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Research Reports |
SF Jeng, PT, ScD, is Associate Professor, School and Graduate Institute of Physical Therapy, College of Medicine, National Taiwan University, No. 7 Chun-Shan South Rd, Taipei, Taiwan (jeng{at}ha.mc.ntu.edu.tw).
LC Chen, PT, MS, is Doctoral Student, Department of Kinesiology, University of Maryland, College Park, Md
KIT Yau, MD, is Professor, School of Medicine, College of Medicine, Fu-Jen Catholic University, and Deputy Director of Education and Neonatologist, Cardinal Tien Hospital, Taipei, Taiwan
Address all correspondence to Dr Jeng
Submitted January 9, 2001;
Accepted July 24, 2001
 | Abstract |
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30 weeks, n=13) classes and 22 full-term infants were evaluated during kicking movements using 4 synchronized cameras and 3-dimensional kinematic analysis when the infants were 2 and 4 months of corrected age. Results. The infants with VLBW and a high gestational age showed similar kicking movements compared with the full-term infants. In contrast, the infants with VLBW and a low gestational age exhibited a higher kick frequency and a shorter flexion phase at 4 months of corrected age. They also exhibited a higher hip-knee correlation and lower variability in the interlimb coordination pattern at 2 and 4 months of corrected age. Discussion and Conclusion. The findings indicate that infants with VLBW, particularly those with a low gestational age, have age-related differences in movement organization and coordination of kicking compared with full-term infants.
Key Words: Kicking movement • Kinematic analysis • Prematurity • Very low birth weight
| Introduction |
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 TopAbstract Introduction MethodResultsDiscussionConclusionReferences |
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Spontaneous motility constitutes the major part of the motor repertoire of infants during their early months of life.6 These self-initiated motor behaviors involve movements of various body parts (upper extremities, lower extremities, neck and trunk) with a fluent and complex appearance, and they are variable in speed, amplitude, and intensity. Recent evidence indicates that newborn infants sustaining adverse events such as apnea,7 chronic lung disease,8 and brain damage9,10 during the neonatal period tend to show alterations in the quality components of spontaneous movements in infants. Furthermore, the presence of such abnormalities in early infancy has been shown to correlate with poor neurologic outcome such as cerebral palsy.8,11,12 These results suggest that assessment of spontaneous motility may be a useful and sensitive method of identifying early neuromotor problems in preterm infants.
Among early motor behaviors, kicking movements have aroused great interest because of their potential role in the development of locomotion.13 Thelen and colleagues13–17 conducted a series of follow-up studies on full-term infants to examine their early kicking movements and relate those movements to the walking ability they later developed. Infants exhibited patterns of kicking movements during their newborn period that have high interjoint coordination (indicated by high pair-wise cross-correlations of joint angles at the hip, knee, and ankle), small phase lags (indicated by small differences between the times at which the joints started moving or reached peak excursion), and constrained movement durations (indicated by invariant durations in the flexion and extension phases).13,17 With maturation, kicking behavior showed reorganization from the newborn stereotyped movements toward more skilled and complex activities. Nevertheless, the spatial and temporal patterns of early kicking movements were found to be similar to those involved in mature walking cycles.13,17 The results indicate that kicking may be a developmental manifestation of a central program later used for locomotion. Therefore, investigation of kicking development in preterm infants may provide a unique means to understand how the earliest spontaneous movements change in these children as they acquire voluntary control.
Assessment of kicking has often been aided with kinematic analysis to measure qualitative aspects of movement.18 Kinematic analysis often involves imaging techniques (eg, television, cinematography, optoelectric systems) that are used to identify particular points on the body and to track these points in space over time.19 Imaging techniques can provide a quantitative assessment of movement that allows us to transform a visually observed movement into something measurable.20 Furthermore, the techniques can provide a comprehensive description of movement patterns of infants by delineating time, displacement, velocity and acceleration, and movement coordination among the body segments.19
Several researchers have investigated the early kicking movements of preterm infants using kinematic analysis,9,10,21–25 however, the movement patterns they described were inconsistent (Tab. 1). Kinematic variables included kick frequency, spatiotemporal organization, interjoint coordination, and interlimb coordination. For example, van der Heide et al10 reported that preterm infants who were at low risk for neurodevelopmental disabilities exhibited a lower correlation of the hip-knee and hip-ankle couplings, indicating low interjoint coordination, than preterm infants with brain damage and full-term infants at 1 month of corrected age (adjusted for prematurity) and that the differences resolved at older ages. In contrast, Vaal et al25 found that full-term infants and preterm infants at low risk for neurodevelopmental disabilities had a lower correlation of the hip-knee, hip-ankle, and knee-ankle couplings than preterm infants with brain damage at 18 and 26 weeks of corrected age. Droit et al23 reported that preterm infants with brain damage showed a higher level of semi-both-leg kicking (simultaneous flexion and nonsimultaneous extension) and less alternate kicking than preterm infants at low risk for neurodevelopmental disabilities during the neonatal period. In contrast, van der Heide et al10 observed no difference in the interlimb coordination patterns between preterm infants with brain damage and preterm infants at low risk for neurodevelopmental disabilities at 1 and 3 months of corrected age.
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| Method |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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From June 1997 to December 1998, a total of 22 infants with VLBW and 22 full-term infants were included in the study. The groups were matched for levels of maternal education, stratified into greater than high school, high school, and less than high school. The perinatal characteristics (ie, GA, birth weight, 1- and 5-minute Apgar scores, presence of chronic lung disease [CLD], presence of intraventricular hemorrhage [IVH], and presence of retinopathy of prematurity [ROP]) of the groups are presented in Table 2. Gestational age was estimated by maternal menstruation date and confirmed by prenatal ultrasonography. Chronic lung disease was defined as lung disease requiring a dependence on oxygen therapy for a duration of more than 28 days.28 The severity of IVH was classified into grades I to IV according to the method of Papile et al.29 The severity of ROP was graded into stages I to IV according to the International Classification of Retinopathy of Prematurity.30
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30 weeks, n=13) classes. This distinction was made on the basis of findings that a short gestation increases the risk of developmental delays in preterm infants.31,32 The infants with a low GA had lower birth weights (t[20]=3.84, P=.01), lower 1-minute Apgar scores (t[20]=2.2, P=.04), and higher incidences of CLD (
2[1]=22, P=.001) and ROP (2[2]=7.1, P=.03) than the infants with a high GA. However, the groups were comparable in the distributions of sex, severity of IVH, and maternal education.
Instrument and Procedures
The infants' kicking movements were recorded, and they were assessed for body weight at 2 and 4 months of corrected age at the neonatal follow-up clinic. During testing, the infants were placed in a supine position on an examination table with a large surface. They wore a specially designed diaper and black shorts to expose the following anatomical landmarks bilaterally: mid-trunk, greater trochanter, lateral femoral epicondyle, lateral malleolus, and fifth metatarsal head (Fig. 1). Reflective ball-shaped markers with a diameter of 1 to 2 cm were placed over these landmarks to define the hip, knee, and ankle joint angles. Infants were tested 1 hour before feeding and were kept in an alert state (state 5, according to the Brazelton Neonatal Behavioral Assessment Scale33). Each infant's head was maintained in the body's midline by an investigator's hand in an effort to control for the effect of tonic neck reflex. Infants were allowed to kick spontaneously for 5 minutes, with the parents or toys in view to minimize frustration.
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with lenses of 8–48 mm). Each camera was connected to a video recorder (SVHS AG1960 and AG1970), an SMPTE Time Code Generator (Horita SR-50
), an Event & Video Control Unit,* and a monitor (Trinitron
). Two cameras were placed on each side of the infants at a distance of 2 m and at the same height as the table surface on which the infants were lying. The cameras were focused on the infants and were angled at 70 degrees to construct a 3-dimensional analysis of the movements of the same limb. The calibration errors, as calculated by the differences between the coordinates of markers measured with cameras and the coordinates of markers in the 3-dimensional space, were of less than 3 mm.34
Data Acquisition and Reduction
A 20-second segment of video recording of continuous active kicking movements was selected for each infant. The video data were digitized and analyzed using the Peak Performance Motion Analysis System (Peak Motus Version 3.01* with a fourth-order Butterworth filter and filtering rate of 6 Hz). The cameras essentially provided a 2-dimensional video image of a 3-dimensional scene on a medium. The 2-dimensional video data set generated from the cameras that recorded the same limb movements was converted into 3-dimensional spatial coordinates using the direct linear transformation method.34 The linear and angular data obtained were used to calculate the variables of kick frequency, spatiotemporal organization, interjoint coordination, and interlimb coordination.
A kick was defined as a flexion and then an extension movement of a lower limb, in which the hip angle change during flexion exceeded 11.5 degrees and the hip angle change during extension was a minimum of 20% of the angular displacement during flexion.35 The kick cycle was characterized by 4 phases: flexion, intra-kick pause, extension, and inter-kick pause (see Fig. 2 for definitions of phases).13 The kick frequency was measured as the number of kicks by each leg during the 20-second period and was converted to cycles per minute. Spatiotemporal variables included the kick amplitude and the 4 kick phases. Kick amplitude was defined as the excursion of hip flexion during a kick cycle. Interjoint coordination was measured by pair-wise cross-correlations of the joint angles at the hip, knee, and ankle for the same limb during the kick cycles (excluding the inter-kick pause) using Pearson product moment correlations (r), and these measurements were transformed to Fisher Z scores.9 Interlimb coordination was measured by frequency (expressed as a percentage) of alternate, unilateral, and synchronous kicking patterns during the 20-second period.14 An alternate kick was defined as simultaneous flexion of one lower extremity and extension of the other lower extremity, with the flexion phase of the 2 limbs overlapping for less than 50% of the movement. A unilateral kick was defined as isolated flexion and extension of one lower extremity while the other lower extremity was in the intra-kick pause phase or the inter-kick pause phase. A synchronous kick was defined as simultaneous flexion (or extension) of both legs during more than 50% of the flexion (or extension) phase, which was determined by the phase duration of the leg exhibiting a higher kick frequency. The predominant interlimb coordination pattern was also determined for each infant as defined by the most frequent type of kicking pattern that occurred.
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| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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Kick Frequency
Analysis of the kick frequency showed no age or group effects but did show an interaction effect (F=10.8; df=2,172; P>.0001) (Tab. 3). Post hoc tests revealed a comparable kick frequency among groups at 2 months of corrected age, but a higher kick frequency in the infants with VLBW and a low GA at 4 months of corrected age (P=.0001). The full-term infants and the infants with VLBW and a high GA exhibited no change in kick frequency across ages, whereas the infants with VLBW and a low GA showed an increase in kick frequency (P<.002).
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Interjoint Coordination
Group effects (F=50.5; df=2,172; P<.001) and age effects (F=3; df=1,173; P>.05) were found for the hip-knee coordination (Fig. 3A). Post hoc tests revealed a borderline higher hip-knee correlation in the infants with VLBW and a low GA than in the full-term infants and the infants with VLBW and a high GA (P=.017 and .048). All groups manifested a decline in the hip-knee correlation with age. The correlation values for the hip-ankle and knee-ankle coordinations were comparable among groups and across ages (Figs. 3B and 3C).
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2=11.8, df=3, P=.003) (Tab. 4). The other groups, however, exhibited no change in the distribution of predominant kicking pattern.
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| Discussion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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We observed a similar tendency for the full-term infants and the infants with VLBW and a high GA to show a decreased kick frequency from 2 to 4 months of corrected age. The infants with VLBW and a low GA began with a lower kick frequency, but subsequently the kick frequency increased to levels higher than those of the full-term infants at 4 months of corrected age. The differences in kick frequency between preterm and full-term infants may relate, in part, to differences in their physical condition and neurological development.
Physical condition could affect a child's physiological energy and activity level.9 In our study, a low GA was associated with less-optimal conditions (ie, low Apgar scores and a high incidence of CLD), which might initially limit an infant's physiological energy and therefore the infant's ability to sustain high activity levels.22,36,37 The gradual recovery of their physical condition from the perinatal insults as time passes, in our view, should improve the child's activity levels and thus increase the child's kicking movements. Furthermore, development of the nervous system may also influence the motor behavior of infants.38 van Wulfften and Hopkins39 documented a broad spectrum of interrelated changes in neurological functions (eg, learning abilities, motor behavior, social competence) in full-term infants from 2 to 4 months of age. Hopkins and Prechtl38 observed that motor behavior specifically shows reorganization from newborn spontaneous movement to achievement of fine-distal, goal-directed movement. The full-term infants and the infants with VLBW and a high GA in our study may have undergone age-appropriate changes in neural functions so that toward 4 months of corrected age, they exhibited only a few kicks and began to play more with their hands, reach for toys, smile, and vocalize.
We found a similar spatiotemporal organization of kicking among the groups, except for the flexion phase. The flexion phase durations were comparable among infants at 2 months of corrected age. Toward 4 months of corrected age, the flexion phase durations were extended in the full-term infants and the infants with VLBW and a high GA but remained unchanged in the infants with VLBW and a low GA. The findings contrasted with those of previous reports9,10 in which the flexion phase durations were consistent in preterm and full-term infants across ages (around 0.4 second). This discrepancy may be accounted for by the use of different joint excursions to determine the presence of kicking. Geerdink et al9 and van der Heide et al10 determined the flexion and extension movement of kicking based on knee joint excursions,17 whereas we studied hip joint excursions based on a previous report by Jensen et al.35 Examination of the kicking movements of the individual infants at 2 months of corrected age revealed rapid and nearly simultaneous flexion (or extension) in the hip and knee that may explain the equivalent durations (around 0.4 second) obtained with the 2 methods. The joint action became more individualized with maturation in the full-term infants and the infants with VLBW and a high GA as their flexions at 4 months of corrected age consisted of an initial flexion of the hip and knee to a semiflexed position, followed by a continuous flexion in the hip with the knee in extension. The inclusion of the time period that the knee is dissociated from the synergistic patterns may have resulted in a longer flexion phase duration during the hip joint excursions.
We identified hip-knee coordination as the only interjoint coupling that distinguished the kicking movements between groups. Despite a decline in the correlation values from 2 to 4 months of corrected age, the hip-knee coordination of the infants with VLBW and a low GA remained consistently higher than those of the full-term infants and the infants with VLBW and a high GA throughout the period. A study of kicking development in full-term infants by Thelen15 also showed high pair-wise joint correlations among the hip, knee, and ankle at a newborn age, followed by a decrease in the joint correlations. The earliest high interjoint correlations may be the result of a very simple coactivation of the 3 joints. The subsequent increase of joint independence, as denoted by declined joint correlation, may provide the variability of movement that allows the emergence of new movement pattern.15 Studies are needed to examine whether the high hip-knee correlation in infants with VLBW and a low GA would limit their ability to acquire selective controls and adaptive motor function at later ages.
Our results failed to support the discriminative usefulness of hip-ankle and knee-ankle coordination that has been reported.9,10,25 This may have been due to differences in sample characteristics and instrumentation between our study and the previous studies.9,10,25 Unlike the studies by Geerdink et al,9 van der Heide et al,10 and Vaal et al25 where selected preterm infants with severe brain damage or without major complications were chosen for comparison, in our study we included preterm infants with VLBW and complications of CLD or ROP. Future investigation is necessary to examine the effects of specific neonatal diseases on the kicking movements of preterm infants. In addition, differences in instrumentation may influence the joint motion data obtained from kinematic analysis. Previous researchers9,10 used one camera for 2-dimensional kinematic analysis to assess single-leg movements. This method contrasts with that of our study, in which we used 4 synchronized cameras to construct a 3-dimensional analysis of bilateral lower-extremity movements. Preterm infants tend to show rotational movements at the hip and ankle during kicking,22 which are more accurately evaluated by the use of instrumentation to construct a 3-dimensional analysis.40
Our results replicated the data of Vaal et al,25 who demonstrated that preterm and full-term infants exhibited similar developmental trends of interlimb coordination as they changed from frequently kicking with a unilateral pattern at 2 months of corrected age to a synchronous pattern at 4 months of corrected age. According to the observations of Touwen,41 full-term infants develop spontaneous leg movements, which follows the sequence from neonatal alternate movements to predominantly asymmetrical movements with a single lower extremity at 6 weeks of age, to predominantly symmetrical movements at 3 months of age, and to largely voluntary movements at 5 months of age. Our findings indicate that prematurity does not alter the sequence of developmental changes in bilateral movement coordination of spontaneous lower-extremity movements.
Short gestation appears to influence the variability of interlimb coordination in the development of kicking movements. The full-term infants and the infants with VLBW and a high GA showed large variation in the distribution of kicking patterns. Although most infants adopted unilateral kicks as their predominant pattern at 2 months of corrected age and the synchronous kicks at 4 months of corrected age, some of the infants had assumed other forms of coordination as the predominant pattern. In contrast, the infants with VLBW and a low GA manifested a skewed distribution of kicking patterns. An extremely high proportion adopted the unilateral kicking pattern at 2 months of corrected age, and this was repeated for the synchronous kicking pattern at 4 months of corrected age. Variability in infant behavior has been proposed to have evolutional and functional benefits because it may facilitate the adaptation of an individual child or a population to an ever-changing environment.42 The skewed distribution of kicking patterns in the infants with VLBW and a low GA, therefore, may imply a lack of variability or flexibility in adjusting bilateral movement coordination to environmental changes during the development of lower-extremity movements.
| Conclusion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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| Footnotes |
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This study was approved by the Institutional Review Committee of the College of Medicine, National Taiwan University.
Part of the data reported in this paper were presented at the Twelfth Biennial International Conference on Infant Studies; July 16–20, 2000; Brighton, United Kingdom.
This work was supported by a grant from the National Health Research Institute (DOH 88-HR-619) of the Department of Health in Taiwan.
* Peak Performances Technologies Inc, 7388 S Revere Pkwy, #601, Englewood, CO 80112. 
Panasonic Broadcast & Television System Co, 1 Panasonic Way, Secaucus, NJ 07094.
Horita Co, PO Box 3993, Mission Viejo, CA 92680.
Sony Corp of America, 1 Sony Dr, Park Ridge, NJ 07656.
|| SAS Institute Inc, PO Box 8000, Cary, NC 27511.
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