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The effect of Resistance training on Gait kinematics and Kinetics in
Children with Cerebral Palsy: A Systematic Review
By Daniel Yazbek
Abstract
Aim: This paper reports a systematic review of Progressive resistance training
(PRT) interventions for children with Cerebral Palsy. The sum of randomised
controlled trials (RCT’s) within this review, aims to quantify if regular strength training
increases gait velocity. Background: Secondary problems associated with Cerebral
Palsy affect normal gait mechanics compared to healthy people. Those with CP have
shown to be significantly weaker than their healthy counterparts. Muscle weakness
has been found to negatively affect walking speed and gait efficiency. Methods: A
comprehensive literature search identified all studies of those which contained the
key words Cerebral palsy (CP), Gait and Resistance training. It included 4 electronic
database journals and two internet search engines. Language was limited to English
and was dated from 1998 – 2012. Progressive resistance training studies and there
effects on gait parameters were selected for review. Results: An overall mean affect
0.06 (-0.33 – 0.46) showed that gait velocity favoured the intervention over the
control group. Conclusion: Muscle weakness may not be the only contributor to
poor gait performance. To achieve a greater overall mean increase in gait velocity,
resistive exercise design incorporating repetitions that involve simultaneous agonist
and antagonist muscle contraction during functional movement, should be combined
with other interventions such as gait training, balance and proprioception. If gait
velocity is to be maximised it is imperative to treat the cause of gait compensations
and to address impaired selective voluntary motor control, abnormal stretch reflexes
and to ensure sufficient heel strike at initial contact.
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Introduction
Cerebral Palsy is a collective term to describe the different categories of neurological
deficits associated within the cerebral areas of the brain (Mockford & Caulton, 2010).
Many researchers believe that non-progressive disturbances such as damage to
blood vessels caused by disrupted oxygen to developing areas of the foetal of infant
brain to be the cause (O'Shea, 2008).
The functional consequences secondary to cerebral lesions include spasticity,
muscle weakness, impaired selective voluntary motor control, hyperreflexia, muscle
hypertonia and poor ability to ambulate (Diane L. Damiano, Laws, Carmines, & Abel,
2006). In those with Cerebral Palsy, it is not that muscle contraction is weak but
rather an inappropriate timing of muscle activation patterns in both agonist and
antagonist muscles, resulting in co-contraction of the joints affected (Prosser, Lee,
Barbe, VanSant, & Lauer, 2010; Prosser, Lee, VanSant, Barbe, & Lauer, 2010).
Gait pattern in young children and adults has been analysed and divided into four
groups (Dobson, Morris, Baker, & Graham, 2007; Winters, Gage, & Hicks, 1987). In
Spastic Hemiplegia, group one and two subjects both exhibit a plantar-flexion
contracture (equinus) on the contralateral side of the cerebral lesion. However, only
group two subjects exhibit foot equinus at all stages of gait including mid stance that
produces an external moment which forces the knee into exaggerated plantar
flexion-extension coupling resulting in knee hyperextension. Both groups
compensate by increasing hip and knee flexion on the affected side to provide an
increase in the swing phase of gait. Group three and four subjects exhibit the same
characteristics of pathological gait as group one and two, however hamstring and
quadriceps overactivity result in insufficient swing phase resulting in vaulting of the
unaffected foot to counter this effect. Hip flexion contracture in group four subject’s
prevent full extension after mid-stance resulting in increased lumbar lordosis to
preserve stride length.
Several researchers have demonstrated a relationship between generalized muscle
weakness and decreased performance in gait, but more specifically with increased
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energy expenditure as a result of ambulation in those with CP (Bohannon, 1989;
Chen et al., 2012). Likewise, several studies have shown that those with cerebral
palsy exhibit highly inefficient gait patterns and increased energy expenditure, which
not all contributes to an increase in horizontal velocity of the body’s centre of mass
(Ballaz, Plamondon, & Lemay, 2010; Goldberg, Requejo, & Fowler, 2010; Russell,
Bennett, Kerrigan, & Abel, 2007). Logically, this implies that a suitable resistance
training program tailored to cerebral palsy patients may improve gait efficiency and
increase gait velocity.
In a review of the literature, correction of equinus deformity through surgical
interventions in an attempt to improve gait has shown not be successful (Shore,
White, & Kerr Graham, 2010). Unfortunately, greater incidence of equinus and
calcaneal deformity in children with hemiplegia were eminent following surgical
procedures. Furthermore, Stebbins et al (2010) analysed gait pelvic kinematics
before and after foot surgery on twelve subjects with spastic hemiplegia.
Interestingly, increased anterior pelvic tilt was evident in the CP group before and
remained uncorrected after surgery. This provides evidence that anterior pelvic tilt of
the pelvis may not always be a secondary compensation for foot equinus deformity
and may occur as a result of hip flexor tightness, weak abdominals or hip extensors.
This has implications as to whether resistance training may have a positive effect, as
failure to address the cause of compensatory mechanisms may lead to a resistance
training program that doesn’t approach the correct muscles around the joints of the
lower extremity.
In addition, children with Cerebral Palsy show to have seventy-percent reduction in
quadriceps’ rate of force development and knee extensor impulse during the loading
response of gait, compared to healthy controls (Moreau, Falvo, & Damiano, 2012). It
is of great interest whether a traditional resistance training program for the knee
extensors might counter this effect since the loading response of gait may require
the quadriceps to produce force at higher contraction velocity.
Overall, the main purpose of this review is to analyse whether resistance training
increases ambulatory function for those with spastic Cerebral Palsy. Furthermore, an
analysis of abnormal gait kinematics and kinetics during stages of gait in those with
Cerebral Palsy will potentially serve great value for Physical therapists and exercise
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physiologists in designing appropriate resistance exercise programs to match the
demands that abnormal gait places on the neuromuscular system.
Methods
Identification and selection of literature
A comprehensive literature search was performed using electronic databases,
including Medline (1998 to Feb 2012); SPORTDiscus (1998 to Feb 2012); Web of
Science (1998 to Feb 2012); and Cinahl (1998 to Feb 2012). The following keywords
were used: ‘Cerebral Palsy’, ‘Gait’, ‘walking’ and ‘strength training’, ‘weight training’
or 'resistance training’. To optimize journal article selection, abstracts and full texts
were selected prior to searching. Any Title Abstract without full text identified in the
database, would be used in the two internet search engines, GOOGLE scholar and
Scirus to identify whether a full text of that title would appear.
A study was included if it met the following criteria:
Participants: Children with Cerebral Palsy (spastic hemiplegia & diplegia) <18
years
CP History: varying disability levels
Outcome measures: Gait velocity
Intervention: Strength or resistance training
Study Design: Single or double blinded Randomized controlled trials
For a study to be excluded, the intervention must be of any other, than resistance
exercise or PRT (e.g. cardiovascular exercise, Electro-stimulation, virtual reality,
etc.). Any study that had 5 or less subjects involved, were also excluded. Any paper
that failed to report outcomes at baseline testing prior to the intervention, were also
excluded.
Selection of data and analysis of quality
The quality of each study was determined by internal validity (intention to treat
analysis, blinding study designs, reporting of subject withdrawals within groups and
randomisation), external validity (inclusion/exclusion criteria) and power analysis
(sample size calculation). Assessment of quality was accomplished by the
attainment of a critical appraisal skills programme (CASP) (Guyatt et al., 1995). This
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programme tool involves 10 screening questions that determine the quality of RCT’S.
Each question will be answered ‘yes’, ‘can’t tell’ and ‘no’ for each RCT, and will be
awarded1 point, zero points or a deduction point respectively, with a total score out
of 10.
Data analysis and synthesis
A mixed method approach was adopted for data synthesis: a narrative review of the
results supplemented by vote counting (Goodwin et al., 2008). Vote counting method
syntheses results by listing all outcomes of each study and identifying the direction of
effect for each outcome. The direction was rated positive if significant differences
were reported in favour of the intervention, negative if the difference supported the
control, equivocal if no significant difference was reported between groups.
Significance was set at p < 0.05.
Meta-analysis was undertaken using MetaEasy Excel add-in (StatAnalysis;
Kontopantelis & Reeves, 2009). A standardised effect size was calculated for each
study and expressed in standard deviation units. An overall effect was calculated
using the DerSimonial-Laird method (DerSimonial & Laird, 1986).
Results
The initial search identified 232 journal articles, and 16 studies remained after the
initial screening. Applying the exclusion/inclusion criteria resulted in only two
randomized controlled trial studies (Figure 1). Due to scarcity of RCT’s, four pre-test-
post-test experimental designs were incorporated so that we could avoid a
conservative approach in analysing the effects that resistance training has on gait in
CP patients. However, only three (two RCT’s & 1 experimental-control design) were
inputted into meta-analysis for synthesis of results. This experimental design was the
only study that incorporated a control group compared to the other non-RCT’s.
Table 1 summarises the quality of the 6 studies. Two studies were of moderate
quality (score ≥ 4 & ≤ 6) and four of low quality (score ≤ 3). All of the included studies
provided an extensive rationale for the use of resistance training as an intervention
for CP. Additionally, selection criteria was defined for all the studies. Only two
studies were RCT’s (Scholtes et al., 2012; Unger, Faure, & Frieg, 2006). Power and
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sample size calculations were only reported in two studies (D. L. Damiano & Abel,
1998; Scholtes, et al., 2012).
Only Three studies reported assessor blinding of pre-testing results during post-
intervention testing (D. L. Damiano & Abel, 1998; Scholtes, et al., 2012; Unger, et al.,
2006). Four studies did not perform an intention to treat analysis (Eagleton, Iams,
McDowell, Morrison, & Evans, 2004; Eek, Tranberg, Zügner, Alkema, & Beckung,
2008; Scholtes, et al., 2012; Unger, et al., 2006). Instead, only those subjects upon
completion of the intervention were accounted, for determining main outcomes.
Three studies reported adequate concealment of randomisation (Lee, Sung, & Yoo,
2008; Scholtes, et al., 2012; Unger, et al., 2006).
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‘
Figure 1. Progression of search for relevant studies
Searched databases (n = 4)
Search engines (n = 2)
Potentially relevant literature identified
(n = 232)
Using key words “Cerebral Palsy” “Gait”,
“walking”, “strength training”, “resistance
training” or “exercise”
1998 – 2012; limited to English
Papers excluded
(n =216)
Not relevant to review
Papers excluded
(n = 10)
Not meeting inclusion criteria or within
exclusion criteria
Papers reviewed
(n = 16)
Papers meeting inclusion criteria
(n = 6)
Included studies
(n = 6)
RCT’s = 2
Included participants
(n = 126)
R.T. = 83
Controls = 43
-Intervention involving adults (n = 2)
- Inappropriate intervention (n = 3)
-Other outcome measures (n =2)
-Inappropriate study design (n = 3)
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Table 1 description quality of selected studies
Study Design
Rationale
Described?
Power/sample
size
calculations
presented?
Selection
criteria
described?
Assessor/participants
blinded?
Adequate
concealment of
randomisation?
Intention to treat
analysis
performed?
*CASPQuality
score
Scholtes et al.
(2012)
Matched RCT Parallel Yes Yes Yes Yes Yes
no (per protocol
analysis)
6 (mod)
Unger et al. (2006) Matched RCT Parallel Yes No Yes
Assessor blinded to
pre-test results.
Yes Not reported 4 (mod)
Damiano et al.
(1998)
Pre-test-post-test
experimental design
Yes Yes Yes
Assessor blinded to
pre-test results
Not reported Not required 3 (Low)
Eagleton et al.
(2004)
Pre-test-post-test
experimental design
Yes No Yes Not reported Not reported Not reported 1 (Low)
Eak et al. (2008)
Pre-test-post-test
experimental design
Yes No Yes Not reported No Not reported 2 (Low)
Lee et al. (2008)
Pre-test-post-test
experimental design
Yes No Yes Not reported Yes Not required 2 (Low)
* CASP score out of
maximum of 10
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Table 2 Variationsandoutcomesof selected studies
Study Subjects Resistance Training Duration Outcome measures Major findings
Scholtes et al.
(2012)
1) 24 PRT ambulant spastic CP
10.4 ± 1.1 yrs. 2) 25 CON CP
10.3 ± 2.3yrs
PRT - Leg Press, Sit to
stand, half knee raise,
lateral step up, 3 sets 8
reps, load ↑ 5% once
reached 8RMCON -
Physio care
36 sessions
(3x/wk., 12
weeks)
POM- timed 10m walk test (cadence,
velocity& stride length) & timed stair
test. SOM - Spasticity, ROM, AMP
(Wingate) & isometric strength
Sig ↑in comfortable & fast walking
speed, ↔ cadence and ↑ stride length.
Sig↑isometric muscle strength 8% & leg
press 14%, ↔anaerobic power &
spasticity, sig ↓KF ROMin PRT > CON
Unger et al.
(2006)
1) 21 PRT CP patients 15.86
yrs., 1 orthotic, 2 assistive
devices (crutch & wheelchair)
2) 10 CON CP patients
16.38yrs
Resistance exercisesnot
reported PRT - 8-12
exercises of 28 station
circuit - upper and
lowerextremities CON -
no explanation
1-3 x per
week/8 weeks
Stride length, cadence & velocity,
knee angle at heel strike, crouch gait
at mid-stance & self-perception Q-
airre
Sum of joint (H,K,A)⁰ at midstance ↓ sig
(p < 0.05) compared to CONS, ↔ stride
length, velocity & cadence compared to
CON & Knee⁰ at heel-strike sig ↓
Damiano et al.
(1998)
1) 6 Diplegics 8.3yrs, 5
Hemiplegics 9.2yrs 2) no Con
Resistance exercisesnot
reported, 4 sets 5 reps
65% 1RM Isometric
strength. Hemiplegics
unilateral & diplegics
bilateral training
18 sessions
(3x/wk., 6
weeks)
Gait velocity,stridelength,cadence,%
stance & % double support gait,
strength, GMFM& EEI
Hemiplegics & Diplegics sig↑ stride
velocity & cadence, no sig ↑EEI & Stride
length, trend ↑% mid stance phase,
trend ↓% double support
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Eagleton et al.
(2004)
1) 7 PRT CP patients (12-20
yrs.) 2) no CON
Free weights &
machines, 80% 1RM10
reps, trunk, hip, knee &
ankle flex & ext.
18 sessions
(3x/wk., 6
weeks)
muscle strength, Stride length,
cadence, velocity & EEI
Sig ↑ in all outcome measures (p < 0.05)
Eak et al. (2008)
16 subjects with Spastic
Diplegia(2 females, 14 males)
GMFCS level 1, n = 10 (12.2 ±
1.8yrs) & level 2, n = 6 (13 ± 2
yrs.)
Resistance exercisesnot
reported. 3 sets 10 reps
progressive increase in
load from 1st - 3rd set
24 sessions
(3x/week, 8
weeks)
3-D Gait analysis, Muscle strength,
GMFM assessment, joint ROMand
spasticity
No sig ↑ gait velocity, sig ↓ cadence,
↑trendstride length,Spasticity↔,sig↑
inall hip muscle groupsandknee flexors,
sig ↑ hip ext. moment & plantar flexing
generating power at push-off
Lee et al. (2008)
1) 9 PRT (4 Diplegic & 5
hemiplegic) 6.3 ± 2.1 yrs. 2) 8
CON (5 Diplegic & 3
Hemiplegic) 6.3 ± 2.9 yrs.
PRT - Squat to stand,
lateral stepup, and stair
walk up and down. 2
sets 10 reps load 0.25,
0.45 or 0.9kg adjustable
weight cuffs as
progression CONS -
Physio, ROMexercise &
Gait training
15 session
(3x/week, 5
weeks)
Gait (velocity,stride length, cadence,
% single & double limp support)
Muscle strength, spasticity & GMFM
Sig ↑ max hip extensor strength, Sig ↑
gait velocity & stride length, ↑ trend for
% single leg support & ↓ trend for %
double limb support, Sig ↑ lateral step
ups & squat to stand, Sig ↑ GMFMscore
D & E compared to CONS, ↔ spasticity
flexion,ROM= Range of motion,(H,K, A⁰) = hip,knee,ankle degrees,GMFM= Gross motorfunctionmeasure,EEI= Energyexpenditure index,RM=
repetitionmaximum, Sig=Significant
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Participants
Three studies lacked control groups (D. L. Damiano & Abel, 1998; Eagleton, et al.,
2004; Eek, et al., 2008). Exclusion and inclusion criteria were similar in four studies
(Eagleton, et al., 2004; Eek, et al., 2008; Scholtes, et al., 2012; Unger, et al., 2006).
However, one study reported that hemiplegic children had to demonstrate at least
20% asymmetry in strength values in a minimum of two of eight muscle groups
tested on their more involved extremity in comparison with contralateral extremity
and Diplegics to have at least 50% weakness from healthy normal (D. L. Damiano &
Abel, 1998).
Only one study reported to exclude those patients with fixed contracture at the hip
and knee joints (Lee, et al., 2008). Three studies failed to report categorisation group
of CP subjects (Eagleton, et al., 2004; Scholtes, et al., 2012; Unger, et al., 2006).
Only one of the three experimental-control groups reported statistical p-values
illustrating no baseline significance between groups (Scholtes, et al., 2012). One
study contained an inappropriate difference in sample size between the intervention
and control group (Unger, et al., 2006). Number of subjects within the intervention
group almost doubled that of the control group.
Two studies failed to recruit an appropriate sample size and resorted to using non-
parametric statistics for data analysis (Eagleton, et al., 2004; Eek, et al., 2008).
Interventions
Two studies included an individual analysis of each child’s muscle strength and gait
pattern abnormalities to program appropriate muscle strengthening exercises (Eek,
et al., 2008; Unger, et al., 2006). However, these studies did not report actual
strengthening exercises to be carried out. Only two out of the six studies explained
the strengthening exercises that were to be carried out through the intervention (Lee,
et al., 2008; Scholtes et al., 2008). These two studies were almost homogenous in
regard to resistive exercise selection but varied greatly in the duration of the entire
intervention with five and thirty-six week sessions carried out respectively. Only one
study reported individualized strengthening exercises that were to be carried out
depending on CP categorisation, being Diplegic or hemiplegic (D. L. Damiano &
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Abel, 1998). Hemiplegics strengthened the unaffected unilateral lower extremity and
diplegics strengthened both extremities.
In regards to the three studies involving controls, only one study failed to report what
type of intervention they received (Unger, et al., 2006). Interestingly, Lee et al (2008)
reported in detail the intervention the controls carried out, however this intervention
was comprised of ROM, gait training and exercise, which was not matched by the
experimental group. In regard to exercise selection, two studies included resistive
exercises for the trunk (Eagleton, et al., 2004; Unger, et al., 2006). In addition, these
were the only studies that reported concurrent lower and upper body strengthening.
Outcomes
The outcomes for all the studies have been summarised (table 2) and presented in
narrative form. Most studies differed in their intervention, duration and outcome
measures. The most common outcome measures between the six studies were Gait
velocity.
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Gait velocity
As can be seen in figure 2, three of the six highly scored studies produced an overall
effect to suggest that progressive resistance exercise most likely results in a small
but significant overall mean increase in gait velocity (standardised mean difference:
0.0625; 95% CI: -0.3323 - 0.4573). Testing for heterogeneity was not significantly
different (X² = 1.26, df = 2, p = 0.53)
Two studies reported no change in gait velocity (Eek, et al., 2008; Scholtes, et al.,
2012; Unger, et al., 2006).
Scholtes et al.
(2012)
Unger et al. (2006)
Lee et al. (2012)
-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5
Standardised Mean Difference (Lower, Upper 95% CI)
Favours control Favours Intervention
Figure 2. Meta-analysis for Gait velocity
Study
Overall 95% CI
0.16 (-0.8 – 1.1)
-0.26 (-0.94 – 0.43)
0.24 (-0.32 – 0.8)
0.06 (-0.33 – 0.46)
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Stride length
Two studies did not improve stride length as an outcome (D. L. Damiano & Abel,
1998; Scholtes, et al., 2012; Unger, et al., 2006), whereas one study reported a trend
increase (Eek, et al., 2008). However, three studies found a significant increase in
stride length (Eagleton, et al., 2004; Lee, et al., 2008; Scholtes, et al., 2012).
Cadence
Only one study reported a reduction in cadence (Eek, et al., 2008), whereas two
studies showed no difference after intervention (Scholtes, et al., 2012; Unger, et al.,
2006)
Other gait parameters
Only Two studies reported Energy expenditure Index (EEI). One study found no
significant differences in energy expenditure after the intervention (D. L. Damiano &
Abel, 1998). According to Eagleton et al (2004), there was a decrease in EEI in four
of the seven subjects despite increased gait velocity after the intervention. However,
three of the seven subjects increased there EEI due to increases in gait velocity,
suggesting no change in energy expenditure.
Two studies reported both a trend decrease in % of double support phase and a
trend for the increase in % mid-stance support phase of the gait cycle (D. L.
Damiano & Abel, 1998; Lee, et al., 2008).
Strength
Two studies reported an increase in strength via manual muscle testing (Eagleton, et
al., 2004; Lee, et al., 2008). Unger et al (2006) failed to report strength
measurements at post testing. Eak et al (2008) found an increase in all hip muscle
groups and knee flexors via myometer testing. Only one study reported an increase
in strength by 14% using an exercise based machine (leg press) that was used
during the intervention (Scholtes, et al., 2012). Damiano et al (1998) found increase
in strength on the affected side in hemiplegics with no change on the unaffected
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side, whereas diplegics increased their strength in targeted muscles with a trend
decrease in antagonist muscle strength.
Spasticity
There was no increase in spasticity reported in three studies (Eek, et al., 2008; Lee,
et al., 2008; Scholtes, et al., 2012)
Range of motion
Three studies reported changes in ROM after the intervention. A reduction in knee
flexion angle at heel strike was reported in two studies (Scholtes, et al., 2012; Unger,
et al., 2006). Eak et al (2008) found a significant increase in hamstring length but
only through goniometric measurement. Two Studies reported no change in
antagonistic muscle length after strengthening the agonist (D. L. Damiano & Abel,
1998; Lee, et al., 2008).
Discussion
Although a small but significant overall mean increase in gait velocity, it is clear that
there are factors other than muscle weakness which might contribute to an
insufficient walking speed.
Unger et al (2006) reported increased knee angle at heel strike which may have
been a consequence of increased knee extension moment during swing phase as a
result from increased inhibition of hamstrings. Resistance training programs for
agonist muscles have shown to reduce antagonist activation to allow greater net
force output (Carolan & Cafarelli, 1992; Tillin, Pain, & Folland, 2011). However,
Damiano, Martellota, Sullivan, Granata & Abel (2000) did not show correlation
between co-contraction and weakness which seems counter-intuitive because
antagonist activity could diminish the net force contribution of the agonist, unless the
agonist simultaneously increased its activity. Even though potential negative effects
of excessive co-contraction include greater total muscle activation during net force
production and altered movement quality and quantity, co-contraction may still be a
useful compensatory strategy in CP to increase joint stability, limit degrees of
freedom, or to allow the motor system to respond to perturbations. In Unger et al
16. 16
(2006), resistance training may have increased agonist muscle recruitment with
corresponding relaxation of antagonists. However this may have reduced joint
stability in CP and compromised force regulation. Therefore, we need to understand
the purpose of co-contraction before setting appropriate resistance training programs
for those with CP, as increased joint stiffness may either reduce net force output or
increase joint stability. This mechanism may only be true if increased knee angle at
heel strike was a consequence of increased relaxation of antagonists.
Goldberg, Requejo & Fowler (2010) demonstrated that Children with good selective
voluntary motor control (SVMC) are more capable of moving out of synergy during
the swing phase of gait (hip flexion with knee extension), while children with poor
SVMC are constrained to move in synergy (simultaneous hip and knee flexion).
Swing phase inappropriate SVMC may be the reason Unger et al (2006) showed no
increase in stride length or gait velocity despite reduced crouch at mid stance. This
suggests that resistance training may have improved mid-stance centre of mass, but
SVMC might become a much higher contributor to the swing phase.
Although the effects of resistance training in Unger et al (2006) might have improved
crouch at mid stance, there are other factors within pathological gait that needs to be
addressed. Russell, Bennett, Kerrigan & Abel (2007) showed that CP patients have
increased knee flexion at double support phase and increased plantar flexion in
single limb stance contributing to wasting of energy and increased centre of mass
(COM) oscillation. Only by addressing equinus foot, there may not need increased
contralateral knee flexion during double support to minimize joint compression stress
upon initial contact, thereby minimizing oscillation and improving gait velocity. Unger
et al (2006) did not include specific exercises for musculature around the ankle and
foot and it has been shown that greater plantar flexion-dorsiflexion range of motion
contributes to increased gait velocity and increased ankle range of motion (Ballaz, et
al., 2010). Additionally, Van der Krogt, Doorenbosch, Becher & Harlaar (2009) found
that with increasing walking speed also increased equinus at foot contact and that
the potential increase in walking speed might have been cancelled out due to
amplified stretch reflexes contributing to increase upward rather than horizontal
momentum therefore creating no difference in gait velocity. Intervention strategies
aimed to ensure heel initial contact may reduce gravitational potential energy
(reduction of the triceps surae stretch reflex) and kinetic energy at impact of
17. 17
contralateral leg, therefore minimizing vertical oscillation and knee flexion during
double leg stance phase.
Furthermore, there was a weak correlation between gait joint kinetics and isometric
strength using a dynamometer (Dallmeijer, Baker, Dodd, & Taylor, 2011). Twenty-
five subjects with bilateral Spastic cerebral Palsy with significant reduction in
isometric strength still exhibited joint moment curves similar to normal values during
gait. Ankle joint moments during gait in CP exceed greatly than that during isometric
strength testing. This indicates that isometric strength doesn’t contain information
regarding dynamic muscle function and that muscle spasticity may in some way
activate a velocity dependant stretch reflex during gait which is not possible during
static conditions. This suggests that abnormal neural control mechanisms that
amplify joint moments may retard horizontal momentum, such that seen in bounce
gait. Therefore, focussed efforts should be in understanding how those with CP can
utilize the velocity dependant stretch reflex to maximize horizontal momentum.
Interestingly, the muscles that may have been targeted in Unger et al (2006), which
contributed to reduced crouch gait may have not positively contributed to terminal
stance or pre-swing. It was shown by Goldberg, Ounpuu & Delp (2003) that knee
extension moments during swing phase were the same between controls and those
with Spastic diplegia. This meant that stiff knee gait may not always be a function of
rectus femoris spasticity but rather inadequate hip flexor moments during pre-swing
which was shown to be significantly weaker in those with CP. Physical therapists
must be mindful that programming for resistance training should take into account all
phases of gait and how they interact with each other to produce normal function.
Exercises that increase hip flexor power at pre swing may have resulted in an
increase flexed knee during swing phase, reduced segment inertia, hip hiking and
consequently increased efficiency and velocity.
Neither study within this review applied rate of force development protocols.
However, several studies have analysed voluntary joint moments in those children
with CP. Compared to controls, they demonstrated differences in moment generation
profiles, including decreased maximum voluntary isometric contractions, decreased
maximum rates of moment development, relaxation and increased time needed to
generate and reduce moments (Downing, Ganley, Fay, & Abbas, 2009; Tammik,
18. 18
Matlep, Ereline, Gapeyeva, & Pääsuke, 2008). Furthermore, Moreau & Damiano
(2012) noted that rate of force development and impulse were more important than
maximal force development in the loading response, as this phase requires less than
two-hundred milliseconds to produce optimal force. Although it would be tempting to
improve rate of force development in CP patients, there may be many increased
risks associated with it such as bone fractures and muscle-tendon strains. It may be
even more dangerous to incorporate this type of training method if a therapist
assumes weakness and no other parameter to be a contributing cause for
dysfunctional gait.
Conversely, Lee et al (2012) showed that increased muscle strength related to an
improvement in gait velocity. Several studies have shown that Muscle weakness
assessed from isometric testing correlated to low gross motor function classification
scores, which in turn correlated with reduced gait efficiency and velocity (D. L.
Damiano, Kelly, & Vaughn, 1995; Eek & Beckung, 2008; Rose & McGill, 2005;
Thompson, Stebbins, Seniorou, & Newham, 2011). However, Lee et al (2012)
showed that manual muscle testing of the hip extensors were the only muscle group
to show a correlation to increased gait velocity and stride length. This may be due to
the fact that manual muscle testing only evaluates isolated muscle groups at
localized joints. Additionally, pathological gait is defined by interactions of multiple
limitations, co-contractions and muscle synergies and that manual muscle testing
focuses on primary and secondary problems, while pathological gait is characterized
by compensation mechanisms (tertiary problems) to overcome the primary and
secondary problems (Rose & McGill, 2005). Therefore, it may not be that muscle
strength associated with manual testing caused an increase in stride length and
velocity but rather the improvement in balance and proprioception associated with
the functional sit to stand and lateral step ups.
Although Unger et al (2006) disregarded weakness to be a rate limiter in improving
gait, perhaps eight weeks of training was not sufficient to realize strength gains. In
addition, Unger et al (2006) failed to report post strength measures and had there
been an increase in strength, then only can we say that weakness was a rate limiter
in improving gait. It is possible that Unger et al (2012) programmed resistance
station circuits that may have been comprised of machine based rather than
functional movements of which reported in Lee et al (2012) and Scholtes et al
19. 19
(2012). Moreover, it may be that increased gait velocity found in Lee et al (2012) was
related due to the fact that those with fixed contracture at the hip and knee joints
were excluded from the subject criteria. It is interesting to note that the control group
within Lee et al (2012) received physical therapy, range of motion exercises and gait
training that were unmatched by the intervention group, despite increased gait
velocity favouring the latter. This might be due to the powerful effect that functional
resistive exercise has on gait rather than the unlikely harmful exercise effects carried
out by the control group. In fact it has been shown that gait training results in
increased walking speed over short distances, improved gross motor skills such as
static and dynamic balance and general gait parameters (Mutlu, Krosschell, & Spira,
2009; Willoughby, Dodd, & Shields, 2009). Therefore, it is illogical to assume that the
intervention carried out by the control group had negative effects on gait which
favoured the intervention group.
Damiano et al (1998) suggested that biomechanical limitation of active and passive
motion caused by spasticity, inadequate muscle length, or abnormal dynamic activity
limited an increase in stride length for those with CP. Additionally, stride length was
not related to strength in lower limbs. Conversely, Lee et al (2012) found an increase
in stride length which rejected the findings of Damiano et al (1998). Failure to
compare and contrast resistance exercise intervention between the two studies is
partly due to Damiano et al (1998) not reporting the resistance exercises to be
carried out. Therefore we assume that the subjects within Lee et al (2012) improved
stride length partly due to increased hip extensor strength which contributed to an
increase hip flexor movement at terminal stance, which resulted in increased angle
of hip flexion at swing phase and therefore stride length. Secondly, increased
ipsilateral strength in single limb support from hip girdle strengthening might have
contributed to larger contralateral limb progression. Subjects within Damiano et al
(1998), increased there velocity by an increase in cadence. This increase in cadence
is probably why energy expenditure index did not differ before and after the
intervention. Children who increased there velocity after training became less
efficient before strengthening, whereas children who had minimal increase in velocity
increased efficiency. Therefore, efficiency is not always related to gait velocity and
programming for resistance training should determine whether the outcome would be
increased cadence or stride length as each parameter may affect efficiency
20. 20
independently. An increase in velocity through increase in stride length produces
greater energy efficiency during gait. In addition, We would have not seen an
increase in gait velocity in Damiano & Abel (1998) if muscle target criteria were such
that only weakest muscles were strengthened.
Although not reported, Unger et al (2006) and Eak et al (2008) implemented ‘specific
resistance exercises’ based on gait pattern abnormalities which did not correlate to a
significant increase in walking speed. This explains that the clinical evaluation of gait
in Cerebral Palsy is far too complex to ensure appropriate resistance exercise
design. Both these studies involved patients who exhibited crouch gait. Physical
therapists may assume that knee extensor strengthening be imperative in reducing
knee flexion moment, improving crouch gait and patella tendon strain. However, van
der Krogt et al (2010) demonstrated that by increasing the degree of crouch gait in
stance position contributed to an increase in stiff-knee gait. This was explained by
insufficient hip extension which caused increased gravitational moments about the
shank acting to extend the knee as it lay more in a horizontal position relative to the
floor. Conversely, with a reduction in crouch gait, lead to increased hip extension
which allowed increased gravitational flexion moments about the thigh segment
which in turn passively increased knee flexion. Therefore, stiff knee gait during swing
can occur purely as the dynamical result of crouch, rather than from altered muscle
function, pathoneurological control or muscle weakness. Consequently, It should be
realized the clinical gait assessment in designing resistance exercise has its
limitations.
As mentioned, Eak et al (2008) ignored the relevance of muscle weakness to
impaired gait. Although there was significant increase in plantar flexion generating
power at push off and increase hip extension moment, there was no change in gait
velocity and there was a reduction in cadence. Perhaps the reduction in cadence
was reflected for the trend increase in stride length which may have been a function
of increased hip and knee joint stability from the resistance exercises. The increase
in joint kinetics was reflected possibly from increased hip and knee stability during
stance so that it enables sufficient power to be produced by the gastrocnemius.
However if cadence were to be maintained, there may have been increased gait
velocity. This implies that exercise therapists should aim to maintain both gait
21. 21
characteristics as resistance exercise may increase stride length at the expense of
cadence (or vice versa) thereby contributing to little or no increase in gait velocity.
This paper presents many limitations based on the poor quality of studies available
to select for review. Although Meta-analysis revealed no significant difference
between studies in detecting heterogeneity, it may be unreliable due to the small
amount of studies inputted. Therefore, It is still difficult to analyse the greatest effect
at which the independent variables influenced gait velocity.
Whether duration, intervention protocol, CP category or inclusion criteria influences
gait velocity is still a question that needs to be addressed. Furthermore, we cannot
fully interpret and analyse the difference in strength interventions as more than half
of the selected studies failed to report actual exercises to be carried out. The scarcity
of randomized controlled trials within this field of study may reflect the apprehensive
attempt to include resistive exercise in those with CP due to the fear of exercise
related spasticity or contracture. However, this review showed that exercise did not
contribute to negative effects such as muscle spasticity. Therefore future research
should be aimed at developing higher quality studies (RCT’S) that keep intervention
duration, CP category and inclusion criteria constant so that we can more confidently
suggest that resistance training does have an impact on gait velocity.
Conclusion
As a result, resistance training for those with CP should be part of an exercise
program. However, this paper clearly presents that muscular strength is only one
minor aspect to improving gait velocity. If gait velocity is to be maximised, physical
therapists must determine which aspects relating to gait need to be addressed and
subsequently improved upon. In addition, the phases of gait are interdependent on
each other for optimal walking efficiency and therefore a dysfunctional phase of gait
might be the effects caused by the phase that preceded it.
23. 23
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