NEURAL PLASTICITY VOLUME 12, NO. 2-3, 2005

Postural Dysfunction During Standing and Walking in Childrenwith Cerebral Palsy: What Are the Underlying Problems and

What New Therapies Might Improve Balance?

Marjorie Hines Woollacott and Anne Shumway-Cook

Department ofHuman Physiology, University ofOregon, Eugene, Oregon; USA1Department ofRehabilitation Medicine, University of Washington, Seattle, Washington," USA

ABSTRACT

In this review we explore studies related toconstraints on balance and walking in childrenwith cerebral palsy (CP) and the efficacy oftraining reactive balance (recovering from a slipinduced by a platform displacement) in childrenwith both spastic hemiplegic and diplegic CP.Children with CP show (a) crouched posture,contributing to decreased ability to recoverbalance (longer time/increased sway); (b) delayedresponses in ankle muscles; (c) inappropriatemuscle response sequencing; (d) increased co-activation of agonists/antagonists. Constraintson gait include (a) crouched gait; (b) increasedco-activation of agonists/antagonists; (c) decreasedmuscle activation; (d) spasticity. The efficiencyof balance recovery can be improved in childrenwith CP, indicated by both a reduction in thetotal center of pressure path used during balancerecovery and in the time to restabilize balanceafter training. Changes in muscle responsecharacteristics contributing to improved recoveryinclude reductions in time of contraction onset,improved muscle response organization, andreduced co-contraction of agonists/antagonists.Clinical implications include the suggestion that

Reprint requests to: M.H. Woollacott, Department ofHuman Physiology, University of Oregon, Eugene, OR 97403,USA

improvement in the ability to recover balance is

possible in school age children with CP.

REACTIVE STANCE BALANCE AND GAITIN CHILDREN WITH CP

Many children with cerebral palsy (CP) havepoor walking abilities and manipulation skills. Onecontributing factor to their problems with gait andreaching movement is poor balance controlbecause the maintenance of stability is critical toall movements. This review paper will summarizethe research on reactive balance control in suchchildren. Balance control is important forcompetence in the performance of most functionalskills, helping a child to recover from unexpectedbalance disturbances, either due to slips and tripsor to self-induced instability when making a move-ment that brings them toward the edge of theirlimit of stability.

Reactive balance control is defined as theability of an individual to recover from anunexpected threat to balance, such as a slip or a

trip. This characteristic is typically measured in thelaboratory using a moveable forceplate on whichthe individual stands. The forceplate is unexpectedlymoved different distances or speeds and individualsasked to respond to the threat without taking a stepor reaching for a handrail unless they wouldotherwise lose balance. One behavioral measure ofreactive balance control is the maximum velocity

(C) 2005 Freund Publishing House Ltd. 211

212 M.H. WOOLLACOTT AND A. SHUMWAY-COOK

of platform movement at which a child can stillmaintain balance without taking a step or reachingfor a handrail. Other measures include the timetaken to recover stability or the total distance ofcenter of pressure (COP, defined as the center ofthe vertical force exerted by the feet on the plat-form) movement during recovery from a platformdisplacement (Shumway-Cook & Woollacott, 2000).

Research has shown that children with CP(spastic hemiplegia and diplegia) have to take a

step at lower platform displacement velocities thantypically developing children of the same age, takea longer time to recover stability, and show morecenter of pressure movement during the recoveryperiod as well (Nashner et al., 1983; Chen &Woollacott, 2003; Shumway-Cook et al., 2003).Figure shows an example of the movement of thecenter of pressure from a child with spastic diplegia

vs a child who is typically developing in responseto the same amplitude and velocity of balancethreat (10 cm at 20 cm/sec). Note that the COP ofthe typically developing child passively movesforward as the platform moves backward. Thechild then efficiently returns the COP to a pointclose to its resting position as the child recoversstability.

In contrast, the child with spastic diplegiashows much greater COP movement before finallyrecovering stability, and in this case, is muchfarther than the typically developing child from theoriginal resting point. This research shows thatchildren with CP have more difficulty recoveringbalance efficiently when exposed to a balancethreat. The next question to be asked is whatneuromuscular constraints contribute to thisreduced efficiency of balance recovery.

COP Path for Forward Sway Perturbation

Typically Developing Spastic Diplegia

EF #1710@20

Tb

COPmax

Plate onset

COPfin

Fig. 1" Graph showing the total COP movement used to recover stability following a platformdisplacement causing forward sway for a typically developing child (left) and a child withspastic diplegia (right). Both children were exposed to similar types of perturbations

POSTURAL DYSFUNCTION IN CHILDREN WITH CP 213

Previous research by Nashner et al (1983) andBurtner et al (1998) has shown that the neuro-muscular response characteristics that contribute tobalance recovery show specific constraints inchildren with CP. For example, Nashner et al(1983) showed that children with spastic hemi-plegia show problems with the timing of muscleresponses. Such problems include delayed onset ofcontraction in the ankle musculature, a proximal-to-distal muscle response sequence (hamstrings/quadriceps muscles activated before gastrocnemius/tibialis anterior) and co-contraction of agonist andantagonist muscles at a joint. Such changes inneuromuscular response characteristics would leadto a slower and less organized recovery of balance.

Burtner et al (1998) performed similar experi-ments comparing the postural responses of childrenwith spastic diplegia of three developmental levels(pre-walkers, early walkers, experienced walkers)with those of typically developing children, ofsimilar developmental levels. The authors firstnoted that it was much more difficult to determinemuscle response onsets and offsets for childrenwith spastic diplegia because they typically havehigh levels of background muscle activity whenquietly standing and long duration responses tobalance threats as they attempted to recoverystability. Like Nashner et al (1983), the authorsalso found that timing of neuromuscular responsesin these children was more typically disorganized(more proximal-distal activation and more co-con-traction) and, unlike typically developing childrenwho show improvement with developmental level,timing did not improve in children with spasticdiplegia.

The investigators then asked whether onecontributing factor to such poor neuromuscularresponse organization might be the crouchedposture in which the children typically stood. Totest this theory, they asked typically developingchildren of the same age to stand in a crouchedposture and then measured their neuromuscular

responses to platform induced slips. The authorsfound that in this position, the responses of thetypically developing children showed (1) morecoactivation of agonists/antagonists and (2) moreproximal-to-distal muscle response timing. Theresults suggest that one contributing factor todisorganized muscle responses in these children istheir musculoskeletal alignment leading toacrouched posture (Burtner et al 1998; Woollacottet al., 1998).

More recent work by Roncesvalles et al (2002)indicates that one contributing factor to the smallerlimits of stability of children with spastic diplegiacompared with typically developing children is apoor ability to increase muscle response amplitudewhen balance threats increase in magnitude. Thegroup compared the muscle response amplitude(normalized and integrated EMG) for similar timeperiods after balance threats of increasing magni-tude were imposed on typically developing childrenand on children with spastic diplegia. The authorsfound that typically developing children increaseresponse size with level of difficulty of balancethreat, whereas children with spastic diplegia areunable to do so.

Research on the gait characteristics of childrenwith CP has shown similar results. Crenna andlnverno (1994) have defined the impairments ingait in children with CP as the following:1. changes in mechanical properties of the

muscle-tendon system (what they call the non-neural component) causing postural alignmentproblems and contributing to the crouch thatalso occurs in gait,

2. impaired muscle activation (what they defineas the paretic component) that reduces muscleresponse output and contributes to fatigue, and

3. loss of selectivity in neuromuscular output (theco-contraction component). In addition, theyfound

4. abnormal velocity dependent EMG recruitment(the spasticity component) (Crenna, 1998).

214 M.H. WOOLLACOTT AND A. SHUMWAY-COOK

The neuromuscular constraints in both reactivebalance and gait are so similar, suggesting thatthey have a common origin. In fact, researchersoften note that gait is made up of both stability (notfalling down) and progression (moving forward)requirements. Thus, it may be that many of theconstraints on gait in children with CP are due to

underlying stability problems, as noted above. Infact, the report of Crenna and Inverno (1994) showsmore coactivation of agonist and antagonist musclesat the hip (quadriceps and hamstrings) when suchchildren are performing unsupported walking (highbalance requirements) than when performingsupported walking (low balance requirements).

REACTIVE BALANCE TRAINING INCHILDREN WITH CP

As research indicates that impaired balanceshows a correlation with functional limitations inchildren with CP (McClenaghan et al., 1992;Crenna, 1998), therapy programs typically have an

increase in postural function as one of their goals,with the aim of creating increased efficiency inboth undisturbed stance and reactive balance control(Butler, 1998). Recently, research was performedto quantify the extent of improvement in balancewith a specific type of balance training involvingreactive balance control in a laboratory setting. Theresearch was modeled after that in a previous study(Sveistrup & Woollacott, 1997), which showed theeffectiveness of intensive practice in reactivebalance control on the organization of posturalresponses to balance threats in typically developingchildren just learning to stand independently.

These training studies (Shumway-Cook et al.,2003; Woollacott et al., in press) examined theeffect of intensive practice in responding to balancethreats created by a moveable platform on recoveryof stability in school age children with CP (meanage 9 y, 4 with spastic diplegia and 2 with spastic

hemiplegia) (Shumway-Cook, et al., 2003). Wehypothesized that this type of balance trainingwould improve reactive balance control in childrenwith CP, specifically improving the performancevariables that were found disorganized in priorresearch. Thus, we expected a reduction in bothCOP movements during balance recovery and intime taken to stabilize balance after a balance threat.We also expected that the improvement would bemaintained for month after the end of training.

Inclusion criteria for the study were the abilityto stand independently for at least 30 seconds andto walk independently, either with or without an

assistive device. Training involved five consecutivedays of reactive balance training on a moveableplatform. The training included 100 perturbationsof about 4-6/min each (along with rest breaks),with platform movements in both anterior andposterior directions at different amplitudes (3-6cm) and speeds (12-24cm/sec). Each participantwore a safety harness and watched children’s videoduring balance practice. The training differed fromother intervention strategies in specifically focusingon reactive balance control during a short intensiveperiod oftraining (5 days at 100 perturbations/day).

As hypothesized, balance training improvedthe ability of the children to recover efficientlyfrom reactive balance threats. Figure 2 shows theCOP traces for one of the trials in which a childwith spastic diplegia recovered from a balancethreat prior to training (a) immediately post-training (b) and a month post-training (c). Thefigure shows a substantial improvement in the totalmovement of the COP during the platformperturbation and recovery during post-training andthe one-month follow-up test, compared to pre-training (Shumway-Cook et al., 2003). In additionto a significant reduction in total COP movement

during balance recovery, there was also a

significant reduction in time to stabilize balance.Figure 3 shows a plot of the mean time

required to re-stabilize balance for different test

POSTURAL DYSFUNCTION IN CHILDREN WITH CP 215

A: SDI Pretest forward sway B: SD 1 Immediate Post Test Forward Sway

150

100

50

-50

-100

150

100

50

0

-50

-100

-150.150 ---1 ’l-150 -100 -50 0 50 100 150 -150 -100 -50 0 50 100 150

C: SD 1 30 Day Post Test Forward Sway

150

100

50

-50

-100

-150

-150 100 -50 0 50 100 150

Fig. 2: Graph showing total COP movement from one pretraining (a), post-training (b), and one month post-trainingtests (c), in a child with spastic diplegia (SD1 child with spastic diplegia #1. age 12 yrs, 11 m) (fromShumway-Cook et al., 2004).

216 M.H. WOOLLACOTT AND A. SHUMWAY-COOK

sessions (pre-training, during the intervention, andpost-training) for each of the six children tested.

One question that is important to ask iswhether improvement on a specific balance skill isassociated with improvement on tests of functionalbalance, such as Dimension D of the Gross MotorFunction Measure (GMFM) (Palisano et al., 1997).Five of six children were tested on the GMFMDimension D before and after training. One childwas unavailable after training. Although theGMFM does not include measures of reactivebalance control, measuring only quiet stance andanticipatory (balance during voluntary movements)balance skills, three of five children showedimprovement on the GMFM. One child with

spastic hemiplegia and one child with diplegiaimproved their scores by 12% and 11%, respectively.A second child with spastic diplegia showed a 3%improvement.

To ascertain specific neuromuscular changesthat were associated with improvement in reactivebalance efficiency post-training, Woollacott et al.(in press) measured muscle response characteristics(surface electromyograms) both pre- and post-training. The authors found the following improve-ments in neuromuscular response characteristicswith training:1. more efficient relative timing of contraction of

distal and proximal muscles involved in thereactive postural muscle responses (distalmuscles contracting before proximals).

2. shorter time to muscle contraction onset aftertraining, contributing to faster balance recovery.and

3. reduced coactivation of agonist and antagonistmuscles.

Figure 4 shows examples of changes in musclecontraction onset from pre-training to post-trainingand to month follow-up tests. Note the reductionin onset of contraction for both platform displace-ments, causing both forward and backward sway.

Woollacott et al (in press) noted that differentcombinations of the above factors were used byeach child, with more substantial improvementbeing found in the less involved children. Forexample, two children with spastic hemiplegiaimproved both contraction timing and reduced co-contraction of agonist/antagonist muscles aftertraining. In contrast, only one of four children withspastic diplegia improved in both timing and levelof co-contraction. Five out of six children reducedonset of contraction for ankle muscles for backwardsway, contributing to a faster balance recovery. Inaddition, two children (one with spastic diplegiaand one with hemiplegia) reduced the time of onsetof contraction for distal muscles and lengthened itfor proximal muscles, contributing to improve-ment in muscle response sequencing. One childwith hemiplegia and two with diplegia showedlater contraction times for antagonist muscles,reducing the coactivation of agonists with

antagonists. Finally, one child with diplegia andtwo with hemiplegia showing smaller antagonistmuscle contractions also reduced the coactivationof agonists and antagonists.

The wide variety of combinations of changesin neuromuscular response characteristics impliesthat each child find its own individual strategy forimproving balance efficiency following training.The results also suggest that children with lessinvolvement (hemiplegia vs diplegia) have morepossibilities for increasing the efficiency of theavailable neuromuscular response characteristics.

The possible neural mechanisms underlyingchanges in neuromuscular response characteristicsinclude the following:

1. improved proprioceptive sensitivity in legmuscles,

2. enhanced synaptic efficacy within primarysensorimotor cortex pathways, or

3. higher level adaptations at the level of cere-bellum or association cortex.

POSTURAL DYSFUNCTION IN CHILDREN WITH CP 217

Mean Forward Sway

5’4.5

) ,3o,5

2.52

.50o5" o

Baseline ntervention Posttest

--,- SD1 = SD2----SD3 x- SD4--=- SH1 SH2

Fig. 3: COP time to stabilization (TTS) of balance after a forward sway perturbation in the six children, duringbaseline, intervention and maintenance (post-test) phases (Abbreviations: SD 1-4 the 4 children with spasticdiplegia. SH 1-2 the 2 children with spastic hemiplegia) (from Shumway-Cook et al., 2004).

150-

100-

50-

0

Children with Spastic Diplegia

Forward SwayTibialis Antedor

Backward Sway

PrelstPoststOne IVIon

Fig. 4" Graph showing time of onset of contraction for the distal agonist muscles (gastrocnemius for forward sway andtibialis anterior for backward sway) for the children with spastic diplegia for pretest, posttest, and one monthfollow-up tests.

218 M.H. WOOLLACOTT AND A. SHUMWAY-COOK

Clinical applications of this study include thesignificant result that reactive balance performancecan be improved in school age children with CP.The data suggest that continued practice in balancerecovery and stability can help children withspastic hemiplegia and diplegia to improve theirability to maintain and recover balance.

SUMMARY

by both faster and better organized muscle con-tractions, including a reduction in the coactivationof agonist and antagonist muscles.

ACKNOWLEDGEMENT

This research was supported by NIH R01 Grant#NS38714 to Dr. Marjorie Woollacott, PI.

In summary, the results of the reported studieson reactive balance control in children with CPsuggest that reactive postural control is reduced inchildren with both s.pastic hemiplegia and diplegia.This reduction includes a longer time to stabilizebalance and more movement of the Center ofPressure during balance recovery. The neuro-muscular response characteristics contributing tothese balance constraints include a delayed onsetof muscle contractions, a disorganized timing ofmuscle responses (proximal muscles activatedbefore distal muscles), and an increased co-activation of antagonist muscles with agonists. Thebalance constraints also contribute to less-efficientwalking performance, with research showing similarneuromuscular response changes in unsupportedlocomotion. Studies testing the efficacy of reactivebalance training in school age children with CPhave shown that balance can be significantlyimproved by as little as 5 days of intensive balancetraining (100 perturbations/day). In three of fivechildren tested, changes found in the efficiency ofreactive balance control, as measured by time tostabilize balance and mean COP displacement,were supported by the improvement on DimensionD of the GMFM. This subtest measures steadystate and/or proactive balance control during stance.

Currently, no test within the GMFM can measurereactive balance performance, thus, this parametercould not be measured directly in a functionalbalance test. The improvements were accompanied

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