Aumentos del volumen muscular después del entrenamiento de fuerza del flexor plantar en niños con parálisis cerebral espástica

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DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY ORIGINAL ARTICLE

Increases in muscle volume after plantarflexor strength training in


children with spastic cerebral palsy
ANNE E MCNEE MPTHY1,2 | MARTIN GOUGH FRCS
1
| MATT C MORRISSEY SCD 2 | ADAM P SHORTLAND PHD 1
1 One Small Step Gait Laboratory, Guy's Hospital, London, UK. 2 Division of Applied Biomedical Research, School of Biomedical and Health Sciences, Kings College,
London, UK.

Correspondence to Anne McNee at One Small Step Gait Laboratory, St Thomas Street, London SE1 9RT, UK. E-mail: anne.mcnee@gstt.nhs.uk

PUBLICATION DATA Children with spastic cerebral palsy (CP) have small, weak muscles. However,
Accepted for publication 31st October 2008. change in muscle size due to resistance training in this group is unknown. We
Published Online 21st January 2009 investigated the effect of plantarflexor strengthening on muscle volume, gait,
and function in 13 ambulant children with spastic CP (seven males, six females;
ACKNOWLEDGEMENTS
mean age 10y 11mo, SD 3y 0mo, range 6y 11mo–16y 11mo; eight with diplegia,
This study was funded by the Nancie Finnie
five with hemiplegia; Gross Motor Function Classification System level I, six;
Charitable Trust. The authors would like to
level II, five; level III, two). Assessments were performed before training, 5 and
thank Jill Larkins and Eskinder Solomon for
assistance with the training, and Nicola
10 weeks into training, and at a 3-month follow-up. Medial and lateral
Fry and the staff at the gait laboratory for gastrocnemius volumes were computed from three-dimensional ultrasound
assistance with data collection. images. The number of unilateral heel raises able to be achieved on each side
was assessed. Function was measured using three-dimensional gait analysis,
the ‘timed up and go’ test, the Gillette Functional Assessment Questionnaire,
and the Functional Mobility Scale. Training involved heel raises or Thera-Band
resistance, 4 times a week for 10 weeks. Medial and lateral gastrocnemius
volumes increased by 17 and 14% at week 5 (p=0.03, p=0.028). This increase was
maintained at week 10 and follow-up (medial gastrocnemius p=0.001, p<0.001;
lateral gastrocnemius p=0.006, p=0.007). Heel raises (mean number) increased
by week 5 (p=0.002). This was maintained at week 10 and follow-up (p<0.001;
p<0.001). No significant change in measured function was observed. Muscle
volume increased in response to training in children with spastic CP. The role
of progressive strength training in maintaining long-term function is discussed.

Children with spastic cerebral palsy (CP) have profound extensors in a group of children with spastic CP over 6
weakness of the muscles of their lower limbs. Using dyna- weeks using free weights. They found an increase in knee
mometry, Wiley and Damiano1 demonstrated that muscle extensor force by up to 160% and a small reduction (5) in
groups in independently ambulant children with spastic knee flexion at initial contact. Using circuit training, Unger
CP produce as little as 52% of the force of those in et al.11 increased the strength of the upper limb, trunk, and
matched typically developing children during maximum proximal lower limb musculature in 23 children with spas-
voluntary contraction. The origin of this profound weak- tic CP over 8 weeks. This training also significantly
ness is multifactorial, with deficits in motor unit activation reduced the degree of crouch by 5. Engsberg et al.12
accounting for as much as 73% of loss of force2 and reduc- found a small increase in walking speed and increased
tions in muscle volume being as much as 50%.3,4 Muscular stride length in four participants who strengthened their
performance may be further compromised by deleterious ankle plantarflexors. In the same study, minimum knee
changes in muscle tissue properties5 and coactivation of flexion in stance and dimension E of the Gross Motor
antagonist muscle groups.6 Function Measure (GMFM) improved in participants who
Resistance training has become an increasingly common trained their dorsiflexors as well as their plantarflexors.
intervention aiming to improve function by increasing Dodd et al.10 describe a lower-limb extensor training pro-
muscular strength.7-12 Damiano et al.7 trained the knee gramme using closed kinetic chain exercises for 10 children

ª The Authors. Journal compilation ª Mac Keith Press 2009


DOI: 10.1111/j.1469-8749.2008.03230.x 429
14698749, 2009, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03230.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
with spastic CP. Combined lower-limb extensor strength casting in the past 3 months, or were not able to comply
increased after 6 weeks of training and remained improved with the requirements of gait analysis or our training sche-
at 12-week follow-up. These authors also found a trend dule. They were also excluded if they had an ankle plantar-
towards improvement in GMFM dimension E. However, flexion contracture greater than 15 or had a knee or hip
this did not reach significance. Overall, short-term fixed-flexion deformity greater than 10. Written informed
strengthening programmes appear to result in increased consent from the parents or guardians of participants was
strength associated with only mild improvements in gait obtained before the first assessment. The participants gave
and function. verbal consent after reading or listening to a short descrip-
The effect of resistance training on muscle size in chil- tion of the project. Twenty-two children agreed to partici-
dren with spastic CP is unknown. To increase the size of pate; 20 started the programme, with 14 completing it and
healthy muscle progressive strength training for a pro- 13 attending for assessment. Ten participants completed
longed period is required. It is thought that improved mus- the follow-up assessment 12 weeks after cessation of
cle activation is responsible for the major portion of training.
strength gained within the first 3 to 5 weeks of training.13
After this time, increases in strength are mainly due to Training programme
hypertrophy. The mild gains in function reported in the The participants trained four times each week for 10
literature after training in individuals with spastic CP may weeks. Three of these sessions took place at home and one
be in part due to the short training period adopted by the session was conducted at the tertiary centre, where the
investigators. exercises were evaluated and progressed by a physiothera-
The potential impact of a strengthening programme pist (AM). Each training session consisted of a 3 to 5 min-
may also vary according to the muscle group(s) targeted. In utes aerobic warm-up, followed by plantarflexor stretches
spastic CP, the distal lower-limb musculature is weaker1 conducted by the participant while standing. Maximum
and may be proportionally smaller than proximal muscles.3 available dorsiflexion was attained and body weight was
In normal human walking, the plantarflexors provide much used to maintain the stretch. The plantarflexor strengthen-
of the force required to support the body and advance the ing exercises were then performed. The session was com-
lower limbs, particularly in mid- and late stance.14 Typical pleted by a 3 to 5 minute cool-down and plantarflexor
changes to the gait pattern of children with spastic CP are stretches. The strengthening exercises were progressive in
ankle plantarflexion through stance and swing, and that loading levels were monitored and adjusted to main-
increased knee and hip flexion in stance.15 Concentrating tain muscle loading as muscle strength increased. The left
on strengthening the plantarflexors rather than more prox- and right plantarflexors were strengthened independently.
imal musculature may improve the functional outcome of The load applied to each side was dependent on the evalu-
training for this group. We hypothesized that a 10-week ated strength of that side. The exercises were performed
programme of plantarflexor strengthening would result in in three to four sets, with participants performing the
muscle hypertrophy, normalization of the gait pattern (par- maximum number of repetitions that they could produce
ticularly improvements in ankle dorsiflexion because of the (minimum of six repetitions up to a limit of 12, corres-
pennate nature of the muscle trained16 and knee extension ponding to 6 to 12 repetitions maximum). Participants
in stance), and an improvement in walking function in a were required to rest for a minimum of 2 minute between
group of children with mild spastic CP. sets. For those participants who were able to perform more
than 12 heel raises, exercises were progressed by adding
METHOD weight to a rucksack worn on the participant’s back. Not
Participants all participants could achieve single-leg heel raises and 10
Ethical approval for the study was granted by the local hos- children began their exercise programme using an elasti-
pital research ethics committee. Participants were recruited cated band (Thera-Band, The Hygenic Corporation,
through the orthopaedic clinic of the Evelina Children’s Akron, OH, USA) to provide resistance to the plantarflex-
Hospital, London, and from three community physio- ors on one or both lower limbs. The Thera-Band exercise
therapy departments (The Phoenix Centre, Bromley, The was performed with the participant in the long-sitting posi-
Kaleidoscope Centre, London, and the Wilfred Sheldon tion, i.e. with the knee in full extension. For those using
Centre, London). The inclusion criteria were a diagnosis the Thera-Band for resistance training, when a limit of 12
of spastic CP and the ability to walk for 10m with or with- repetitions was reached, their exercises were progressed by
out the use of a mobility aid. Participants were excluded if using a heavier Thera-Band or by changing to heel raises.
they had undergone surgery in the past year, or had had The training routine (sets, repetitions, types, and load)
botulinum toxin A injections in the past 6 months or serial was recorded in a diary. During the 3-month period after

430 Developmental Medicine & Child Neurology 2009, 51: 429–435


14698749, 2009, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03230.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
training, the amount of exercise completed by each partici- (achieved through manual manipulation) with the knee in
pant was not monitored. full extension. A three-dimensional volume containing the
muscle was reconstructed. Muscle cross-sectional area was
Assessment measured at each of 10 equally spaced sections along the
Each participant was examined by two authors (AS, AM) length of the muscle. Volume was calculated using disk
and other gait laboratory staff before the training period summation. Raw volume data and volume data normalized
(baseline), 5 weeks into training (week 5), on completion of to body mass were analysed.
the 10-week training (week 10), and at 12-week follow-up
after completion of training. Assessment and training were Statistical analysis
always conducted on different days. Maximum passive One-way repeated-measure analysis of variance was
ankle dorsiflexion range of movement with the knee held used to test for the effects of the strengthening regime
in both flexion and extension was measured using a hand- on muscle volume, passive ankle range of motion, and
held goniometer. Body height, mass, and lower limb length specific gait parameters. A Fisher least-significant-
were measured. The number of heel raises that each partic- difference post-hoc test was used to ascertain significant
ipant could perform on each lower limb was counted.17 changes between assessments. A p value <0.05 was con-
The ‘timed up and go’ test,18 Functional Mobility Scale,19 sidered significant. Functional scores and number of
and Gillette Functional Assessment Questionnaire20 were heel raises were compared using the Friedman test. For
used to assess functional mobility. the variables that showed significant changes, Conover
A three-dimensional analysis system (7-camera Vicon post-hoc tests were applied, again at a significance level
612, Vicon, Oxford, UK) was used to evaluate each partici- of 95%.
pant’s barefoot gait pattern at a self-selected speed. The
mean of five trials from the right and left lower limbs at RESULTS
each assessment was analysed. Minimum knee flexion in Thirteen participants (seven males, six females) aged
stance and peak dorsiflexion were extracted from the aver- between 6 years 11 months and 16 years 11 months (mean
aged data. Self-selected walking velocity, cadence, and 10y 11mo, SD 3y) participated in training. Eight partici-
stride length were also measured. pants had a diagnosis of diplegia and five had hemiplegia.
A freehand three-dimensional tracking system (Com- Two participants required a Kaye walker for assistance with
pactScan, TomTec GMBH, Munich, Germany) was used walking (Gross Motor Functional Classification System
to acquire the images from the video output of an ultra- [GMFCS] level III ). All others were independently ambu-
sound scanner (SSD-1000, ALOKA, Tokyo, Japan) while lant (six at GMFCS level I; five at GMFCS level II).
simultaneously recording the position and orientation of Ten participants (15 limbs) began training using a
the ultrasonic probe.21 Longitudinal scans were taken from Thera-Band as resistance. During the 10-week pro-
the calcaneus to the femoral condyles following the courses gramme, six participants (seven limbs) progressed to heel
of the Achilles tendon and head of the gastrocnemii raise exercises, two participants (two limbs) used a combi-
(Fig. 1). Scans were taken on both legs with the participant nation of heel raises and Thera-Band exercises, and four
prone, and the ankle at its resting angle (relaxed position of participants (six limbs) were unable to progress to heel
the foot) and at the angle of maximum passive dorsiflexion raise exercises. Significant increases in the number of heel
raises achieved were seen on both sides between baseline
and week 5 (p=0.002), baseline and week 10 (p<0.001), and
baseline and follow-up (p<0.001; Table I). No significant
change was seen between the other time intervals. Those
participants unable to perform any heel raises before train-
ing showed the least improvement in the number of heel
raises achieved.
MG muscle belly

Knee Foot Ankle range of motion


The mean ankle dorsiflexion range before training was
1.7 measured with the knee in extension and 8.7 mea-
Figure 1: Longitudinal ultrasonic image of the medial gastrocnemius sured with the knee in flexion. There were mild increases
from one female participant (age 8y 5mo) before exercising. MG, in dorsiflexion range at week 5 (0.8 knee extended, 3 knee
medial gastrocnemius. flexed). These changes were maintained at week 10 and
follow-up; however, they were not statistically significant.

Muscle Volume after Training in Spastic CP Anne E McNee et al. 431


14698749, 2009, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03230.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
Table I: Median values (range) for functional measures at different points in the strengthening programme. Timed Up and Go scores expressed as
mean (SD)

Baseline Week 5 Week 10 Follow-up

Functional Mobility Scale 17 (4)18) 17 (8)18) 17 (8)18) 17 (5)18)


Gillette Functional Assessment Questionnaire 9 (2)10) 9 (2)10) 9 (7)10) 9 (8)10)
Timed Up and Go, s 5.6 (0.7) 5.5 (0.9) 5.63 (0.7) 5.37 (0.8)
Heel raises, n 1 (0)30) 4.5 (0)50)a 10 (0)50)b 9.5 (0)60)c
Participants, n 13 13 13 10

a
Significant difference between baseline and week 5 (p<0.05); bsignificant difference between baseline and week 10 (p<0.05); csignificant
difference between baseline and follow-up (p<0.05). Week 5, 5 weeks after commencement of the programme; week 10, at the end of the
10-week programme; Follow-up, 12 weeks after the end of the programme.

Table II: Mean (SD) of the absolute and normalized medial gastrocnemius (MG) and lateral gastrocnemius (LG) volumes at different points in the
strengthening programme

Baseline Week 5 Week 10 Follow-up

MG volume, ml 58.7 (26.0) 69.8 (32.3)a 72.5 (30.6)b 80.5 (38.4)c,d


LG volume, ml 42.3 (20.0) 46.6 (20.6)a 49.9 (21.5)b 50.9 (23.7)c
Normalized MG volume, ml ⁄ kg 1.6 (0.6) 1.7 (0.5)a 1.9 (0.7)b 1.7 (0.5)c
Normalized LG volume, ml ⁄ kg 1.1 (0.5) 1.2 (0.4) 1.3 (0.4)b 1.16 (0.5)
Limbs, n 26 26 26 20

a
Significant difference between baseline and week 5 (p<0.05); bsignificant difference between baseline and week 10 (p<0.05); csignificant
difference between baseline and follow-up (p<0.05); dsignificant difference between week 5 and follow-up (p<0.05). Week 5, 5 weeks after
commencement of the programme; week 10, at the end of the 10-week programme; Follow-up, 12 weeks after the end of the programme.

Muscle volume
Muscle volumes measured with the ankle in maximum
dorsiflexion and at rest were not significantly different. Vol- 3
Normalized Vol (ml/kg)

umes reported are from the maximum dorsiflexion angle. 2.5


b
Table II shows the change in absolute and normalized 2 a c
b
medial and lateral gastrocnemius volume over the assess- 1.5 a c
ment period, with changes in the medial gastrocnemius 1
volume displayed in Figure 2. Medial and lateral gastro- 0.5

cnemius volume increased by 16.6 and 13.5% respectively 0


PreE Wk5 Wk10 FU Typically
between baseline and week 5 (p<0.003 and p=0.028). By Developing
week 10, the volumes of the medial and lateral gastro-
cnemius were 23.1 (p=0.001) and 23.6% (p=0.006) greater
Figure 2: Mean medial gastrocnemius (MG, black solid bars) and
than at baseline. Although the mean levels of muscle
lateral gastrocnemius (LG, grey and white striped bars) volume (SD 1
volume increased between week 5 and week 10 for both
standard error) over the 10-week training period and at follow-up.
the medial and the lateral gastrocnemius, these changes did a
Significant difference between baseline (PreE) and week 5 (wk5)
not reach significance. At follow-up, muscle volume was (p<0.05); bsignificant difference between baseline and week 10 (wk10)
increased by 30.5% in the medial gastrocnemius and (p<0. 05); csignificant difference between baseline and follow-up 12
19.7% in the lateral gastrocnemius compared with baseline weeks after the end of the programme (FU) (p<0.05). Normalized MG
measurements (p<0.001, p=0.007). There was no significant and LG volume in a typically developing group of 15 children (four
change in muscle volume between week 10 and follow-up males, 11 females) are also illustrated on the right (age, mean 9 y
(medial gastrocnemius: p=0.422, p=0.625). Muscle volume 6mo; range 6y 4mo–13y 3mo; MG, grey solid; LG, grey striped).
was divided by body mass to account for the confounding

432 Developmental Medicine & Child Neurology 2009, 51: 429–435


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Table III: Mean (SD) gait parameters at different points in the strengthening programme

Baseline Week 5 Week 10 Follow-up

Knee flexion single support,  14.3 (6.1) 16.1 (4.8) 13.4 (6.3) 14.5 (6.2)
Maximum ankle dorsiflexion, second half stance  11.7 (10.7) 12.6 (10.2) 12.0 (9.2) 10.7 (11.1)
Cadence, steps ⁄ min 117.9 (20.9) 120.1 (17.1) 119.6 (14.8) 121.8 (10.1)
Walking speed, m ⁄ s 1.03 (0.3) 1.08 (0.3) 1.06 (0.2) 1.12 (0.2)
Time spent in single support, % 38.7 (3.4) 39.0 (3.2) 38.8 (2.6) 39.4 (2.2)
Participants, n 13 13 13 10

Week 5, 5 weeks after commencement of the programme; week 10, at the end of the 10-week programme; Follow-up, 12 weeks after the
end of the programme.

effects of skeletal growth. Normalized medial gastrocne- function observed may have been limited compared
mius muscle volume showed significant increases between with a more comprehensive exercise programme. Wid-
baseline and week 5 (p=0.003), week 10 (p<0.001), and fol- ening the scope of our intervention to include other
low-up (p<0.002; Table II). Normalized lateral gastrocne- muscle groups might have been of more functional
mius volume showed a significant increase between benefit to the participants.
baseline and week 10 (p=0.014). No significant change in At baseline, many of the children in this study showed
normalized lateral gastrocnemius volume over any other only mild gait deviations and scored close to the top of the
intervals was seen. functional scales employed. Gait analysis performed in a
controlled environment such as the gait laboratory and the
Spatio-temporal parameters functional measures used here may not be sensitive to any
No significant change in self-selected walking speed, stride genuine improvements in walking function that these chil-
length, or cadence over the assessment period was found. dren achieved after training. Other measures aimed at test-
No kinematic parameter selected showed significant ing higher levels of function may better detect
change (Table III). Three independently ambulant partici- improvements in more able participants.
pants walked with greater than 15 of knee flexion in stance This was a longitudinal study where participants acted
at baseline and all showed a reduction in knee flexion at as their own controls. A randomized controlled trial may
week 10. account for the potentially confounding effects of growth
and natural history. However, when muscle volume was
Functional performance normalized for body weight, percentage increases were
The functional scores increased slightly through the period found to be similar to those using the actual volume mea-
of the study although the differences failed to reach signifi- surements (Table II).
cance (Table I). Strength was not directly measured because of the poor
reliability reported for plantarflexor strength testing using
DISCUSSION a hand-held dynamometer.22 The standing heel raise test
We originally hypothesized that progressive plantarflexor has been proposed as a better test of plantarflexor function
strengthening for 10 weeks would result in increases in than dynamometry.17 Additionally, it is likely that the
plantarflexor volume and would improve the gait pattern participants in our study had improvements in motor unit
and functional walking performance of a group of children recruitment during the heel raise test over the training
with spastic CP. Significant increases in plantarflexor vol- period, but we did not measure muscular activation.
ume were seen; although the indices of gait and mobility At follow-up, muscle bulk was maintained. Our results
improved they did not reach statistical significance. The may be confounded by some (four) participants electing to
results presented here are similar to those of others, who independently continue with their exercises during this 12-
found that training led to substantial increases in strength week period. However, Dodd et al.10 found lower-limb
but moderate or undetectable changes in measured func- extensor strength to be maintained 12 weeks after a 6-week
tion.7–12 training programme. Darrah et al.9 also demonstrated
overall body strength to be maintained 10 weeks after
Limitations training.
Because only the plantarflexors were targeted in the The increases in muscle volume observed are greater
training programme, the potential improvement in than those reported in healthy populations. Aagaard

Muscle Volume after Training in Spastic CP Anne E McNee et al. 433


14698749, 2009, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8749.2008.03230.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
et al.23 described a 14-week programme to strengthen the CONCLUSION
quadriceps in a group of 11 adult male participants. They Preservation of muscle function and mobility is one of the
showed a 14% increase in muscle volume measured by primary aims in the management of children with spastic
magnetic resonance imaging. Others report an increase up CP, and intervention is often directed at the plantarflexors.
to 11.4% in the cross-sectional area of the knee extensors This is the first study to demonstrate that muscle hypertro-
in groups of elderly people after training.24 No study has phy is possible after progressive overload training in a pae-
reported changes in plantarflexor muscle volume during diatric population. If it transpires that increases in muscle
training. Perhaps the magnitude of change in muscle vol- volume result in maintenance of function for this patient
ume reported here is related to the plantarflexor muscle group, strengthening may turn out to be one of the most
group, the age of the participants, or the reduced volume important interventions available to ambulant individuals
of the muscles before training. with spastic CP.
One participant reported discomfort in the region of the
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