Muscle strength
and focus on their child’s ability to walk. Population-based
training to improve
gait function in
children with cerebral
palsy
Meta Nyström Eek* PT MSc, Department of Clinical
Sciences;
Roy Tranberg CPO BSc,
Roland Zügner PT MSc, Lundberg Laboratory for
Orthopaedic Research, Department of Orthopaedics,
Sahlgrenska University Hospital;
Kristina Alkema PT, Disability Administration, Habilitation
Centre;
Eva Beckung PT, PhD, Department of Physiotherapy,
Institute of Neuroscience and Physiology at the
Sahlgrenska Academy, University of Gothenburg, Sweden.
*Correspondence to first author at Regionala barn-och
ungdomshabiliteringen, Box 21 062, SE 418 04 Göteborg,
Sweden
E-mail: meta.nystrom-eek@vgregion.se
DOI: 10.1111/j.1469-8749.2008.03045.x
The aim of the study was to investigate the influence of
muscle strength training on gait outcomes in children with
cerebral palsy. Sixteen children (two females, 14 males, Gross
Motor Function Classification System levels I–II, mean age
12y 6mo, range 9y 4mo–15y 4mo) underwent muscle strength
measurement using a handheld device, Gross Motor Function
Measure (GMFM) assessment, three-dimensional gait
analysis, joint range of motion assessment, and grading of
spasticity before and after 8 weeks of training. All
participants had a diagnosis of spastic diplegia and could walk
without aids. Training consisted of exercises for lower
extremity muscles with free weights, rubber bands, and body
weight for resistance, three times a week. Values for muscle
strength below normal were identified in all children; this was
most pronounced at the ankle, followed by the hip muscles.
After training, muscle strength and GMFM scores increased,
velocity was unchanged, stride length increased, and cadence
was reduced. There was an increase in hip extensor moment
and power generated at push off. Eight weeks of muscle
strength training can increase muscle strength and improve
gait function.
Developmental Medicine & Child Neurology 2008, 50: 759–764 759
Parents of children with cerebral palsy (CP) often ask about
studies show that about 69% of children with CP are classi-
fied as walking with or without aids1,2 according to the Gross
Motor Function Classification System (GMFCS), and that age
at first walking is often delayed.3 A Canadian study of gross
motor development showed improvement of motor function
at early ages until around 5 years, when an average of 90% of
motor development potential has been reached, and that
there is a plateau in gross motor development at about 7
years of age.4 Bell et al. and Johnson et al. demonstrated a
decrease in gait function and pattern through adolescence
and adulthood expressed as a decrease in gait velocity, stride
length, and sagittal joint excursions over time.5,6 Surveys of
adults with CP show decreased walking ability with age.3,7
Possible factors interfering with normal gait pattern in CP
include spasticity, muscle contractures, bony deformities,
loss of selective motor control, and muscle weakness.8
Recent research has focused on muscle weakness. Wiley and
Damiano,9 and Ross and Engsberg10 described muscle weak-
ness as more pronounced distally and found an imbalance
across joints. Several studies of different methods for
muscle strength training show that it is possible to increase
muscle strength in children with CP.11–15 The influence
of muscle strength training on walking ability has been
reported as an increase in the Gross Motor Function Measure
scores (GMFM).12–17
Gait can be measured with three-dimensional (3D) gait
analysis, which provides a description of gait pattern geome-
try (kinematics) and forces (kinetics). Variables such as gait
velocity, cadence, and stride length have been reported to
increase with training11,14 as well as improved kinematics in
the sagittal plane.17 Only one report on kinetics has been
identified, which showed no change in ankle plantar
moment after training of dorsiflexors and plantarflexors.17
Gait can also be measured in terms of efficiency, energy
expenditure index, or physical cost index. One study
reported better efficiency after training15 and two others saw
no change.11,13
Muscle strength in children with CP can be measured reli-
ably with handheld devices.18,19 Damiano et al. demon-
strated that data should be reported as torque (force · lever
arm) to enable comparisons between individuals and over
time.20 A recent study reported normative data obtained with
a handheld device and calculations of torque, and based on
this presented equations for predicted values for each muscle
group based on age, body weight, and sex.21 This makes
comparison possible both over time in one individual and
between individuals of different age and weight.
The aim of this study was to investigate whether muscle
strength training could influence gait function (as measured
by the GMFM) and gait pattern (kinematics and kinetics)
in children with CP between the ages of 9 and 15 years.
The aim was also to use torque and normative values in the
comparison.
Method
PARTICIPANTS
Potential participants were identified from the medical
records of habilitation centres around Göteborg. Inclusion
criteria were bilateral spastic CP, age 10 to 15 years, and

GMFCS levels I and II (walking without aids). Children had
to be able to follow instructions and participate in a group.
Exclusion criteria were orthopaedic surgery or botulinum
toxin injections in the past 12 months. The Ethics Committee
at the Medical Faculty at the University of Göteborg approved
this study. Written informed consent was obtained from
parents of each participant.
PROCEDURE
Examination before and after a period of muscle strength
training consisted of: muscle strength measurement, GMFM,
3D gait analysis, joint range of motion (ROM) measurement,
and grading of spasticity. In terms of the International Classi-
fication of Functioning, Disability and Health,22 these meth-
ods measure ‘body function’ (muscle strength, 3D gait
analysis, ROM, and spasticity) and ‘activity’ (GMFM).
Muscle strength was measured with a handheld device: a
myometer (adapted Chatillon dynamometer; Axel Ericson
Medical AB, Göteborg, Sweden) using the ‘make’ technique,
where the child gradually builds up force against the myome-
ter for about 5 seconds. Three attempts were made for each
muscle group and the maximum-recorded force value was
used for data analysis. Lever arm was measured with a tape
measure, and torque (Nm) was calculated by multiplying
force by the length of each lever arm. Data were also com-
pared to a normative predicted value based on an equation
with parameters for age, body weight, and sex.21 Measure-
ments were divided by the predicted value giving a percent-
age for every muscle group in each child. This made it
possible to compare muscle groups and to compare children
with different ages and weights. Eight muscle groups were
tested (hip extensors, flexors, abductors and adductors; knee
extensors and flexors; and ankle dorsiflexors and plantarflex-
ors) with the same testing positions as in the normative
study.21 For ankle plantarflexors no normative predicted
value was available for children over the age of 9 years.
Gross motor function was tested with GMFM domains D:
standing, and E: walking, running, and jumping. The Gross
Motor Ability Estimator software which was included in the
GMFM-66 version23 was used to calculate a score.
3D gait analysis was carried out with a motion capture sys-
tem consisting of six infrared cameras (ProReflex Qualisys
AB, Göteborg, Sweden) and two Kistler force plates (Kistler
9281C, Kistler Instruments AG, Winterthur, Switzerland)
working synchronically at 240Hz. Recordings of motion and
calculations were made with the software QtracC version
2.51, QtracV version 2.60, and QGait 2.0 (Qualisys Medical
AB, Göteborg, Sweden).24 At least three acceptable trials for
each child were collected. Parents confirmed that the perfor-
mance was representative of their children’s regular gait pat-
tern. 3D gait data were compared with the laboratory
reference database for children between 10 and 15 years of
age (27 children, mean age 12y 11mo). Gait velocity, stride
length, and cadence were compared with age norms.25
ROM was measured in the lower extremities using a regu-
lar plastic goniometer (hip extension, hip abduction, knee
flexion, popliteal angle, and ankle dorsiflexion). Deviations
outside 2 standard deviations from normal values were
noted.26,27
Spasticity was tested in four muscle groups with the Ash-
worth scale:28 0=hypotonus; 1=normal; 2=resistance
through less than half ROM; 3=resistance through most of
760 Developmental Medicine & Child Neurology 2008, 50: 759–764
14698749, 2008, 10, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03045.x by Cochrane Chile, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ROM; and 4=difficult to move passively. Examination was
done with children lying in a relaxed supine position for hip
adductors, hamstrings, and plantarflexors, and in a prone
position for rectus femoris. Scores for each child were
totalled and divided by number of muscles tested, a method
described by Ostensjø et al.29 The summary index was then
categorized: no increase (£1), mild (>1 to £2), or moderate
(>2).
Muscle strength measurements, GMFM, ROM, and spas-
ticity were tested by two of the authors (MNE, KA who are
physiotherapists and gait analysis was carried out by the
gait laboratory staff). Testing was performed the week
before training started and a week after training. Muscle
strength was also tested 2 weeks before training and 2
weeks after training. Mean muscle strength measurements
in Nm before, were compared with mean measurements
after training.
Before training started there was an individual analysis of
each child based on muscle strength measurements and 3D
gait analysis, identifying muscles with the most pronounced
muscle weakness and most important gait pattern abnormali-
ties (like a small abducting moment in the hip, too much
knee flexion during stance, or no power generation in the
ankle at push off). This resulted in an individual training pro-
gramme for each child, containing specific training instruc-
tions for four different muscle groups.
The training period lasted for 8 weeks, three times a week:
twice a week at home with parental assistance and once a
week in a small group with a physiotherapist at the physio-
therapy department after school. Children were divided into
small training groups based on age. At home they carried out
the individual programme with three sets of 10 repetitions
for each muscle group: first set easy, second medium, and
third with a heavy load – 10 Repetition Maximum (10RM).
Resistance was provided by adjustable weight cuffs for the
medium and heavy sets. Rubber bands and body weight were
used for the easy set and when it was not possible to use
weight cuffs. Weight resistance was increased during the
training period when the children could do more than 10
repetitions with the 10RM weight.
The group session consisted of a low intensity short
warm-up session with a cycle ergometer, rowing machine, or
step-up. After initial warm-up, children carried out their indi-
vidual programmes with strength training exercises. Stretch-
ing of hamstrings, rectus femoris, and plantarflexor muscles
followed the training session. All meetings ended with a
group activity chosen by the children (different games). The
sessions lasted for one hour and a half in total. Each child
had a training diary, indicating dates and resistance. Group
training sessions and decisions on increasing resistance were
carried out by two physiotherapists.
STATISTICAL ANALYSES
Non parametric tests were used as the group was small
and data could not be proved to be normally distributed.
Gait data for the CP group and laboratory reference data-
base were analyzed with the Mann–Whitney U test. All
differences before and after training were analyzed with
the Wilcoxon signed rank test except for spasticity grad-
ing where the paired sign test was used. Significance
level was set at p<0.05. Statistical tests were performed
using StatView software (SAS Institute Inc).
 14698749, 2008, 10, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03045.x by Cochrane Chile, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Results (Table II). When results were divided into groups of targeted
Twenty-four children met inclusion criteria, and of these or non-targeted muscle groups, there was a visible increase
eight chose not to participate. Of the 16 participating chil- in hip extensors and flexors in all children. Stronger hip
dren there were 14 males and two females with a mean age abductors, adductors, and ankle plantarflexors were found in
of 12 years and 6 months (range 9y 4mo–15y 4mo). Accord- those who had targeted these muscle groups. Knee flexors
ing to the GMFCS, 10 children were classified at Level I and and ankle dorsiflexors were stronger in those who did not
six at Level II (Table I). Two training diaries were not avail- target these muscle groups.
able. Of a possible 24 training sessions, 14 children per-
formed a mean of 18 sessions (range 11–23y; 76%). There GMFM
was no report of negative events caused by the training dur- Three of the children scored 100% before training. For the
ing the period. There was no change in children’s regular other children there was a statistically significant increase
therapy and no one was using orthoses. after training (Table III). This increase was mostly attribut-
able to the ability to stand on one leg (seven children had a
MUSCLE STRENGTH higher item score than before training) and to hop on one
All children could lift their legs against gravity with resistance. foot (four had a higher item score).
Values below normative predicted were identified in all chil-
dren (Table II). Weakness was most pronounced at the ankle, GAIT
followed by hip muscles. Muscles around the knee were Gait velocity, stride length, and cadence were within age
strongest, with values within normative predicted ranges for norms except in two cases where stride length was short for
knee extensors in 12 children. Torque values for plantarflex- age. Velocity did not change after the training period,
ors were below normative values (for 9-year-old children cadence was reduced, and there was a tendency to increased
40.2 Nm).21 Most of the children undertook training exer- stride length (Table III).
cises for ankle dorsiflexors (n=12) and plantarflexors
(n=12), hip abductors (n=12), and hip extensors (n=10),
based on the pre-testing examination. Table III: Results from Gross Motor Function Measure
After the training period there was a significant increase in (GMFM) and time–distance gait parameters (n= 16)
muscle strength in all hip muscle groups and in knee flexors
Before training, After training, Wilcoxon
median (range) median (range) signed rank
Table I: Mean (SD) age, weight, and height of participants p
according to Gross Motor Function Classification System
(GMFCS) level GMFM 84.8 (66.7–100) 90 (67.4–100) 0.003
Velocity, 1.2 (1–1.5) 1.25 (0.9–1.6) 0.859
GMFCS level Age, y Weight, kg Height, cm m ⁄ sec
Stride, m 1.1 (0.9–1.4) 1.15 (0.9–1.5) 0.059
I, n=10 12.2 (1.8) 36 (7.1) 146 (12) Cadence, 132 (108–151) 130.5 (104–149) 0.016
II, n=6 13 (2) 43.9 (8.9) 150 (10) steps ⁄ min

Table II: Muscle strength before and after traininga

Muscle group Before training period, After training period, Comparison before and after training, p-value
median (range) and % of median (range) All n=32 Targeted Non-targeted
predicted normal value muscle group muscle group

Hip extensors, Nm 49.8 (22.2–106.5) 55.2 (26.7–161.5) <0.001 0.001, n=20 0.049, n=12
61.6 (34.9–104.6)
Hip flexors, Nm 44.5 (16.9–97) 49 (20.9–121.3) <0.001 0.025, n=8 <0.001, n=24
67.1 (30–110.1)
Hip abductors, Nm 38.8 (19.3–89.7) 42.5 (23–109.3) <0.001 <0.001, n=24 0.263, n=8
62.8 (37–113.4)
Hip adductors, Nm 39.7 (21.8–94.3) 45.4 (24.7–105.5) 0.001 0.002, n=12 0.117, n=20
66.4 (41.9–109.4)
Knee extensors, Nm 51.1 (24.2–106.4) 57.7 (22.1–98.6) 0.955 0.917, n=6 0.869, n=26
84.6 (52.1–113.5)
Knee flexors, Nm 44 (23.2–97.1) 46.3 (27.6–107.9) 0.001 0.075, n=6 0.006, n=26
83.8 (51.3–124.9)
Ankle dorsiflexors, Nm 10.9 (0.6–20.5) 11.5 (0–25.7) 0.057 0.339, n=25 0.018, n=7
46 (2–68.8)
Ankle plantarflexors, Nm 30.4 (13–65.3) 33 (14.1–73.8) 0.132 0.014, n=25 0.311, n=7
a
Results are presented as torque (Nm) and as a percentage of predicted normal value21 (except for ankle plantarflexors which is only
torque). n=number of legs. Wilcoxon signed rank p-values based on Nm data.

Strength Training and Gait in CP Meta Nyström Eek et al. 761


Kinematic and kinetic gait pattern parameters were tested,
and children with CP differed significantly from normal for
sixteen of these variables which were chosen for statistical
testing (Table IV). There was a significant increase in hip
extensor moment and plantarflexor generating power at
push-off after the training period (see example Fig. 1).
CONTRACTURES AND SPASTICITY
Decreased ROM outside 2SDs from normal was present in all
children. After the training period there was a statistically
significant increase in hamstring length, with a median
(range) of 135 (120–165) before, and 136 (125–155) after
(p=0.002) but no change in other muscle groups.
Increased muscle tone was graded as no increase in two
of the children, mild in 12, and moderate in two. There was
no statistical difference in spasticity grading after the training
period.
Discussion
This study shows an increase in muscle strength, and measur-
able positive changes in gait function and pattern with train-
ing. This is comparable with the findings from earlier studies,
which also showed some significant changes and trends in
both muscle strength and gait function.12,14
GMFM scores increased at group level, which was slightly
unexpected as three children had already scored 100 (full)
before training. Items that showed changes were most often
standing on one leg and hopping on one foot, which require
stability and strength at hip and ankle. The ability to balance
on one leg is very important for many tasks in everyday life,
such as negotiating obstacles and climbing stairs. Several
studies on the natural history of gross motor development in
children with CP shows that there is not much increase in
the GMFM after 7 years of age.4,30,31
This study shows that an intervention can make a change
in the GMFM even after these ages. Wang and Yang report a
change of 3.71 on the GMFM-66 to be a clinically visible
improvement.32
14698749, 2008, 10, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03045.x by Cochrane Chile, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Gait analysis showed increased stride length and plantar-
flexor generating power at push off after training. This could
be explained by better stability around both hip and knee
that increases stability in stance and which makes it easier for
the ankle plantarflexors to push off actively. The increased
stride length and push off corresponds well with the increase
in muscle strength around the hips and with the increase in
balance on one leg visible in the GMFM.
There is a need for further analysis of the relationship
between muscle strength and gait pattern to augment under-
standing of gait deviations in CP, and for planning effective
treatment and training. Some earlier studies of the effects of
strength training on gait have shown increased velocity with
training.11,14 This was not found in the current study. Some
children varied in velocity during the same session but there
was no pattern of systematic change after the training period.
Children in the current study all walked without assistive
devices and their gait velocity was already within normal age
variation. Studies with increased velocity after training
included children walking with assistive devices, who proba-
bly had a low walking velocity before training.
W/Kg
3
2
1
0
0 10 20 30 40 50 60 70 80 90 100
–1
–2
–3
Figure 1: Ankle generating power. Grey band, lab reference,
dotted line, mean before, solid line, mean after.

Table IV: Gait analysis data for 16 children (both legs)

Gait variable Before training, After training, pc

median (range) median (range)

Kinematics, Hip Extension in stance )2.9 ()19.8 to 12.5) )3.8 ()19.5 to 18.4) 0.135
Flexion in stance 45.4 (17.4 to 71.4) 46.7 (16.9 to 76.1) 0.155
Knee Initial contact 17.9 (5.7 to 43.7) 19.5 (3 to 46.9) 0.421
Extension in stance 6.1 ()18.5 to 28.1) 6 ()20 to 25.6) 0.231
Ankle Initial contact )4.3 ()22.1 to 5.8) )5.9 ()17.5 to 3.9) 0.940
Dorsiflexion in stance 8.9 ()8.6 to 17.5) 7.1 ()4.1 to 19.5) 0.903
Dorsiflexion in swing )0.4 ()17 to 30) )1.1 ()17.1 to 14.8) 0.184
Kineticsa Hip Extension moment 0.66 ()0.1 to 1.38) 0.78 (0.11 to 1.30) 0.015
Flexion moment 0.59 (0.33 to 1.30) 0.71 (0.37 to 1.30) 0.067
Abduction moment 1 0.52 (0.12 to 1.25) 0.51 (0.23 to 1.28) 0.860
Abduction moment 2 0.44 (0.12 to 0.86) 0.48 (0.16 to 0.91) 0.088
Knee Extension moment 0.76 (0.19 to 1.69) 0.67 (0.26 to 2.32) 0.899
Flexion momentb )0.41 ()0.93 to 0.10) )0.38 ()0.99 to 0.14) 0.318
Ankle Plantarflexion moment 1.08 (0.70 to 1.60) 1.11 (0.75 to 1.71) 0.193
Generating power 1.59 (0.64 to 3.17) 1.91 (0.35 to 3.75) 0.046
Absorbing power 1.22 (0.44 to 7.52) 1.18 (0.52 to 4.34) 0.772
a
Nm ⁄ kg body weight for moment, and W ⁄ kg for power; bKnee flexion moments reported as negative values (in italic) reflects an exten-
sion moment of the knee; cWilcoxon signed-ranks test p<0.05.

762 Developmental Medicine & Child Neurology 2008, 50: 759–764


Is increased muscle strength the factor that determines
better gait? Many of the children in the current study had
reduced ROM before the training started, and the pro-
gramme included a stretching session. However, the only
change in ROM that could be observed was a small increase
in the hamstrings (which was clinically not remarkable and
within measurement error) and there was no change in spas-
ticity grading. Studies on the relationship between clinical
measurements and gait parameters found that muscle
strength and selective motor control correlated better with
gait data than ROM and spasticity.33,34
Gormley stated that CP is a disorder that manifests dif-
ferently in each child, and for optimal results of interven-
tions an individual analysis is needed together with an
individual plan for treatment.8 This is the main reason this
study developed individual programmes for the children,
but it led to problems when comparing data, as the group
was small which made the use of subgroups difficult. The
result that there was increased strength in muscle groups
that were not targeted in the training was unexpected. It is
likely that this effect can be explained in terms of the
human body being a system where activation of one mus-
cle group also requires activation of other muscle groups
needed for stabilization of adjacent joints. This stabilizing
mechanism may give a training effect and can explain why,
for example, muscle strength in the hip flexors increased
although they were only included in the programme for
some of the children. Almost all the children in this study
had weakness in the dorsiflexors, and these muscles were
included in the programmes for most of them; however,
there was no increase of strength in the dorsiflexors. This
is a muscle group that is often difficult to activate in isola-
tion and, therefore, may need special attention. This has
been carried out in a previous study focusing on training
dorsiflexors with the help of computer-assisted biofeed-
back, and increased strength was reported.35
Conclusion
Eight weeks of individually-designed training with a focus on
muscle strength not only increased muscle strength, but also
improved gait function in children with CP. Increase in mus-
cle strength is one of the major factors for the improvement
in gait function so the current results support muscle
strength training as a means of improving gait in children
with CP.
Accepted for publication 11th January 2008.
Acknowledgement
We thank the Norrbacka-Eugenia foundation, the Research and
Development Foundation of Göteborg and Bohuslän, Linnéa
och Josef Carlsson foundation, and Petter Silfverskiöld foundation
for funding this research.
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