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Specific characteristics of abnormal general movements are associated with functional outcome at school age
Early Human Development 95 (2016) 9–13
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Specific characteristics of abnormal general movements are associated with functional outcome at school age Elisa G. Hamer a,c, Arend F. Bos b, Mijna Hadders-Algra a,⁎ a b c
Department of Pediatrics, Division of Developmental Neurology, University of Groningen, University Medical Center, Groningen, The Netherlands Department of Pediatrics, Division of Neonatology, University of Groningen, University Medical Center, Groningen, The Netherlands Department of Neurology, Radboud University Medical Center, Nijmegen, The Netherlands
a r t i c l e
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Article history: Received 12 August 2015 Received in revised form 13 January 2016 Accepted 19 January 2016 Keywords: General movements High risk infants Cerebral palsy Follow-up School age Neurodevelopment
a b s t r a c t Background: Assessing the quality of general movements (GMs) is a non-invasive tool to identify at early age infants at risk for developmental disorders. Aim: To investigate whether specific characteristics of definitely abnormal GMs are associated with developmental outcome at school age. Study design: Observational cohort study (long-term follow-up). Subjects: Parents of 40 children (median age 8.3 years, 20 girls) participated in this follow-up study. In infancy (median corrected age 10 weeks), the children (median gestational age 30.3 weeks; birth weight 1243 g) had shown definitely abnormal GMs according to Hadders-Algra (2004). Information on specific GM characteristics such as the presence of fidgety movements, degree of complexity and variation, and stiff movements, was available (see Hamer et al. 2011). Outcome measures: A standardised parental interview (presence of CP, attendance of school for special education, Vineland Adaptive Behavior Scale to determine functional performance) and questionnaires (Developmental Coordination Disorder Questionnaire [DCD-Q] to evaluate mobility and Child Behavior Checklist to assess behaviour) were used as outcome measures. Results: Six children had cerebral palsy (CP), ten children attended a school for special education, and eight children had behavioural problems. Both the absence of fidgety movements and the presence of stiff movements were associated with CP (p = 0.001; p = 0.003, respectively). Stiff movements were also related to the need of special education (p = 0.009). A lack of movement complexity and variation was associated with behavioural problems (p = 0.007). None of the GM characteristics were related to DCD-Q scores. Conclusions: The evaluation of fidgety movements and movement stiffness may increase the predictive power of definitely abnormal GMs for motor outcome — in particular CP. This study endorses the notion that the quality of GMs reflects the integrity of the infant's brain, assisting prediction of long-term outcome. © 2016 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In early infancy, the assessment of general movements (GMs) is the best clinical predictor for neuromotor development in high risk infants [1,2]. GMs are endogenously generated spontaneous movements and their quality reflects the integrity of the infant's brain [3]. GMs are present from early foetal life until goal-directed motor behaviour arises, Abbreviations: ATNR, Asymmetric tonic neck reflex; CBCL, Child Behavior Checklist; COPCA, Coping with and caring for infants with special needs; CP, Cerebral palsy; DCD-Q, Developmental Coordination Disorder Questionnaire; DSM, Diagnostic and Statistical Manual of Mental Disorders; GMs, General movements; VABS, Vineland Adaptive Behavior Scale. ⁎ Corresponding author at: University Medical Center Groningen, Department of Developmental Neurology, Hanzeplein 1, 9713 GZ Groningen, The Netherlands. Tel.: +31 50 3614247; fax: +31 50 3619158. E-mail address: [email protected] (M. Hadders-Algra).
http://dx.doi.org/10.1016/j.earlhumdev.2016.01.019 0378-3782/© 2016 Elsevier Ireland Ltd. All rights reserved.
i.e., typically around 4 months corrected age. Normal GMs are complex movements in which all body parts participate; they are characterised by variation [4]. In abnormal GMs, complexity and variation are reduced. The presence of definitely abnormal GMs is associated with perinatal brain lesions and developmental disorders, including cerebral palsy (CP) [1,5]. Recently, we were able to demonstrate that specific movement characteristics might enhance prediction of definitely abnormal GMs (classified according to Hadders-Algra, 2004 [4]) around 3 months of age, i.e., so-called fidgety-GM age [6]. Both the absence of fidgety movements and the presence of predominantly stiff movements were associated with a higher chance of CP at 18 months. None of the other movement characteristics investigated were associated with functional motor performance or cognitive outcome at that age. It is known that associations between early neurological signs and developmental outcome may change with age, as the child's brain
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experiences significant changes during development [7,8]. Also, the age of 18 months corrected age, used in Hamer et al. 2011 [6], is relatively early for the diagnosis of CP. For instance, the Surveillance of Cerebral Palsy Europe only includes children older than 5 years of age [9]. Moreover, 18 months corrected age is early in terms of outcome in other domains, e.g., functional and behavioural outcomes. The primary aim of the present study is therefore to investigate whether the specific characteristics of definitely abnormal GMs that were related to motor outcome at 18 months, i.e., fidgety movements and predominantly stiff movements (further denoted as stiff movements), are related to developmental outcome at school age. In addition, we studied whether the other movement characteristics studied in Hamer et al. [6], such as the degree of complexity and variation, were associated with outcome at school age.
2. Methods This study is part of the VIP-project (Dutch; Vroegtijdig Interventie Project), a randomised controlled trial studying the effects of the early intervention program COPCA (Coping with and Caring for infants with special needs — a family centred program [10]) in comparison to traditional infant physiotherapy. The developmental outcome in the two intervention groups was similar [11]. Inclusion in the VIP-project was based on the presence of definitely abnormal GMs [4]. The general movement assessment includes at least 5 min of video recording of spontaneous motor behaviour in an awake, non-crying state. As previously reported, MHA and AFB reanalysed the video recordings of the VIP infants (n = 46, median age at GM assessment 10.3 [range 9–13] weeks corrected age) with respect to the following characteristics: presence of fidgety movements, degree of complexity and variation, presence of cramped-synchronised GMs, stiff or jerky movements, and spontaneous occurrence of the asymmetric tonic neck reflex (ATNR) pattern (Table 1) [6]. In addition, we computed a movement abnormality score (MAS; range 0–2) based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
2.1. Follow-up assessment at school age We sent an invitation letter for the present follow-up study to the parents whose children participated in the follow-up assessment at 18 months (n = 44). For the follow-up at school age, we used a structured parental telephone interview (Vineland Adaptive Behavior Scale [VABS], medical history, educational achievement) and parental questionnaires (Developmental Coordination Disorder Questionnaire [DCD-Q] and Child Behavior Check List [CBCL]). During the interview the parents specified the child's educational achievement, including the need of special education. Notwithstanding the fact that the Dutch government is in favour of inclusive education, children with special needs often attend schools for special education. Both the parents and the interviewer (EGH) were unaware of the specific general movement characteristics of the child.
Using the VABS we assessed the child's functional status in four domains: communication, daily living skills, socialisation and motor skills [12]. The four domains can each be subdivided in 2–4 subdomains, e.g., expressive communication, play and leisure time, and fine motor skills. We calculated the scores for each domain (n = 4) and subdomain (n = 11). The VABS has proven to be reliable and valid in both typically developing children and in children with developmental disorders, such as CP [13,14]. The domain communication, daily living skills and socialisation can be applied until 18 years of age. The motor skill domain is designed for children up to 6 years of age and for older children with motor impairments. We used the DCD-Q to assess mobility [15]. This short questionnaire covers 17 items on control during movement, fine motor skills/ handwriting, gross motor skills, and general coordination. A higher total score indicates worse performance. The DCD-Q is reliable and valid, as is the Dutch translation [16]. The CBCL is a widely used parental questionnaire containing 113 items concerning the child's behaviour [17]. The scores were dichotomised as normal or borderline vs. in the clinical range (i.e., above the 97th percentile) on the following six Diagnostic and Statistical Manual of Mental Disorders (DSM) oriented scales: affective, anxiety, somatic, attention deficit/hyperactivity, oppositional defiant, and conduct problems. The reliability and validity of the Dutch version of the CBCL are good [17,18]. The Medical Ethics Committee of the University Medical Center Groningen approved the study (trial number NL39954.042.12). 2.2. Data analysis Statistical analysis was performed using SPSS version 20. We used non-parametric tests since the data did not show a normal distribution. Regression analysis was used to control for type of intervention. To adjust for multiple comparisons, differences with a p-value ≤ 0.01 were considered to be statistically significant. Psychometric properties and confidence intervals (CIs) were calculated with the use of MedCalc statistical software (version 11.6, Ostend, Belgium). 3. Results We obtained follow-up data from 40 children (91%, median age; 8 years + 4 months; Table 2). The participating children did not differ from the non-participating children in baseline characteristics (sex, gestational age, birth weight, educational level of the parents, maternal age at birth, type of intervention or CP at 18 months CA — data not shown). 3.1. GM characteristics: Motor and functional outcome Six parents reported that their child had CP. Both the absence of fidgety movements and the presence of stiff movements were associated with CP (Table 3, Fisher's exact test; p = 0.001 and p = 0.003, respectively). The absence of fidgety movements and the presence of stiff
Table 1 Specific GM characteristics. Fidgety movements Complexity and variation of the movements Cramped-synchronised movements ATNR pattern Stiff or jerky movement quality
Fidgety movements are circular movements of small amplitude and moderate speed and variable acceleration of neck, trunk and limbs in all directions. Complex movements are movements during which the infant actively produces frequent changes in direction of the participating body parts. The GM variation represents the temporal variation of the movements. This means that across time, the infant produces continuously new movement patterns. Cramped-synchronised movements appear rigid and lack normal smooth and fluent character; all limb and trunk muscles contract and relax almost simultaneously. The asymmetric tonic neck reflex (ATNR) consists of the extension of the arm and leg on the side to which the head is turned, with flexion of the contralateral limbs. GM fluency indicates the presence of smooth, supple and graceful movements. Stiff movements and jerky movements are a type of non-fluent motor behaviour. Non-fluent movements can be predominantly jerky, stiff or consist of a mix of jerky and stiff movements.
For details on the scoring of the specific GM-characteristics see Hamer et al. [6].
E.G. Hamer et al. / Early Human Development 95 (2016) 9–13
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0.075, p = 0.154, p = 0.162, and p = 1.000, respectively) or to the VABS and DCD-Q scores (data not shown).
Table 2 Group characteristic. Background
n = 40
Gestational age in weeks + days, median (range) Preterm (b37 weeks), n Birth weight in grams, median (range) Sex, n of girls Severe brain lesion, na Follow-up Age at follow-up in years + months, median (range) Diagnosis of CP, n Attendance of special education, n VABS, median (range)⁎ Communication Daily living skills Socialisation Motor skills DCD-Q scores, median (range)⁎⁎ Behavioural problems (according to the CBCL), n⁎⁎
30 + 2 (25 + 0 − 40 + 0) 36 1243 (635–4750) 20 5 8 + 4 (7 + 6 − 10 + 1) 6 10 230 (185–246) 268 (51–314) 170 (113–184) 144 (15–146) 64 (33–85) 8
Note: The VABS scores of children with missing DCD-Q or CBCL scores did not differ from those with available DCD-Q or CBCL scores. a Severe brain lesion: periventricular leukomalacia grades 3 and 4, periventricular haemorrhagic infarction, or thalamus/basal ganglia lesion (see Hamer et al., 2011) [6]. ⁎ n = 39. ⁎⁎ n = 34.
3.2. GM characteristics: Type of education and behavioural outcome The attendance of special education (n = 10, including 6 with CP) was associated with the presence of stiff movements (47% vs. 9%, p = 0.009), not with the other movement characteristics (Table 3). The MAS was also associated with the need of special education (Fig. 1b, MAS0-1 15% vs. MAS2 71%; p = 0.006). Eight children had atypical and clinically relevant CBCL scores; three of them had CP and attended a school for special education. The other five children had no CP and attended mainstream education. One movement characteristic was associated with behavioural outcome; children with a total lack of GM complexity and variation more often had clinically abnormal CBCL scores (55% vs. 9%, p = 0.007) compared to children whose GMs showed some complexity and variation. The lack of movement complexity and variation was not associated with abnormal scores on one of the subscales. None of the above mentioned associations were influenced by the type of intervention received in infancy (data not shown). 4. Discussion
movements were not related to the VABS scores or the DCD-Q scores (Table 3). Children with a MAS of 2 more often had CP (71% vs. 3%, Fig. 1a, p = 0.0005) and had lower VABS motor skills (total and gross motor skills, Fig. 2) and personal scores than children with lower MAS scores (Table 3). The specificity and positive predictive value of a MAS of 2 points was higher than that of the specific signs, i.e., the absence of fidgety movements and the presence of stiff movements, alone (Table 4). The degree of complexity and variation (some [n = 27] vs. none [n = 13]), the presence of the ATNR pattern (n = 11), the presence of jerky movements (n = 29), and the presence of cramped-synchronised movements (n = 5) were not related to the development of CP (p =
Our study indicates that in children with definitely abnormal general movements the absence of fidgety movements and the presence of stiff movements are related to worse functional motor outcome at school age, including CP. The presence of stiff movements was also related to the need of special education. In addition, a lack of complexity and movement variation was associated with the presence of behavioural problems. The association between the absence of fidgety movements and the presence of stiff movements and CP replicated the findings at 18 months of age [6]. It has been previously shown that the absence of fidgety movements is related to CP [1–5], but not to intelligence at school age [19], which is in line with our results. Our finding regarding the presence of stiff movements corresponds to Groen et al. (2005), who
Table 3 GM characteristics and outcome at school age. FM present
FM absent
p-value
Not stiff
Stiff present
p-value
MAS 0-1
MAS 2
p-value
n = 31
n=9
n = 23
n = 17
n = 33
n=7
Cerebral palsy Special education
1 (3%) 5 (16%)
5 (56%) 5 (56%)
0.001* 0.029
0 (0%) 2 (9%)
6 (35%) 8 (47%)
0.003* 0.009*
1 (3%) 5 (15%)
5 (71%) 5 (71%)
0.0005* 0.006*
VABS domains Communication Daily living skills Socialisation Motor skills VABS subdomains C — receptive C — expressive C — written D — personal D — domestic D — community S — interpersonal relationships S — play and leisure time S — coping skills M — gross motor M — fine motor
n = 30 233 (200–246) 270 (215–314) 171 (131–184) 144 (127–146)
n=9 228 (185–243) 250 (51–283) 163 (113–178) 112 (15–146)
0.284 0.054 0.384 0.042
n = 23 229 (223–301) 268 (223–301) 171 (131–183) 144 (132–146)
n = 16 236 (185–244) 264 (51–314) 168 (113–184) 141 (15–146)
0.921 0.437 0.746 0.035
n = 32 231 (200–246) 270 (215–314 171 (131–184) 144 (127–146)
n=7 230 (185–243) 215 (51–283) 163 (113–176) 77 (15–145)
0.462 0.049 0.255 0.007*
45 (39–46) 148 (134–152) 40 (18–52) 158 (141–169) 37 (15–52) 71 (44–93) 64 (54–69) 62 (50–66) 44 (20–55) 84 (72–84) 61 (49–62)
44 (35–46) 148 (134–151) 35 (0–48) 153 (27–164) 32 (6–42) 65 (18–88) 64 (58–69) 57 (18–66) 42 (31–48) 52 (94–84) 60 (11–62)
0.191 0.831 0.159 0.039 0.159 0.402 0.883 0.658 0.460 0.025 0.107
45 (39–46) 148 (138–152) 39 (31–52) 158 (141–167) 38 (32–50) 67 (44–92) 63 (56–67) 62 (50–66) 44 (20–55) 84 (72–84) 62 (54–62)
45 (35–46) 148 (134–151) 40 (0–51) 156 (27–169) 36 (6–52) 75 (18–93) 64 (54–69) 61 (18–66) 43 (29–53) 82 (4–84) 60 (11–62)
0.989 0.582 0.767 0.239 0.043 0.810 0.301 0.275 0.789 0.035 0.050
45 (39–46) 148 (134–152) 40 (18–52) 158 (141–169) 37 (15–52) 69 (44–93) 64 (54–69) 62 (50–66) 44 (20–55) 84 (72–84) 61 (49–62)
44 (35–46) 148 (134–151) 38 (0–48) 140 (27–161) 32 (6–42) 71 (18–88) 64 (58–69) 57 (18–66) 42 (31–45) 49 (4–84) 56 (11–62)
0.378 0.734 0.359 0.010* 0.122 0.578 0.707 0.507 0.287 0.004* 0.037
DCD-Q Total score
n = 28 67 (44–85)
n=7 44 (25–70)
0.020
n = 19 64 (44–85)
n = 16 63 (25–71)
0.133
n = 29 65 (44–85)
n=6 41 (25–70)
0.012
CBCL DSM clinical score
n = 28 5 (18%)
n=6 4 (57%)
0.055
n = 19 4 (21%)
n = 16 5 (31%)
0.700
n = 29 5 (17%)
n=6 4 (67%)
0.027
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a. Diagnosis of CP
b. Attendance of special education
Fig. 1. a. Diagnosis of CP. 1b. Attendance of special education. Association between movement abnormality score (MAS) and a) CP and b) attendance of school for special education. The MAS (range 0–2) is based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
Fig. 2. GM characteristics and VABS motor skills' total score. Data are presented as median values (horizontal bars), interquartile ranges (boxes) and ranges (vertical lines) with outliers (circles).
reported that the (rare) occurrence of predominantly stiff movements at fidgety age was associated with an unfavourable neurological outcome [20]. The additional associations between a) the presence of stiff movements and the need of special education and b) a higher MAS and a lower VABS personal domain score suggest that the predictive value of these characteristics extends beyond the motor domain. The notion that GMs are not only predictive for motor outcome is supported by others; several studies reported for instance an association between GM quality and cognition at school age [19,21,22]. Our finding that a lack of complexity and variation is associated with behavioural problems is partly in line with previous studies showing a relation between reduced complexity and variation and attention problems [23,24]. In contrast to previous studies, we found an
unspecific association: a lack of movement complexity and variation was not associated with specific behavioural problems. Hitzert et al. (2014) reported a similar unspecific association between monotonous movements and behavioural problems in term born infants [22]. These findings support the notion that movement complexity and variation, which may be considered as two forms of movement variation [4], reflect the overall integrity of neural connectivity, especially of periventricular connectivity [2]. A reduced connectivity increases the vulnerability for impairments in several domains, including the likelihood of the development of behavioural problems [25]. This study illustrates the importance of follow-up beyond preschool age. At 18 months CA, ten children were diagnosed with CP [6]. At school age, one of these children was lost to follow-up, and three
Table 4 Psychometric properties of FMs and stiff movements. Cerebral Palsy
Sensitivity
(95% CI)
Specificity
(95% CI)
PPV
(95% CI)
NPV
(95% CI)
Abscence of fidgety movements Presence of stiff movements MAS 2 (absence of FMs and presence of stiff movements)
83 100 83
(36–100) (54–100) (36–100)
88 68 94
(73–97) (49–83) (80–99)
56 35 71
(21–86) (14–62) (29–96)
97 100 97
(83–100) (85–100) (84–99)
Special education
Sensitivity
(95% CI)
Specificity
(95% CI)
PPV
(95% CI)
NPV
(95% CI)
Abscence of fidgety movements Presence of stiff movements MAS 2 (absence of FMs and presence of stiff movements)
50 80 50
(19–81) (44–97) (19–81)
87 70 93
(69–96) (51–85) (78–99)
25 47 71
(13–41) (23–72) (29–96)
84 91 85
(66–95) (72–99) (68–95)
The MAS (range 0–2) is based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
E.G. Hamer et al. / Early Human Development 95 (2016) 9–13
other children ‘outgrew’ CP — according to their parents' report. In addition, the need for special education and behavioural outcome could not be determined at a younger age. Associations between early risk factors and developmental outcome may become stronger with increasing age; some dysfunctions may only emerge when the brain develops new functions, a phenomenon which is especially encountered in high risk infants, such as infants born preterm [8]. The development of the young nervous system may also resolve early neurological abnormalities. Within our cohort, eight of the ten children with CP at 18 months corrected age had shown stiff GMs [6]. The present study indicates that all six children who were indeed diagnosed with CP – at school age – had shown stiff GMs. This study further underlines that the presence of more abnormal signs is associated with a higher risk for developmental problems — a well-known phenomenon in paediatric neurology. For example, in our study group the presence of stiff movements was associated with high sensitivity and negative predictive values, but its positive predictive value was low. However, in combination with the absence of fidgety movements (MAS score of 2 points), its positive predictive value for CP and attendance of a school for special education rose. On the other hand, it may also be good to realise that the majority of our study group did not develop CP, had no behavioural problems and was not in need of special education — despite the fact that they had definitely abnormal GMs and most of them were born below 32 weeks gestational age. This underscores the notion that the prediction of developmental outcome in early infancy is notoriously difficult [2]. The high follow-up rate, the long-term follow-up and the detailed analysis of movement characteristics are the strengths of this study. The most important limitation of the study is the small sample size; this limits generalisability — including generalisability of predictive values. The use of parental questionnaires may be considered as another limitation. For example, very mild forms of CP may have been unreported. However, parents outperform professionals in providing information on functional outcome in daily life. Lastly, we regard the ceiling effect of the motor skills domain of the VABS as a limitation. This may explain why we merely found trends between GM characteristics (absence of fidgety movements and presence of stiff movements) and VABS motor skill scores. However, the MAS was significantly associated with the total and gross motor outcome measured with the VABS. We conclude that the predictive power of definitely abnormal general movements for motor outcome – in particular CP – may be enhanced by including the evaluation of fidgety movements and movement stiffness. This study endorses the notion that the quality of general movements reflects the integrity of the infant's brain, and assists prediction of long-term outcome. Conflict of interest None declared. Acknowledgements We are grateful to all the children and their families for participating in the VIP project. The study was financially supported by the Johanna KinderFonds, Stichting Fonds de Gavere, the Cornelia Stichting and the Graduate School for Behavioural and Cognitive Neurosciences (BCN).
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EGH was financially supported by the Junior Scientific Masterclass Groningen and the BCN. None of the funders were involved in the study design, data collection, data analysis, and manuscript preparation or publication decisions. References [1] Bosanquet M, Copeland L, Ware R, Boyd R. A systematic review of tests to predict cerebral palsy in young children. Dev Med Child Neurol 2013;55:418–26. [2] Hadders-Algra M. Early diagnosis and early intervention in cerebral palsy. Front Neurol 2014;5:185. [3] Einspieler C, Prechtl HF. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev 2005;11:61–7. [4] Hadders-Algra M. General movements: a window for early identification of children at high risk for developmental disorders. J Pediatr 2004;145:S12–8. [5] Prechtl HFR, Einspieler C, Cioni G, Bos AF, Ferrari F, Sontheimer D. An early marker for neurological deficits after perinatal brain lesions. Lancet 1997;349:1361–3. [6] Hamer EG, Bos AF, Hadders-Algra M. Assessment of specific characteristics of abnormal general movements: does it enhance the prediction of cerebral palsy? Dev Med Child Neurol 2011;53:751–6. [7] Nelson KB, Ellenberg JH. Children who “outgrew’ cerebral palsy. Pediatrics 1982;69: 529–36. [8] Allen MC. Neurodevelopmental outcomes of preterm infants. Curr Opin Neurol 2008;21:123–8. [9] Cans C. Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers. Dev Med Child Neurol 2000;42:816–24. [10] Dirks T, Blauw-Hospers CH, Hulshof LJ, Hadders-Algra M. Differences between the family-centered “COPCA” program and traditional infant physical therapy based on neurodevelopmental treatment principles. Phys Ther 2011;91:1303–22. [11] Blauw-Hospers CH, Dirks T, Hulshof LJ, Bos AF, Hadders-Algra M. Pediatric physical therapy in infancy: from nightmare to dream? A two-arm randomized trial. Phys Ther 2011;91:1323–38. [12] Van Berckelaer-Onnes IA, Buysse WH, Dijkxhoorn YM, Gooyen JBM, van der Ploeg JA. Dutch translation of the Vineland Adaptive Behavior Scales. Leiden: University of Leiden; 1997. [13] Msall ME. Measuring functional skills in preschool children at risk for neurodevelopmental disabilities. Ment Retard Dev Disabil Res Rev 2005;11:263–73. [14] Voorman JM, Dallmeijer AJ, Schuengel C, Knol DL, Lankhorst GJ, Becher JG. Activities and participation of 9- to 13-year-old children with cerebral palsy. Clin Rehabil 2006;20:937–48. [15] Wilson BN, Crawford SG, Green D, Roberts G, Aylott A, Kaplan BJ. Psychometric properties of the revised Developmental Coordination Disorder Questionnaire. Phys Occup Ther Pediatr 2009;29:182–202. [16] Schoemaker MM, Flapper BCT, Verheij NP, Wilson BN, Reinders-Messelink HA, de Kloet A. Evaluation of the Developmental Coordination Disorder Questionnaire as a screening instrument. Dev Med Child Neurol 2006;48:668–73. [17] Verhulst FC, Ende J, Koot van der H. Manual CBCL/4–18. Rotterdam: EUR/AZR/Sophia Children's Hospital, Department of child Psychiatry; 1996. [18] De Groot A, Koot HM, Verhulst FC. Cross-cultural generalizability of the Child Behavior Checklist cross-informant syndromes. Psychol Assess 1994;6:225–30. [19] Butcher PR, van Braeckel K, Bouma A, et al. The quality of preterm infants' spontaneous movements: an early indicator of intelligence and behavior at school age. J Child Psychol Psychiatry 2009;50:920–30. [20] Groen SE, de Blécourt ACE, Postema K, Hadders-Algra M. General movements in early infancy predict neuromotor development at 9 to 12 years of age. Dev Med Child Neurol 2005;47:731–8. [21] Bruggink JL, Van Braeckel KN, Bos AF. The early motor repertoire of children born preterm is associated with intelligence at school age. Pediatrics 2010;125:e1356–63. [22] Hitzert MM, Roze E, van Braeckel KNJA, Bos AF. Motor development in 3-month-old healthy term-born infants is associated with cognitive and behavioural outcomes at early school age. Dev Med Child Neurol 2014;56:869–76. [23] Hadders-Algra M, Groothuis AMC. Quality of general movements in infancy is related to neurological dysfunction, ADHD, and aggressive behaviour. Dev Med Child Neurol 1999;41:381–91. [24] Hadders-Algra M, Bouwstra H, Groen SE. Quality of general movements and psychiatric morbidity at 9 to 12 years. Early Hum Dev 2009;85:1–6. [25] Skranes J, Vangberg TR, Kulseng S, et al. Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 2007;130:654–66.
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Specific characteristics of abnormal general movements are associated with functional outcome at school age Elisa G. Hamer a,c, Arend F. Bos b, Mijna Hadders-Algra a,⁎ a b c
Department of Pediatrics, Division of Developmental Neurology, University of Groningen, University Medical Center, Groningen, The Netherlands Department of Pediatrics, Division of Neonatology, University of Groningen, University Medical Center, Groningen, The Netherlands Department of Neurology, Radboud University Medical Center, Nijmegen, The Netherlands
a r t i c l e
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Article history: Received 12 August 2015 Received in revised form 13 January 2016 Accepted 19 January 2016 Keywords: General movements High risk infants Cerebral palsy Follow-up School age Neurodevelopment
a b s t r a c t Background: Assessing the quality of general movements (GMs) is a non-invasive tool to identify at early age infants at risk for developmental disorders. Aim: To investigate whether specific characteristics of definitely abnormal GMs are associated with developmental outcome at school age. Study design: Observational cohort study (long-term follow-up). Subjects: Parents of 40 children (median age 8.3 years, 20 girls) participated in this follow-up study. In infancy (median corrected age 10 weeks), the children (median gestational age 30.3 weeks; birth weight 1243 g) had shown definitely abnormal GMs according to Hadders-Algra (2004). Information on specific GM characteristics such as the presence of fidgety movements, degree of complexity and variation, and stiff movements, was available (see Hamer et al. 2011). Outcome measures: A standardised parental interview (presence of CP, attendance of school for special education, Vineland Adaptive Behavior Scale to determine functional performance) and questionnaires (Developmental Coordination Disorder Questionnaire [DCD-Q] to evaluate mobility and Child Behavior Checklist to assess behaviour) were used as outcome measures. Results: Six children had cerebral palsy (CP), ten children attended a school for special education, and eight children had behavioural problems. Both the absence of fidgety movements and the presence of stiff movements were associated with CP (p = 0.001; p = 0.003, respectively). Stiff movements were also related to the need of special education (p = 0.009). A lack of movement complexity and variation was associated with behavioural problems (p = 0.007). None of the GM characteristics were related to DCD-Q scores. Conclusions: The evaluation of fidgety movements and movement stiffness may increase the predictive power of definitely abnormal GMs for motor outcome — in particular CP. This study endorses the notion that the quality of GMs reflects the integrity of the infant's brain, assisting prediction of long-term outcome. © 2016 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In early infancy, the assessment of general movements (GMs) is the best clinical predictor for neuromotor development in high risk infants [1,2]. GMs are endogenously generated spontaneous movements and their quality reflects the integrity of the infant's brain [3]. GMs are present from early foetal life until goal-directed motor behaviour arises, Abbreviations: ATNR, Asymmetric tonic neck reflex; CBCL, Child Behavior Checklist; COPCA, Coping with and caring for infants with special needs; CP, Cerebral palsy; DCD-Q, Developmental Coordination Disorder Questionnaire; DSM, Diagnostic and Statistical Manual of Mental Disorders; GMs, General movements; VABS, Vineland Adaptive Behavior Scale. ⁎ Corresponding author at: University Medical Center Groningen, Department of Developmental Neurology, Hanzeplein 1, 9713 GZ Groningen, The Netherlands. Tel.: +31 50 3614247; fax: +31 50 3619158. E-mail address: [email protected] (M. Hadders-Algra).
http://dx.doi.org/10.1016/j.earlhumdev.2016.01.019 0378-3782/© 2016 Elsevier Ireland Ltd. All rights reserved.
i.e., typically around 4 months corrected age. Normal GMs are complex movements in which all body parts participate; they are characterised by variation [4]. In abnormal GMs, complexity and variation are reduced. The presence of definitely abnormal GMs is associated with perinatal brain lesions and developmental disorders, including cerebral palsy (CP) [1,5]. Recently, we were able to demonstrate that specific movement characteristics might enhance prediction of definitely abnormal GMs (classified according to Hadders-Algra, 2004 [4]) around 3 months of age, i.e., so-called fidgety-GM age [6]. Both the absence of fidgety movements and the presence of predominantly stiff movements were associated with a higher chance of CP at 18 months. None of the other movement characteristics investigated were associated with functional motor performance or cognitive outcome at that age. It is known that associations between early neurological signs and developmental outcome may change with age, as the child's brain
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experiences significant changes during development [7,8]. Also, the age of 18 months corrected age, used in Hamer et al. 2011 [6], is relatively early for the diagnosis of CP. For instance, the Surveillance of Cerebral Palsy Europe only includes children older than 5 years of age [9]. Moreover, 18 months corrected age is early in terms of outcome in other domains, e.g., functional and behavioural outcomes. The primary aim of the present study is therefore to investigate whether the specific characteristics of definitely abnormal GMs that were related to motor outcome at 18 months, i.e., fidgety movements and predominantly stiff movements (further denoted as stiff movements), are related to developmental outcome at school age. In addition, we studied whether the other movement characteristics studied in Hamer et al. [6], such as the degree of complexity and variation, were associated with outcome at school age.
2. Methods This study is part of the VIP-project (Dutch; Vroegtijdig Interventie Project), a randomised controlled trial studying the effects of the early intervention program COPCA (Coping with and Caring for infants with special needs — a family centred program [10]) in comparison to traditional infant physiotherapy. The developmental outcome in the two intervention groups was similar [11]. Inclusion in the VIP-project was based on the presence of definitely abnormal GMs [4]. The general movement assessment includes at least 5 min of video recording of spontaneous motor behaviour in an awake, non-crying state. As previously reported, MHA and AFB reanalysed the video recordings of the VIP infants (n = 46, median age at GM assessment 10.3 [range 9–13] weeks corrected age) with respect to the following characteristics: presence of fidgety movements, degree of complexity and variation, presence of cramped-synchronised GMs, stiff or jerky movements, and spontaneous occurrence of the asymmetric tonic neck reflex (ATNR) pattern (Table 1) [6]. In addition, we computed a movement abnormality score (MAS; range 0–2) based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
2.1. Follow-up assessment at school age We sent an invitation letter for the present follow-up study to the parents whose children participated in the follow-up assessment at 18 months (n = 44). For the follow-up at school age, we used a structured parental telephone interview (Vineland Adaptive Behavior Scale [VABS], medical history, educational achievement) and parental questionnaires (Developmental Coordination Disorder Questionnaire [DCD-Q] and Child Behavior Check List [CBCL]). During the interview the parents specified the child's educational achievement, including the need of special education. Notwithstanding the fact that the Dutch government is in favour of inclusive education, children with special needs often attend schools for special education. Both the parents and the interviewer (EGH) were unaware of the specific general movement characteristics of the child.
Using the VABS we assessed the child's functional status in four domains: communication, daily living skills, socialisation and motor skills [12]. The four domains can each be subdivided in 2–4 subdomains, e.g., expressive communication, play and leisure time, and fine motor skills. We calculated the scores for each domain (n = 4) and subdomain (n = 11). The VABS has proven to be reliable and valid in both typically developing children and in children with developmental disorders, such as CP [13,14]. The domain communication, daily living skills and socialisation can be applied until 18 years of age. The motor skill domain is designed for children up to 6 years of age and for older children with motor impairments. We used the DCD-Q to assess mobility [15]. This short questionnaire covers 17 items on control during movement, fine motor skills/ handwriting, gross motor skills, and general coordination. A higher total score indicates worse performance. The DCD-Q is reliable and valid, as is the Dutch translation [16]. The CBCL is a widely used parental questionnaire containing 113 items concerning the child's behaviour [17]. The scores were dichotomised as normal or borderline vs. in the clinical range (i.e., above the 97th percentile) on the following six Diagnostic and Statistical Manual of Mental Disorders (DSM) oriented scales: affective, anxiety, somatic, attention deficit/hyperactivity, oppositional defiant, and conduct problems. The reliability and validity of the Dutch version of the CBCL are good [17,18]. The Medical Ethics Committee of the University Medical Center Groningen approved the study (trial number NL39954.042.12). 2.2. Data analysis Statistical analysis was performed using SPSS version 20. We used non-parametric tests since the data did not show a normal distribution. Regression analysis was used to control for type of intervention. To adjust for multiple comparisons, differences with a p-value ≤ 0.01 were considered to be statistically significant. Psychometric properties and confidence intervals (CIs) were calculated with the use of MedCalc statistical software (version 11.6, Ostend, Belgium). 3. Results We obtained follow-up data from 40 children (91%, median age; 8 years + 4 months; Table 2). The participating children did not differ from the non-participating children in baseline characteristics (sex, gestational age, birth weight, educational level of the parents, maternal age at birth, type of intervention or CP at 18 months CA — data not shown). 3.1. GM characteristics: Motor and functional outcome Six parents reported that their child had CP. Both the absence of fidgety movements and the presence of stiff movements were associated with CP (Table 3, Fisher's exact test; p = 0.001 and p = 0.003, respectively). The absence of fidgety movements and the presence of stiff
Table 1 Specific GM characteristics. Fidgety movements Complexity and variation of the movements Cramped-synchronised movements ATNR pattern Stiff or jerky movement quality
Fidgety movements are circular movements of small amplitude and moderate speed and variable acceleration of neck, trunk and limbs in all directions. Complex movements are movements during which the infant actively produces frequent changes in direction of the participating body parts. The GM variation represents the temporal variation of the movements. This means that across time, the infant produces continuously new movement patterns. Cramped-synchronised movements appear rigid and lack normal smooth and fluent character; all limb and trunk muscles contract and relax almost simultaneously. The asymmetric tonic neck reflex (ATNR) consists of the extension of the arm and leg on the side to which the head is turned, with flexion of the contralateral limbs. GM fluency indicates the presence of smooth, supple and graceful movements. Stiff movements and jerky movements are a type of non-fluent motor behaviour. Non-fluent movements can be predominantly jerky, stiff or consist of a mix of jerky and stiff movements.
For details on the scoring of the specific GM-characteristics see Hamer et al. [6].
E.G. Hamer et al. / Early Human Development 95 (2016) 9–13
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0.075, p = 0.154, p = 0.162, and p = 1.000, respectively) or to the VABS and DCD-Q scores (data not shown).
Table 2 Group characteristic. Background
n = 40
Gestational age in weeks + days, median (range) Preterm (b37 weeks), n Birth weight in grams, median (range) Sex, n of girls Severe brain lesion, na Follow-up Age at follow-up in years + months, median (range) Diagnosis of CP, n Attendance of special education, n VABS, median (range)⁎ Communication Daily living skills Socialisation Motor skills DCD-Q scores, median (range)⁎⁎ Behavioural problems (according to the CBCL), n⁎⁎
30 + 2 (25 + 0 − 40 + 0) 36 1243 (635–4750) 20 5 8 + 4 (7 + 6 − 10 + 1) 6 10 230 (185–246) 268 (51–314) 170 (113–184) 144 (15–146) 64 (33–85) 8
Note: The VABS scores of children with missing DCD-Q or CBCL scores did not differ from those with available DCD-Q or CBCL scores. a Severe brain lesion: periventricular leukomalacia grades 3 and 4, periventricular haemorrhagic infarction, or thalamus/basal ganglia lesion (see Hamer et al., 2011) [6]. ⁎ n = 39. ⁎⁎ n = 34.
3.2. GM characteristics: Type of education and behavioural outcome The attendance of special education (n = 10, including 6 with CP) was associated with the presence of stiff movements (47% vs. 9%, p = 0.009), not with the other movement characteristics (Table 3). The MAS was also associated with the need of special education (Fig. 1b, MAS0-1 15% vs. MAS2 71%; p = 0.006). Eight children had atypical and clinically relevant CBCL scores; three of them had CP and attended a school for special education. The other five children had no CP and attended mainstream education. One movement characteristic was associated with behavioural outcome; children with a total lack of GM complexity and variation more often had clinically abnormal CBCL scores (55% vs. 9%, p = 0.007) compared to children whose GMs showed some complexity and variation. The lack of movement complexity and variation was not associated with abnormal scores on one of the subscales. None of the above mentioned associations were influenced by the type of intervention received in infancy (data not shown). 4. Discussion
movements were not related to the VABS scores or the DCD-Q scores (Table 3). Children with a MAS of 2 more often had CP (71% vs. 3%, Fig. 1a, p = 0.0005) and had lower VABS motor skills (total and gross motor skills, Fig. 2) and personal scores than children with lower MAS scores (Table 3). The specificity and positive predictive value of a MAS of 2 points was higher than that of the specific signs, i.e., the absence of fidgety movements and the presence of stiff movements, alone (Table 4). The degree of complexity and variation (some [n = 27] vs. none [n = 13]), the presence of the ATNR pattern (n = 11), the presence of jerky movements (n = 29), and the presence of cramped-synchronised movements (n = 5) were not related to the development of CP (p =
Our study indicates that in children with definitely abnormal general movements the absence of fidgety movements and the presence of stiff movements are related to worse functional motor outcome at school age, including CP. The presence of stiff movements was also related to the need of special education. In addition, a lack of complexity and movement variation was associated with the presence of behavioural problems. The association between the absence of fidgety movements and the presence of stiff movements and CP replicated the findings at 18 months of age [6]. It has been previously shown that the absence of fidgety movements is related to CP [1–5], but not to intelligence at school age [19], which is in line with our results. Our finding regarding the presence of stiff movements corresponds to Groen et al. (2005), who
Table 3 GM characteristics and outcome at school age. FM present
FM absent
p-value
Not stiff
Stiff present
p-value
MAS 0-1
MAS 2
p-value
n = 31
n=9
n = 23
n = 17
n = 33
n=7
Cerebral palsy Special education
1 (3%) 5 (16%)
5 (56%) 5 (56%)
0.001* 0.029
0 (0%) 2 (9%)
6 (35%) 8 (47%)
0.003* 0.009*
1 (3%) 5 (15%)
5 (71%) 5 (71%)
0.0005* 0.006*
VABS domains Communication Daily living skills Socialisation Motor skills VABS subdomains C — receptive C — expressive C — written D — personal D — domestic D — community S — interpersonal relationships S — play and leisure time S — coping skills M — gross motor M — fine motor
n = 30 233 (200–246) 270 (215–314) 171 (131–184) 144 (127–146)
n=9 228 (185–243) 250 (51–283) 163 (113–178) 112 (15–146)
0.284 0.054 0.384 0.042
n = 23 229 (223–301) 268 (223–301) 171 (131–183) 144 (132–146)
n = 16 236 (185–244) 264 (51–314) 168 (113–184) 141 (15–146)
0.921 0.437 0.746 0.035
n = 32 231 (200–246) 270 (215–314 171 (131–184) 144 (127–146)
n=7 230 (185–243) 215 (51–283) 163 (113–176) 77 (15–145)
0.462 0.049 0.255 0.007*
45 (39–46) 148 (134–152) 40 (18–52) 158 (141–169) 37 (15–52) 71 (44–93) 64 (54–69) 62 (50–66) 44 (20–55) 84 (72–84) 61 (49–62)
44 (35–46) 148 (134–151) 35 (0–48) 153 (27–164) 32 (6–42) 65 (18–88) 64 (58–69) 57 (18–66) 42 (31–48) 52 (94–84) 60 (11–62)
0.191 0.831 0.159 0.039 0.159 0.402 0.883 0.658 0.460 0.025 0.107
45 (39–46) 148 (138–152) 39 (31–52) 158 (141–167) 38 (32–50) 67 (44–92) 63 (56–67) 62 (50–66) 44 (20–55) 84 (72–84) 62 (54–62)
45 (35–46) 148 (134–151) 40 (0–51) 156 (27–169) 36 (6–52) 75 (18–93) 64 (54–69) 61 (18–66) 43 (29–53) 82 (4–84) 60 (11–62)
0.989 0.582 0.767 0.239 0.043 0.810 0.301 0.275 0.789 0.035 0.050
45 (39–46) 148 (134–152) 40 (18–52) 158 (141–169) 37 (15–52) 69 (44–93) 64 (54–69) 62 (50–66) 44 (20–55) 84 (72–84) 61 (49–62)
44 (35–46) 148 (134–151) 38 (0–48) 140 (27–161) 32 (6–42) 71 (18–88) 64 (58–69) 57 (18–66) 42 (31–45) 49 (4–84) 56 (11–62)
0.378 0.734 0.359 0.010* 0.122 0.578 0.707 0.507 0.287 0.004* 0.037
DCD-Q Total score
n = 28 67 (44–85)
n=7 44 (25–70)
0.020
n = 19 64 (44–85)
n = 16 63 (25–71)
0.133
n = 29 65 (44–85)
n=6 41 (25–70)
0.012
CBCL DSM clinical score
n = 28 5 (18%)
n=6 4 (57%)
0.055
n = 19 4 (21%)
n = 16 5 (31%)
0.700
n = 29 5 (17%)
n=6 4 (67%)
0.027
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a. Diagnosis of CP
b. Attendance of special education
Fig. 1. a. Diagnosis of CP. 1b. Attendance of special education. Association between movement abnormality score (MAS) and a) CP and b) attendance of school for special education. The MAS (range 0–2) is based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
Fig. 2. GM characteristics and VABS motor skills' total score. Data are presented as median values (horizontal bars), interquartile ranges (boxes) and ranges (vertical lines) with outliers (circles).
reported that the (rare) occurrence of predominantly stiff movements at fidgety age was associated with an unfavourable neurological outcome [20]. The additional associations between a) the presence of stiff movements and the need of special education and b) a higher MAS and a lower VABS personal domain score suggest that the predictive value of these characteristics extends beyond the motor domain. The notion that GMs are not only predictive for motor outcome is supported by others; several studies reported for instance an association between GM quality and cognition at school age [19,21,22]. Our finding that a lack of complexity and variation is associated with behavioural problems is partly in line with previous studies showing a relation between reduced complexity and variation and attention problems [23,24]. In contrast to previous studies, we found an
unspecific association: a lack of movement complexity and variation was not associated with specific behavioural problems. Hitzert et al. (2014) reported a similar unspecific association between monotonous movements and behavioural problems in term born infants [22]. These findings support the notion that movement complexity and variation, which may be considered as two forms of movement variation [4], reflect the overall integrity of neural connectivity, especially of periventricular connectivity [2]. A reduced connectivity increases the vulnerability for impairments in several domains, including the likelihood of the development of behavioural problems [25]. This study illustrates the importance of follow-up beyond preschool age. At 18 months CA, ten children were diagnosed with CP [6]. At school age, one of these children was lost to follow-up, and three
Table 4 Psychometric properties of FMs and stiff movements. Cerebral Palsy
Sensitivity
(95% CI)
Specificity
(95% CI)
PPV
(95% CI)
NPV
(95% CI)
Abscence of fidgety movements Presence of stiff movements MAS 2 (absence of FMs and presence of stiff movements)
83 100 83
(36–100) (54–100) (36–100)
88 68 94
(73–97) (49–83) (80–99)
56 35 71
(21–86) (14–62) (29–96)
97 100 97
(83–100) (85–100) (84–99)
Special education
Sensitivity
(95% CI)
Specificity
(95% CI)
PPV
(95% CI)
NPV
(95% CI)
Abscence of fidgety movements Presence of stiff movements MAS 2 (absence of FMs and presence of stiff movements)
50 80 50
(19–81) (44–97) (19–81)
87 70 93
(69–96) (51–85) (78–99)
25 47 71
(13–41) (23–72) (29–96)
84 91 85
(66–95) (72–99) (68–95)
The MAS (range 0–2) is based on the absence of fidgety movements (1 point) and the presence of stiff movements (1 point).
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other children ‘outgrew’ CP — according to their parents' report. In addition, the need for special education and behavioural outcome could not be determined at a younger age. Associations between early risk factors and developmental outcome may become stronger with increasing age; some dysfunctions may only emerge when the brain develops new functions, a phenomenon which is especially encountered in high risk infants, such as infants born preterm [8]. The development of the young nervous system may also resolve early neurological abnormalities. Within our cohort, eight of the ten children with CP at 18 months corrected age had shown stiff GMs [6]. The present study indicates that all six children who were indeed diagnosed with CP – at school age – had shown stiff GMs. This study further underlines that the presence of more abnormal signs is associated with a higher risk for developmental problems — a well-known phenomenon in paediatric neurology. For example, in our study group the presence of stiff movements was associated with high sensitivity and negative predictive values, but its positive predictive value was low. However, in combination with the absence of fidgety movements (MAS score of 2 points), its positive predictive value for CP and attendance of a school for special education rose. On the other hand, it may also be good to realise that the majority of our study group did not develop CP, had no behavioural problems and was not in need of special education — despite the fact that they had definitely abnormal GMs and most of them were born below 32 weeks gestational age. This underscores the notion that the prediction of developmental outcome in early infancy is notoriously difficult [2]. The high follow-up rate, the long-term follow-up and the detailed analysis of movement characteristics are the strengths of this study. The most important limitation of the study is the small sample size; this limits generalisability — including generalisability of predictive values. The use of parental questionnaires may be considered as another limitation. For example, very mild forms of CP may have been unreported. However, parents outperform professionals in providing information on functional outcome in daily life. Lastly, we regard the ceiling effect of the motor skills domain of the VABS as a limitation. This may explain why we merely found trends between GM characteristics (absence of fidgety movements and presence of stiff movements) and VABS motor skill scores. However, the MAS was significantly associated with the total and gross motor outcome measured with the VABS. We conclude that the predictive power of definitely abnormal general movements for motor outcome – in particular CP – may be enhanced by including the evaluation of fidgety movements and movement stiffness. This study endorses the notion that the quality of general movements reflects the integrity of the infant's brain, and assists prediction of long-term outcome. Conflict of interest None declared. Acknowledgements We are grateful to all the children and their families for participating in the VIP project. The study was financially supported by the Johanna KinderFonds, Stichting Fonds de Gavere, the Cornelia Stichting and the Graduate School for Behavioural and Cognitive Neurosciences (BCN).
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