the surgery. This is in
DISCUSSION line with a very recent report32 that suggests that the gait evalu-
It is well documented that the gait patterns of patients with ation should be performed at least 3 years after surgery to give the
CP deviate from normal, taking into consideration gait anal- most predictive outcome of the treatment. The same research
ysis data.29 For instance, decreased power production from the group had previously reported that triceps surae lengthening led to
plantarflexors of children with hemiplegia during walking has significant increase in the plantarflexor moment 3 years after the
been previously reported,30 and our study supports this as well. operation.33
Despite the improvement in the ankle joint kinematics at E1, the The group that followed a specific strength-training program
moment and power of the plantarflexors tended to decrease. This in addition to regular PT during the rehabilitation period failed
could be attributed to the decreased walking speed, which affects to show any significant advantages compared with the group
the power production.31 In addition, the increased duration of the that had only conventional PT. This contrasts with previous
double-support phase could also explain why the ankle moment— studies that have documented well the advantages of strength
and consequently power— decreased at E1. The earlier-mentioned training in patients with CP. However, there are several expla-
parameters recovered between E1 and E2. This shows that al- nations for these contradictory conclusions.
Table 2: Results of the Statistical Analysis for the Gait Analysis Data
95% Confidence Interval for Differences Between
Walking speed (cm/s) ⫺13.3 to 21.9 ⫺20.7 to 51.2 ⫺7.5 to 0.1 6.0 to 51.2
Stance phase duration (% of gait cycle) ⫺4.51 to 2.65 0.21 to 4.96 ⫺3.38 to 0.79 ⴚ5.65 to ⴚ2.11
Stride duration (s) ⫺0.49 to 0.29 0.04 to 0.55 ⫺0.10 to 0.23 ⴚ0.44 to ⴚ0.02
Stride length (cm) ⫺7.1 to 14.8 ⫺7.8 to 5.6 ⫺3.3 to 11.7 ⫺1.2 to 11.8
Normalcy index ⫺91 to 170 ⴚ168 to ⴚ27 ⴚ227 to ⴚ106 ⴚ129 to ⴚ10
Maximum hip extension (deg) ⫺3.4 to 5.0 ⫺4.3 to 1.9 ⫺5.4 to 1.6 ⫺3.6 to 2.2
Minimum knee flexion during terminal swing (deg) ⫺2.9 to 8.4 ⴚ23.2 to ⴚ12.8 ⴚ18.8 to ⴚ10.3 0.4 to 6.6
Maximum plantarflexion during stance-swing
transition (deg) ⫺3.0 to 5.7 9.1 to 20.0 5.7 to 17.4 ⫺6.3 to 0.3
Maximum hip power absorption (W/kg) ⫺0.240 to 0.192 ⫺0.271 to 0.041 ⴚ0.592 to ⴚ0.128 ⴚ0.419 to ⴚ0.072
Maximum knee power absorption during loading
response (W/kg) ⫺0.217 to 0.392 ⫺0.240 to 0.115 ⫺0.492 to 0.215 ⫺0.319 to 0.167
Maximum plantarflexion moment (Nm/kg) ⫺0.131 to 0.161 ⫺0.215 to 0.003 ⫺0.080 to 0.087 0.032 to 0.186
Maximum plantarflexion power generation (W/kg) ⫺0.880 to 0.050 ⫺0.609 to 0.088 ⫺0.210 to 0.620 0.166 to 0.765
Most of the studies in the past have used more intense and increase children’s motivation (like exercises in the form of
short-term training protocols, with regular supervision,12,14 which games) are necessary to enhance the tolerance of the strength
nonetheless required children to make scheduled visits to the training. It is probable that if in the present study the children
rehabilitation center and in some cases to use special equip- had been able to choose into which group they wanted to be
ment, such as isokinetic dynamometers.7,10,13,15 This kind of placed, the effects of strength training might have been more
approach is probably ideal for research purposes, but because pronounced. Moreover, it should not be ruled out that some
of time and cost limitations most patients are not able to follow children belonging to the control group could be physically
such a training program for a long or even short period. For this more active than some children that belonged to the training
reason, and in accordance with more recent studies,5,8,14 a group. It was not possible to control such factors, because it
home-based training program was suggested in the present would have been ethically inappropriate to force the children
study. However, when practicing at home the research team has who participated in the study as the control group to be phys-
less control de facto over the frequency and intensity of train- ically inactive.
ing. Dodd et al8 indicated that the lack of changes in function- Another factor that might have limited the training intensity
ally important gait parameters, such as walking speed, after in the present study is the nature of the performed exercises,
strength training may be attributed to the fact that training which involved mainly more than 1 joint and were associated
sessions were assessed at home and that the minimized thera- with functionally important everyday activities. Although the
pist supervision could have resulted in a lower-than-optimal principle of specificity is an important issue for training in the
training intensity. Our results support this statement. healthy population, low levels of motor control may not permit
The strength-training protocols in most of the previous stud- the training effects to be transferred to functional tasks like
ies, which have been effective for children with CP, had gait.9 Execution of these exercises by patients with CP requires
durations of 6 to 8 weeks. Damiano et al9 recommended that an ordinary level of motor control that may not be available.
the strength-training duration should be longer than 6 weeks to Previous studies increased the homogeneity of the examined
be effective. Studies of patients with spinal cord injuries also groups by excluding more severely affected patients and taking
suggest long-term strength training.34 In the present study, the into consideration specific gait parameters.8 In the current
training program was long term (⬇40wk) to cover the time study no such exclusion criterion took place, probably resulting
period after the operation when children show a loss of muscle in the fact that some patients were not able to execute their
force production (D Patikas et al, unpublished data, 2006). training programs as efficiently as others. Another consequence
However, there are some objective difficulties in making such of using multijoint exercises in patients with CP is that the use
a home-based protocol as intense as possible during this long of greater load to increase the training intensity is restricted,
time period, and therefore it cannot be ruled out that the moti- compared with studies that used single-joint movements with
vation of some children may have decreased while performing maximal resistance.10 In our study, the possibility of increasing
the same training protocol. This cannot rule out the possibility training intensity after the surgery was limited, because most
that subjects were “underdosed” to strength training and did not children were able to execute the exercises moving against
get stronger. Furthermore, the children’s mental maturity may gravity at the beginning of the training period (sometimes even
also influence the outcome of training. The age of the children with assistance) and gradually were able to use external resis-
in the present study ranged from 6 to 16 years old. This tance with elastic bands.
imposes a noteworthy variability in the way they understand Only a limited number of studies examined the effect of
the aspect of strength training (as a part of the treatment or as strength training in children compared with a control group that
an obligation for their parents). Such factors may increase the did not perform strength training.8,10 In the most recent ran-
variance within the strength-training group, suppress the con- domized controlled study,8 there was only a trend for the
trast between strength-training and control groups, and make strength-training group to improve in the walking speed and
comparisons between different studies difficult. Methods to GMFM parameters when compared with the control group.
Fig 3. Normalcy index and kinematic parameters for the control and strength-training groups, prior to, 1 year after, and 2 years after surgery.
(A) Normalcy index, (B) minimum knee flexion during terminal swing, (C) maximum hip extension, and (D) maximum plantarflexion during
stance to swing transition. The normative values with SD are represented by the continuous horizontal line and the grey zone (nⴝ29). NOTE.
Values are mean ⴞ SD. *Significant differences between the measurements for the merged group (CGⴙSG) that were examined at E0, E1,
and E2.
Although the GMFM is sensitive enough to detect changes data, the impact of the applied strength-training program was
caused by therapeutic interventions in children with CP,35 this not sufficient to overcome the radical changes that occur in the
was not confirmed in the present study, neither for the GMFM musculoskeletal system after surgery. This can be verified by
scores nor for the other examined parameters. However, the the fact that some temporal parameters that showed worsening
strength-training group in the study of Dodd et al8 had lower— at E1 recovered at E2, although none of the patients followed
although statistically insignificant (P⫽.07)—GMFM scores a strength-training program between E1 and E2.
than the control group during the baseline measurement, which
possibly subdued the likelihood that the strength-training group CONCLUSIONS
would improve. In the current randomized study, this situation The outcome of a specific strength-training protocol applied
was unluckily reversed (the control group had lower GMFM in children with CP may be affected by several factors such as
scores at E0), and this might partially explain the lack of the optimal duration, intensity, and frequency of the training
differences between the groups. session. These factors are still to be defined for optimization of
Although all participants in the present study were diagnosed the training effectiveness, although it is more likely that these
with diplegic spastic CP, we observed a considerable variance parameters should be determined individually for each patient.
on several clinical and gait parameters, and this necessitated The lack of differences between the groups in the present study
specialized surgical treatments, depending on the clinical status could be attributed to the immense effect that the surgery had
of each patient. Consequently, the surgery outcome could be on both groups and should not discourage the application of
neither standardized nor predicted. According to the presented strength training in children with CP. Apart from the psycho-
Fig 4. Kinetic parameters for the control and strength-training groups prior to, 1 year after, and 2 years after surgery. (A) Maximum hip power
absorption, (B) maximum plantarflexor moment, (C) maximum knee power absorption during loading responses, and (D) maximum ankle
power generation. The normative values with SD are represented by the continuous horizontal line and the grey zone (nⴝ29). NOTE. Values
are mean ⴞ SD. *Significant differences between the measurements for the merged group (CGⴙSG) that were examined at E0, E1, and E2.
logic benefits that children have after such training,11,36 a special- 4. Wiley ME, Damiano DL. Lower-extremity strength profiles in
ized training protocol targeted to well-motivated patients may spastic cerebral palsy. Dev Med Child Neurol 1998;40:100-7.
have the potential to counteract the obligatory muscle weak- 5. Damiano DL, Vaughan CL, Abel MF. Muscle response to heavy
ening after the operation. resistance exercise in children with spastic cerebral palsy. Dev
Med Child Neurol 1995;37:731-9.
Acknowledgments: We acknowledge Sven Schneider, PhD (De-
partment of Orthopaedic Surgery, University of Heidelberg) for his 6. Bobath B. Motor development: its effect on general development
support concerning the statistical analysis of the data and Tim The- and application to the treatment of cerebral palsy. Physiotherapy
ologis, MD (Nuffield Department of Orthopaedic Surgery, University 1971;57:526-32.
of Oxford, UK) for editing and commenting on the manuscript. 7. MacPhail HE, Kramer JF. Effect of isokinetic strength-training on
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