postural in children born pretermdownloads.hindawi.com/journals/np/2005/573752.pdf · preterm...

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

Postural Behavior in Children Born Preterm

Bjorg Fallang and Mijna Hadders-Algra2

Oslo University College, Health Sciences, Physiotherapy Programme, O130 Oslo, Norway;University Hospital Groningen, Department ofNeurology, Groningen, The Netherlands

SUMMARY

The present paper presents clinical andneurophysiological data of postural behavior inpreterm children without CP. Clinical follow-up studies of preterm infants until toddler andschool age have reported that low-risk preterminfants may have atypical postural behavior interms of reduced amount of rotation duringcrawling, delayed dynamic balance, delayedonset of and a poor quality of early walkingbehavior. At school age, dysfunctions such asproblems in standing on one leg and poorhopping are reported. Neurophysiological dataof postural control at early age indicated thepresence of a dysfunction in the capacity tomodulate postural activity, and the posturalactivity has been characterized by temporaldisorganization of EMG responses. Posturalresponses to goal-directed reaching in supinelying have been recorded and analyzed in termsof the total body center of pressure. In this

study, preterm infants show less mobile posturalbehavior compared with full-term infants. Ininfancy, the less mobile postural behaviorseemed to be adequate as it was related to bettergoal-directed reaching quality, but the resultsindicated that the relatively immobile posturalbehavior during reaching in early age wasrelated to less favorable neuromotor behaviorin school-age.

Reprint requests to: Bjrg Fallang, Oslo University College,Health Sciences, Postbox 4, St. Olavs Place, 0130 Oslo,Norway; e-mail [email protected]

INTRODUCTION

Preterm birth challenges the development ofmotor control not only because ofan increased riskof periventricular hemorrhage and leukomalaciabut also because the infant starts extrauterine lifewith an immature and more vulnerable motor andsensory system. As a result, one of the frequentlyoccurring sequelae of preterm birth is a lack ofadequate postural control during motor activities.This occurs not only in children with cerebralpalsy (CP) but also in those without CP. in.thepresent paper, we aim at discussing the clinicaland neurophysiological data of postural behaviorin preterm children without CP.

CLINICAL DATA ON POSTURAL BEHAVIORIN PRETERM CHILDREN

In early infancy, deviations in the posturalbehavior of preterm infants have been described astransient dystonia, a postural behavior reminiscentof postures exhibited during the dystonic stage ofdiplegia. This means that the infants may showbrisk tendon reflexes and when held in the verticalposition, extended and adducted legs with planti-flexed feet, rigid arms with fisted hands, whilehead control depends on body position (Drillien.1972). De Groot and colleagues (1992) describedthe postural behavior of preterm infants in terms offaulty muscle power, defined as an imbalancebetween the active adjustments to changes inposture and passive muscle tone. Excess ofextension behavior has also been reported as

(C) 2005 Freund & Pettman, U.K. 175

176 Bo FALLANG AND M. HADDERS-ALGRA

"fixing behavior" with extremities to the supportsurface (Gorga et al., 1985), and as extension andshoulder retraction in sitting (Georgieff et al.,1986). The incidence of transient dystonia orfaulty muscle power in children who do not

develop cerebral palsy has been reported to bebetween 28 percent (Sommerfelt et al., 1996) and40 percent (de Groot et al., 1995).

Follow-up studies of preterm infants intotoddler and school age have reported that evenlow-risk preterm infants may have dysfunctions inpostural control; for instance they show a reducedamount of rotation during crawling, delayeddynamic balance, delayed onset of independentwalking, and a poor quality of early walkingbehavior (Gorga et al., 1988; de Groot et al., 1995,1997; Bylund et al., 1998). At school age,dysfunctions in balance control are expressed asproblems in standing on one leg (Forslund &Bjerre, 1989; Marlow et al., 1989; Herrghrd et al.,1993), poor hopping, and clumsy walking(Sommerfelt et al., 1993). The relationshipbetween the early deviations in postural musclepower regulation (at 4 months) and developmentduring the first year of life has been addressed bythe group of de Groot in both low- and high-riskpreterm infants. In low-risk preterm infants, earlypostural dysregulation has been associated with

poorer sitting performance, asymmetries (de Grootet al., 1995, 1997) and non-optimal hand functions

(Plantinga et al., 1997) at 9 months of age. In high-risk preterm infants, early muscle dysregulationand dysfunctional postural behavior at 12 monthswere the best predictors for neurodevelopmentaloutcome at 7 years of age (Samsom et al., 2002).When de Vries and de Groot (2002) re-examined a

selected low-risk sample of these preterm infants,however, the authors were unable to confirm a

relationship between muscle dysregulation at 4months and motor performance in terms of trunk

rotation at 2.6 years. In a study with preterminfants without cerebral palsy, Sommerfelt et al.

(1996) reported a trend toward more neuromotor

problems at 5 years in children with early transientdystonia. Therefore, how these early deviations inpostural behavior are related to the posturaldeviations described at school age is not clear.Although, the implications are still uncertain,dystonia might be an important trait in earlybehavior and should probably be included in theevaluation of low-risk infants. Insight into theemergence and nature of these problems isimportant in order to know when and howtherapeutic interventions might be introduced.

NEUROPHYSIOLOGICAL DATA ON POSTURALBEHAVIOR IN PRETERM CHILDREN

In studies for which EMG recordings havebeen applied, postural muscle activity of pretermchildren differs from that of full-terms. One study(Hadders-Algra et al., 1999) evaluated posturalactivity in response to platform perturbations insitting children aged 11/2 to 41/2 years. The authorsreported that preterm children with periventricularwhite matter lesions and those with normalultrasound scans were less able to modulatepostural muscle activity to initial sitting position.As the preterm children also showed an increased

sensitivity to velocity dependent stretch, it was

suggested that in preterm children, the normalbalance between feedforward and feedback controlof posture has been replaced by a form of controlduring which feedback processes dominate.

The longitudinal study of van der Fits et al.(1999), in which postural muscle activity duringreaching in various positions of full-term andpreterm infants was assessed between the ages of 3and 18 months, confirmed the presence of a

dysfunction in the capacity to modulate posturalactivity. The study also showed that preterm infantsolder than 4 months activated more posturalmuscles during reaching than full-term infants did,and that the postural adjustments of preterm infantswere characterized by temporal disorganization.

POSTURAL BEHAVIOR IN CHILDREN BORN PRETERM 177

Recently we carried out a small series of studieson qualitative and quantitative aspects of posturalbehavior at 4 and 6 months corrected age in 12 full-term (Fallang et al., 2000) and 32 preterm infantswho did not develop cerebral palsy (Fallang et al.,2003b). The preterms were divided into two groups,11 infants were allocated to a high-risk group (meangestational age 28 weeks) if they had either one ormore of the following problems: Apgar score lessthan 3 at 5 minutes, respiratory problems, or apersistent ductus arteriosus. Twenty-one low-riskpreterms were without these problems (meangestational age 30 weeks). The infants were placedin a supine position on a forceplate, with anattractive toy above them to reach for. Theforceplate below the infant recorded the posturaladjustments during the reach. The movemen of thetotal body center of pressure (COP) was analyzed interms of total travel path and maximum velocity inboth cranial-caudal and medial-lateral direction. Inaddition to the forceplate data, kinematic data of thereaching movement were collected. The kinematicsof the reaching hand was analyzed in terms of peaksin the velocity profile called movement units (MU).Earlier analysis ofMUs in full-term infants revealedthat reaching movements in general become morestraight-lined and exhibit fewer corrections in themovement path with increasing age (von Hofsten,1982, Thelen et al., 1993).

We found that the total body COP of preterminfants differed markedly from that of full terms.The preterm infants showed a relatively immobilepostural behavior, i.e. a very small travel path ofCOP, during reaching compared with full-terminfants at both 4 (Fig. a) and 6 months (Fig. b),whereas no differences were found between thelow-risk and high-risk preterms. In addition, themaximum velocity of COP of preterm infants was

substantially lower than that of full-term infants atboth testing ages. Two additional differences inpostural control were found between full-term andpreterm infants in relation to direction and to age.

The full-term infants showed more COP movementsin medial-lateral direction than in cranial-caudaldirection, and the size of the COP movementsdecreased with age in full-term infants, whereas nodirectional or age-related changes were found in thepreterm infants (Fig. a,b). The differences inpostural behavior between full-term and preterminfants could not be explained by differences inanthropometrics. The only perinatal parameter inpreterm infants associated with postural behaviorwas gestational age at birth, whereas no relationbetween postural behavior and perinatal parameterslike birthweight, respiratory morbidity, or ultra-sound scans of the neonatal brain or sex was found.

We wondered whether the different posturalbehavior of preterm infants was a sign of neuraldysfunction or could be regarded as a functionaladaptation of the infant in response to the earlyextrauterine environment. Arguments in favor ofthe latter view were that the less mobile total bodymovement during reaching at 6 months wasassociated with better quality of reaching, a highergestational age at birth (above 28 weeks), and withthe presence of normal general movements at 4months (Figs. 2 and 3). In general a highergestational age is associated with a lower rate ofneurodevelopmental morbidity (Allen, 2002), andnormal general movements point to the integrity ofthe function of the central nervous system(Hadders-Algra, 2004). At 4 months of age, lessmobile COP behavior was associated with shorterduration of the reach and less number ofmovement units, at 6 months it was related to

reaching movements characterized by mediumvelocity with few movement units (Fallang et al.2003a,b). We therefore concluded that at earlyage, the relatively immobile postural behaviorduring reaching might be considered a functionaladaptation. Nevertheless, we wondered whetherthe atypical and at early age adaptive posturalbehavior of preterm infants could be a marker oflater dysfunction as well.

178 B. FALLANG AND M. HADDERS-ALGRA

m0,15-

0,12

,o9

0,03-

low-risk PT high-risk PT fullterm

0,12-

0,03

121 10 110low-risk PT high-risk PT fullterrn

Fig. I: (adapted from Fallang et al. 2003). Displacement in both the medial-lateral (horizontally lined boxes)andcranial-caudal (vertically lined boxes) directions are smaller in both low-risk and high-risk preterm infantscompared to full-term infants, at 4 months (panel a; p<0.001 and at 6 months (panel b; difference between full-term and preterm infants in medial-lateral direction p<0.01, rest of comparisons: p<0.05)


fno:o-

0,05

0,04

0,03

0,02

0,01

0,00

Normal GM Mildly abnormal

Fig. 2: COP displacement at 6 months and its relation to quality of General Movements (GMs) at 4 months in preterminfants. Difference between normal and mildly abnormal GMs: p<0.05

0.t0

0.02

mMABC above15th MABC below15th

Fig. 3: The relationship between displacement of COP in medial-lateral direction at 6 months of age and MovementABC (MABC) scores above and below the 15th percentile at school-age in preterm and full-term children.Difference between two Movement ABC groups: p<0.01.


RELATIONSHIP BETWEEN COP AT EARLYAGE AND NEUROMOTOR BEHAVIOR AT

SCHOOL-AGE

To understand the implications of our earlierfindings of the relatively immobile posturalbehavior in preterm infancy, we also did a follow-up study on these children to elaborate on possibleassociations between this early postural behaviorand neuromotor behavior at school-age. Fifty-twopreterm children were available for follow-up at 6years of age. They were assessed with MovementABC (Henderson & Sugden, 1992) and Touwen’s(1979) neurological assessment. The objective ofMovement ABC is to identify children with motorproblems in the three subsections: manualdexterity, ball skills, and balance skills. Theassessment is widely used (Geuze et al., 2001).The total score can be converted to a percentilescore, reflecting the child’s score compared to anormative sample. A percentile ranking above 15th

is considered normal, between 5th and 15th is in theborderline range, and below 5th percentile the childis considered as having problems. Touwen’s(1979) neurological assessment is a standardizedneurological assessment constructed to detectminor neurological abnormalities, which can beclassified as simple or complex forms of minorneurological dysfunction (MND). Simple MNDreflects the presence of a normal but non-optimallywired brain, which can be attributed to geneticconstitution, or to stressful events during early lifesuch as preterm birth. Complex MND can beconsidered a clinically significant brain dysfunction(Hadders-Algra, 2003).

Our hypothesis that the relatively immobilepostural behavior during reaching at an early agecould be an adequate functional adaptation toextra-uterine demands did not seem to hold true

for neuromotor behavior at school age. The results

Fallang et al. Quality of reaching and postural control inyoung pretema infants is related to neuromotor outcome at 6years. Pediatr Res (accepted for publication).

indicated that the relatively immobile posturalbehavior during reaching in early age was relatedto less favorable neuromotor behavior in schoolage, e.g. this postural behavior at 4 months wasassociated with simple MND (p < 0.05, groupedfull-term and preterm). The postural behavior at 6months was associated with a worse score on theMovement ABC (p < 0.01, grouped full-term andpreterm; Fig. 3). This finding suggests that thisrelatively immobile postural behavior points to amild form of brain dysfunction. When we analyzedthe associations between COP behavior andsubscores of Movement ABC, we found that worsescores on balance skills were related to reducedCOP movement (p < 0.01), but not to hand motoror ball skills.

CONCLUDING REMARKS

How can we understand these findings? Inpreterm infants, reduced postural movement

during reaching (Fallang et al., 2003b) might beanalogous to the lack of modulation and excessivetrunk muscle activity found in EMG studies inresponse to reaching (van der Fits et al., 1999) andto the observation of "fixing" behavior reported byGorga and colleagues (1988) and de Groot andcoworkers (1997). This may be interpreted as afunctional strategy: the infant is freezing degreesof freedom to perform the reaching. On the otherhand, this freezing of degrees of freedom mayhamper the dynamic, normal exploration andvariation of solutions during the process oflearning new behavior that are prevailing innormal development (Touwen, 1993), which inthis context was to learn successful reaching.Variation in postural muscle activity characterizesthe postural behavior of typically developingchildren in response to perturbation of the supportsurface (Hirschfeld & Forssberg, 1994; Hadders-Algra et al., 1996), in response to loosing trunksupport (Harbourne & Mac Neela, 1993), and in


response to voluntary reaching activity (van derFits et al., 1999).

What then are the clinical implications? Therelatively immobile postural behavior duringreaching at early age was not related to clinicallysignificant brain dysfunction in the form ofcomplex minor neurological dysfunction. Suchbehavior was associated with less optimal motordevelopment, however, which might indicate thatpreterm infants are at risk of experiencing poorexplorative motor behavior and lack of variation inmovements. As variation in the movementrepertoire seems to be important in normal motorbehavior (Hadders-Algra, 2000) we have to payattention to this aspect of development. Whenearly intervention is applied, we should thereforewarrant and stimulate the infant to explore moremotor solutions in the early learning of newbehavior. So far, the results from the kineticstudies cannot be directly implemented intoclinical use. However, the results from clinicalstudies by, for example Gorga et al. (1988), deGroot et al. (1997), and Samsom et al. (2002), andthe detailed neurophysiological studies of reachingand postural behavior (van der Fits et al., 1999;Fallang et al., 2003a,b), can help in designing newor in improving present clinical instruments or ingiving directions for clinical observations. As weextend our knowledge of the minor and moderatemotor problems in preterm children, the assess-ments may be more specifically attuned to theproblems in this group.

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