Locomotion in children with cerebral palsy - UFRGS

Artigo de revisão

Locomotion in children with cerebral palsy: a review with special reference to the displacement of the center of mass and energy cost Locomoção de crianças com paralisia cerebral: uma revisão de literatura, com especial referência ao deslocamento do centro de massa e custo energético Clarissa Schuch1 Leonardo A. Peyré-Tartaruga2

ABSTRACT The aim of the study was to review aspects of the displacement of the center of mass and energy cost of walking in children with cerebral palsy. The methodology used was a bibliographical review, whose articles had been chosen using the database PubMed and Google Scholar. There is unanimity from the studies that describe the locomotion of the hemiplegic children with increased vertical displacement of center of mass, inefficient exchange between kinetic and potential energy and elevated energy cost when compared with normal children. The mechanisms that explain these findings seem to have strong relation with the muscular co-contraction and the deformity in plantarflexion. Therefore, evaluation of the locomotion through cinematography and energy expenditure index is efficient to detect the effects of medical and therapeutic interventions. KEYWORDS Cerebral palsy - Hemiplegia - Gait.

RESUMO O objetivo do estudo foi revisar aspectos relacionados ao deslocamento do centro de massa e gasto energético na caminhada de crianças hemiplégicas decorrentes da Paralisia Cerebral (PC). A metodologia empregada foi uma revisão bibliográfica, cujos artigos foram escolhidos utilizando a base de dados PubMed e Google Scholar. Há uma unanimidade entre os estudos, que descrevem a locomoção das crianças hemiplégicas com maior deslocamento vertical do centro de massa (CM), ineficiente troca entre energia cinética e potencial e maior gasto energético quando comparadas às crianças saudáveis. Os mecanismos que explicam esses achados não estão bem definidos, mas parecem ter forte relação com a co-contração muscular e a deformidade em

Universidade Federal do Rio Grande do Sul - Laboratório de Pesquisa do Exercício, Porto Alegre, RS, Brasil, e-mail: [email protected] ² Universidade Federal do Rio Grande do Sul - Laboratório de Pesquisa do Exercício, Porto Alegre, RS, Brasil, e-mail: [email protected] 1

Ciência em Movimento | Ano XII | Nº 23 | 2010/1

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Locomotion in children with cerebral palsy: flexão plantar presentes nos pacientes hemiplégicos. Portanto, meios de avaliação da locomoção como a cinemetria e índice de gasto energético são eficazes para acompanhar a trajetória dos resultados das intervenções terapêuticas. PALAVRAS-CHAVE Paralisia cerebral – Hemiplegia - Marcha.

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Locomotion in children with cerebral palsy: INTRODUCTION

support. For people with neuromuscular disorders su-

Gait is a basic requirement for daily activity and is

ch as stroke or CP, the CM vertical excursion may be

known to be one of the most universal and complex

increased (RUSSEL et al., 2007).

of all human activities. It is a complex motor skill go-

The smoothness of the vertical body’s CM displa-

verned by several inter-linked pathways from the cor-

cement to minimize energy expenditure depends on

tex to the muscles. However, impairment of gait is

several kinematic determinants: foot rockers, knee fle-

frequently responsible for long-term disability (MAU-

xion wave in stance phase, knee flexion in swing phase,

RITZ, 2002). Gait analysis of children with cerebral

pelvic rotation, and pelvic list (MASSAAD et al., 2006).

palsy (CP) or post stroke adults has been used to stu-

The understanding of the alterations that occur to

dy the basic biomechanics of their walking, which, in

the musculoskeletal and physiological level in the

turn, has assisted in therapeutic and surgical decision

walking have clinical implications for therapies aiming

making (OLNEY et al., 1987).

to improve walking economy in patients with gait di-

Cerebral palsy is a static encephalopathy that may

sorders that affect CM motion and metabolic cost su-

be defined as a nonprogressive disorder of posture

ch as hip joint replacement, lower limb amputation,

and movement, often associated with spasticity, mus-

stroke, and CP (ORTEGA; FARLEY, 2005).

cle weakness, ataxia, rigidity, epilepsy and abnorma-

Minimization of energy expenditure has long been

lities of speech, vision and intellect, resulting from

considered a fundamental characteristic of walking.

damage to the developing brain (ROMKES & BRUN-

This line of reasoning has led researchers to examine

NER, 2007; DAMIANO et al., 2000). Hemiplegic CP is

this mechanism of energy conservation in persons

typically associated with single hemisphere injury and

with walking disabilities (BENNET et al., 2005).

there is involvement of predominantly one body side with relative sparing of the contralateral limbs.

An essential question to the functionality in the locomotion relates to the total energy cost for this

Thus, the CP is a condition that interferes in the

activity. Understanding how the modifications of the

acquisition of motor skills in infancy, which are essen-

mechanics influence the energy cost of the locomo-

tial to the performance of activities and tasks of daily

tion assisting in the determination of the main para-

routine. Specific abnormalities of gait are associated

meters for the pathological gait.

with variations in type and degree of CP’s impairment.

Considering these assumptions, important in the

The involvement of upper motor neurons may result

process of rehabilitation of CP patients, this study ai-

in neuromuscular disorders which include; hyperacti-

ms at analyzing the movement of CM and energy cost

vity of stretch reflexes, morphological changes of the

in hemiplegics children, whose methodology consists

tendons, muscles and connective tissue, muscle we-

of a bibliographical review using the database Pub-

akness and a decrease in the number of motor units

med and Google Scholar in the period 1950 to 2008.

(BURTNER et al., 1999; HOLT et al., 2000).

The choice of this period for selection of articles is due

The most commonly observed characteristics of

the existence of classic items like Saunders et al. in

gait in children with spastic CP include limited hip and

1953 entitled “The major determinants in normal and

knee range of motion, excessive hip adduction and

pathological gait” and articles about pendular mecha-

internal rotation, anterior pelvic tilt, pelvic obliquity,

nism of human walking by Cavagna and colleagues in

and persistent plantar flexion at the ankle. Common

1963 and 1977. These articles are fundamental to un-

characteristics of CP gait include decreased heel stri-

derstanding the current findings on the mechanics

ke, decreased walking speed, decreased stride length

and energetics of locomotion.

and/or cadence, and decreased ability to increase velocity on demand compared with adolescents without

LOCOMOTION AND MOVEMENT

impairments (AYCICEK; AKIN, 2006).

OF CENTER OF MASS

During walking the body center of mass (CM)

MECHANICAL MODEL OF

moves up and down, reaching a maximum during sin-

THE INVERTED PENDULUM

gle limb support and a minimum during double limb

The human locomotion is described as an alternate Ciência em Movimento | Ano XII | Nº 23 | 2010/1

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Locomotion in children with cerebral palsy: movement of loss and recovery of balance with variation

and gravitational potential taking place in opposition of

in the CM. When the person moves forward during stance

phase as described by CAVAGNA et al., (1963) and the-

phase, the CM body changes its position and causes im-

refore with a process of reconversion between kinetic

balance of the body (CHAMBERS; SUTHERLAND, 2002).

energy and gravitational potential (Recovery - R):

Although the locomotion is the result of a complex series of actions which connect segments of the activation of the muscles engaging forces and producing

R(%) = 100

Wf + Wv – Wext Wf + Wv

Eq. 3

torques transmitted through tendons generating the movement in various parts of the body, the human walk

where Wf is forward work, Wv is vertical work, and

is characterized as a model capable of minimizing the

Wext is external work.

expenditure of energy through the inverted pendulum, The recovery of energy quantifies the ability to

as figure 1.

store mechanical energy using the model of the pendulum. In an ideal pendulum the exchange of energy is complete. However, the maximum recovery of energy during walking is moderately high (about 60%) and it depends on the step length and the speed of walking (SAIBENE; MINETTI, 2003). Recent literature suggests a contribution of elastic energy to the mechanisms of walking through the storage of energy and releasing in the Achilles tendon and possibly through the arch of the foot (ISHIKAWA et al., 2005), but the model inverted pendulum seems to be the

22

main mechanism to minimize energy in walking (PEYRÉFigure 1. Mechanical model of human locomotion proposed by Cavagna et al., 1976: inverted pendulum for walking.

TARTARUGA, 2008, VANDERPOOL et al., 2008). During each stage of walking, the potential gravitational energy and kinetic energy of CM range from

The locomotion, analyzed by the behavior of the CM,

a minimum to a maximum value. A priori, active mo-

suffers influence of three fundamental mechanical ener-

vements of an organism are assumed to be powered

gies that are: gravitational potential energy (Ep), kinetic

by muscles: positive muscle work (concentric con-

energy (Ek) and elastic energy (SAIBENE; MINETTI,

traction) to increase potential energy and kinetic

2003) demonstrated by the equations that follow:

energy, and negative muscle work (eccentric contraction) to absorb potential energy and kinetic ener-

Ep = mgh Eq. 1

gy. Both positive and negative muscular work requires the expenditure of chemical energy. During

Ek = mv 2

2

Eq. 2

Where m is mass (kg), g is acceleration of gravity (9.8 ms-2), h is the vertical distance (meters), v is speed of body CM (ms-1). In walking, potential energy (Ep) is high when the CM is on the point of body contact with the ground, while the potential gravitational energy begins to decline and horizontal kinetic energy (Ek) gets a gradual increase. These patterns between horizontal kinetic energy


walking, both the positive and the negative work actually done by the muscles to sustain the mechanical energy changes of the CM (positive and negative external work) are reduced by the pendular transduction from potential energy to kinetic energy and vice versa (CAVAGNA et al., 2002). The mechanical cost of terrestrial locomotion is determined by ground reaction forces (GRF) in order to re-accelerate and move the body against gravitational force in a cycle of step. The method for analyzing work and mechanical external cost, using dynamometric

Locomotion in children with cerebral palsy: platforms was introduced by Cavagna and colleagues

Wtot = Wext + Wint Eq. 7

(1963; 1964). Since then, the external work has been investigated in different conditions and populations

where Wtot is total mechanical work, Wext is external

(FORMENTI et al., 2005; FORMENTI; MINETTI, 2007;

work and Wint (J.kg-1. m-1).

CAVAGNA et al., 1983; SCHEPENS et al., 1998). The external work is commonly measured by the

In an inverted pendulum conceptualization, mi-

GRF, where potential and kinetic energy of the CM is

nimization of work is achieved by the maximization

calculated. The positive work performed by the muscles

of the recovery of mechanical energy. For recovery

to move the CM during walking is also measured, deter-

to be maximized, the potential energy and kinetic

mined by the sum of the positive increases of the curve

energy curves must be equal in amplitude and op-

of total mechanical energy of the CM (potential and ki-

posite (180°) in phase (BENNETT et al., 2005).

netic) (WILLEMS et al., 1995; HECKE et al., 2007).

By the way, the recover y of energy during walking in children with CP is only two-thirds of that

Eextot = Ep + Ek Eq. 4

in typically developing children (AYCICEK; ISCAN, 2006; ORTEGA; FARLEY, 2005). Punctually it was

where Eextot is total external work, Ep is potential ener-

possible to find that children with CP showed less

gy, and Ek is kinetic energy (J.kg-1).

recovery of energy, greater vertical displacement of CM; lower exchange between potential and kinetic

Wext = ΔEextot Eq. 5

energy contributing to the increase in mechanical work. It was also observed that children with CP

where Wext is external work, ΔEextot is variation of the

walk with a shorter stride length and compensate

positive increments of Eextot (J.kg . m ).

with a higher stride frequency. Thus one may con-

-1

-1

clude that children with CP are mechanically less In contrast, the work necessary to accelerate the limbs with respect to the body CM during locomotion

efficient in their walking, for adopting a less pendular locomotion (ORTEGA; FARLEY, 2005).

is a concept introduced by FENN (1930) and succes-

Some researchers hypothesized that minimizing

sively formalized as mechanical internal work (CAVAG-

vertical movements of the CM during walking would

NA; KANEKO, 1977). By summing the kinetic energy

reduce the metabolic cost (SAUNDERS et al., 1953).

curves of single segments in a way to allow energy

However, an alternative view suggests that, minimi-

to transfer only among within-limb segments, and by

zing the vertical motion of the CM during walking

summing all the energy increases in the resulting cur-

does not reduce the mechanical work required to mo-

ves, internal work was calculated.

ve the CM and approximately double the metabolic

The mechanical internal work needed to accelera-

cost (ORTEGA; FARLEY, 2005). Because vertical mo-

te the limbs with respect of the body CM, has been

tion allows inverted pendulum energy exchange and

modeled by MINETTI (1998) as:

reduces the mechanical work required to accelerate

[ ( )]

–. Wint,theor = 0.1sf s 1+

d 1–d

the CM in normal walking. Other factors probably

2

Eq. 6

contribute to the high metabolic cost of flat-trajectory walking, including greater muscle force generation

–. where, sf is stride frequency (strides.s ), s is

to support body weight and greater positive muscle

average horizontal speed (m.s-1) and d is duty factor

refore maintaining normal levels of vertical CM mo-

(ratio of contact time and stride time).

tion and an extended stance limb are important fac-

-1

The value of total work is obtained by adding the

work performed to compensate co-contraction. The-

tors to reduce the metabolic cost of walking.

internal and external work, carried out by adding the cur-

MASSAAD et al. (2004) have demonstrated that

ves of kinetic energy of the body segments and sum of

the most crucial determinants optimizing the vertical

the curves of potential and kinetic energy of the CM.

CM displacement are the heel strike and the heel Ciência em Movimento | Ano XII | Nº 23 | 2010/1

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Locomotion in children with cerebral palsy: rise. In patients with CP, both these heel rocker mo-

fore, these children demonstrate 1.3 to 1.6 times

vements are affected, which could partly explain the

greater vertical CM displacement than normal one.

increase in this displacement. On the other hand, torsional deformities often observed in CP could in-

ENERGY COST OF LOCOMOTION

terfere with the pelvic rotation, which is another po-

In response to an inability of walking, a child

tential determinant in smoothing the vertical CM

with CP adapts using compensation to minimize the

displacement (CROCE et al., 2001). Raising the CM

additional energy expenditure. The effectiveness

higher onto a plantar flexed foot would present some

and the penalties associated with this compensa-

biomechanical advantages. In fact, the ankle loading

tion depend, mainly on the severity of the inability

torque is increased on a stiffer gastrocnemius–so-

and cardiovascular suitability of the patient (SAIBE-

leus muscle–tendon complex, which leads to a re-

NE; MINETTI, 2003; WATERS; MULROY, 1999).

bound in the manner of a pogo stick. Thus, higher

The metabolic cost of walking is determined by

vertical CM displacement could compensate for the

mechanical tasks such as generating force to sup-

lack of energy exchange of the CM by increasing the

port body weight, performing work to redirect and

elastic potential storage (HOLT et al., 2000).

accelerate the center of mass from step to step,

The decrease in forward CM displacement indicates a shorter step length that could be explained

24

swinging the limbs, and maintaining stability (GRABOWSKI et al., 2005).

by a weak push-off, and/or an excessive decelera-

A variety of methods have been used by clini-

tion of the leg in late swing due to the hyperactivity

cians and researchers to assess the energy expen-

in knee flexors. In total, these ‘abnormal’ three-di-

diture of movement in children with motor dysfunc-

mensional CM displacements may be a compensa-

tion (PICCININI et al., 2007; ROSE et al., 1990; GRA-

tory mechanism that allows individuals with CP to

BOWSKI et al., 2005). The quantification of the ener-

walk despite their impairments, and to do it in a way

gy expended while walking can provide objective

that minimizes metabolic costs. This interpretation

data in order to help evaluation of patients with

would suggest that walking patterns adopted by in-

walking disabilities and to help assess the effecti-

dividuals with CP might not be limitations but adap-

veness of therapeutic interventions, such as ortho-

tations to the changed dynamics (FONSECA et al.,

tics prescriptions, physical therapy or surgery. For

2001; HOLT et al., 2000, MASSAAD et al. 2004).

this reason, energy expenditure can be considered

For some authors the most crucial gait determi-

a useful tool for assessment of functional ability,

nant is the third foot rocker in association with heel

because its interpretation provides an indication of

rise, which explains up to 75% of the reduction in

endurance, fatigue and ability to accomplish the

vertical CM displacement in normal gait (MASSAAD

routine daily task of locomotion.

et al., 2006). Third foot rocker occurs when the plan-

It is known that children with CP typically ex-

tar flexor muscles move the ankle from dorsiflexion

pend 2 to 3 times as much energy in submaximal

into plantar flexion during push-off at the end of

walking as age-matched controls without CP (BEN-

stance phase. This plantar flexion induces a relative

NETT et al., 2005; ROSE et al., 1990). This increased

elongation of the lower limb length, which raises

energy use means that children with CP operate

the height of the CM when it has reached its lowest

closer to their maximum level of effort and are pro-

points of downward displacement, thus reducing

ne to fatigue at low walking intensities.

the vertical CM displacement.

Other researchers reported that a “poor pattern

In children with CP, whatever the topographical

of exchange between potential and kinetic energy

types and levels of severity in motor involvement,

of the head, arms, torso segment contributed to

they often show an equinus gait pattern with a de-

high total energy costs” (OLNEY et al., 1987).

ficient third foot rocker (i.e. a reduced ankle plantar-

The study by JOHNSTON et al. (2004) compared

flexion range of motion in third foot rocker) and a

the energy cost of walking in children with CP clas-

reduction in plantar flexor power at push-off. There-

sified at different levels of the Gross Motor Function


Locomotion in children with cerebral palsy: Classification System (GMFCS) with that in children

re. That is, interventions that improve their poor bio-

with typical development. Children with CP dis-

mechanics or increase aerobic capacity can make

played a higher energy cost of walking than the ty-

significant improvements in their walking efficiency

pically developing children. A strong correlation was

(WATERS; MULROY, 1999).

found between the energy cost of walking and

PICCININI et al. (2007) also found high values for

GMFCS level. This indicates increasing energy cost

the rate of energy expenditure and oxygen cost in chil-

of walking with increasing severity of functional in-

dren with CP revealing to be as important parameters

volvement. The reasons for the differences between

to characterize the cost of energy. The group affected

the levels include the severity of the involvement of

by the CP walked with a lower velocity and higher oxy-

force, co-contraction, spasticity or inefficient trans-

gen cost that may be due to the presence of simulta-

fers of energy between the segments of the body.

neous contraction of agonist and antagonist muscle.

Children with CP have been shown to expend

As in children with CP the study of MIAN et al.

greater energy during walking when assessed by

(2006) showed that the elderly without involvement

measuring either oxygen uptake or heart rate (HE-

of walking have a high metabolic cost of walking and

CKE et al., 2007; JOHNSTON et al. 2004).

a greater internal work accompanied by shorter steps

The measurement of oxygen consumption can al-

and increasing in step frequency. The elderly have also

so be a method to quantify the efficiency of walking

increased muscle co-contraction that may be a stra-

(BOWEN et al., 1998). Gait analysis allows the clinician

tegy to improve articulate stability and explanation of

to quantify specific mechanical aspects of walking;

the high metabolic cost of locomotion.

however, it cannot measure directly the overall effi-

This research observed no substantial change in

ciency of walking. Oxygen consumption (VO2) during

total mechanical work during walking in older adults,

walking can be measured directly with an automated

however recent observations suggest there is a reor-

or non-automated system (KEEFER et al., 2004).

ganization of neuromuscular control with a decline in

Drawbacks associated with the direct measure-

the relative contribution of ankle musculature for su-

ment of VO2 include the cumbersome nature of the

pport and propulsion with a concomitant rise in the

testing process and the high monetary cost required

contribution of hip musculature.

to purchase metabolic data collection systems. Con-

The constitution of the muscles and tendons of

sequently, indirect methods have also been employed

the ankle allows an effi cient production of work,

to assess locomotion energy cost.

however replacing the use of the structures of the

The energy expenditure index is an indirect me-

ankle muscles of the hip may contribute to the me-

thod used to evaluate energy cost. It is obtained by

tabolic cost of walking both in healthy elderly and

subtracting the resting heart rate (HR) from the exer-

in children with CP.

cise HR and dividing the difference by the walking speed (WATERS; MULROY, 1999; KEEFER et al., 2004).

All the aforementioned studies indicate that muscle co-contraction of the lower limbs or spasticity

However, Keefer et al. (2004) suggest that the

during walking increases the expenditure of energy

energy expenditure index to estimate the expenditure

causing the displacement of the center of gravity to

of energy in CP children walking should be applied

vary, leading to a less efficient pattern of walking.

with care. Findings from this study showed no rela-

Changes to the transfer of energy between the seg-

tionship between energy expenditure index based on

ments also contribute to the increase in energy ex-

heart rate and gross VO2 for different speeds in chil-

penditure, and children with CP have atypical pat-

dren with spastic hemiplegia.

terns of movement that may interfere in natural ex-

On the other hand, researches carried out in order to ascertain whether the use of ortheses and/or

change or in the transfer of kinetic and potential energy between the body segments.

surgical treatment would decrease energy expendi-

Muscle co-contraction can be defined as the si-

ture in locomotion of children with CP showed that

multaneous activation of agonist and antagonist mus-

there is an improve in the rate of energy expenditu-

cle groups crossing the same joint and acting in the Ciência em Movimento | Ano XII | Nº 23 | 2010/1

25

Locomotion in children with cerebral palsy: same plane (DAMIANO et al., 2000). Mechanically,

possible to state that children with CP use strategies,

this activation pattern increases joint stiffness while

not only from a biomechanical point of view but also

limiting agonist force production. Despite its inherent

in terms of energy expended during walking. They

inefficiency, co-contraction is a common motor con-

walk in low speed to keep the consumption of oxygen

trol strategy primarily activated when a person needs

to a level close to normal.

increased joint stability or improved movement accuracy. But over-activation of the antagonist leads to a high metabolic cost, represented by the increase in oxygen consumption.

26

CONCLUSION In the classic model of the inverted pendulum that describes the human locomotion, the minimization of

Increased co-contraction has been shown qualita-

work is affected by the maximum recovery of mecha-

tively during gait in children with CP. Although resear-

nical energy, but the conversion of energy during

chers have not yet precisely quantified co-contraction

walking in children with CP is smaller than the one

during movement in persons with CP, the degree of

found in normal children.

antagonistic coactivity has been estimated mathema-

The main findings of the studies suggest that the

tically in this population using several different com-

locomotion of children with CP has a greater vertical dis-

putational methods.

placement of CM, poor relationship of exchange betwe-

Possibly the electromyographic cost is an impor-

en potential and kinetic energy, increasing of the mecha-

tant tool to explain the energy of hemiplegics patients

nical work, less speed, smaller step length and increa-

adding important information to measures of external

sing of the step frequency. In other words, children with

and internal work, widely discussed in this review.

CP are mechanically less efficient in their locomotion.

Recently, a new hypothesis about the energy of

These children also have shown greater cost ener-

the human walking, known as “electromyographic

gy during walking than healthy children when assessed

cost of human locomotion”, has offered new insights

by measures of oxygen consumption and heart rate.

into the mechanisms that explain the mass-depen-

The co-contraction and equinus foot deformity are

dent metabolic expenditure necessary to go through

factors that are directly related to lower efficiency of

determined distance (PEYRÉ-TARTARUGA, 2008).

movement of hemiplegics children.

The equine foot deformity is another factor stron-

One may conclude that energy expenditure index

gly related to the high metabolic cost. This position of

and cinematography help assess the walking of chil-

the ankle suggests a biomechanics adaptation that

dren affected by the CP. Through them it is possible to

facilitates the use of dynamic resources available, be-

follow the trajectory of the results of therapeutic in-

cause it provides a mechanism to transport the body

terventions and, thus, contribute to functional impro-

CM in a model of mass spring, improving the ability

vement of patients.

to use a spastic triceps surae (HOLT et al., 2000).

Among them there are some suggestions for fu-

This reinterpretation may have important effects

ture research in the area of human locomotion: imple-

for methods of rehabilitation. The lengthening of cal-

menting physical therapies interventions to tone’s

caneus tendon is frequently used to minimize plantar

inhibition and assessing changes in gait patterns, eva-

flexion, however, if it is an adaptation, the procedure

luating internal work between internal affected leg

for lengthening can have deleterious effects on the

and not affected one, investigating the electromyogra-

ability to walk, or at least it can change the gait pattern

phic cost of locomotion in patients with CP, exploring

in no beneficial way.

the pendular mechanisms to minimize energy into

Through the data presented in researches, it is


other levels of involvement of CP.

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