Does a detailed assessment of poor repertoire general movements help to identify those infants who will develop normally?

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1 Early Human Development (2006) 82, Does a detailed assessment of poor repertoire general movements help to identify those infants who will develop normally? Yayohi Nakajima a,b,1, Christa Einspieler a, *, Peter B. Marschik a, Arend F. Bos c, Heinz F.R. Prechtl a a Institute of Physiology, Developmental Physiology and Developmental Neurology, Center for Physiological Medicine, Medical University of Graz, Harrachgasse 21/5, A-8010 Graz, Austria b Department of Infant s Brain and Cognitive Development, Tokyo Women s Medical University, Japan c Department of Paediatrics, Division of Neonatology, Beatrix Children s Hospital, University Hospital Groningen, the Netherlands Accepted 20 July 2005 KEYWORDS Fidgety movements; Neurological outcome; Qualitative assessment; Prediction; Preterm infant Abstract Background: The assessment of the quality of general movements (GMs) in young infants is a reliable and valid diagnostic tool for detecting brain dysfunction early in life. Poor repertoire GMs are the most frequently observed abnormal GMs during the preterm, term and early postterm period. However, their predictive value for the neurological outcome is low. Aim: To find out whether a detailed scoring of poor repertoire GMs might lead to a better prediction of the neurological outcome. Subjects: We studied 18 preterm infants who were repeatedly videoed from birth to 22 weeks postterm age, including several recordings assessed as poor repertoire GMs. At 8 to 10 years, six children were neurologically normal, six had mild neurological abnormalities, and the remaining six were classified as cerebral palsy. Study design: Each GM globally assessed as poor repertoire was scored in details according to several aspects of neck and trunk, arm and leg movements applying Prechtl s optimality concept. Results: By and large, the detailed score of poor repertoire GMs was not related to the neurological outcome. Abbreviations: GMs, general movements; IVH, intraventricular haemorrhage; PVL, periventricular leukomalacia. * Corresponding author. Tel.: ; fax: address: christa.einspieler@meduni-graz.at (C. Einspieler). 1 Present address: Japanese Red Cross Medical Center Tokyo, Japan /$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved. doi: /j.earlhumdev

2 54 Y. Nakajima et al. Conclusion: For the clinical application of the GM assessment, it remains important to assess the fidgety movements of those infants with poor repertoire GM trajectories in order to predict their outcome. D 2005 Elsevier Ireland Ltd. All rights reserved. 1. Introduction The young human nervous system generates endogenously, i. e. without being constantly triggered by specific sensory input, a variety of motor patterns. From the many spontaneous movement patterns appearing during the course of development from foetus to young infant, the one most effective for the functional assessment of the integrity of the young nervous system are the general movements (GMs). GMs are complex, occur frequently, and last long enough to be observed properly. They involve the whole body in a variable sequence of arm, leg, neck and trunk movements. They wax and wane in intensity, force and speed, and they have a gradual beginning and end. Rotations along the axis of the limbs and slight changes in the direction of movements make them fluent and elegant and create the impression of complexity and variability [1]. While before term we call them foetal or preterm GMs [2], at term age until about 6 to 9 weeks postterm age, they are called writhing movements [3]. Even if age-related minor differences exist, GMs have, by and large, a similar appearance from early foetal life until the end of the second month postterm [2]. At 6 to 9 weeks postterm age, GMs with a writhing character gradually disappear while GMs with a fidgety character, the so-called fidgety movements, emerge. Fidgety movements are of small amplitude, moderate speed and variable acceleration of neck, trunk and limbs. They are present up to the end of the first half year of life when intentional and antigravity movements start to dominate [3,4]. GMs in low-risk, high-risk and brain-damaged infants are not different with respect to the rate of their occurrence, i. e. their quantity [5,6], but they do differ with respect to their quality [1,2,4]. GMs loose their complex and variable character and have either a poor repertoire, or are cramped synchronised, or chaotic. This holds true for the preterm and writhing GMs. Fidgety movements can be either abnormal or absent [2,4]. It is particularly the fidgety movements, which are a good predictor for the later neurological outcome. Whereas the specificity reaches 95%, sensitivity for cerebral palsy is equally high [4,7 12]. During the preterm and writhing GM period only the abnormal pattern of cramped synchronised GMs has a high predictive value for later spastic cerebral palsy [13]. The abnormal pattern of poor repertoire GMs is frequent in infants with brain ultrasound abnormalities [2,6]. GMs are called poor repertoire if the sequence of the successive movement components is monotonous and movements of the different body parts do not occur in the complex way as seen in normal GMs [2,6,12]. A number of studies reported on the development of infants with poor repertoire GMs. These studies were carried out in different atrisk groups, such as infants with periventricular leukomalacia and haemorrhages [4,10,13 15], hypoxic ischaemic encephalopathy [4,16], unilateral brain lesion [9,11], transient intraparenchymal echodensity [17], or chronic lung disease [8,18]. The majority of infants with poor repertoire GMs showed this abnormal GM pattern consistently during the preterm and writhing GM period, but only half of them remained abnormal and had an unfavourable outcome. Other infants normalised already at term age or during the first months post term and remained normal. Some infants deteriorated from poor repertoire to cramped synchronised GMs, and had an unfavourable outcome. Cramped synchronised GMs appear rigid; all limb and trunk muscles contract and relax almost simultaneously [4,6]. If we consider the neurological outcome of all cases with poor repertoire GMs reported in these 11 studies, nearly half of the children developed normally, and almost the same proportion developed minor, moderate or severe neurological impairments [4,8 12,14 18]. This clearly demonstrates that poor repertoire GMs have a low predictive value. During several discussions among experts in the field of GM assessment but also among trainees [19] the question was raised if a more detailed analysis could improve the predictive value of this abnormal GM pattern. Hence, the aim of this study was to design a detailed scoring of poor repertoire GMs and to address the following questions:! Is a detailed scoring of poor repertoire GMs related to fidgety movements and the neurological outcome?! Does a detailed scoring of poor repertoire GMs document an improvement or deterioration within the individual developmental trajectory of the poor repertoire GMs? 2. Subjects and methods 2.1. Subjects The study group consisted of 18 infants (five girls and 13 boys). All were born preterm and admitted at the Neonatal Intensive Care Unit of the Beatrix Children s Hospital, University Hospital Groningen, the Netherlands between 1992 and As the aim of the study was to apply a detailed scoring of poor repertoire GMs and to relate this detailed scoring to the outcome, all study cases had to have poor repertoire GMs. In addition, we had to make sure that a normal outcome, mild neurological impairments, and cerebral palsy were proportionally represented. One of the authors (AFB) selected videos of infants, who were originally prospectively studied, and applied the following selection criteria: (a) a series of video recordings of GMs from birth to, at most, 22 weeks post term age, including several recordings assessed as poor repertoire GMs; and (b) the neurological outcome at 8 to 10 years,

3 Does assessment of poor repertoire GMs identify infants who will develop normally? 55 which was normal in six children; six had mild neurological impairments according to Touwen s neurological examination [20], such as problems in the sensorimotor apparatus, co-ordination of the extremities, fine-manipulative ability or dyskinesia; the remaining six infants had cerebral palsy (three diplegia, two hemiplegia and one dystonic hyperkinetic cerebral palsy; Table 1). The infants gestational age at birth was between 25 and 33 weeks with a median of 28 weeks; the birth weight ranged from 595 to 1550 g (median: 942 g); 10 infants were appropriate-for-gestational age and eight were small-for-gestational age. In addition, the result of serial brain ultrasound recordings during preterm age was known. Only one infant (case 2, Table 1) had normal brain ultrasound findings. Prolonged flares were seen in 15 infants; three were associated with grade 1 IVH; one infant only had grade 1 IVH. Case 18 (Table 1) had cystic leukomalacia (grade 2 PVL) [21]. All infants were videoed between 4 and 10 times (median: seven recordings) during their preterm age until 8 weeks post term. One to two recordings within 3 to 5 months revealed normal (n =7), abnormal (n =4) or an absence of fidgety movements (n =7) (Tables 1 and 2). All infants participated in previous studies [7 10,14,17,18,22] with informed consent of the parents and according to the standards set by the local research ethics committee Video recording and analysis of poor repertoire GMs All infants were videoed during active wakefulness while lying supine in the incubator or the cot. The infants wore a small nappy or a short sleeved bodysuit [23]. Before a postmenstrual age of 34 weeks, the infants were fed continuously by gavage feeding; after 34 weeks they were fed an hour before the observation session. Video recording was started within the first or second week of life, exceptional (n =3) in the third week. The assessment was based on almost weekly recordings of at least three GMs, the latter lasting some 5 min in total. After a pilot study on five other preterm infants with poor repertoire GMs, a scoring sheet was designed in order to describe and differentiate the features of poor repertoire GMs in more detail (see Appendix A). Applying Prechtl s optimality concept [24], the majority of the 17 items was scored 2 to 0, a high score indicating an optimal performance. A maximum score of 34 would have indicated the most optimal GM performance but, of course, was not expected from an infant with abnormal, i. e. poor repertoire, GMs. Therefore, we calculated the reduced optimality score (maximum score = 34 minus summary score) indicating the degree of deviation from the optimum. The higher the reduced optimality score was, the worse were the GMs. To document the improvement or deterioration of poor repertoire GMs the difference between the last and the first reduced optimality score within a poor repertoire GM trajectory was used Statistics Using SPSS 11.0, we first calculated the data for the weekly recordings, but also combined our assessments into three age periods: early preterm period (27 to 31 weeks), late preterm period (32 to 37 weeks) and writhing movement period (38 weeks postmenstrual age to 8 weeks post term). As the data were not normally distributed we used the Spearman Rank Correlation, the Kruskal Wallis test, and the Wilcoxon test. For the nominal variables the Pearson Chi-Square and the Sign test were used. A two-tailed p- value of less than 0.05 was considered significant. 3. Results 3.1. Interobserver agreement All recordings were analysed off-line by AFB (from 1992 to 1995) and CE (during 2004; not knowing the child s history) for the global assessment with an interscorer agreement of 98%. The detailed scoring was performed by YN, PBM and CE without knowing the child s history and its neurological outcome with an interscorer agreement for the different age periods between 82% and 100%. These objectivity data are in the line with previous results [2,12,19] GM trajectories and outcome Due to the gestational age at birth, only 12 infants were recorded during the early preterm period. Thirty-three of their 34 video recordings (97%) were assessed as poor repertoire. During the late preterm period all infants were recorded. From these 58 recordings, 41 (71%) proved to be poor repertoire. During the writhing movement period the infants were less often videoed; 36 recordings were available. Twenty-one of them (58%) were assessed as poor repertoire GMs. All but one infant (case 7, Table 1) had poor repertoire GMs from the first recording onwards. Poor repertoire GMs were usually present for several weeks (median: 9, IQR: 4 to 15 weeks). Consistent poor repertoire GMs were seen in nine infants. Table 1 indicates that their fidgety movements were either normal (cases 1 and 5), abnormal (cases 7, 10, 11 and 12), or absent (cases 9, 16 and 17). Also their outcome varied from normal to cerebral palsy (Table 1). Three other infants with a poor repertoire GM trajectory (cases 2, 4 and 8) had transiently chaotic GMs (Table 1). Chaotic GMs are movements of large amplitude and occur in a chaotic order without any fluency or smoothness [2,7,25]. The outcome of these infants was normal in two and mildly abnormal in the third child. The poor repertoire GMs of four infants (cases 13, 14, 15 and 18) deteriorated into cramped synchronised GMs in the late preterm period (Table 1). None of these infants had fidgety movements and their outcome was cerebral palsy. Only in two infants (cases 3 and 6) the GMs normalised at 34 weeks and were followed by normal fidgety movements and a normal outcome Detailed scoring of poor repertoire GMs and outcome Some infants with poor repertoire GMs had also cramped but not synchronised movements of their arms or legs. Whereas these cramped movements were hardly observed during the early preterm period (one out of 12 infants recorded), they

4 56 Table 1 Individual developmental trajectories of GMs including the reduced optimality score for poor repertoire GMs, presence and quality of fidgety movements and neurological outcome at 8 to 10 years Case Weeks postmenstrual age PR,10 PR,15 PR,15 PR,19 PR,16 PR,20 PR,18 N N 2 PR,9 PR,14 Ch PR,9 PR,13 PR,24 N N 3 PR,8 PR,10 N N N N N N N N N 4 PR,6 PR,8 Ch Ch PR,22 PR,25 N N 5 PR,9 PR,6 PR,11 PR,6 PR,10 PR,17 PR,14 PR,11 N N 6 PR,15 PR,13 N N N N N N 7 N PR,10 PR,21 PR,22 PR,22 PR,19 AF MA 8 PR,8 PR,5 N PR,9 PR,7 Ch Ch Ch PR,18 N MA 9 PR,13 PR,12 PR,13 PR,15 PR,11 PR,19 PR,21 PR,19 F- MA 10 PR,11 PR,4 PR,16 PR,21 PR,21 PR,20 AF MA 11 PR,12 PR,4 PR,4 PR,11 PR,8 PR,9 PR,21 PR,22 AF MA 12 PR,11 PR,7 PR,9 PR,8 PR,6 PR,22 PR,26 PR,23 AF MA 13 PR,8 PR,10 PR,17 CS CS CS CS CS F- CP 14 PR,11 PR,17 PR,6 PR,11 PR,14 CS CS F- CP 15 PR,11 PR,15 PR,16 CS CS CS F- CP 16 PR,6 PR,7 PR,24 PR,18 F- CP 17 PR,9 PR,10 PR,3 PR,8 PR,8 PR,12 PR,19 PR,24 PR,22 F- CP 18 PR,9 PR,8 PR,18 CS CS CS CS F- CP The three different age periods are marked grey or white. FMs, fidgety movements; PR, poor repertoire; CS, cramped synchronised; Ch, chaotic; N, normal; AF, abnormal fidgety movements; F-, absence of fidgety movements; MA, mildly abnormal according to Touwen s neurological assessment [20]; CP, cerebral palsy. FMs Outcome Y. Nakajima et al.

5 Does assessment of poor repertoire GMs identify infants who will develop normally? 57 Table 2 Fidgety movements and neurological outcome at 8 to 10 years Fidgety movements were frequently present during the later preterm period (13 out of 18 infants, Sign test, p b0.01). All 12 infants assessed as poor repertoire writhing movements had cramped components. This finding was, however, neither related to the quality of the fidgety movements nor to the outcome (Pearson Chi-Square, n.s.). The weekly assessed reduced optimality score for poor repertoire GMs (Table 1) was neither related to the quality of the fidgety movements nor to the neurological outcome (Kruskal Wallis test, n. s.). The same held true for the average reduced optimality score for the three different age periods. Independent of the outcome, the higher the reduced optimality score in the early preterm period was, the higher it was in the late preterm period (r = 0.68; p b 0.05). However, both scores were not related to the detailed score of the poor repertoire writhing movements. Independent of the duration of a poor repertoire GM trajectory, a large deterioration between the first and the last reduced optimality score indicated an unfavourable neurological outcome (Wilcoxon test, p b 0.05). The reduced optimality score deteriorated 9 points (median, IQR: 6 to 13 points) in children who developed mild neurological impairments or cerebral palsy. Children who developed normally had almost no difference between the first and the last reduced optimality score (median: 3, IQR: 1 to 10 points) Fidgety movements and outcome As indicated in Table 2 it was only the fidgety movements that predicted specifically the outcome (Pearson Chi- Square, p b0.001). 4. Discussion Outcome Normal (n =6) Mild neurological impairments (n =6) Normal (n =7) Abnormal (n =4) Absent (n =7) Cerebral palsy (n =6) Poor repertoire GMs are frequently seen among very young infants [26]. They can be followed by normal, abnormal, or an absence of fidgety movements and thus a normal or impaired neurological outcome [4]. Hence, their predictive value is low. On the other hand, poor repertoire GMs clearly demonstrate that the infant s nervous system is not in an optimal condition at the time of the recording. The definition of poor repertoire GMs [2,4,12] is broad and also defined by exclusionary criteria, such as the lack of complexity. Therefore, we considered it worthwhile to perform a detailed scoring of each poor repertoire GM and hoped for an improvement of its predictive value. Unfortunately, we did not succeed. The reduced optimality score did not predict the neurological outcome. Only a deterioration of 9 or more points from the first to the last video recording of the poor repertoire GM trajectory was related to an unfavourable outcome. However, detailed scoring did not allow a re-synthesis from the details to the total picture as too much Gestalt was lost with this semi-quantitative approach. Several attempts have been made to semiquantify the quality of preterm and writhing GMs. Ferrari et al. [6] published a list of criteria including amplitude, speed, movement character, sequence, range in space, onset and offset of GMs, but only used it to semi-quantify the GM quality of infants with brain malformations [25]. Einspieler [27] adapted this scoring system by calculating a motor optimality score, which was useful for further statistical application. Our detailed scoring (see Appendix A) was based on those previous attempts but modified according to the needs to assess poor repertoire GMs only. Some infants with poor repertoire GMs had additional cramped components. As these stiff movements were certainly not synchronised, they could be easily distinguished from another abnormal GM pattern, the cramped synchronised GMs. Interestingly, cramped components were rarely seen in the poor repertoire GMs of young preterm infants, i.e. before 32 weeks. Thereafter, the presence of these components increased and was present in all poor repertoire writhing GMs irrespective of the neurological outcome. Beside Prechtl s method of GM assessment with his discrimination between normal and abnormal age-specific GM patterns [1,2], various attempts to sub-classify GMs have been reported. Van Kranen-Mastenbroek et al. [28] classified GMs into five sub-types according to the speed, fluency, and the variability of movements. These sub-types were different between appropriate- and small-for-gestational age infants but were not related to the outcome at 9 months. Different degrees of fluency, spacio-temporal variability and sequencing were used by Kakebeeke et al. [29,30] to sub-classify GMs, but again were not related to the neurological outcome. Hadders-Algra and co-workers defined the limited presence of complexity, a limited variation in sequencing of the various body parts and the absence of fluency as dmildly abnormalt [31 33]. This description might be equivalent to poor repertoire GMs. Based on EMG recordings of 16 infants Hadders-Algra et al. sub-classified mildly abnormal GMs into fragmented or tense GMs or both. Tense GMs were only present in two infants around term age, one infant developing a cerebral palsy and the other neurologically normal. Fragmented GMs were reported in another six infants during their late preterm period as well as during term age; again their outcome varied from normal to cerebral palsy [31]. Recent reviews by Hadders-Algra confirmed that dmildly abnormalt GMs have a low predictive value before the third month. Only afterwards, they are related to the development of minor neurological dysfunction, attention deficit hyperactivity disorder, and aggressive behaviour [33]. A detailed analysis of the different aspects and components of poor repertoire GMs could not improve the predictive value of this abnormal GM pattern. The global assessment of the different age-specific GM patterns is based on visual Gestalt perception. In his paper dgestalt Perception as a Source of Scientific KnowledgeT the Nobel prize laureate Konrad Lorenz pointed out that dgestalt perception is able to take into account a greater number of individual details and more relationships between these than in any rational calculationt [34]. Hence, it was not surprising that a detailed

6 58 Y. Nakajima et al. scoring of a specific movement pattern did not add substantial knowledge to the assessment of this pattern. As a conclusion: GM assessment is a worthwhile method to be used in combination with neuroimaging. For the clinician applying the GM assessment it remains mandatory to assess the fidgety movements of those infants with poor repertoire preterm or writhing GMs as only the presence or absence of fidgety movements have the known high predictive value for the neurological outcome [2,4,12]. Acknowledgements Peter B. Marschik was supported by the Austrian Science Fund (FWF) project number P16984-W02. We appreciate the help of R.M van Asperen, D.M de Leeuw, H.F. van Duinen and A.C.Roodenburg, who assisted in recording the infants on videotape. Appendix Items used for the detailed scoring of poor repertoire GMs applying Prechtl s optimality concept [24]. Rotatory components were assessed for movements of neck, trunk, arms and legs separately. In addition, movement amplitude, speed, onset, offset, cramped components, and a tremulous character were assessed for upper and lower limbs, respectively. The spatial component was assessed for upper limbs only. Scores are given in brackets.! Rotatory components: present, fluent and elegant (2); few rotations (1); no rotations (0).! Movement amplitude: variable, full range (2); predominantly small range (1); predominantly large range (1); mainly medium range (1).! Speed: variable (2); monotonously slow (1); monotonously fast (1); mainly medium speed (1).! Space: from horizontal to vertical plane (2); mainly horizontal, on the surface (1); mainly vertical, arms lifted (1).! Onset: smooth (2); minimal fluctuations (1); abrupt (0).! Offset: smooth (2); minimal fluctuations (1); sudden release (0).! Tremulous character: absent (2); unilaterally present (1); bilaterally present (0).! Cramped components: absent (2); unilaterally present (1); bilaterally present (0). 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