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Research Reports |
JC van der Heide, DipPhy, Msc, is Human Movement Scientist, Stella Maris Scientific Institute, Pisa, Italy
PB Paolicelli, MD, is Child Neurologist, Infant Section, Stella Maris Scientific Institute
A Boldrini, MD, is Head, Neonatal Intensive Care Unit, University of Pisa, Italy
G Cioni, MD, is Senior Researcher, Division of Child Neurology and Psychiatry, Department of Procreation and Developmental Medicine, University of Pisa, and Child Neurologist and Head, Infant Section, Stella Maris Scientific Institute, 56018 Calambrone, Pisa, Italy (cioni{at}inpe.unipi.it). Address all correspondence to Dr Cioni
Submitted June 10, 1998;
Accepted February 28, 1999
| Abstract |
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Key Words: Brain lesions Cerebral palsy General movements Kicking movements Preterm infants
| Introduction |
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Kicking movements have been observed in fetuses with anencephaly and intact lumbar and thoracic spinal cords,4 and stepping movements have been reported in infants with anencephaly.5 These findings support the hypothesis that early precursors of locomotion are controlled by spinal networks. These spinal centers are probably also used in independent walking,1 although the nature of the underlying mechanisms of transformation from immature to mature locomotion is still controversial. According to some authors,6,7 the key factor for the emergence and development of independent walking is the maturation of higher locomotion centers and postural control systems. Other authors,1 however, contend that mature locomotion may result from the convergence of several interacting factors, including the biomechanical properties of the moving limbs, postural positions, emotional states, and environmental constraints.
Kicking movements have also been studied by clinicians interested in the effects of environment or brain lesions. Preterm infants have been studied most often because they are exposed for weeks or months to environmental conditions very different from those experienced in utero. Moreover, preterm infants are at high risk for brain lesionsperiventricular leukomalacia (PVL), in particularwhich often cause a permanent impairment of LE movements.8 The major long-term sequela of PVL is spastic diplegia, which is observed in the majority of preterm infants with cystic PVL and in some infants with noncystic PVL and is often called "prolonged periventrical flare."8
Heriza9,10 studied the kicking behavior of low-risk pre-term infants from birth to term age. These infants showed an organized kicking behavior, expressed in high correlation among hip, knee, and ankle joint movements; small phase lags; and constrained duration of flexion and extension phases. Heriza also reported some age effects and some differences from full-term controls. Geerdink et al11 conducted a longitudinal study on preterm infants and full-term infants at the postterm ages of 6, 12, and 18 weeks. Some differences in the kinematic characteristics of kicking were found. At 6 weeks, preterm infants showed lower hip and ankle movement correlation values than full-term infants showed.
Only Droit et al12 studied (cross-sectionally) kicking movements in preterm infants with brain lesions, detected by brain ultrasound, in comparison with lowrisk preterm infants. There were no differences between the 2 groups of infants at 31 to 35 weeks of postmenstrual age. Some differences, however, were observed at 37 to 39 weeks. These differences did not lie in the frequencies of LE movement but in inter-LE coordination and temporal organization of the kicking cycles. Low-risk infants exhibited more alternate LE movements and fewer semi-bilateral LE movements (simultaneous flexion and nonsimultaneous extension) compared with infants with brain injury. In the low-risk infants, the duration of the pause between flexion and extension was shorter, whereas flexion and extension periods were similar for all infants. Although there were differences, quantitative analysis of kicking characteristics was not clinically useful because of the large overlap in findings between the 2 groups.
Recently, abnormalities of spontaneous movements, consisting of reduced complexity and lack of fluency and variability, in preterm and full-term infants with brain injury have been described by Prechtl and co-workers1317 and Hadders-Algra and Groothuis.18 Such abnormalities can be detected by visual Gestalt perception, in particular for general movements (GMs) (ie, movement patterns in which all body parts are involved). Several researchers1118 have confirmed the value of Prechtl's method of GM qualitative assessment for early detection of brain dysfunctions. A review of this new approach has recently been published by Einspieler et al.17 The GMs of fetuses and of preterm, full-term, and young infants can be evaluated on the basis of observed qualities of normal and abnormal movements.13,15,17 Researchers have argued that there is a robust character of this method: reported interobserver agreement is between 78% and 98%, and reported kappa coefficients are between .84 and .92 (see Einspieler et al17 for a review of reliability studies on this method). The sensitivity of this assessment for predicting later neurological outcome is very high (above 90%) in all studied age groups (preterm; full-term; and 1-, 2-, and 3-month age epochs).17 Specificity is quite low at preterm age and reaches 82% to 100% at 3 months postterm.17 This method was designed to detect early motor abnormalities predictive of later cerebral palsy, and it has been useful in predicting more subtle neurological dysfunctions.15,18
In the study by Droit et al,12 qualitative Gestalt evaluation of the GMs, of which kicking movements are part, was carried out using the same videotape recordings used for kicking analysis. The observer was blinded to the results of the kicking analysis and to the neurological data. The results showed a close correlation with the presence of brain lesions and with the neurological outcome. This study confirms the high diagnostic and prognostic value of the qualitative assessment of spontaneous motility in newborn infants. The evaluation seemed to be more predictive of the outcome than the quantitative analysis of kicking characteristics; however, the study had limitations. For example, the infants were observed only until term age, there were no full-term controls, and only a few aspects of kicking movements (ie, interlimb coordination and temporal organization) could be checked because of the method of video recording.
In our study, we included preterm infants with PVL and preterm and full-term infants without brain lesions, all observed at the same postterm ages of 1 or 3 months. The methods for recording and analyzing kicking movements were extended, compared with the study by Droit et al.12 In addition to GM assessment, a qualitative evaluation of LE movements was added. The questions we addressed were:
| Method |
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During a 1-year period, 23 preterm infants were admitted to the study and were videotaped at the postterm ages of 1 or 3 months (see "Procedure" section). We used a cross-sectional design because of the difficulty in getting frequent assessments of full-term and preterm infants without brain injury in outpatient clinics of the NICU. Twelve subjects were low-risk preterm infants, and 11 subjects were preterm infants with PVL. Two infants with PVL were borderline small for gestational age (they scored between 5% and 10% on the intrauterine growth chart19), one at the age of 1 month and one at the age of 3 months. All infants were followed until the age of 18 months. At that age, they were given a neurological examination based on Touwen's criteria,22 carried out by an experienced child neurologist (GC or PBP). Seven infants with PVL showed cerebral palsy (4 with spastic diplegia, 1 with hemiplegia, 1 with tetraplegia, and 1 with a diskinetic form of cerebral palsy), 1 infant with PVL had mild developmental motor retardation, and 3 infants with PVL had no other abnormalities. The main clinical findings for these infants are reported in Table 1.
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=1,592 g, SD=272, range=1,300 2,090; t=2.55, P <.05) than the low-risk infants did. Low-risk infants and infants with PVL were also divided according to the postterm age at which they were videotaped. Six low-risk infants (3 girls and 3 boys) and 5 infants with PVL (2 girls and 3 boys) were observed at the postterm age of 1 month (±1 week). The other 6 low-risk infants (4 girls and 2 boys) and the other 6 infants with PVL (1 girl and 5 boys) were observed at the postterm age of 3 months (±1 week). The comparison group (Tab. 1) consisted of 12 full-term infants without brain injury, born at a gestational age of 37 weeks or more. Six infants (4 girls and 2 boys) were videotaped at 1 month of age, and 6 infants (3 girls and 3 boys) were videotaped at 3 months of age. One 3-month-old infant in the comparison group was borderline small for gestational age (5%10% on the intrauterine weight chart). Their outcome at 18 months was normal.
Procedure
All infants were videotaped during a neurological follow-up at the NICU of the University of Pisa. We used a Panasonic S-VHS video camera* placed on a tripod perpendicular to a large examination table at a distance of 2 m from the infants. All infants were videotaped from the lateral plane while lying in a supine position.
For the analysis of kicking movements, we made 1-cm marks with a pencil on each infant's right and left LEs at the lateral border of the base of the fifth metatarsal head, at the lateral malleolus, at the lateral femoral condyle, and at the hip crease. Marker placements were determined by physical examination. The movement of each LE was then recorded separately, with the child's head held in the middle position by an examiner while the infant was allowed to kick. After the infant had kicked with one LE for at least a minute, he or she was turned around and the movement of the other LE was recorded. The recording then continued for another 5 to 10 minutes with the infant's head free to allow a qualitative analysis of LE movements and of GMs.
Instrumentation
For the kinematic analysis of the kicking movements, we used the Video Pointer system.
The Video Pointer system is a computer program that digitizes and transfers images to a personal computer. On each image, an observer (JCvdH) pointed with the mouse at the marked different joints (Fig. 1). The Video Pointer was linked to the S-VHS video recorder, which had a frame frequency of 24 Hz. The marked points were considered as coordinates of the Cartesian system, and joint angles were calculated from these coordinates (Fig. 2). The intraobserver reliability (expressed as Pearson product-moment correlation coefficients) was measured at 2 different moments for 20 randomly selected joint angles of seven 5-second segments. The intraobserver reliability values were .96 for the hip, .94 for the knee, and .77 for the ankle.
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For the kinematic analysis of kicking, a minimum of 7 kicks per infant was used. Preferably, serial kicks (ie, a single LE movement repeated in the same form at least 3 times at regular short intervals, with a kick cycle below 10 seconds2,23) were analyzed, but if the infant exhibited too few serial kicks, single kicks were also analyzed. We analyzed 119 segments of videotape of between 1 and 7 seconds (range=1921 segments for each of the 6 groups of infants; mean number of segments per infant=3.4, SD=0.98, range=26). The mean duration of the segments was 11.4 seconds per infant (SD=3.68, range=521). The mean of the number of kicks per infant was 7.5 (SD=1.99, range=514).
Selection criteria for the segments of videotape to be analyzed were as follows: at least one kick had to be present, all marks had to be visible, and the LEs had to move (preferably) in the sagittal plane. As in previous studies,2,9,10 the right LE was chosen for the temporal analysis, except for 13 infants whose left LE was chosen because not enough segments with right LE kicking were observed.
The duration of each phase of the kick cycle was calculated. The initiation and termination of the flexion and extension phases of movement were coded from the computer monitor by the observer (JCvdH) according to the criteria of Thelen et al.2 The flexion phase lasted from the frame at which continuous movement (for at least 5 frames) in a horizontal plane toward the body was first noticed until the frame at which movement stopped or changed horizontal direction. The extension phase began when the foot moved continuously away from the body and continued until horizontal movement ceased. The intrakick pause was calculated as the number of frames between the ending of flexion and the beginning of extension. The interkick pause was computed as the number of frames between the ending of extension and the beginning of flexion. The calculation of the intrakick and interkick pauses was carried out in the opposite way if the infant kicked from a flexed rest position. A mean of the phases was calculated from all the analyzed kicks per infant, and a group median was calculated from these means.
To assess intra-LE coordination, Pearson product-moment pairwise cross-correlations were calculated for each pair of joints: hip and knee, hip and ankle, and knee and ankle. Two to 5 segments (
=3.37, SD=0.97) of continuous kicking for a period of 1 to 3 seconds were chosen for each infant. A group median of these cross-correlations was calculated.
To assess inter-LE coordination, 4 kicking patterns were assessed, as in previous studies1,12,23: single LE kicking (flexion and extension of one LE), alternate LE kicking (flexion of one LE and simultaneous extension of the other LE), kicking with both LEs (simultaneous flexion and simultaneous extension of both LEs), and semi-bilateral LE kicking (simultaneous flexion and nonsimultaneous extension). The percentage of the presence of the different types of patterns was calculated for each infant. A group median was calculated from these percentages.
The Kruskal-Wallis nonparametric analysis of variance24 was used to analyze the data for the 6 groups of infants, by means of the SPSS/PC package,25 in order to check for the presence of differences related to preterm birth, brain lesion, or age at recording for these variables. A probability value of [H11349].05 was considered significant.
Qualitative scoring of LE movements.
The following variables were scored from the whole videotape recording of the infant:
Qualitative assessment of GMs.
Rhythmical kicking movements occur as part of a GM.12,15 A global judgment of normal or abnormal quality of the GMs was made, according to Prechtl's method,17 from the same videotape recordings used for the analysis of kicking. In addition, the 2 main types of GM abnormalities (ie, cramped-synchronized and poor repertoire) were identified. According to the definitions of these movement characteristics previously reported,13,17 GMs are considered as showing a poor repertoire when the sequence of the successive movement components is monotonous and movements of the different body parts do not occur in the normal complex way, as seen in normal GMs. The GMs are scored as cramped-synchronized when, in addition to there being a poor repertoire, there is rigid movement that lacks normal smoothness, with all limbs and the trunk contracting and relaxing almost simultaneously.1218
Qualitative assessment of LE movements and of GMs was carried out independently on the videotape recordings of all infants by 2 members of the research team (JCvdH and GC), one of whom was aware of the group to which the infant belonged. Interobserver agreement varied from 82% to 93% for the different LE movement variables, and it was of 87% for GM assessment.
Behavioral condition.
The prevalent behavioral condition of the infant during the period in which the examiner kept the infant's head in the midline position was checked. A 6-point scale26 was used: 1=asleep; 2=drowsy; 3=awake, alert, little or no movement; 4=awake, moving; 5=fussy; and 6=crying.
| Results |
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Quantitative Analysis
Kicking frequency.
The results reported in Table 2 show a large variability in the frequency of kicking movements in all groups, as indicated by the high values of interquartile ranges. No differences related to preterm birth, presence of PVL, or age at testing were observed in the Kruskal-Wallis analysis. A lower kicking frequency was observed in infants with PVL from 1 to 3 months of age (
2 =3.31, P=.07), and a higher kicking frequency was observed at 1 month of age in the same group in comparison with low-risk preterm infants (
2 =3.33, P=.07). In view of the small sample size, a Type II error may have occurred. These findings were probably due to the number of infants with PVL who had consistent crying behavior during the recording at 1 month of age; infants kick more often while they are crying.23
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2 =7.04, P=.01).
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2 =11.21, P <.01) and hip and ankle correlations (
2 =8.09, P <.01) than did the age-matched full-term infants. The low-risk infants at 1 month of age had a lower mean rank for hip and knee correlations (
2 =9.26, P <.01) and hip and ankle correlations (
2 =10.58, P <.01) than did the age-matched infants with PVL.
Inter-LE coordination.
The percentages of the different types of kicking movements observed in all infant groups are reported in Table 5. In all groups, single LE kicking occurred more frequently than other types of kicking. Again, the percentages of the different types of movements varied greatly, and no differences were found.
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Amplitude of LE movements.
One infant in the PVL group at 1 month and another infant at 3 months showed LE movements predominantly of small amplitude.
Speed of LE movements.
Predominantly slow movements were observed only in the PVL group, in one infant at 1 month, and in 2 infants at 3 months.
Segmental foot movements.
All infants with PVL at 1 month and 4 of the 6 infants at the age of 3 months showed rare or no segmental foot movements. On the contrary, all low-risk preterm and full-term infants had frequent segmental movements. A difference was found at 1 month (
2 =7.33, P=.006). Interestingly, the 2 infants (infants 19 and 22) in the PVL group who showed consistent segmental movements at 3 months of age had a normal outcome.
Assessment of GM Quality
The results of Gestalt assessment of the GMs are reported in Table 1. An abnormal quality of GMs (poor repertoire) was found in only one infant of the low-risk preterm groups (at 1 month). All the other low-risk preterm infants and age-matched full-term infants showed GMs of normal quality.
No infants with PVL had normal GMs, and all infants with PVL showed a poor repertoire. Five infants (3 at 1 month and 2 at 3 months) also had cramped-synchronized characteristics. These 5 infants were those who were later found to have spastic diplegia or tetraplegia. Three of the 6 infants who had only poor-repertoire GMs showed normal development at the age of 18 months. One of the other 3 infants had mild developmental retardation, another had left hemiplegia, and another had a diskinetic form of cerebral palsy. Differences were found between the PVL group and the other groups of infants (
2=4.64, P=.03 at 1 month with low-risk preterm infants;
2=8.33, P=.003 with full-term infants;
2=8.33, P=.003 at 3 months with both groups). A comparison of these differences and those observed for the other movements (kicking and LE movement) between the preterm low-risk infants and the preterm infants with PVL is shown in Table 6.
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| Discussion |
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The results of this study cannot be considered as conclusive because of the small number of subjects, the cross-sectional instead of longitudinal design of the research, and the limits of our quantitative analysis. Our findings, however, suggest that, at least for the examined kicking characteristics, no clear differences can be observed between the various groups of infants.
A high frequency of kicking was found in all infants, similar to that reported at the same ages by Geerdink et al.11 These authors found a decrease in kicking frequency from 6 to 18 weeks in both preterm and full-term infants that we could not confirm. As in the study by Droit et al,12 carried out on preterm infants before term age and at term, we found no effect of brain lesions (PVL) on the frequency of kicking.
No differences related to preterm birth, PVL, or age were obtained for the temporal organization of kicking, with the exception of a slight reduction of interkick pause, in particular in full-term infants from 1 to 3 months. We could not confirm a longer intrakick pause in preterm infants with brain injury, in comparison with low-risk subjects, as reported by Droit et al12 at term age, nor a shorter intrakick pause in preterm infants, in comparison with age-matched full-term infants, as described by Geerdink et al.11
Kicking movements were well-organized in all infants, as indicated by the high interjoint correlation for the 3 pairs of articulations. Our cross-correlation values were very similar to those reported by Thelen23 in full-term infants without brain injury at the ages of 1 and 3 months. We found small differences between the groups of infants only for hip and knee and hip and ankle joint pairs, either in relation to preterm birth or lesions or in relation to recording age. Our findings largely confirm those reported previously,911 with some differences. We found that at 1 month, low-risk preterm infants had lower correlations between hip and knee movements and between hip and ankle movements, in comparison with full-term and preterm infants with PVL. Geerdink et al11 also reported that, at 6 weeks, preterm infants had lower hip and ankle movement correlation values than did age-matched full-term infants. In contrast to our data, they found the same difference for the knee and ankle joint pair but not for the hip and knee joint pair. Geerdink et al did not report data concerning brain ultrasound or outcome findings for the infants in their study.
Again in contrast to our findings, Piek et al27 recently reported a stronger coupling between knee and ankle movements in preterm infants, in comparison with full-term infants, at the ages of 8 to 20 weeks. The different ages at recording might account for these discordant results.
Our data indicated a possible developmental effect for all of our groups. Cross-correlation values for hip and knee and hip and ankle pairs tended to be lower at 3 months than at 1 month for full-term infants and preterm infants with PVL, whereas the opposite was observed for low-risk preterm infants. This tendency probably explains why no differences were observable between the groups at the age of 3 months. The full-term infants in the longitudinal studies by Thelen23 and Geerdink et al11 also showed a tendency toward a decrease of cross-correlation values among the 3 joints over time. As with our low-risk preterm infants, Geerdink et al11 reported an increase of interjoint cross-correlation in preterm infants and no more differences with full-term infants at the age of 12 weeks.
The analysis of interlimb coordination, carried out by computation of the percentages of the different types of kicking (eg, single LE kicking, kicking with both LEs) indicated that the most frequently occurring pattern of kicking at both ages in all groups was single LE kicking with the right or left LE. These findings confirm those previously reported by Thelen et al2 for full-term infants without brain injury between 1 and 5 months of age. We did not find any differences among the groups. Our data do not confirm Droit and colleagues' report12 that preterm infants with brain injury have less alternate kicking movements than do preterm controls at 37 to 39 weeks of postmenstrual age. Again, age differences might account for the different results. For example, Yokochi et al28 reported that kicking with both LEs, characterized by simultaneous flexion and extension of the hips and knees, was the most frequently occurring leg movement in a supine position in infants with diplegia observed between 3 and 12 months. This finding suggests an age-dependent effect of brain lesions on the different types of inter-LE coordination.
| Conclusions |
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Another question that we wanted to address concerned the prognostic value of a detailed analysis of kicking in relation to later neurological impairment, and particularly to cerebral palsy. As previously reported for other quantitative aspects of neonatal movement patterns, such as frequency of occurrence of GMs and of several other movement patterns,13 frequency and type of finger movements,29 and frequency and temporal characteristics of kicking movements at preterm and term age,12 it was impossible to predict the outcome of our infants from quantitative evaluation of kicking patterns, at least f or the kinematic variables observed and at the ages of 1 and 3 months postterm.
We were able to confirm, however, that the qualitative observation of GMs, carried out using the same videotape recordings from which the complex and time-consuming kinematic analysis of kicking was made, could reveal which infants were likely to develop a motor disorder. In particular, our findings confirm the strict correlation between cramped-synchronized GMs and the later outcome of spastic diplegia and tetraplegia previously indicated in other studies.1316
The presence of severe brain lesions and later outcomes correlate with global Gestalt perception of movements but not with analysis of single characteristics of kicking movements. Supraspinal lesions might alter in several ways the complexity and variability of GMs, and our Gestalt perception, as suggested by Lorenz,30 can take into account a great number of individual movement features and the relationships among them. Trained observers can easily and reliably detect these movement abnormalities, as shown by the high interobserver agreement in our study (see Einspieler et al17 for a review of this method).
Overall judgments of the normality of spontaneous movements in a young infant are influenced by the presence or absence of segmental distal movements of the hand or foot. These can be described as smooth, small movements in all directions, sometimes isolated, more often as a part of a more global movement, but not as a full pattern of arm or leg flexion or extension involving 2 or 3 main joints of a limb. They greatly contribute to the variability, fluency, and complexity of the infant movement repertoire. Therefore, it is not surprising that, in our infants, the presence or absence of segmental foot movements correlated well with the neurological outcome.
Kinematic components and electromyographic patterns of LE movements shown during walking by children with cerebral palsy differ in several ways from those observable in children without cerebral palsy.7,31 Other studies are needed to establish how early those differences can be identified in stepping or walking patterns, and whether and when they can also be observed in kicking movements. Thus far, qualitative assessment of spontaneous LE movements or GMs seems to be appropriate for clinical purposes in newborns and very young infants.
| Footnotes |
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This study was approved by the Research Technical Committees of the Stella Maris Foundation and the Italian Ministry of Health.
This research was supported by grants from the Italian Ministry of Foreign Affairs, the Rens-Holle Stichting and the Hersenstichting (to JCvdH), and the Italian Ministry of Health (RC 2/96) (to GC).
Some of the results of this study were presented orally at the 2nd Meeting of the European Society of Pediatric Neurology, October 8-11, 1997, Maastricht, the Netherlands.
* Panasonic Co, Div of Matsushita Electric Co Ltd, PO Box 288, Osaka 530-91, Japan. ![]()
B Nelson, Conseil en Syst Inform, 8 R Cour des Noues, 75020 Paris, France. ![]()
| References |
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