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Article |

Cramped Synchronized General Movements in Preterm Infants as an Early Marker for Cerebral Palsy FREE

Fabrizio Ferrari, MD; Giovanni Cioni, MD; Christa Einspieler, PhD; M. Federica Roversi, MD; Arend F. Bos, MD, PhD; Paola B. Paolicelli, MD; Andrea Ranzi, PhD; Heinz F. R. Prechtl, MD, DPhil, FRCOG(Hon)
[+] Author Affiliations

From the Institute of Paediatrics and Neonatal Medicine, University of Modena, Italy (Drs Ferrari, Roversi, and Ranzi); the Institute of Developmental Neurology, Psychiatry, and Educational Psychology, University of Pisa, and the Stella Maris Foundation, Calambrone, Pisa, Italy (Drs Cioni and Paolicelli); the Department of Physiology, University of Graz, Austria (Drs Einspieler and Prechtl); and the Department of Paediatrics, Beatrix Children's Hospital, University of Groningen, Groningen, the Netherlands (Dr Bos).


Arch Pediatr Adolesc Med. 2002;156(5):460-467. doi:10.1001/archpedi.156.5.460.
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Published online

Objective  To ascertain whether specific abnormalities (ie, cramped synchronized general movements [GMs]) can predict cerebral palsy and the severity of later motor impairment in preterm infants affected by brain lesions.

Design  Traditional neurological examination was performed, and GMs were serially videotaped and blindly observed for 84 preterm infants with ultrasound abnormalities from birth until 56 to 60 weeks' postmenstrual age. The developmental course of GM abnormalities was compared with brain ultrasound findings alone and with findings from neurological examination, in relation to the patient's outcome at age 2 to 3 years.

Results  Infants with consistent or predominant (33 cases) cramped synchronized GMs developed cerebral palsy. The earlier cramped synchronized GMs were observed, the worse was the neurological outcome. Transient cramped synchronized character GMs (8 cases) were followed by mild cerebral palsy (fidgety movements were absent) or normal development (fidgety movements were present). Consistently normal GMs (13 cases) and poor repertoire GMs (30 cases) either lead to normal outcomes (84%) or cerebral palsy with mild motor impairment (16%). Observation of GMs was 100% sensitive, and the specificity of the cramped synchronized GMs was 92.5% to 100% throughout the age range, which is much higher than the specificity of neurological examination.

Conclusions  Consistent and predominant cramped synchronized GMs specifically predict cerebral palsy. The earlier this characteristic appears, the worse is the later impairment.

Figures in this Article

IN THE PAST 20 years, there has been a dramatic reduction in neonatal mortality of low-birth-weight and very low-birth-weight infants but a relative increase in the incidence of cerebral palsy among children with low birth weight and short gestation.14 An increased survival rate is associated with an increased proportion of infants with cerebral palsy, and it has been suggested that the reduction in neonatal mortality and the concomitant relative increase in cerebral palsy might be associated5 because the prevalence of cerebral palsy rises sharply the lower the weight of the infant at birth.68 Cerebral palsy occurs in 8% to 10% of very preterm babies, and approximately 40% of all children with cerebral palsy were born preterm.8,9

An early prediction of cerebral palsy will lead to earlier enrollment in rehabilitation programs. Unfortunately, reliable identification of cerebral palsy in very young infants is extremely difficult.10 It is generally reported that cerebral palsy cannot be diagnosed before several months after birth1115 or even before the age of 2 years.16 A so-called silent period, lasting 4 to 5 months or more, and a period of uncertainty until the turning point at 8 months of corrected age have also been identified.12,13 The neurological symptoms observed in the first few months after birth in preterm infants who will develop cerebral palsy are neither sensitive nor specific enough to ensure reliable prognoses. Irritability, abnormal finger posture, spontaneous Babinski reflex,17,18 weakness of the lower limbs,19 transient abnormality of tone,12,13,2024 and delay in achieving motor milestones11 are some of the neurological signs that have been described in these high-risk preterm infants. All these symptoms may be encountered before the onset of cerebral palsy or during "transient dystonia,"21 dissociated motor development,25,26 and other transient neurological disturbances,23,24 which disappear during the first or second year of life. Moreover, no correlations have been found among any of these symptoms and the severity of future motor impairment. Therefore, traditional neurological examination fails to predict the development and severity of cerebral palsy.10,16

Neurological examination of newborns and young infants is mostly based on the study of neonatal reflexes, such as grasping, Moro reflex, rooting, and tonic asymmetric response and evoked responses, such as those involved in passive and active muscle tone. Little attention is paid to the spontaneous activity of the baby. More than 10 years ago, Prechtl et al2729 introduced a new approach to neurological evaluation based on spontaneous motor activity, rather than reflexes and evoked responses. Theoretical and empirical considerations suggest that the quality of endogenously generated motor activity is a better indicator of neural function integrity than many items in the neurological examination.27 In fact, fetuses and newborn infants exhibit a large number of endogenously generated motor patterns, which are produced by central pattern generators located in different parts of the brain. Moreover, substantial indications suggest that spontaneous activity is a more sensitive indicator of brain dysfunction than reactivity to sensory stimuli in reflex testing. Various studies2940 have demonstrated that in newborn infants affected by different brain lesions, spontaneous motility does not change in quantity, but it loses its elegance, fluency, and complexity. General movements (GMs) have been selected from among the whole repertoire of spontaneous motor patterns because of their complexity and frequent occurrence. A range of abnormalities in the quality of GMs, such as hypokinesis, poor repertoire, abnormal or absent fidgety movements, and chaotic and cramped synchronized GMs, have been described. Visual gestalt perception is a powerful and reliable instrument for detecting these alterations in the complexity of movements. Cramped synchronized character, the most severe motor abnormality, has been found to be predictive of severe neurological impairment.29,32,34,35 Recently, the absence or abnormality of GMs of fidgety character, or fidgety movements, at 47 to 60 weeks' postmenstrual age has been shown to be a high-validity predictor of future neurological impairment, specifically cerebral palsy.34

A collaborative study with a large cohort of high-risk preterm infants was specifically designed to achieve a better understanding of the relationship among cramped synchronized GMs, later cerebral palsy, and the severity of functional impairment. More specifically, 3 main questions were addressed. First, are cramped synchronized GMs an early and specific marker of later cerebral palsy? Second, is the emergence and development of cramped synchronized GMs somehow related to the severity of cerebral palsy? And third, are GMs as powerful a prognostic tool as ultrasound abnormalities alone and traditional neurological examination, or are they even more powerful?

High-risk preterm infants were enrolled at the University of Modena and the University of Pisa (Italy) for a prospective, collaborative study of GM observation. The scientific Research Committee of the Italian Ministry of Health, Rome, approved the study. Infants who fulfilled the following criteria—mother's last menstrual date reliably known, gestational age less than 37 completed weeks, ultrasound abnormalities highly suggestive of brain parenchymal insult, repeated GM assessment and neurological examination until about 56 to 60 weeks' postmenstrual age, and neurological follow-up until 2 to 3 years' corrected age—were included in the study. We excluded infants with chromosomal defects or major malformations of the brain or other organs. All infants with GM observation or neurological examination missing at more than 1 key age were also excluded. We enrolled 93 infants, but 9 were omitted because of missing data. Eighty-four infants were included in the final sample. The clinical data of the study group are listed in Table 1. Some infants had taken part in previous studies,29,32,34 and all parents gave their informed consent.

Table Graphic Jump LocationTable 1. Clinical Characteristics of 84 High-Risk Preterm Infants*
ULTRASOUND SCANS

On the basis of serial ultrasound scans, performed with 5- to 7.5-MHz heads, we included infants with cystic (34 cases) or noncystic (34 cases) abnormalities of the white matter. Cystic lesions were categorized as small and localized, extensive periventricular, and/or subcortical cysts. Noncystic lesions consisted of increased periventricular echogenicity, characterized by globular, blotchy, coarse hyperechoic ultrasound images localized in the periventricular region that were seen both in coronal and parasagittal views, persisted for 2 weeks or longer, and resolved without subsequent development of cysts or enlargement of the lateral ventricles (adapted from Dammann and Leviton41). Sixteen infants with intraventricular hemorrhage grades 3 and 3+, according to Volpe,42 were also included. Ultrasound abnormalities were reviewed blindly by an expert in ultrasounds (A.B.) who was unaware of the clinical history and development of the infants.

OBSERVATION OF GMs

Videotape recordings were usually made at 3-week to 5-week intervals from birth until the preterm infants were discharged from the hospital. During the study period, each infant was recorded 5 to 10 times. Serial assessments of GM quality were displayed on a time axis to trace individual developmental trajectories.27 Because the functional repertoire changes at various ages, we divided our longitudinal data into 4 "key age" periods: preterm (up to 37 weeks' postmenstrual age), term age (38-42 weeks' postmenstrual age), 43 to 46 weeks' postmenstrual age, and 47 to 60 weeks' postmenstrual age. The quality of the GMs of infants recorded in Modena was assessed in Pisa (G.C.), and infants recorded in Pisa were assessed in Modena (F.F.). In addition, one of us (H.F.R.P.), who was unaware of the infants' clinical histories and ultrasound results, reassessed the quality of GMs. Interobserver agreement in the judgment of the quality of GMs was 90.2%. If investigators disagreed, an agreement was reached after reassessment and discussion. From birth until the end of the second month postterm, GMs were scored as normal, poor repertoire, or cramped synchronized. From 47 to 60 weeks' postmenstrual age, GMs of a fidgety character were scored as present (normal or abnormal) or absent. When more than 1 judgment per age period was available for a single subject, the first observation for this age period was used. In addition, GMs of a cramped synchronized character could be scored until 60 weeks' postmenstrual age (Figure 1).

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Figure 1.

Types of normal (N) and abnormal (A) general movements (GMs) in 84 high-risk preterm infants during preterm, term, and the first 5 months of postterm age. F indicates fidgety; PR, poor repertoire; CS, cramped synchronized; and CH, chaotic.

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DEFINITIONS

General movements are gross movements that involve the whole body; they may last from a few seconds to several minutes. They appear early in gestation (9-10 weeks' postmenstrual age) and are the most complex of the whole repertoire of endogenously generated distinct movements.

What is particular about normal GMs is the variable sequence of arm, neck, and trunk movements. They wax and wane in intensity, force, and speed, and they have a gradual beginning and end. The majority of the sequence of extension and flexion movements of arms and legs is complex, with superimposed rotations and, often, slight changes in the direction of the movement. These additional components make the movement fluent and elegant and create the impression of complexity and variability. Despite this variability, GMs must be considered as a distinct coordinated pattern that is easy to recognize each time it occurs.

In poor repertoire GMs, the sequence of the components of the successive movements is monotonous, and the movements of the different body parts do not occur in the complex way seen in normal GMs.

Cramped synchronized GMs appear rigid and lack the normal smooth and fluent character. All limb and trunk muscles contract and relax almost simultaneously.

Fidgety movements are an ongoing stream of small, circular, and elegant movements of the neck, trunk, and limbs; they emerge at 6 to 9 weeks' and disappear around 15 to 20 weeks' postterm age. Abnormal fidgety movements look like normal fidgety movements, but their amplitude, speed, and jerkiness are moderately or greatly exaggerated.

Abnormal GM quality could persist throughout the entire period of observation or just part of it. We called an individual developmental trajectory with the same GM abnormality throughout the study period consistent. When GM abnormality was observed transiently during preterm and/or term age only, we used the term transient. When cramped synchronized GMs (preceded by poor repertoire GMs) were present for even longer and did not disappear until 60 weeks' postmenstrual age, the term predominant was used.

NEUROLOGICAL EXAMINATION AND FOLLOW-UP

During the preterm and term periods, neurological examination was carried out in accordance with the Dubowitz and Dubowitz43 and Prechtl44 protocols, respectively. During the first 5 months' postterm and afterward, videotapes of spontaneous motility and clinical checks were accompanied by a standardized neurological assessment, based on items from Touwen.45 The neurological assessment was also videotaped. Any abnormal signs in the neurological examinations were noted. During the preterm period, we looked for the following abnormalities from the Dubowitz protocol: abnormal posture, generalized or segmental hypotonia or hypertonia, hypokinesis, abnormal head control, frequent tremors or startles, absent or abnormal responses or reflexes, hyporeactivity to stimulation, and irritability.43,46 The results of the Prechtl examination, performed at term, were classified according to the syndromes indicated in the summary form.44 The neurological examination was scored as abnormal when at least 1 of the abnormalities mentioned above was present. Additionally, at the age of 2 to 3 years, a developmental test according to the Griffiths Developmental Scales47 was performed. At this age, the outcome was classified as "normal" (no neurological signs) or "cerebral palsy." Cerebral palsy was defined as "a chronic disability characterized by aberrant control of movement or posture, appearing early in life and not the result of recognized progressive disease."48(p707) At 2 to 3 years of age, the severity of motor disability was scored in accordance with the classification system for gross motor function in children with cerebral palsy recently proposed by Palisano et al.49 We distinguished mild (grade 1) and moderate to severe motor impairment (grades 2-5). In addition, we defined minor neurological deficits: mild sensory deficits, strabismus, severe postural delay without corticospinal tract dysfunction, and/or a score between 50 and 84 on the Griffiths Developmental Scales.

INTEROBSERVER RELIABILITY

The neurological examinations in Modena and in Pisa were performed by two of us (F.F. and G.C., respectively). To assess functional impairment in cerebral palsy, the same authors reviewed the neurodevelopmental records and videotapes of the infants at the time of the last clinical check. Preterm infants from Pisa were scored by one of us (F.F.), and while another of us (G.C.) scored infants from Modena; these scores were compared with the original scores given by local physical therapists and pediatric neurologists. In case of disagreement, an agreement was reached after reassessment and discussion.

STATISTICAL ANALYSIS

The receiver operating characteristic curve analysis was used to compare the power of ultrasounds and GMs to predict cerebral palsy.50 Receiver operating characteristic curve analysis provides a powerful means of assessing a test's ability to discriminate between 2 groups of patients, with the advantage that the analysis does not depend on the threshold value selected. To test the correlation between the time of appearance of the cramped synchronized GMs and the severity of motor impairment in children with cerebral palsy, a Yates trend test (2-tailed)51 was used. This test estimates the trend based on regression concepts and is more appropriate and sensitive than a χ2 test for p × q contingency tables. A P value of <.05 was considered statistically significant. A standard formula was used to calculate the likelihood ratio of GMs, the cramped synchronized character of GMs, and findings from neurological examination.

NEUROLOGICAL OUTCOME

At 2 to 3 years of age, 40 infants were healthy, and 44 had spastic-type cerebral palsy (22 subjects had diplegia, 14 had tetraplegia, and 8 had hemiplegia). Fifteen infants showed grade 1 motor impairment, according to Palisano et al,49 5 infants had grade 2, 5 had grade 3, 9 had grade 4, and 10 had grade 5. With the exception of 1 infant with a mild hearing defect, no case of minor neurological disorder was observed.

Ultrasound Findings

Severe ultrasound abnormalities (ie, extensive cysts and germinal matrix–intraventricular hemorrhage grade 3+) were present in 31 infants and, with 1 exception, led to cerebral palsy. Minor ultrasound abnormalities (persisting increased echogenicity, small and localized cysts, and germinal matrix–intraventricular hemorrhage grade 3) were present in 53 infants. The majority of cases (39 infants) had a normal outcome; cerebral palsy with mild (7 infants) or moderate to severe (7 infants) impairment was also observed (Table 2).

Table Graphic Jump LocationTable 2. Ultrasound Scan Results and Neurological Outcome in 84 High-Risk Preterm Infants*
Developmental Trajectories

The time course of GM quality in relation to the neurological outcome is provided in Table 3 and Figure 2. The duration and consistency of GM quality determined to a high degree the normality or severity of the abnormal outcome. All 33 preterm infants who displayed predominant (19 cases) or consistent (14 cases) cramped synchronized character GMs throughout the study period developed cerebral palsy. None of them displayed fidgety movements between 47 to 60 weeks' postmenstrual age. By contrast, 13 infants with consistent normal GMs, 4 infants with transient poor repertoire GMs, 19 infants with consistent poor repertoire GMs, and 4 infants with transient cramped synchronized GMs had a normal outcome. Despite the different patterns of developmental trajectory, these infants had fidgety movements in common (3 showed abnormal fidgety movements). The only exception was 1 infant with no fidgety movements who showed a prolonged postural delay that disappeared at 3 years of age and was classified as normal (Table 4). Of the preterm infants with consistent poor repertoire GMs (7 cases) and transient cramped synchronized GMs (4 cases) who later developed cerebral palsy, 10 had no fidgety movements, and 1 had exaggerated fidgety movements. The relationship between the age of appearance of predominant or consistent cramped synchronized GMs and the severity of the neurological impairment demonstrates that the earlier the cramped synchronized quality GMs appear, the worse is the outcome. The Yates trend test (T, 3.207; P<.005) proved the statistical significance of this statement.

Table Graphic Jump LocationTable 3. Types of Developmental Trajectories and Neurological Outcome in 84 High-Risk Preterm Infants*
Place holder to copy figure label and caption
Figure 2.

Types of developmental trajectories and neurological outcome in 84 high-risk preterm infants. N indicates normal movements; PR, poor repertoire; and CS, cramped synchronized.

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Table Graphic Jump LocationTable 4. Fidgety Movements (FMs) and Neurological Outcome in 84 High-Risk Preterm Infants
PREDICTIVE VALUE OF ULTRASOUND SCANS AND GMs

The areas under the receiver operating characteristic curve analysis for GMs and ultrasound scans were quite large (97.4 and 88.3, respectively), which shows that they are both accurate tests. A statistically significant difference was found between the 2 methods (P = .001). The quality of GMs was a better index to predict neurological outcome in a group of infants who were selected on the basis of abnormal ultrasound findings (Figure 3).

Place holder to copy figure label and caption
Figure 3.

The area under the receiver operating characteristic (ROC) curve for quality of general movements (GMs) and ultrasound (US) scans in high-risk preterm infants. The ROC curve is generated by plotting the proportion of true-positive results against the proportion of false-positive results for each value of a test. The curve for an arbitrary test (AT) that is expected to have no discriminatory value appears as a diagonal line, whereas a useful test has an ROC curve that rises rapidly and reaches a plateau.

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LIKELIHOOD RATIO AND ACCURACY OF GMs AND NEUROLOGICAL EXAMINATION IN PREDICTING CEREBRAL PALSY

The positive likelihood ratio of cramped synchronized GMs for predicting cerebral palsy is much higher than that of neurological examination throughout the age range. The negative likelihood ratio for predicting cerebral palsy based on GM quality was also much higher than that for neurological examination during the study period.

The GM observation was 100% sensitive throughout the age range; neurological examination was less sensitive during the study period. The sensitivity of cramped synchronized GMs was low (46.5%) in the preterm period because of those infants with cramped synchronized GMs preceded by poor repertoire GMs. Sensitivity rose to 65%, 78.7%, and 77.2% at term, early postterm period, and fidgety age, respectively, because of preterm infants who developed cerebral palsy after transient cramped synchronized GMs or consistent poor repertoire GMs. Even more striking was the difference in specificity when cramped synchronized GMs were compared with neurological examination. The specificity of the former was extremely high (92.5% to 100%) for all age ranges; it was invariably much higher than that afforded by neurological examination (Table 5).

Table Graphic Jump LocationTable 5. Age Period−Related Likelihood Ratios (LRs) and Accuracy for General Movement (GM) Observation, Cramped Synchronized Character, and Neurological Examination With Respect to Cerebral Palsy*

Two major findings emerge from this study. First, the cramped synchronized character of GMs, if consistent in time or predominant from preterm birth to 5 months' postterm age, specifically predicts later cerebral palsy. Second, the time of appearance of cramped synchronized GMs predicts the degree of later functional impairment caused by cerebral palsy: the earlier the appearance, the more severe the functional impairment.

Our study also confirmed observations from previous investigations.32,52 Normal fidgety movements following transient abnormalities of GM quality point to a normal outcome, absence of fidgety movements suggests a neurological deficiency, and GMs are a more powerful prognostic tool than traditional neurological examination and ultrasound scan.34

The severity and prognostic value of the cramped synchronized character of GMs were known from previous studies.29,32 However, the finding that this motor abnormality is a specific marker of later cerebral palsy is new. A detailed analysis of the developmental trajectories of GMs in a large group of preterm infants affected by major or minor abnormalities detected by ultrasound demonstrates that the consistent or predominant cramped synchronized character of GMs, irrespective of the severity of the ultrasound abnormalities, is always followed by cerebral palsy.

The study has practical and obvious implications. It offers clues about the selection criteria for a strict neurological follow-up. Preterm infants who are waiting for a definite diagnosis of brain integrity are usually enrolled in prospective neurological follow-up programs based on their clinical history and the ultrasound findings rather than a functional assessment, which involves the evaluation of mental and motor performance. Recent studies5355 have shown that mental retardation and learning deficiencies are common among preterm infants tested at school age. We are not sure whether normal, or only mildly abnormal, GMs at these early ages exclude these minor deficiencies at a later age. This study stresses the importance of functional assessment based on early observations of spontaneous motor behavior. The normal quality of GMs identifies those infants who are not affected by brain dysfunction and who will develop normally; they do not need strict neurological surveillance. In contrast, prolonged cramped synchronized character GMs identify infants who are most likely to develop cerebral palsy. They are the ones who need and can possibly benefit from early intervention.

The first videotape should be recorded as soon as possible after birth, when the effects of analgesia and/or sedation have worn off and the small preterm infant is in stable physical condition. Regular videotape recordings will preferably be made until 47 to 60 weeks' postmenstrual age. When cramped synchronized GMs are spotted, it is wise to continue recording to determine whether they are transient or consistent and whether fidgety movements will appear.

A review of various studies56 highlights that the technique of GM assessment is reliable (interscorer agreement, 78%-98%) and easy to learn. In our experience, a training course followed by a few months of practice on clinical material (ie, serial videotapes of a few infants) introduces the beginner to the clinical application of the method. The pattern of cramped synchronized GMs is the easiest to spot because all or most of the limbs contract and relax almost simultaneously with a monotonous sequence. The method has been widely accepted and recognized2940 as a simple, noninvasive, and powerful diagnostic and prognostic tool, and we think that assessment of spontaneous motility is a substantial part of the neurological examination. Medical staff involved in the neurological follow-up of high-risk newborn infants could benefit from the gestalt approach, which can be learned through specific training courses. Practice recognizing GMs from videotapes would enhance clinicians' abilities to detect the early signs of brain dysfunction.

Accepted for publication January 17, 2002.

This study was supported in part by the Italian Ministry of Health (Current Research Project 1994) and the ITI Company, Modena, Italy.

We thank Alberto Berardi, MD, who blindly evaluated the ultrasound scans, and Luca Ori, who made the videotapes of some infants in the intensive care unit and the outpatient clinic at the University of Modena. We also thank the staff of the neonatal intensive care unit of the University of Pisa, where some of the cases were observed, and Giovanni Battista Cavazzuti, MD (Department of Paediatrics, University of Modena), and Pietro Pfanner, MD (Department of Child Neuropsychiatry, Unversity of Pisa), for their continuous support of our research.

Since physical diagnosis is a visual skill, we have included video clips of four infants:

You will need Quick Time to view these videos:

What This Study Adds

Cerebral palsy occurs in 8% to 10% of very preterm infants, whereas approximately 40% of all children with cerebral palsy are born preterm. An early prediction of cerebral palsy will lead to earlier rehabilitation programs. Unfortunately, reliable identification of cerebral palsy in very young infants is extremely difficult.10 It is generally reported that cerebral palsy cannot be diagnosed before several months after birth1115 or even before the age of 2 years. In addition, traditional neurological examination fails to predict the development and severity of cerebral palsy

Our study demonstrates that the cramped synchronized character of GMs, if consistent in time or predominant from preterm birth to 5 months' postterm age, specifically predicts later cerebral palsy. Second, the time of appearance of cramped synchronized GMs predicts the degree of later functional impairment of cerebral palsy: the earlier the appearance, the more severe is the functional impairment.

The study has practical and obvious implications. It offers clues about the selection criteria for a strict neurological follow-up and helps the physician involved in the follow-up recognize the early signs of cerebral palsy and, consequently, begin early rehabilitation programs.

Corresponding author and reprints: Fabrizio Ferrari, MD, Institute of Paediatrics and Neonatal Medicine, University of Modena, Policlinico Universitario, 41100 Modena, Italy (e-mail: ferrarif@unimo.it).

MacGillivray  ICampbell  DM The changing patterns of cerebral palsy in Avon. Paediatr Perinat Epidemiol. 1995;9146- 155
Link to Article
Hagberg  BHagberg  GOlow  Ivon Wendt  L The changing panorama of cerebral palsy in Sweden, V: the birth year period 1979-82. Acta Paediatr Scand. 1989;78283- 290
Link to Article
Hagberg  BHagberg  GOlow  I The changing panorama of cerebral palsy in Sweden, VI: prevalence and origin during the birth year period 1983-86. Acta Paediatr. 1993;82387- 393
Link to Article
Hagberg  BHagberg  GOlow  Ivan Wendt  L Changing panorama of cerebral palsy in Sweden, VII: prevalence and origin in the birth year period 1987-90. Acta Paediatr. 1996;85954- 960
Link to Article
Hagberg  BHagberg  GZetterstrom  R Decreasing perinatal mortality: increase in cerebral palsy morbidity? Acta Paediatr Scand. 1989;78664- 670
Link to Article
Hagberg  BHagberg  GStanley  FedAlberman  Eed Prenatal and perinatal risk factors in a survey of 681 Swedish cases. The Epidemiology of the Cerebral Palsies London, England William Heinemann Medical Books1989;116- 134Clinics in Developmental Medicine vol 87
Emond  AGolding  JPeckham  C Cerebral palsy in 2 national cohort studies. Arch Dis Child. 1989;64848- 852
Link to Article
Pharoah  POCooke  TCooke  RWRosenbloom  L Birthweight specific trends in cerebral palsy. Arch Dis Child. 1990;65602- 606
Link to Article
Escobar  GJLittenberg  BPetitti  DB Outcome among surviving very low birthweight infants: a meta-analysis. Arch Dis Child. 1991;66204- 211
Link to Article
Illingworth  RS The diagnosis of cerebral palsy in the first year of life. Dev Med Child Neurol. 1966;8178- 194
Link to Article
Allen  MAlexander  GR Using gross motor milestones to identify very preterm infants at risk for cerebral palsy. Dev Med Child Neurol. 1992;34226- 232
Link to Article
Saint-Anne Dargassies  S Normality and normalization as seen in a long-term neurological follow-up of 286 truly premature infants. Neuropadiatrie. 1979;10226- 244
Link to Article
Saint-Anne Dargassies  S Neurodevelopmental symptoms during the first years of life. Dev Med Child Neurol. 1972;14235- 246
Link to Article
Weisglas-Kuperus  NBaerts  WSauer  PJJ Early assessment and neurodevelopmental outcome in very low birth-weight infants: implications for paediatric practice. Acta Paediatr. 1993;82449- 453
Link to Article
Futagi  YTagawa  TOtani  K Primitive reflex profiles in infants: differences based on categories of neurological abnormality. Brain Dev. 1992;14294- 298
Link to Article
Bennett  FCAvery  GBedFletcher  MAedMacDonald  Ged Developmental outcome. Neonatology: Pathophysiology and Management of the Newborn Philadelphia, Pa JB Lippincott Co1994;1367- 1386
Dubowitz  LMSLevine  MJedBennett  MJedPunt  Jed Clinical assessment of the infant nervous system. Fetal and Neonatal Neurology and Neurosurgery Edinburgh, Scotland Churchill Livingstone1988;41- 58
de Vries  LDubowitz  LM Cystic leukomalacia in preterm infants: site of lesions in relation to prognosis. Lancet. 1985;21075- 1076
Link to Article
Volpe  JJ Hypoxic-ischemic encephalopathy: neuropathology and pathogenesis. Neurology of the Newborn 3rd ed Philadelphia, Pa WB Saunders Co1995;279- 313
de Vries  LRegev  RPennock  JM Ultrasound evolution and later outcome of infants with periventricular densities. Early Hum Dev. 1988;16225- 233
Link to Article
Drillien  CM Abnormal neurological signs in the first year of life in low birth-weight infants: possible prognostic significance. Dev Med Child Neurol. 1972;14575- 584
Link to Article
Ingram  TT The early manifestations in course of diplegia in childhood. Arch Dis Child. 1955;30244- 250
Link to Article
Amiel-Tison  CGrenier  A Neurological Evaluation of the Newborn and the Infant.  New York, NY Masson1983;
Amiel-Tison  CKorobkin  REsque-Vaucouloux  MT Neck extensor hypertonia: a clinical sign of insult to the central nervous system of the newborn. Early Hum Dev. 1977;1181- 190
Link to Article
Bobath  BBobath  K Motor Development in the Different Types of Cerebral Palsy.  London, England William Heinemann Medical Books1975;
Hagberg  BLundberg  A Dissociated motor development simulating cerebral palsy. Neuropadiatrie. 1969;1187- 199
Link to Article
Prechtl  HF Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23151- 158
Link to Article
Cioni  GPrechtl  HF Preterm and early postterm motor behavior in low-risk premature infants. Early Hum Dev. 1990;23159- 191
Link to Article
Ferrari  FCioni  GPrechtl  HF Qualitative changes of general movements in preterm infants with brain lesions. Early Hum Dev. 1990;23193- 231
Link to Article
Albers  SJorch  G Prognostic significance of spontaneous motility in very immature preterm infants under intensive care treatment. Biol Neonate. 1994;66182- 187
Link to Article
Geerdink  JJHopkins  B Qualitative changes in general movements and their prognostic value in preterm infants. Eur J Pediatr. 1993;152362- 367
Link to Article
Cioni  GFerrari  FEinspieler  CPaolicelli  PBBarbani  MTPrechtl  HF Comparison between observation of spontaneous movements and neurologic examination in preterm infants. J Pediatr. 1997;130704- 711
Link to Article
Bos  AFvan Loon  AJHadders-Algra  MMartijn  AOkken  APrechtl  HF Spontaneous motility in preterm, small-for-gestational age infants, II: qualitative aspects. Early Hum Dev. 1997;50131- 147
Link to Article
Prechtl  HFEinspieler  CCioni  GBos  AFFerrari  FSontheimer  D An early marker of developing neurological deficits after perinatal brain lesions. Lancet. 1997;3491361- 1363
Link to Article
Prechtl  HFFerrari  FCioni  G Predictive value of general movements in asphyxiated full-term infants. Early Hum Dev. 1993;3591- 120
Link to Article
Ferrari  FPrechtl  HFCioni  G  et al.  Posture, spontaneous movements and behavioral state organization in infants affected by brain malformation. Early Hum Dev. 1997;5087- 113
Link to Article
Bos  AFMartijn  Avan Asperen  RMHadders-Algra  MOkken  APrechtl  HF Qualitative assessment of general movements in high-risk preterm infants with chronic lung disease requiring dexamethasone therapy. J Pediatr. 1998;132300- 306
Link to Article
Bos  AFMartijn  AOkken  APrechtl  HF Quality of general movements in preterm infants with transient periventricular echodensities. Acta Paediatr. 1998;87328- 335
Link to Article
Cioni  GBos  AFEinspieler  C  et al.  Early neurological signs in preterm infants with unilateral intraparenchymal echodensity. Neuropediatrics. 2000;31240- 251
Link to Article
Bos  AFVenema  IMBergervoet  MZweens  MJPratl  Bvan Eykern  LA Spontaneous motility in preterm infants treated with indomethacin. Biol Neonate. 2000;78174- 180
Link to Article
Dammann  OLeviton  A Duration of transient hyperechoic image of white matter in very low birth weight infants: a proposed classification. Dev Med Child Neurol. 1997;392- 5
Link to Article
Volpe  JJ Intraventricular hemorrhage in the premature infant: current concepts, pt 2. Ann Neurol. 1989;25109- 116
Link to Article
Dubowitz  LDubowitz  V The Neurological Assessment of the Preterm and Full-term Infant.  London, England William Heinemann Medical Books1981;Clinics in Developmental Medicine Vol 79
Prechtl  HF The Neurological Examination of the Full-term Newborn Infant. 2nd rev ed London, England William Heinemann Medical Books1977;Clinics in Developmental Medicine vol 63
Touwen  BCL Neurological Development in Infancy.  London, England William Heinemann Medical Books1976;Clinics in Developmental Medicine vol 58
de Vries  LSDubowitz  LMDubowitz  VPennock  JM A Colour Atlas of Brain Disorders in the Newborn.  London, England Wolfe1990;
Griffiths  R The Ability of Babies.  London, England University Press1954;
Ellenberg  JHNelson  KB Early recognition of infants at high risk for cerebral palsy: examination at age 4 months. Dev Med Child Neurol. 1981;23705- 716
Link to Article
Palisano  RRosenbaum  PWalter  SRussel  SWood  EGaluppi  B Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39214- 223
Link to Article
Metz  CE Basic principles of ROC analysis. Semin Nucl Med. 1978;8283- 298
Link to Article
Yates  F The analysis of contingency tables with groupings based on quantitative characters. Biometrika. 1948;35176- 181
Link to Article
Cioni  GPrechtl  HFFerrari  FPaolicelli  PBEinspieler  CRoversi  MF Which better predicts later outcome in full-term infants: quality of general movements or neurological examination? Early Hum Dev. 1997;5071- 85
Link to Article
Taylor  HGKlein  NMinich  NHack  M Middle-school–age outcomes in children with very low birthweight. Child Dev. 2000;711495- 1511
Link to Article
Taylor  HGKlein  NHack  M School age consequences of birth weight less than 750 grams: a review and update. Dev Neuropsychol. 2000;17289- 321
Link to Article
Hack  MTaylor  HGKlein  NMercuri-Minich  N Functional limitations and special health care needs of 10- to 14-year-old children weighing less than 750 grams at birth. Pediatrics. 2000;106554- 560
Link to Article
Einspieler  CPrechtl  HFFerrari  FCioni  GBos  A The qualitative assessment of general movements in preterm, term, and young infants: review of the methodology. Early Hum Dev. 1997;5047- 60
Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

Types of normal (N) and abnormal (A) general movements (GMs) in 84 high-risk preterm infants during preterm, term, and the first 5 months of postterm age. F indicates fidgety; PR, poor repertoire; CS, cramped synchronized; and CH, chaotic.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Types of developmental trajectories and neurological outcome in 84 high-risk preterm infants. N indicates normal movements; PR, poor repertoire; and CS, cramped synchronized.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

The area under the receiver operating characteristic (ROC) curve for quality of general movements (GMs) and ultrasound (US) scans in high-risk preterm infants. The ROC curve is generated by plotting the proportion of true-positive results against the proportion of false-positive results for each value of a test. The curve for an arbitrary test (AT) that is expected to have no discriminatory value appears as a diagonal line, whereas a useful test has an ROC curve that rises rapidly and reaches a plateau.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Clinical Characteristics of 84 High-Risk Preterm Infants*
Table Graphic Jump LocationTable 2. Ultrasound Scan Results and Neurological Outcome in 84 High-Risk Preterm Infants*
Table Graphic Jump LocationTable 3. Types of Developmental Trajectories and Neurological Outcome in 84 High-Risk Preterm Infants*
Table Graphic Jump LocationTable 4. Fidgety Movements (FMs) and Neurological Outcome in 84 High-Risk Preterm Infants
Table Graphic Jump LocationTable 5. Age Period−Related Likelihood Ratios (LRs) and Accuracy for General Movement (GM) Observation, Cramped Synchronized Character, and Neurological Examination With Respect to Cerebral Palsy*

References

MacGillivray  ICampbell  DM The changing patterns of cerebral palsy in Avon. Paediatr Perinat Epidemiol. 1995;9146- 155
Link to Article
Hagberg  BHagberg  GOlow  Ivon Wendt  L The changing panorama of cerebral palsy in Sweden, V: the birth year period 1979-82. Acta Paediatr Scand. 1989;78283- 290
Link to Article
Hagberg  BHagberg  GOlow  I The changing panorama of cerebral palsy in Sweden, VI: prevalence and origin during the birth year period 1983-86. Acta Paediatr. 1993;82387- 393
Link to Article
Hagberg  BHagberg  GOlow  Ivan Wendt  L Changing panorama of cerebral palsy in Sweden, VII: prevalence and origin in the birth year period 1987-90. Acta Paediatr. 1996;85954- 960
Link to Article
Hagberg  BHagberg  GZetterstrom  R Decreasing perinatal mortality: increase in cerebral palsy morbidity? Acta Paediatr Scand. 1989;78664- 670
Link to Article
Hagberg  BHagberg  GStanley  FedAlberman  Eed Prenatal and perinatal risk factors in a survey of 681 Swedish cases. The Epidemiology of the Cerebral Palsies London, England William Heinemann Medical Books1989;116- 134Clinics in Developmental Medicine vol 87
Emond  AGolding  JPeckham  C Cerebral palsy in 2 national cohort studies. Arch Dis Child. 1989;64848- 852
Link to Article
Pharoah  POCooke  TCooke  RWRosenbloom  L Birthweight specific trends in cerebral palsy. Arch Dis Child. 1990;65602- 606
Link to Article
Escobar  GJLittenberg  BPetitti  DB Outcome among surviving very low birthweight infants: a meta-analysis. Arch Dis Child. 1991;66204- 211
Link to Article
Illingworth  RS The diagnosis of cerebral palsy in the first year of life. Dev Med Child Neurol. 1966;8178- 194
Link to Article
Allen  MAlexander  GR Using gross motor milestones to identify very preterm infants at risk for cerebral palsy. Dev Med Child Neurol. 1992;34226- 232
Link to Article
Saint-Anne Dargassies  S Normality and normalization as seen in a long-term neurological follow-up of 286 truly premature infants. Neuropadiatrie. 1979;10226- 244
Link to Article
Saint-Anne Dargassies  S Neurodevelopmental symptoms during the first years of life. Dev Med Child Neurol. 1972;14235- 246
Link to Article
Weisglas-Kuperus  NBaerts  WSauer  PJJ Early assessment and neurodevelopmental outcome in very low birth-weight infants: implications for paediatric practice. Acta Paediatr. 1993;82449- 453
Link to Article
Futagi  YTagawa  TOtani  K Primitive reflex profiles in infants: differences based on categories of neurological abnormality. Brain Dev. 1992;14294- 298
Link to Article
Bennett  FCAvery  GBedFletcher  MAedMacDonald  Ged Developmental outcome. Neonatology: Pathophysiology and Management of the Newborn Philadelphia, Pa JB Lippincott Co1994;1367- 1386
Dubowitz  LMSLevine  MJedBennett  MJedPunt  Jed Clinical assessment of the infant nervous system. Fetal and Neonatal Neurology and Neurosurgery Edinburgh, Scotland Churchill Livingstone1988;41- 58
de Vries  LDubowitz  LM Cystic leukomalacia in preterm infants: site of lesions in relation to prognosis. Lancet. 1985;21075- 1076
Link to Article
Volpe  JJ Hypoxic-ischemic encephalopathy: neuropathology and pathogenesis. Neurology of the Newborn 3rd ed Philadelphia, Pa WB Saunders Co1995;279- 313
de Vries  LRegev  RPennock  JM Ultrasound evolution and later outcome of infants with periventricular densities. Early Hum Dev. 1988;16225- 233
Link to Article
Drillien  CM Abnormal neurological signs in the first year of life in low birth-weight infants: possible prognostic significance. Dev Med Child Neurol. 1972;14575- 584
Link to Article
Ingram  TT The early manifestations in course of diplegia in childhood. Arch Dis Child. 1955;30244- 250
Link to Article
Amiel-Tison  CGrenier  A Neurological Evaluation of the Newborn and the Infant.  New York, NY Masson1983;
Amiel-Tison  CKorobkin  REsque-Vaucouloux  MT Neck extensor hypertonia: a clinical sign of insult to the central nervous system of the newborn. Early Hum Dev. 1977;1181- 190
Link to Article
Bobath  BBobath  K Motor Development in the Different Types of Cerebral Palsy.  London, England William Heinemann Medical Books1975;
Hagberg  BLundberg  A Dissociated motor development simulating cerebral palsy. Neuropadiatrie. 1969;1187- 199
Link to Article
Prechtl  HF Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23151- 158
Link to Article
Cioni  GPrechtl  HF Preterm and early postterm motor behavior in low-risk premature infants. Early Hum Dev. 1990;23159- 191
Link to Article
Ferrari  FCioni  GPrechtl  HF Qualitative changes of general movements in preterm infants with brain lesions. Early Hum Dev. 1990;23193- 231
Link to Article
Albers  SJorch  G Prognostic significance of spontaneous motility in very immature preterm infants under intensive care treatment. Biol Neonate. 1994;66182- 187
Link to Article
Geerdink  JJHopkins  B Qualitative changes in general movements and their prognostic value in preterm infants. Eur J Pediatr. 1993;152362- 367
Link to Article
Cioni  GFerrari  FEinspieler  CPaolicelli  PBBarbani  MTPrechtl  HF Comparison between observation of spontaneous movements and neurologic examination in preterm infants. J Pediatr. 1997;130704- 711
Link to Article
Bos  AFvan Loon  AJHadders-Algra  MMartijn  AOkken  APrechtl  HF Spontaneous motility in preterm, small-for-gestational age infants, II: qualitative aspects. Early Hum Dev. 1997;50131- 147
Link to Article
Prechtl  HFEinspieler  CCioni  GBos  AFFerrari  FSontheimer  D An early marker of developing neurological deficits after perinatal brain lesions. Lancet. 1997;3491361- 1363
Link to Article
Prechtl  HFFerrari  FCioni  G Predictive value of general movements in asphyxiated full-term infants. Early Hum Dev. 1993;3591- 120
Link to Article
Ferrari  FPrechtl  HFCioni  G  et al.  Posture, spontaneous movements and behavioral state organization in infants affected by brain malformation. Early Hum Dev. 1997;5087- 113
Link to Article
Bos  AFMartijn  Avan Asperen  RMHadders-Algra  MOkken  APrechtl  HF Qualitative assessment of general movements in high-risk preterm infants with chronic lung disease requiring dexamethasone therapy. J Pediatr. 1998;132300- 306
Link to Article
Bos  AFMartijn  AOkken  APrechtl  HF Quality of general movements in preterm infants with transient periventricular echodensities. Acta Paediatr. 1998;87328- 335
Link to Article
Cioni  GBos  AFEinspieler  C  et al.  Early neurological signs in preterm infants with unilateral intraparenchymal echodensity. Neuropediatrics. 2000;31240- 251
Link to Article
Bos  AFVenema  IMBergervoet  MZweens  MJPratl  Bvan Eykern  LA Spontaneous motility in preterm infants treated with indomethacin. Biol Neonate. 2000;78174- 180
Link to Article
Dammann  OLeviton  A Duration of transient hyperechoic image of white matter in very low birth weight infants: a proposed classification. Dev Med Child Neurol. 1997;392- 5
Link to Article
Volpe  JJ Intraventricular hemorrhage in the premature infant: current concepts, pt 2. Ann Neurol. 1989;25109- 116
Link to Article
Dubowitz  LDubowitz  V The Neurological Assessment of the Preterm and Full-term Infant.  London, England William Heinemann Medical Books1981;Clinics in Developmental Medicine Vol 79
Prechtl  HF The Neurological Examination of the Full-term Newborn Infant. 2nd rev ed London, England William Heinemann Medical Books1977;Clinics in Developmental Medicine vol 63
Touwen  BCL Neurological Development in Infancy.  London, England William Heinemann Medical Books1976;Clinics in Developmental Medicine vol 58
de Vries  LSDubowitz  LMDubowitz  VPennock  JM A Colour Atlas of Brain Disorders in the Newborn.  London, England Wolfe1990;
Griffiths  R The Ability of Babies.  London, England University Press1954;
Ellenberg  JHNelson  KB Early recognition of infants at high risk for cerebral palsy: examination at age 4 months. Dev Med Child Neurol. 1981;23705- 716
Link to Article
Palisano  RRosenbaum  PWalter  SRussel  SWood  EGaluppi  B Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39214- 223
Link to Article
Metz  CE Basic principles of ROC analysis. Semin Nucl Med. 1978;8283- 298
Link to Article
Yates  F The analysis of contingency tables with groupings based on quantitative characters. Biometrika. 1948;35176- 181
Link to Article
Cioni  GPrechtl  HFFerrari  FPaolicelli  PBEinspieler  CRoversi  MF Which better predicts later outcome in full-term infants: quality of general movements or neurological examination? Early Hum Dev. 1997;5071- 85
Link to Article
Taylor  HGKlein  NMinich  NHack  M Middle-school–age outcomes in children with very low birthweight. Child Dev. 2000;711495- 1511
Link to Article
Taylor  HGKlein  NHack  M School age consequences of birth weight less than 750 grams: a review and update. Dev Neuropsychol. 2000;17289- 321
Link to Article
Hack  MTaylor  HGKlein  NMercuri-Minich  N Functional limitations and special health care needs of 10- to 14-year-old children weighing less than 750 grams at birth. Pediatrics. 2000;106554- 560
Link to Article
Einspieler  CPrechtl  HFFerrari  FCioni  GBos  A The qualitative assessment of general movements in preterm, term, and young infants: review of the methodology. Early Hum Dev. 1997;5047- 60
Link to Article

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