Kinematic and Qualitative Analysis of Lower-Extremity Movements in Preterm Infants With Brain Lesions.

Key Words: Brain lesions, Cerebral palsy, General movements, Kicking movements, Preterm infants.

Kicking movements are rhythmical in infants, and these cyclical lower-extremity (LE) movements are seen with the infant in a supine position from birth until about 10 months of age.[1] These movements have recently been studied by researchers interested in normal and abnormal motor development. Thelen et al[2] hypothesized that there might be a relationship among kicking movements, infant stepping, and early locomotion. They noticed that these movement patterns have a similar spatial and temporal pattern and, therefore, concluded that they might be generated by the same neural structures. Experiments carried out in different species (see Marder and Calabrese[3] for a review) have indicated that central pattern generators (CPGs), located at spinal cord level, are probably responsible for some rhythmic activities such as breathing, sucking, crawling, and walking. There is also some evidence that, in human fetuses, neonates, and young infants, the neural control of kicking and stepping movements might be exerted by CPGs in the spinal cord.

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 lesions--periventricular leukomalacia (PVL), in particular--which 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]

Heriza[9,10] studied the kicking behavior of low-risk preterm 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 al[11] 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 al[12] studied (cross-sectionally) kicking movements in preterm infants with brain lesions, detected by brain ultrasound, in comparison with low-risk 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-workers[13-17] 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 researchers[11-18] 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 al[17] 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:

* Is there any difference in the main characteristics of kicking movements (ie, frequency, temporal organization, intrakick and interkick coordination) between full-term infants with brain injury and low-risk preterm infants at the same postterm age?

* Is there any relationship between kicking characteristics and age of the infants (ie, any difference in kicking characteristics between 1- and 3-month-old infants)?

* What is the effect of severe brain lesions on kicking movements at both ages?

* What is the prognostic value of the observation of the main characteristics of kicking movements, in comparison with qualitative assessment of LE movements and of GMs?

Method

Subjects

Our subjects were enrolled, after informed consent was obtained from the parents, at the neonatal intensive care unit (NICU) of the University of Pisa. On the basis of the aims of our study, we were interested in collecting data from preterm infants who fulfilled the following criteria: (1) gestational age of less than 37 weeks, (2) birth weight of greater than the fifth percentile on the intrauterine weight chart,[19] (3) singleton birth, and (4) serial brain ultrasonography showing either no abnormalities or grade 1 intraventricular hemorrhage according to Levene et al[20] or transient (ie, lasting less than 7 days) periventricular hyperechogenicity (also called "periventricular flare") (low-risk group), or showing prolonged (ie, longer than 7 days) periventricular hyperechogenicity (or flare) or cystic PVL (PVL group). Flare and PVL were classified according to de Vries et al.[21]

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 char[19]), 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.

Table 1. Clinical Data of All Study Infants(a)

                                   Birth         Gestational
Subjects                     Sex   Weight (g)     Age (wk)

Preterm low-risk infants
    (1 mo)
  1                           F      2,180          34
  2                           F      2,040          36
  3                           M      2,230          35
  4                           M      1,710          34
  5                           F      1,750          34
  6                           M      2,020          34
Preterm low-risk infants
    (3 mo)
  7                           F      2,100          33
  8                           F      2,000          33
  9                           F      2,530          35
  10                          M      1,250          30
  11                          F      1,340          30
  12                          M      3,250          35
Preterm infants with PVL
    (1 mo)
  13                          F      1,680          32
  14                          F      1,300          30
  15                          M      1,745          32
  16(b)                       M      1,940          36
  17                          M      1,400          29
Preterm infants with PVL
    (3 mo)
  18                          M      2,090          34
  19                          M      1,492          32
  20                          M      1,740          34
  21 (b)                      M      1,300          33
  22                          F      1,550          31
  23                          M      1,280          29
Full-term infants (1 mo)
  24                          F      2,940          40
  25                          M      3,900          41
  26                          F      2,950          38
  27                          F      3,520          40
  28                          F      3,580          40
  29                          M      2,770          40
Full-term infants (3 mo)
  30(b)                       M      2,320          41
  31                          F      2,880          38
  32                          M      3,700          40
  33                          F      2,500          38
  34                          M      3,850          40
  35                          F      3,200          41

                             Serial Brain       General Movement
Subjects                     Ultrasound         Quality

Preterm low-risk infants
    (1 mo)
  1                          Normal             Normal
  2                          Transient flare    Normal
  3                          Transient flare    Normal
  4                          Transient flare    Normal
  5                          Transient flare    Normal
  6                          Transient flare    Normal
Preterm low-risk infants
    (3 mo)
  7                          Transient flare    Normal
  8                          Transient flare    Normal
  9                          Transient flare    Normal
  10                         Transient flare    Normal
  11                         Transient flare    Normal
  12                         Normal             Poor repertoire
Preterm infants with PVL
    (1 mo)
  13                         Cystic PVL         Cramped-synchronized
  14                         Cystic PVL         Cramped-synchronized
  15                         Prolonged flare    Cramped-synchronized
  16(b)                      Prolonged flare    Poor repertoire
  17                         Cystic PVL         Poor repertoire
Preterm infants with PVL
    (3 mo)
  18                         Cystic PVL         Cramped-synchronized
  19                         Prolonged flare    Poor repertoire
  20                         Cystic PVL         Poor repertoire
  21 (b)                     Cystic PVL         Poor repertoire
  22                         Prolonged flare    Poor repertoire
  23                         Prolonged flare    Cramped-synchronized
Full-term infants (1 mo)
  24
  25
  26
  27
  28
  29
Full-term infants (3 mo)
  30(b)
  31
  32
  33
  34
  35

                             Neurological
Subjects                     Outcome (18 mo)

Preterm low-risk infants
    (1 mo)
  1                          Normal
  2                          Normal
  3                          Normal
  4                          Normal
  5                          Normal
  6                          Normal
Preterm low-risk infants
    (3 mo)
  7                          Normal
  8                          Normal
  9                          Normal
  10                         Normal
  11                         Normal
  12                         Normal
Preterm infants with PVL
    (1 mo)
  13                         Diplegia
  14                         Diplegia
  15                         Diplegia
  16(b)                      Normal
  17                         Dyskinetic CP
Preterm infants with PVL
    (3 mo)
  18                         Tetraplegia
  19                         Normal
  20                         Left hemiplegia
                             Mild developmental
  21 (b)                     retardation
  22                         Normal
  23                         Diplegia
Full-term infants (1 mo)
  24                         Normal
  25                         Normal
  26                         Normal
  27                         Normal
  28                         Normal
  29                         Normal
Full-term infants (3 mo)
  30(b)                      Normal
  31                         Normal
  32                         Normal
  33                         Normal
  34                         Normal
  35                         Normal

(a) F = female, M = Male, PVL = periventricular leukomalacia, CP = cerebral palsy.

(b) Borderline small for gestational age (5%-10%)

The mean gestational age of the 12 low-risk infants was 33.6 weeks (SD = 1.9, range = 30-36), and their mean birth weight was 2,033 g (SD = 528, range = 1,710-3,250). The mean gestational age of the 11 infants with PVL was 32 weeks (SD = 22, range = 19-36). The infants with PVL had lower birth weights ([bar] X = 1,592 g, SD = 272, range = 1,300-2,090; t = 2.55, P [is less than] .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 ([+ or -] 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 ([+ or -] 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.([dagger]) 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.

[Figures 1-2 ILLUSTRATION OMITTED]

Data Analysis

Quantitative analysis of kicking movements. To assess kicking frequency, a new kick was counted when there was a new flexion movement after an extension movement. The kicking frequency was calculated for each LE as the number of kicks per minute. The mean recording time of the kicking period per subject was 228 seconds (SD = 132, range = 60-540).

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 seconds[2,23]) 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 = 19-21 segments for each of the 6 groups of infants; mean number of segments per infant = 3.4, SD = 0.98, range = 2-6). 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 = 5-14).

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 pair-wise cross-correlations were calculated for each pair of joints: hip and knee, hip and ankle, and knee and ankle. Two to 5 segments ([bar] X = 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 studies[1,12,23]: 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 variance[24] 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 [is less than or equal to] .05 was considered significant.

Qualitative scoring of LE movements. The following variables were scored from the whole videotape recording of the infant:

* Frequency of LE movements: The scores were 1 = frequent, 2 = rare.

* Amplitude of LE movements: The scores were l = variable, 2 = predominantly large or predominantly small.

* Speed of LE movements: The scores were 1 = variable, 2 = predominantly slow or predominantly fast.

* Frequency of segmental foot movements: Segmental foot movements were defined as distal movements in any plane, carried out in isolation or as a part of a GM, but not as a part of a global pattern of LE flexion or extension. The scores were 1 = frequent, 2 = rare or absent.

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.[12-18]

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 scale[26] was used: 1 = asleep; 2 = drowsy; 3 = awake, alert, little or no movement; 4 = awake, moving; 5 = fussy; and 6 = crying.

Results

Behavioral Condition

The majority of the infants remained in a state of active wakefulness during the recording of kicking movements. Fussing and crying, however, were observed in some low-risk preterm infants (1 infant at 1 month of age and 2 infants at 3 months of age) and especially in the infants with PVL (4 infants at 1 month of age and 2 infants at 3 months of age).

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 I to 3 months of age ([chi square] = 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 ([chi square] = 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]

Table 2. Medians and Interquartile Ranges (IQR) of Kicking Frequency of Both Lower Extremities (Number of Kicks/Minute)

                                                      Preterm Low-
                    Full-term        Full-term        Risk Infants
                    Infants (1 mo)   Infants (3 mo)   (1 mo)

                    Median   IQR     Median   IQR     Median   IQR

Kicking frequency   14.5     13      6.8      19      12.1     9.5

                    Preterm Low-     Preterm          Preterm
                    Risk Infants     Infants With     Infants With
                    (3 mo)           PVL (1 mo)       PVL (3 mo)

                    Median   IQR     Median   IQR     Median   IQR

Kicking frequency   18.3     35      20       16      11.9     11

Temporal organization. The phase durations of kicking movements are shown in Table 3. Again, a high variability of results was found for all groups, with no differences among them for the different variables. The only exception was a tendency for a shorter interkick pause at 3 months than at 1 month, which was observed for all groups. Such a difference reached a significant level in the full-term infants ([chi square] = 7.04, P = .01).

Table 3. Medians and Interquartile Ranges (IQR) of Phase Durations (in Milliseconds)

                  Full-term        Full-term        Preterm Low-
                  Infants          Infants          Risk Infants
                  (1 mo)           (3 mo)           (1 mo)

                  Median    IQR    Median    IQR    Median    IQR

Flexion              380     89       414     221      348      92
Intrakick pause      458    410       146     656      375     412
Extension            418    234       435     302      409     107
Interkick pause      689    448       500     393      542   1,828
Kick cycle         1,934    929     1,444   1,246    1,548   2,005

                  Preterm Low-     Preterm          Preterm
                  Risk Infants     Infants With     Infants With
                  (3 mo)           PVL (1 mo)       PVL (3 mo)

                  Median    IQR    Median    IQR    Median    IQR

Flexion              470      94      394     265      403    108
Intrakick pause      516     456      592     222      396    271
Extension            374     141      475     353      423    125
Interkick pause      505   1,346      844     668      398    466
Kick cycle         1,518   1,119    2,249   1,033    1,484    488

Intra-LE coordination. Table 4 shows the Pearson product-moment correlation coefficients (medians and IQRs) for the different pairs of joints (hip and ankle, hip and knee, knee and ankle) in all infant groups at 1 and 3 months. The movements of the LE joints were highly coordinated in all groups, as expressed by the coefficient levels.

Table 4. Medians and Interquartile Ranges (IQR) of the Correlation Coefficients Between the Different Joints

                                               Preterm Low-
             Full-term        Full-term        Risk Infants
             Infants (1 mo)   Infants (3 mo)   (1 mo)

             Median   IQR     Median   IQR     Median   IQR

Hip/knee      .85     .20      .79     .74      .69     .51
Hip/ankle     .59     .35      .51     .60      .21     .53
Knee/ankle    .76     .35      .83     .26      .67     .34

             Preterm Low-     Preterm          Preterm
             Risk Infants     Infants With     Infants With
             (3 mo)           PVL (1 mo)       PVL (3 mo)

             Median   IQR     Median   IQR     Median   IQR

Hip/knee      .70     .42      .82     .16      .72     .19
Hip/ankle     .50     .68      .64     .27      .52     .34
Knee/ankle    .80     .34      .81     .28      .75     .37

The Kruskal-Wallis analysis was used to compare the joint movement correlations obtained for the different groups of infants. It revealed differences related to preterm birth and the presence of brain lesions. Low-risk preterm infants at 1 month of age had a lower mean rank for hip and knee correlations ([chi square] = 11.21, P [is less than] .01) and hip and ankle correlations ([chi square] = 8.09, P [is less than] .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 ([chi square] = 9.26, P [is less than] .01) and hip and ankle correlations ([chi square] = 10.58, P [is less than] .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.

Table 5. Medians and Interquartile Ranges (IQR) of the Percentages of the Different Types of Kicking(a)

                                             Preterm Low-
          Full-term        Full-term         Risk Infants
          Infants (1 mo)   Infants (3 mo)    (1 mo)
Type of
Kicking   Median   IQR     Median   IQR      Median   IQR

SLR         48.6   14.5      26.2   12.8       30.9   23
SLL         38.2   15.9      46.6   45.7       39.7   37.1
ALT          7.1    9.5       8.3   21.1       15.5   17.4
BL           2      5.2       5.7   13.2        1.9    6.1
SBL          4.4    4.3       4.9   13          6     15.5

          Preterm Low-     Preterm Infants   Preterm Infants
          Risk Infants     With PVL          With PVL
          (3 mo)           (1 mo)            (3 mo)
Type of
Kicking   Median   IQR     Median   IQR      Median   IQR

SLR         31.4   28.7      37.5   21.1       30.1   22.6
SLL         32.1   23        23.9    3.7       43.1   16.5
ALT         12.2   19.2      17.6   17.2        7.4   16.8
BL           4.9   10         5.3    7.9        9.7   19.7
SBL         11.7   16        10.6    5.6        6.3    6.7

(a) SLR = single right lower-extremity kicking, SLL = single left lower-extremity kicking, ALT = alternate lower-extremity kicking, BL = kicking with both lower extremities, SBL = semi-bilateral lower-extremity kicking.

Qualitative Scoring of LE Movements

Frequency of LE movements. Only 2 infants with PVL were scored as having rare LE movements at the age of 3 months. (see explanation of qualitative scoring methods in "Data Analysis" section)

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 ([chi square] = 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 ([chi square] = 4.64, P = .03 at 1 month with low-risk preterm infants; [chi square] = 8.33, P = .003 with full-term infants; [chi square] = 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.

Table 6. Significant Differences Observed Between Preterm Low-Risk Infants and Preterm Infants With Periventricular Leukomalacia for the Different Movement Variables Analyzed

Variable                                    1 Month   3 Months

Kicking frequency
Temporal organization
Intra-lower extremity coordination
  Hip/knee correlation                       P<.01
  Hip/ankle correlation                      P<.01
Inter-lower extremity coordination
Qualitative assessment of lower-extremity
    movements
  Segmental movements                        P<.006
Qualitative assessment of general
    movements                                P<.03     P<.003

Discussion

The aim of our research was to study the impact of different factors, such as preterm birth, postterm age, and brain lesions, on kicking movements in the first weeks after term. Moreover, we were interested in assessing the prognostic value of some kinematic features of kicking, in comparison with qualitative assessment of LE movements and of GMs.

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 al[12] 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 Thelen[23] 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,[9-11] 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 al[11] 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 al[27] 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 Thelen[23] and Geerdink et al[11] 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 al[11] 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 al[2] 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' report[12] 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 al[28] 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

We conclude, according to the results of kinematic analysis of our subjects, that the mechanisms responsible for kicking are hardly influenced, at the studied ages, by the extrauterine environment or by supraspinal factors. As we noted earlier, even fetuses with anencephaly can show kicking movements.

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.[13-16]

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 al[17] 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.

(*) Panasonic Co, Div of Matsushita Electric Co Ltd. PO Box 288, Osaka 530-91, Japan.

([dagger]) B Nelson, Conseil en Syst Inform, 8 R Cour des Noues , 75020 Paris France.

References

[1] Thelen E. Development of locomotion from a dynamic system approach. In: Forssberg H, Hirschfeld H, eds. Movement Disorders in Children. Vol 36. Basel, Switzerland: S Karger AG, Medical and Scientific Publishers; 1992:169-173. Medicine and Sport Science Series.

[2] Thelen E, Bradshaw G, Ward JA. Spontaneous kicking in month-old infants: manifestation of a human central locomotor program. Behav Neural Biol. 1981;32:45-53.

[3] Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev. 1996;76:687-717.

[4] Visser GHA, Laurini RN, de Vries JIP, et al. Abnormal motor behaviour in anencephalic fetuses. Early Hum Dev. 1985;12:173-182.

[5] Peiper A. Cerebral Function in Infancy and Childhood. New York, NY: Consultants Bureau; 1963.

[6] Forssberg H. Ontogeny of human locomotor control, I: infant stepping, supported locomotor, and transition to independent locomotion. Exp Brain Res. 1985;57:480-493.

[7] Forssberg H. A neural control model for human locomotion development: implications for therapy. In: Forssberg H, Hirschfeld H, eds. Movement Disorders in Children. Vol 36. Basel, Switzerland: S KargerAG, Medical and Scientific Publishers; 1992:174-181. Medicine and Sport Science Series.

[8] Volpe JJ. Neurology of the Newborn. 3rd ed. Philadelphia, Pa: WB Saunders Co; 1995.

[9] Heriza CB. Organization of leg movements in preterm infants. Phys Ther. 1988;68:1340-1346.

[10] Heriza CB. Comparison of leg movements in preterm infants at term with healthy full-term infants. Phys Ther. 1988;68:1687-1693.

[11] Geerdink JJ, Hopkins B, Beek WJ, Heriza CB. The organization of leg movements in preterm and full-term infants after term age. Dev Psychobiol. 1996;29:335-351.

[12] Droit S, Boldrini A, Cioni G. Rhythmical leg movements in low-risk and brain-damaged preterm infants. Early Hum Dev. 1996;44:201-213.

[13] Ferrari F, Cioni G, Prechtl HFR. Qualitative changes of general movements in preterm infants with brain lesions. Early Hum Dev. 1990;23:193-231.

[14] Prechtl HFR, Ferrari F, Cioni G. Predictive value of general movements in asphyxiated fullterm infants. Early Hum Dev. 1993;35:91-120.

[15] Prechtl HFR, Einspieler C, Cioni G, et al. An early marker for neurological deficits after perinatal brain lesions. Lancet. 1997;349: 1361-1363.

[16] Cioni G, Ferrari F, Einspieler C, et al. Comparison between observation of spontaneous movements and neurologic examination in preterm infants. J Pediatr. 1997;130:704-711.

[17] Einspieler C, Prechtl HFR, Ferrari F, et al. The qualitative assessment of general movements in preterm, term, and young infants: review of the methodology. Early Hum Dev. 1997;50:47-60.

[18] Hadders-Algra M, Groothuis AMC. Relation of the quality of general movements at 3 months and neurological and behavioural development at school-age. Brain Dev. 1998;20:425-426.

[19] Pedrotti D, Macagno F, Gagliardi L, et al. Standard neonatali di crescita intrauterina elaborati dalla task force della SIN. SINinforma. 1997;1:1-4.

[20] Levene MI, Fawer CL, Lamont RF. Risk factors in the development of intraventricular haemorrhage in the preterm neonate. Arch Dis Child. 1982;57:410-417.

[21] de Vries LS, Eken P, Dubowitz LMS. The spectrum of leukomalacia using cranial ultrasound. Behav Brain Res. 1992;49:1-6.

[22] Touwen BCL. Neurological Development in Infancy. Vol. 58. London, England: William Heinemann Medical Books Ltd; 1976.

[23] Thelen E. Developmental origins of motor coordination: leg movements in human infants. Dev Psychobiol. 1985;18:1-22.

[24] Siegel S, Castella J. Nonparametric Statistics for Behavioral Sciences. 2nd ed. New York, NY: McGraw-Hill Inc; 1988.

[25] Norusis M. SPSS/PC+ [TM] 4.0 Base Manual. Chicago, Ill: SPSS Inc; 1990.

[26] Brazelton TB, Nugent JK. Neonatal Behavioral Assessment Scale. 3rd ed. London, England: MacKeith Press; 1995.

[27] Piek JP, Gasson N. Spontaneous kicking in full-term and preterm infants: intralimb and interlimb coordination. Australian Educational Developmental Psychology. 1997;14:23-34.

[28] Yokochi K, Inukai K, Hosoe A, et al. Leg movements in the supine position of infants with spastic diplegia. Dev Med Child Neurol. 1991;33: 903-907.

[29] Konishi Y, Prechtl HFR. Finger movements and fingers postures in pre-term infants are not a good indicator of brain damage. Early Hum Dev. 1994;36:89-100.

[30] Lorenz KZ. Gestalt perception as a source of scientific knowledge. In: Lorenz KZ, ed. Studies in Animal and Human Behaviour. Vol 2. London, England: Methuen & Co Ltd; 1971:281-322.

[31] Crenna P. Spasticity and "spastic" gait in children with cerebral palsy. Neurosci Biobehav Rev. 1997;22:571-578.

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 ([e-mail]). Address all correspondence to Dr Cioni.

Concept and research design were provided by Cioni; writing, by van der Heide; data collection, by Paolicelli and Boldrini, with assistance in ultrasound examination from Laura Bantalena and Pascal Biver; data analysis, by van der Heide, with computer programming assistance from Alberto Mura; and consultation, including review of manuscript prior to submission, by van der Heide, Boldrini and Cioni, with review of English language usage by Paul Morse.

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.

This article was submitted June 10, 1998, and was accepted February 28, 1999.