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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Ciência em Movimento | Ano XII | Nº 23 | 2010/1
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
21
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
Ciência em Movimento | Ano XII | Nº 23 | 2010/1
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
23
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
Ciência em Movimento | Ano XII | Nº 23 | 2010/1
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
Ciência em Movimento | Ano XII | Nº 23 | 2010/1
other levels of involvement of CP.
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