the organization of leg movements in preterm and full-term infants after term age

The Organization of Leg Movements in Preterm and Full-Term Infants after Term Age JULIA J. GEERDINK Department of Medical Allied Health Professions University of North Carolina Chapel Hill, North Carolina

BRIAN HOPKINS Department of Psychology Lancaster University Lancaster, United Kingdom

WIERO J . BEEK Faculty of Human Movement Sciences Free University Amsterdam, The Netherlands

CAROLYN B. HERIZA School of Allied Health Professions St. Louis University St. Louis, Missouri

In a sample of 13 full-term and 10 preterm infants, the development of kicking movements was studied at 6, 12, and 18 weeks (corrected) age. In healthy full-term infants some characteristics are strikingly stable, such as the duration of the flexion and extension phase and the within-joint organization. These parameters did not differ in preterm compared to full-term infatns. For other features, however, developmental changes and differences were observed. Full-term infants tended to decrease their kick frequencies slightly with age. In preterm infants much higher initial kick rates were found, followed by a steep decrease, which resulted in kick frequencies comparable to the full-term levels after the (corrected) age of 12 weeks. There is a tight coupling between the movements in the different joints of the leg in full-term newborns. Preterm infants, in contrast, initially show much lower cross-correlations between hip and ankle and between knee and ankle.

Reprint requests should be sent to Brian Hopkins, Department of Psychology, Lancaster University, Lancas- ter LA1 4YF, United Kingdom.

Received for publication 11 May 1994 Revised for publication 22 August 1995 Accepted for publication 22 December 1995

Developmental Psychobiology 29(4):335-351 (1996) 0 1996 by John Wiley & Sons, Inc. CCC 0012-1630/96/040335~17

336 GEERDINK ET AL.

This is particularly the case for those preterm infants who were born before 32 weeks gestation. Again, the differences resolved after the age of 12 weeks, which might be related to a transformation in neural functions reported previously around this age. The initial differences in the characteristics of kicking appeared to be more readily explainable by differences in neurological condition than by contrasts in leg volume or postural control. 0 1996 John Wiley & Sons, Inc.

Introduction Preterm birth and intrauterine growth retardation (IUGR) are often associated with

developmental problems, particularly deviances in motor development (Gorga, Stern, & Ross, 1985; Piper, Byrne, Darrah, & Watt, 1989). The present study focuses on spontaneous kicking movements, which form a striking feature of the movement repertoire of infants in the supine position (Thelen, 1981). So far, this behavior has been studied mainly in full-term infants. The main focus has been on the activity level of the infants, i.e., kick frequency, and on the organization of the movements in terms of temporal and spatiotemporal characteristics, as well as the relationship between the different joint angles. Little is known about the effect of prematurity and IUGR on the development of leg movements. The activity level and movement organization in preterm infants are likely to differ from their full-term counterparts, especially in very young and growth-retarded preterm infants. In order to examine whether a low gestational age or growth retardation affected the development of kicking movements, preterm infants with and without IUGR are compared with full-term infants who are not growth-retarded.

Both preterm birth and IUGR often give rise to neurological problems. In order to distinguish the effects of these two risk factors from those of minor neurological problems, an independent measure of neurological condition is used, namely, the assessment of spontaneous movement quality (Prechtl, 1990). This qualitative assessment provides a new and promising means of detecting minor neurological differences between preterm infants and has a high predictive value for later outcome (Geerdink & Hopkins, 1993b). Consequently, it is expected that distinctions based on movement quality will be more strongly related to differences in leg movements than those derived on the basis of medical risk factors.

For upright stepping, research by Thelen and co-workers (1984) has suggested that somatic growth is related to the disappearance of these leg movements. Another rate- limiting factor in motor development is postural control (Touwen, 1976). In preterm infants, problems in postnatal growth (Ross, Lipper, & Auld, 1985) and postural control (Gorga et al., 1985) are often observed. It is probable that such problems manifest themselves in the development of kicking movements.

The present study focuses on the question of whether spontaneous kicking movements develop in the same way in preterm infants as in full-term infants after term age. In doing so, it asks whether any deviations in this development can be accounted for by differences in pregnancy duration, birthweight status, and neurological condition. In addition, the role of somatic growth (defined as change in leg volume) and postural control (defined as the ability to hold the head in the midline position) as possible rate- limiting factors will be considered. The development of kicking movements will be studied on the basis of the following parameters that have previously been investigated in full-term infants: (a) Kick frequency, (b) temporal organization, (c) within-joint spatiotemporal organization, and (d) between-joint correlation.

LEG MOVEMENTS IN PRETERM INFANTS 337

Methods

Subjects The sample consisted of 10 preterm infants (4 male, 6 female) with gestational ages

ranging from 27 to 34 weeks and 13 healthy full-term controls (4 male, 9 female) born after pregnancies of 38 to 42 weeks. All infants were Caucasian and singleton, living in or around Amsterdam, The Netherlands. To distinguish the effect of preterm birth and IUGR from the frequently occurring, additional medical complications and neurological abnormalities, the preterm infants were carefully selected for the absence of problems such as chromosomal anomalies, cardiac diseases, other congenital abnormalities, cerebral hemorrhages more than second degree, and periventricular leucomalacia. The medical records were screened for the absence of such medical complications other than a birth weight which was Small-for-Gestational-Age (SGA). Subsequently, asphyxia and neurological abnormalities were excluded by a child neurologist. Infants were classified as SGA when their birth weight was below the 10th percentile of the Amsterdam growth cures adjusted for parity and gender (Kloosterman, 1970). Appropriate-for-Gestational- Age (AGA) infants, on the other hand, had birth weights abcve the 25th percentile of the growth curves. By excluding infants with congenital and chromosomzl anomalies and small mothers (< 1.60 M ) , the SGA infants were considered to have suffered from late-occurring IUGR, which results in asymmetrical growth retardation. Indeed, all SGA preterm infants participating in this study had ponderal indices below the 10th percentile adjusted for gestational age (Miller & Hassanein, 1971), whereas the AGA preterm infants had values above the 10th percentile. The gestational ages and birthweight percentiles of all subjects are given in Table la.

The preterm infants were not only distinguished in terms of birth-weight status, namely, SGA (n = 5) or AGA (n = 5 ) , but also as to whether they were born before (n = 4) or after 32 weeks gestation ( n = 6). This distinction was made on the basis of findings showing that 32 weeks is a critical age, as infants born before this age run a higher risk for later developmental problems (Largo et al., 1989; Low et al., 1985). The analyses concerning temporal and spatiotemporal organization, as well as intralimb coordination, required extensive microanalyses. For pragmatic reasons, we limited the size of the samples involved in these analyses to 6 full-term and 8 preterm infants. The mean gestational ages for the preterm groups are given Table lb. For all analyses, the numbers of those born before or after 32 weeks pregnancy duration were equal for the SGA and AGA groups.

The preterm infants were not only classified on the basis of the medical risk factors, birth-weight status, and pregnancy duration, but also in terms of individual nervous system functioning as reflected in assessments of spontaneous movement quality. From the repertoire of spontaneous movements, general movements (GMs) were selected for these assessments. GMs (which involve head, trunk, and extremities) are assigned a normal quality when executed with complexity, fluency, and variations in speed and amplitude (Prechtl, 1990) as can be observed in healthy infants. When the appearance of GMs is strikingly rigid, awkward, and monotonous, they are classified as abnormal. A third category-mildly abnormal quality-was added for GMs which were not rigid but lacked a consistent impression of complexity and variation (Geerdink & Hopkins, 1993a). The interrater agreement between three observers, who were unaware of the research questions, ranged from 87-93%. On the basis of the assessments of GM quality from videorecordings at 6, 12, and 18 weeks, 5 preterm infants were classified as normal

338 GEERDINK ET AL.

Table l a Subject Information

~~ ~

Gestational Age Movement Subject Gender (weeksdays) Percentile Quality

Preterm 1. M 29h p5 A SGAs 2. M 314 <p2 3 A

3. M 33' <p2 3 N 4. F 336 p5 N 5 . F 340 P5-P,0 A

Preterm 6. F 27 ' p75 A AG As I . M 28O p25 N

8. F 333 P50 N 9. F 333 P50 A

10. F 343 p25 N

Full-term 11. F 40° p75 infants 12. F 41 ' pso

13. M 382 P50 14. F 395 pso 15. F 394 p25-p50 16. F 395 p2s-p50 17. M 406 P75-Pw

19. M 396 P75-Pw 20. F 41' PIS

23. F 414 pz5-p50

18. F 406 p50

21. F 40° p50-p75

22. F 41' p25

N N N N N N N N N N N N N

and 5 as (mildly) abnormal at all ages. All full-term controls showed a normal movement quality at all ages.

Procedure The infants were videotaped by two synchronized cameras for 15 min at 6, 12, 18,

and 24 weeks (corrected) age. During these recordings, they were lying supine and naked on a purpose-built bed surrounded by white curtains and with an ambient temperature

Table lb The Mean Gestational Age by Group for the 8 Preterm Infants Involved in the Analyses Concerning Temporal and Spatiotempo- ral Organization and Intralimb Coordination

Group Mean Gestational Age (Weekdays) -t SD

Birthweight status SGA AGA

Pregnancy duration < 32 weeks > 32 weeks

32' ? l6 305 2 3'

29' t 2O 334 2 03

Movement quality Abnormal Normal

31' t 25 314 t 30


maintained at 27 2 1°C and a relative humidity of 28 t 8%. One camera, which was hidden in the ceiling above the child, was used to record the total amount of kicking in both legs. The first fragment of 5 min during which the infant was awake and active but not crying was selected for this analysis. A second camera was placed on the right side of the infant to record the joint angles of the leg while kicking. From the recording made by this camera, a short fragment of videotape was selected with a duration of up to 10 s. We selected only those fragments in which the infant was continuously kicking in the air, with the legs positioned at right angles to the camera, preferably making alternating leg movements with the head in the midline position. In order to be sure we had selected fragments without any internal or external rotations of the thigh, a second check was made from the recordings made by the overhead camera. The resultant mean duration of these fragments was 7.0 t 2.5 s.

Measures From the recordings made with the camera in the ceiling, kicking frequency was

assessed using an interactive computer program. Each time a flexed position was reached after an extension, the observer pushed a button (for left and right leg separately). The total number of kicks were then summed by the computer. All assessments were performed by the same observer.

From the recordings made by the side camera, the coordinates of markers on the lateral thigh at the hip crease (hip), the lateral femoral condyle (knee), the lateral malleolus (ankle), and the lateral base of the fifth toe (toe) were sampled at a frequency of 50 Hz using an xy plotter. The interrater reliabilities for these assessments were very high between three observers (kappa I) 0.93). From these coordinates the angle, and subsequently the angular velocity, was calculated for the hip, knee, and ankle joints. The angle of the hip was calculated relative to a horizonal axis (representing the position of the trunk).

Phase durations were calculated from the excursions from the knee joint. While it is arbitrary as to which joint is selected for such calculations, we chose the knee so that the resultant findings could be compared directly to those of Heriza (1988a, 1988b), who used this joint to derive the phase durations for her preterm infants. Using the knee joint, we assessed the durations of the following four kick phases: flexion (continuous decrease in angle of at least 20 degrees, until the joint started to exhibit smaller fluctuations around the flexed position), intrakick pause (fluctuations between flexion and extension), extension (continuous increase in angle of at least 20 degrees), and the interkick pause (small fluctuations between the end of extension and the start of a flexion belonging to a new kick cycle).

Data on the joint angles were also used to calculate pairwise cross-correlations between the hip, knee, and ankle. For the purpose of group comparisons, the cross- correlations were transformed to Fisher 2 scores. Because the majority of infants did not produce usable episodes of kicking at 24 weeks, this age was excluded from further analysis.

To study the influence of differences in leg volume, the leg was represented in simplified form as a cylinder. The content of this cylinder was calculated at each age on the basis of the length of the leg (crown-heel minus crown-rump length) and circumference of the calf, which can be measured more reliably than the circumference of the thigh. Subsequently, the change in volume between 6 and 18 weeks was calculated as a measure of leg growth.

340 GEERDINK ET AL.

Table 2 Mean Number of Kicks (5 SD) Per Min (Over a 5-min Sequence) in Preterm (PT) ( n = 10) and Full-term (FT) Infants ( n = 23)

6 Weeks 12 Weeks 18 Weeks

PT 22.8 t 16.2 17.2 t 16.0 9.0 2 8.2 8.6 +- 7.6 FT 11.4 k 6.6 9.8 t 4.6

Head control was expressed in terms of the percentage of time the infants held their head in midline position while lying supine. This was calculated as the percentage of time, out of a 5-min period of videorecording, during which the infant held nose and chin within the area limited by left and right nipple (Michel, 1981). Observers were trained in order to reach an interobserver kappa of .80 or above. Like those who judged GM qualities, these observers were also unaware of the research questions.

Data Analyses For group comparisons, the preterm infants were distinguished in three ways on

the basis of pregnancy duration (below vs. above 32 weeks), birthweight status (SGA vs. AGA), and movement quality (abnormal vs. normal). To reduce the probability of Type I errors when making more than one comparison, a post-hoc Bonferroni t test was applied. The preterm subgroups were compared with the full-term infants over age using a (3 x 3 ) (Group x Age) repeated measures analysis of variance (ANOVA) design. Subsequently, the estimates of leg growth, leg volume, and head control were added to the design as covariates using ANCOVA. Our goal in doing so was not to correct for preexisting group differences on the covariates. Rather, we used these analyses to examine whether a possible group difference in one of the independent variables was only found because of a difference in a covariate, i.e., whether a covariate completely explained the group difference for an independent variable.

To determine whether a varaible can be used as a covariate in ANCOVA, three requirements must be fulfilled (Lovell, Franzen, & Golden, 1987). First, the relationship between covariate and dependent variable should be significant. Second, the groups should differ significantly on the covariate. Finally, the Fisher 2 transformed correlation between covariate and dependent variable should not differ significantly between any two groups.

Results

Kick Frequency The total kick frequency in both legs appeared to be higher in preterm compared

to full-term infants (Table 2 ) . This difference was most striking at 6 weeks, with the kick rate of the preterm infants being twice as high as that of the full-term controls. The difference was still considerable at the age of 12 weeks, but resolved at 18 weeks.

Analyzing the differences between SGA and AGA preterm infants and full-term controls over age revealed a significant main effect for both group, p < 0.05, and age,


Table 3 Mean Durations (* SD) of the Different Phases of the Kick Cycle for Preterm (PT) (n = 8) and Full-Term (FT) Infants ( n = 6) During a Kicking Bout

PT FT PT FT PT FT Age 6 Weeks 6 Weeks 12 Weeks 12 Weeks 18 Weeks 18 Weeks

Flexion 0.28 t 0.09 0.31 t 0.10 0.29 ? 0.10 0.37 2 0.13 0.26 * 0.11 0.33 2 0.12 Intrakick 0.12 f 0.17 0.21 f 0.16 0.23 & 0.21 0.44 t 0.31 0.19 2 0.18 0.43 t 0.36 Extension 0.27 ? 0.11 0.30 2 0.10 0.29 2 0.15 0.33 2 0.09 0.20 L 0.06 0.23 2 0.07 Interkick 0.44 0.55 0.78 * 0.69 0.50 t 0.45 0.60 2 0.23 0.38 2 0.34 0.40 -C 0.50

p = 0.05, but no interaction effect. Surprisingly, the AGA infants had higher kick rates than their SGA counterparts.

Examining the effect of gestational age at birth resulted in a strikingly similar picture. Comparing the preterm infants born before 32 weeks, those born after more than 32 weeks, and the full-term controls revealed a significant main effect for pregnancy duration, p < 0.05, and age, p = 0.05, but no interaction. The preterm infants born after 32 weeks showed higher kick rates than those born earlier.

Dividing the preterm infants on the basis of their movement quality and comparing them to the full-term controls revealed significant main effects for group, p = 0.02, and age, p = 0.05, without interaction between them. The preterm infants with normal CMs showed the highest kick frequencies.

When applying the Bonferroni t test to these data, however, the acceptance level for statistical significance is lowered in such a way that the group differences based on the medical risk factors, low gestational age, and IUGR are no longer significant. Only movement quality still significantly differentiates the groups for kick frequency.

Leg volume or growth did not meet the requirements to be used as a covariate in the different comparisons. The development of head control, as expressed in terms of the percentages of time the infants held their head in midline position at each age, was significantly related to the kick frequencies, p < 0.05, and differed between the groups for all three comparisons. Furthermore, pairwise comparisons of the relationship between the percentage of midline head position and kick frequency revealed no significant differences. Thus, head control could be used as a covariate. Group effects, however, did not disappear after the inclusion of this covariate. Thus, it can be concluded that head control was related to kick frequency, but it was not the only factor underlying the group differences in kicking behavior.

Temporal Organization To examine whether the difference in kick rate was reflected in specific parts of

the kick cycle the durations of flexion phase, intrakick pause, extension phase, and interkick pause were calculated. A striking consistency in the duration of both the extension and flexion phases was found between preterm and full-term infants as well as between the different ages, clustering around 0.3 s. (Table 3). No significant differences over age or group were found using any of the criteria for grouping the infants. The preterm infants differed from the full-term controls, however, in terms of shorter intrakick pauses, p 5 0.005, whereas no significant differences were found between the preterm groups.

342 GEERDINK ET AL.

Table 4 Mean Percentages of Total Flexion and Extension Time (* SD) that had Passed Before the Peak Velocities Were Reached in Both Preterm ( P T ) ( n = 8) and Full-Term (FT) Infants ( n = 6 )

PT FT

Flexion Extension Flexion Extension

6 wks 58.3 t 5.2 57.8 t 5.7 60.3 t 4.6 46.9 2 14.8 12 wks 58.3 2 6.7 58.1 2 7.1 54.6 * 16.0 58.7 2 10.5 18 wks 61.6 -C 7.7 57.1 * 8.0 65.0 t 8.8 54.7 * 15.S

In Table 3 the standard deviations reflect differences between subjects. To examine whether the durations of flexion and extension were not only consistent between infants but also within subjects, individual coefficients of variation were calculated Water, 1981). This coefficient is the ratio between each child’s standard deviation and mean ( x 100%) over different kicks. It was consistently low for flexion and extension in full- term infants (ranging over age from 40 to 50 and from 36 to 52, respectively) as well as in preterm infants (ranging from 38 to 44 and from 37 to 51, respectively). The coefficients of variation for the intra- and interkick pauses, however, were much higher, ranging over age from 118 to 145 and from 106 to 179, respectively, in full-term infants and from 108 to 395 and 136 to 178, respectively, in preterm infants. As values above 100 indicate that the SD is larger than the mean, this illustrates that the durations of the pauses not only differ between infants but also markedly within individuals at all ages.

Within-Joint Organization

This type of organization was assessed quantitatively by computing the percentage of time it took the knee joint to attain peak velocity in both the flexion and extension phases. As can be seen from Table 4, the peak velocity was reached at a comparable percentage time in the full-term and preterm groups. No significant differences were found in comparing these groups.

A qualitative assessment of within-joint organization was made by means of phase- plane diagrams of the knee, which portray the relationship between the angle of one joint and its angular velocity. In such a portrait, velocity assumes a negative value during flexion and a positive one during extension of the joint. The portraits of the preterm infants were expected to be more square-shaped because of their purported tendency to overshoot. However, all graphs showed some degree of deceleration before reaching full extension or flexion in both preterm and full-term infants, in that each one contained convex segments indicating smooth increases and decreases in velocity.

Be tween-Join t Coordination

The relationship between the joint angles over time was calculated in terms of pairwise cross-correlations, which were transformed to Fisher 2 scores. The Z scores for the correlations between hip and knee were high in the preterm as well as full-term


infants, showing a slight but not significant decrease with age (Figure 1). There were no significant differences between the full-term and the preterm groups, as can be appreciated from Figures la, Ib, and lc. For the correlations between hip and ankle and between knee and ankle, however, the groups differed noticeably, with lower values in the preterm infants. The differences between full-term infants and the different subgroups of preterm infants were analyzed again using a (3 x 3) (Group X Age) ANOVA. These group comparisons are illustrated separately in Figures 2 through 4.

When subdividing the preterm infants on the basis of growth retardation (Figures 2a and 2b), the main effect of group did not reach statistical significance for either hip-ankle, p = 0.09, or knee-ankle correlations, p = 0.06. The subdivision based on pregnancy duration appeared to have a stronger effect (Figures 3a and 3b). Strikingly lower correlations were found in the infants born before 32 weeks gestation, particularly at 6 and 12 weeks. There was a significant main effect for group on the hip-ankle correlation, p < 0.01, and a group effect, p < 0.05, together with a Group X Age interaction, p = 0.01, for the knee-ankle correlation. Differences between the preterm infants assessed as having normal GMs and those with abnormal movements compared to the full-term controls (Figures 4a and 4b) yielded a main group effect for the hip-ankle correlation only, p < 0.05.

Some group differences did not retain statistical significance when the Bonferroni t test was applied. For the between-joint correlation, only the effect of pregnancy duration remained significant.

Leg volume was significantly related, p < 0.02, to the knee-ankle correlations in all group comparisons, whereas a relationship with the hip-ankle correlations was only found for the comparison based on pregancy duration. The groups, however, did not differ significantly in leg volume. Therefore, this factor could not be used as a covariate. Growth of the leg and the development of head control were not related to any of the cross-correlations.

Discussion and Conclusions To date, the development of spontaneous leg movements in preterm infants has

only been studied up to term age and, apart from a single case study on an infant born at 26-weeks gestation (Heriza, 19911, this was only done in low-risk, borderline preterm infants with gestational ages of 34 to 36 weeks (Heriza, 1988a, 1988b). In the present study, data were collected on postterm development and we included only preterm infants with gestational age of 34 weeks or less.

Kick Frequency The kick frequencies found for full-term infants at 6, 12, and 18 weeks (1 1.4 t 6

to 8.6 k 7 per min) were lower than the rate of 19 -+ 10 kicks/min described by Thelen and Fisher (1982) at the age of 2 weeks. This could be partly due to differences in behavioral state because “arousal” was found to affect the level of activity. In the present study, kicking behavior was only analyzed when the infants were not crying, whereas that of Thelen and Fisher included crying infants. Another explanation for the difference in kick rates might be the fact that the infants in our study were older than

344 GEERDINK ET AL.

1.8

1.5

1.2 0.9

0.6

0.3

0.0

-0.3 -0.6 1

PTSGA II PTAGA o m

6

b zscore

1.8

1.5

1.2 0.9 0.6 0.3

0.0

." IL

Hip-Knee

18 age in weeks

PTS32wks PT > 32 wks

o n

T T

-0.3 1 -0.6

6 12 18 age in weeks

Hip-KIlW PTAbnormal c zscore PT Normal

o m 2.41 2.1 T 1.8

1.5

1.2 0.9

0.6

0.3 0.0

-0.6 -0.3 1 6 12 18

age in weeks

Fig. I . Mean Fisher Z transformed cross-correlations (+ SD) between the hip and knee joint for full- term and preterm infants with a SGA or AGA birth-weight status (la), for full-term and preterm infants born before or after 32 weeks gestation (Ib), and for full-term and preterm infants with a normal or abnormal movement quality (Ic).


Hip-Ankle m PTSGA PT AGA

o n

1.2

0.9

0.6

0.3

0.0

-0.6 -0.3 1 6 12 18

age in weeks

b z-score KneeAnkle W PTSGA

T 1.5

1.2

0.9

0.6

0.3

0.0

-0.6 -0.3 1 6 12 18

age in weeks

Fig. 2. Mean Fisher Z transformed cross-correlations (+ SD) between the hip and ankle joint (2a) and between the knee and ankle joint (2b) for full-term and preterm infants with a SGA or AGA birth-weight status.

those of Thelen and Fisher. A slight decrease over age was also found by Thelen and co-workers (1982, 1987). As experimentally verified for stepping (Thelen et al., 1984), somatic growth (i.e., changes in the ratio between fat and muscle tissue) may have been a contributing factor to this decrease.

The latter finding was based on a comparison between younger and older full-term infants, but it could also be applicable in comparing full-term infants with preterm infants of the same (corrected) age. The preterm subjects initially showed higher kick rates, but subsequently approached the full-term level with age, which might be related to differences in the mass of the legs. This suggestion could not be confirmed in this study using estimates of leg volume.

Before term age, it has been reported that preterm infants show a trend to increase the kicking frequency with age (Heriza, 1988a, 1988b). This increase may be related to an improvement in physical condition which expresses itself in higher levels of activity. Thus, kick frequencies may be influenced by several factors with opposing effects. A larger leg volume (and weight) seems to be related to a decrease in kick rate, which would explain the lower values for the older versus the younger infants

346 GEERDINK ET AL.

a Z-sc~n HipAnkle

0.9 0.6 0.3

0.0 -0.3 4 I -0.6 1 A


Knte-AllklC PTS32wks

1.5 1.2 0.9 0.6 0.3 0.0

-".V


Fig. 3. Mean Fisher 2 transformed cross-correlations (+ SD) between the hip and ankle joint (3a) and between the knee and ankle joint (3b) for full-term and preterm infants born before or after 32 weeks gestation.

in the study of Thelen and Fisher (1982) and for the full-term compared to the preterm infants. On the other hand, it can be assumed that improved physical condition will result in an increase in kick rate. Differences in physical condition may explain the finding that infants with IUGR, birth before 32 weeks, or a persistent abnormal movement quality had lower kick frequencies than the other preterm infants. Thus, preterm infants born under less-optimal conditions might lack the energy to sustain high activity levels.

It has been proposed that kicking movements result from interactions between different subsystems which can develop asynchronously (Thelen, 1985). Accordingly, Heriza (1991) has suggested that differences between preterm and full-term infants may stem in part from differences in behavioral state, body build, and passive muscle tone. The latter may influence the kick rate through the fact that higher muscle tension is related to shorter pauses, i.e., to higher kick frequencies. In the present study the effects of state and body build were accounted for. Differences in passive muscle tone might very well play an additional role because preterm infants have been docu-


1.5

1.2 T

PTNormal 0f.1-

0.9

0.6 0.3 0.0

-0.6 1 6 12 18

age in weeks

b Zscore Kmc-Ankle H PTAbnormal U PTNormal O m

2.4 2.1

1.8

1.5

1.2

0.9 0.6

0.3 0.0

-0.3 1 -"."


Fig. 4. Mean Fisher Z transformed cross-correlations (+ SD) between the hip and ankle joint (4a) and between the knee and ankle joint (4b) for full-term infants and preterm infants with a normal or abnormal movement quality.

mented to show higher muscle tension than their full-term counterparts (de Groot, van der Hoek, Hopkins, & Touwen, 1993).

Temporal Organization Differences in kick rate did not seem to influence the durations of the flexion and

extension phases in any group. Group differences were only found for intrakick pauses, which appear to play a modulatory role in the duration of the total kick cycle. These pauses, as well as those between kicks, were highly variable both between and within infants at all ages. The durations of both flexion and extension did not change significantly with age within any group nor were there any differences between preterm and full-term infants at any age. As such, these parts of the kick cycle do not seem to be influenced by preterm birth or IUGR, the former being in accordance with findings involving a comparison of preterm infants born after more than 34 weeks gestation with full-term infants at term age (Heriza, 1988b).

348 GEERDINK ET AL.

Within-Joint Organization Similarities between the preterm and full-term infants were also found for the within-

joint spatiotemporal organization of kicking. No consistent differences could be detected between the groups at any age. All infants showed some deceleration in speed at around the halfway mark in both flexion and extension. In a previous study on vertical kicking, i.e., air stepping, healthy full-term infants also showed maximum velocities in the midrange of the joint movement (Jensen, Thelen, & Ulrich, 1989). However, that study only involved 1 infant at 2 weeks and another at 3 months. Our data provide additional information which suggests that within-joint spatiotemporal organization represents a developmental invariant. Despite the clinical impression that preterm infants in general tend to show “overshooting” in their movements, i.e., that their movements are hyper- metric, they did not attain peak velocities closer to full extension or flexion than the full-term infants. The findings that both preterm and full-term infants reached the peak velocity in movements of their knee joints well before full extension or flexion was attained and showed round-shaped, phase-plane diagrams indicate that control is not restricted to the extremes of the movement, as in the ballisticlike movements observed during mature walking (Winstein & Garfinkel, 1989). While no differences were found between preterm and full-term infants for within-joint organization, this was not the case for the between-joint organization.

Between-Joint Coordination In the full-term infants, the angular change in the knee appeared to be tightly

coupled to that in hip and ankle at 6 weeks. A slight, though not significant, decrease in the cross-correlations between all three joints was found over age. The correlation values between the ages of 6 and 18 weeks were comparable to those reported previously between 1 and 4 months, being lowest for hip-ankle (Thelen, 1985). However, many of the infants involved in our study decreased their kick rate to such an extent that it was impossible to obtain data on kick bouts at the age of 24 weeks. Thus, we could not replicate the more dramatic fall in cross-correlations reported around the age of 5 months (Thelen, 1985).

In a previous case study on a high-risk, preterm infant (Heriza, 1991), the hip-ankle and knee-ankle correlations were comparable to those of full-term infants between 1 and 4 months (corrected) age. In our study, however, a striking difference was found between full-term and preterm infants. Whereas the full-term infants initially had a tight coupling between all joints, reflecting a freezing of the degrees of freedom, the preterm infants showed low cross-correlations between the angles of hip and ankle as well as knee and ankle. As such, the preterm infants did not follow the sequence of an initial phase of tight interjoint coupling followed by a decrease in cross-correlations as found in the full-term infants. Such a sequence appears to be a characteristic feature in the development of movement coordination, having also been found for reaching in human infants (von Hofsten, 1984) and for grooming in young mice (Golani & Fentress, 1985).

In summary, preterm birth and IUGR appear to be related to distinctive deviations from the developmental course of kicking in full-term infants, which are subsequently resolved after the (corrected) age of 12 weeks. Although it seems that the preterm infants at that age have overcome their initial deviations, it is, as yet, unknown whether such differences might not reappear at a later age.


General Conclusions In the present study, the preterm infants were divided in three different ways,

based on pregnancy duration, IUGR, and movement quality. One of the goals in doing so was to examine which classification would be most directly related to deviances in the development of leg movements. Based on our findings it is not possible to give a univocal answer to this question. Movement quality, reflecting nervous system functioning, was expected to be the best predictor of developmental deviances and for kick frequency this proved to be correct. For the between-joint correlation, on the other hand, it was the pregnancy duration that best distinguished differences in leg movements.

Any differences found in kicking movements, however, appeared to fade away around the age of 12 weeks. Comparable findings were obtained with regard to individual assessments of neurological condition reflected in movement quality (Geer- dink & Hopkins, 1993b). The disappearance of deviations in motor behavior around the age of 3 months has been highlighted previously by Prechtl (1990) relative to a transformation in neural functions around this age. This transformation involves a change from a fetal motor repertoire to one more adapted to the extrauterine environment. According to this view, the disappearance of some of the early dysfunctions may occur as a result of this change. Together with previous reports indicating that the prediction of poor developmental outcome improves after the age of 3 months (Ellenberg & Nelson, 1981; Geerdink & Hopkins, 1993b; Ross, Lipper, & Auld, 1986), our findings emphasize the importance of sequential examinations for detecting neuromotor dysfunctions.

The present study reveals that kicking movements in preterm infants develop in comparable ways to full-term infants after term age. Some features of these movements were strikingly stable over age for both preterm and full-term infants (namely, the durations of flexion and extension phases, within-joint organization), while others showed different developmental courses between the two groups (kick frequency, between-joint organization). A recurrent finding was that those parameters that are stable in the full-term infants are similar in the preterm infants. Those characteristics that change over age in the full-term group not only change with age in preterm infants but do so from a different initial level. Distinguishing such similarities and differences enables us to pinpoint those movement parameters that can be usefully incorporated into instruments for the early detection of those infants at most risk for developmental disorders.

Given these findings, it would be of considerable theoretical and clinical interest to study the development of kicking movements in preterm infants with documented brain lesions such as periventricular leucomalacia. Theoretically, they are of interest because they constitute an “experiment in nature” for answering questions about the role of supraspinal control in the development of movement coordination. Clinically, they are important because of the high risk they run for cerebral palsy, and yet it has proved difficult to identify early in development those who will eventually manifest this disease. Combining serial brain scans and sequential assessments of some of the movement parameters focused on in the present study may provide the requisite degree of detection. In addition, future research should include the collection of follow-up data until school age. This will provide a better understanding of the relationship between early deviances in the characteristics of leg movements and the long-term developmental outcome. As such, this research might aid the identification of infants at risk for developmental problems in limb coordination.

350 GEERDINK ET AL.

Notes We are indebted to Sylvie Droit and Pieter Mies for their help in the collection of the data, to Tom

Welter and Tamme Westra for providing the computer programs, to Magdalien Waardenburg for preparing the figures, and to Albert Gramsbergen and Knoek van Soest for their comments on the manuscript. This study was supported in part by grants from the Free University Stimulation Fund, the Winthrop-Phelps Society, and the ParooUWitte Bedjes Fund, and stems from a cooperative program of research between the Faculties of Human Movement Sciences and Medicine of the Free University, Amsterdam.

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