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• W2899948557 abstract "To identify developmental trajectories of hand function in infants aged 3 months to 12 months with unilateral cerebral palsy (CP). Infants at high risk of unilateral CP were recruited from 3 months of age from follow-up programmes and clinics in Sweden, the Netherlands, Italy, and Australia. Measurements on the Hand Assessment for Infants (HAI) were completed until 12 months of age. Group-based trajectory modelling was used to identify subgroups of infants with similar trajectories of development. Multinomial logistic regression determined associations between demographic variables and trajectory membership. Ninety-seven infants (52 males, 45 females; median gestational age 38wks [interquartile range 30–40wks]) were included. Infants were assessed between two and seven times (mean 4, SD 1.2) with a total of 387 observations. A three-group trajectory model identified a ‘low-functioning group’ (n=45: 46%), ‘moderate-functioning group’ (n=30: 31%), and ‘high-functioning group’ (n=22: 23%). Mean posterior probabilities (0.91–0.96) and odds of correct classification (26.3–33.2) indicated good model fit. Type of brain lesion, sex, side of hemiplegia, country, gestational age, and access to intensive intervention were not associated with group membership. Three trajectories of hand function development for infants with unilateral CP were identified and indicate some greater distinctions between groups with increasing age. The HAI is a valuable measure, capturing development of hand function of infants with unilateral CP over time. Identificar la trayectoria del desarrollo de la función manual en niños de 3 a 12 meses con parálisis cerebral unilateral (PC). Fueron evaluados niños con alto riesgo de PC unilateral desde los 3 meses de edad en programas de seguimiento en clínicas en Suecia, Países Bajos, Italia y Australia. Las mediciones con la Hand Assessment for Infants (HAI) fueron completadas hasta los 12 meses de edad. Se utilizó la trayectoria modelada de un grupo basal para identificar subgrupos de niños con similar trayectoria de desarrollo. La regresión logística multinomial determinó las asociaciones entre las variables demográficas y la pertenencia a la trayectoria. Noventa y siete niños (52 masculinos, 45 femeninos; edad gestacional media 38 semanas [rango 30–40 semanas]) fueron incluidos. Los niños fueron evaluados entre dos y siete veces (media 4, SD 1,2) con un total de 387 observaciones. Un modelo de trayectoria de tres grupos identificó un¨ grupo de bajo funcionamiento¨(n=45: 46%), un ¨grupo de moderado funcionamiento¨ (n=30: 31%), y un ¨grupo de alto funcionamiento¨ (n=22: 23%). La probabilidad media posterior (0,91–0,96) y las probabilidades de clasificación correcta (26,3–33,2) indicaron un buen ajuste del modelo. El tipo de lesión cerebral, sexo, localización de la hemiplejía, país, edad gestacional y el acceso a la intervención no fue asociado a la membresía del grupo. En niños con PC unilateral fueron identificados tres trayectorias del desarrollo de la función manual, los cuales indicaron mayor distinción entre los grupos a mayor edad. El HAI es una medida valiosa, capturando el desarrollo de la función manual de los niños con PC bilateral en el tiempo. Identificar trajetórias de desenvolvimento da função manual em lactentes com idade entre 3 e 12 meses com paralisia cerebral unilateral. Lactentes com alto risco para paralisia cerebral unilateral foram recrutadas aos 3 meses de idade em programas de follow-up e clínicas na Suécia, Países Baixos, Itália e Austrália. Medidas da Avaliação manual para lactentes (AML) foram realizadas até os 12 meses de idade. A modelagem de trajetória baseada em grupos foi usada para identificar subgrupos de lactentes com trajetórias similares de desenvolvimento. Uma regressão logística multinomial determinou associações entre variáveis demográficas e a trajetória utilizada. Noventa e sete lactentes (52 do sexo masculino e 45 do sexo feminino; mediana da idade gestacional de 38 semanas [intervalo interquartil 30-40 semanas]) foram incluídos. Os lactentes foram avaliados entre duas e sete vezes (média 4, DP 1,2) com um total de 387 observações. Um modelo de trajetória de três grupos identificou um ‘grupo de baixa função’ (n= 45: 46%), ‘grupo de moderada função’ (n=30: 31%) e ‘grupo de alta função’ (n=22: 23%). Probabilidades posteriores médias (0,91-0,96) e chances de classificação correta (26,3-33,2) indicaram bom ajuste do modelo. O tipo de lesão cerebral, sexo, lado da hemiplegia, país, idade gestacional e acesso a intervenção não foram associados a participação no grupo. Três trajetórias de desenvolvimento de função manual para lactentes com paralisia cerebral unilateral foram identificados e demonstram maiores diferenças entre os grupos com o aumento da idade. A AML é uma medida valiosa, capturando o desenvolvimento da função manual em lactentes com paralisia cerebral unilateral ao longo do tempo. This article is commented on by Holmefur on page 507 of this issue. This article's abstract has been translated into Spanish and Portuguese. Follow the links from the abstract to view the translations. Infants with early brain lesions are at risk of developing cerebral palsy (CP). The brain abnormalities or insults can occur at different time points during pregnancy or in the neonatal period1 and the lesions affect motor function to different extents.2 Asymmetric hand preference is an early clinical sign of unilateral CP and is commonly recognized by parents at early age. However, children are commonly not diagnosed with unilateral CP until the second year of life or even later.3 So far, the lack of a valid assessment to measure hand function in infants with early signs of upper limb asymmetry has hampered investigation of early development of asymmetric hand function. The recently developed Hand Assessment for Infants (HAI) for infants 3 months to 12 months of age4 can assess the degree and quality of goal-directed manual actions performed with each hand separately and both hands together, enabling quantification of the degree of asymmetry in upper limb function. This allows the possibility of investigating the developmental progression of hand function at an early age by repeated measurement of the same individual over time. The use of the HAI in conjunction with neuroimaging may also assist in early diagnosis but further studies are needed to investigate the predictive use of the HAI at early age. To interpret the impact of any targeted upper limb early intervention, an understanding of the trajectory of hand development for infants at risk of unilateral CP is necessary. In Western countries, determining the trajectory of hand development can only be considered in the context of infants already receiving some kind of early intervention or involvement in research interventions. New knowledge of increased plasticity of the young brain indicates that early intensive intervention might be more effective than later treatment and enhances development of the neuromotor system.5-7 Early development for children at high risk of CP has previously been described for reaching, in which children demonstrate some development over time but with reduced kinematic quality than typically developing children.8, 9 For older children with unilateral CP, from 18 months of age, the ability to use the impaired hand in bimanual activities has been described and it increases over time, but to a varying extent depending on the child's initial ability.10 Children with higher initial ability at 18 months of age, measured on the Assisting Hand Assessment, had a faster rate and reached their limit of development at approximately 3 years of age, whereas children with the most severe hand function had a very slow rate, reaching their limit of development at 8 years of age.10 The type of brain lesion and region of the brain injury influenced the level and rate of development.11 Children whose brain lesions occurred close to term (typically neonatal stroke) showed slower and poorer hand development than those whose brain injuries occurred at an earlier gestational age (typically periventricular haemorrhagic infarction). The strongest predictor of poor hand function development in older children was the presence of simultaneous lesions in the basal ganglia and thalamus.11, 12 What remains unclear is the rate of development of hand function in infants later diagnosed with unilateral CP. This study aimed to: (1) derive and compare developmental trajectories of hand function measured on the newly developed HAI4 in infants at 3 months to 12 months of age with unilateral CP; and (2) investigate whether type of brain lesion, gestational age, and motor intervention – factors that are known to affect hand function in older children with unilateral CP – are associated with trajectory group membership. A convenience sample of infants at high risk of developing unilateral CP including a known neonatal event that affected the brain and/or clinical signs of unilateral CP of unknown origin were referred for investigation of hand function below 12 months of age. Infants were recruited from 2006 to 2016 in different follow-up programmes and clinics at Astrid Lindgren Children's Hospital, Stockholm, Sweden; Wilhelmina Children's Hospital, Utrecht, the Netherlands; IRCCS Fondazione Stella Maris, Pisa, Italy; and Cerebral Palsy Alliance, Sydney, Australia. Referrals occurred from 3 months corrected age. The recruitment was based on a combination of signs from neurological examinations including the Hammersmith Infant Neurological Evaluation, General Movements Assessment, and/or Alberta Infant Motor Scale, and, when available, magnetic resonance imaging (MRI).3 From this convenience sample, infants were only included in the current study if they had: (1) a diagnosis of CP that was verified after 12 months of age by a paediatric neurologist; and (2) had two or more assessments on the HAI before 12 months of age (Table 1). The diagnostic criteria were based on the recommendations of the Surveillance of Cerebral Palsy in Europe.13 Infants with severe visual impairment, affecting the test situation, were excluded. All parents had given informed consent to the research and publication of the results. The study was preapproved by Stockholm Regional Ethical Review Board and in the other participating countries by the relevant institutional or regional review boards (Italy: Stella Maris Scientific Institute and University of Pisa; Australia: Sydney Children's Hospital Network, Cerebral Palsy Alliance, and the University of Notre Dame. After recruitment, the infants continued through follow-up programmes and usual care in the different countries; however, the frequency and content of usual care differed. All infants, however, saw a physical therapist on a regular basis, approximately once a week in Italy and the Netherlands, once a month in Sweden, and varying between once a week and once a month in Australia. Less commonly, infants saw an occupational therapist during the first year of life. Several infants were participants in previous clinical trials investigating new interventions (Table 1). This included six infants from Goals - Activity - Motor Enrichment (GAME);7 and four from Upper Limb Baby Early Action-observation Training, a training performed during the first 3 months of age.14 Thirty-six infants received constraint-induced movement therapy, which involved 30 hours to 40 hours of specific hand training performed during the first year of life.15 Seventeen of them were included from a retrospective study,16 and 19 from a randomized controlled trial of constraint-induced movement therapy/infant-massage.6 Infants from Utrecht (n=5) received erythropoietin treatment at birth.17 Data were collected mainly in the hospitals during regular follow-up of the children or at different time points when included in clinical trials. If infants had been born preterm, age corrected for prematurity was always used. There was at least 1 month between assessments. Assessments were videotaped and later scored by certified experienced assessors including two from Italy and two from Sweden. The HAI is a newly developed standardized observation-based test for infants aged 3 months to 12 months that assesses the degree and quality of goal-directed manual actions performed with each hand separately as well as both hands together.4 The test procedure comprises a semi-structured, video-recorded 10-minute to 15-minute play session. A test kit of carefully selected toys is presented to the infant to encourage and elicit toy exploration, making a wide range of motor actions observable. During these play sessions, the child was seated in an infant seat/bouncer or high-chair depending on sitting ability. Construct validity of the HAI was evaluated by Rasch measurement model analysis.4 Both hands are scored on 17 items (12 unimanual and five bimanual items) on a 3-point rating scale. The total raw scores are transformed in the Rasch analysis into an interval level, both hand measure, on a 0 to 100 HAI-unit scale where a higher score indicates better performance. The unimanual items are scored separately for each hand sum (EaHS) with scores ranging from 0 to 24. The EaHS of the affected hand are reported. Additionally, from the EaHS, an asymmetry index is calculated quantifying the percentage difference between hands, with a higher number reflecting larger asymmetry.4 Brain lesions were characterized on the basis of available neuroimaging, collected for clinical purposes at various time points and with various protocols during the first year of life, mainly at term. All images were visually assessed by experienced neuroradiologists unaware of the clinical diagnosis and functional outcome. The basic patterns of damage were classified as normal, periventricular white-matter lesion, focal ischaemic or haemorrhagic lesions, and miscellaneous or unclassifiable lesions (others) according to the Surveillance of Cerebral Palsy in Europe.13 All statistical analyses were performed using Stata 14.1 (StataCorp LP, College Station, TX, USA). Characteristics of the cohort were summarized using means and standard deviations or medians and interquartile ranges for continuous variables, or percentages for categorical variables. Group-based trajectory modelling (GBTM) using the ‘traj’ Plugin in Stata,18 with a censored normal model, was used to identify and describe subgroups of infants that had similar trajectories of hand development (measured on the HAI both hand measure). GBTM is a specialized type of finite mixture modelling aimed at identifying distinctive clusters or groups of people who follow similar trajectories.19 Latent class analysis using maximum likelihood estimation enables trajectory parameters to be derived using all available HAI-unit values. GBTM models the relationship between hand function and time, allowing each trajectory to have a different shape, estimating the proportion of the population belonging to each trajectory group, and determining each infant's probability of belonging to each trajectory group. Each infant is then assigned to a trajectory group on the basis of the highest probability for membership. To determine the most appropriate number of trajectory groups, models were fitted ranging from one to four groups. First-order (linear) to third-order (cubic) models were tested to determine the shape of change of each trajectory group. Models were excluded if there were one or more groups with a small proportion of observations (<10 infants).19 Bayesian information criteria were compared between models, with a smaller Bayesian information criterion indicating a better model fit. The likelihood of an individual belonging to a group is calculated by posterior probability. The final model was evaluated using the average posterior probabilities of group membership, odds of correct classification and correspondence between estimated group probabilities, and the proportion of infants assigned to the group.20 The characteristics of each trajectory population were then summarized for demographic variables that might impact upper limb function for infants with unilateral CP (e.g. gestational age, type of brain lesion, motor training intervention). Associations between demographic variables with trajectory membership were examined using multinomial regression. Ninety-seven infants with a confirmed diagnosis of unilateral CP and a median gestational age of 38 weeks (interquartile range [IQR] 30–40wks) were included. Demographic details are summarized in Table 1. There were 52 males (54%). Infants were from Sweden (n=56: 58%), Italy (n=19: 20%), the Netherlands (n=16: 16%), and Australia (n=6: 6%). They were assessed between two and seven times (mean 4, SD 1.2) with a total of 387 unique observations. The median age at the first assessment was 19 weeks corrected age (IQR 14–29wks; range 11–44wks). Table 2 presents the number of assessments conducted across each month of age and number of repeated measures available. The fitted trajectories for a three-group model are depicted in Figure 1 and the coefficients summarized in Table SI (online supporting information). The model had an appropriate proportion of the sample in each group: ‘low-functioning group’ 46%, ‘moderate-functioning group’ 31%, and ‘high-functioning group’ 23%. The mean posterior probabilities ranged from 0.91 to 0.96, exceeding the recommended 0.70.20 Odds of correct classification ranged between 26.3 and 33.2, exceeding 5.0, which indicates a good model fit20 (Table SII, online supporting information). Scores on the HAI both hand measure for the total sample for each month of age and each trajectory group are summarized in Table 3. Trajectory group 1, the low-functioning group, had a slow increase in development of hand function which seemed to plateau at around 9 months to 10 months of age. This group had a median EaHS on the affected hand of 3 (IQR 3–6) at 6 months (maximum score 24) that did not change by 12 months of age. This low-functioning group had a median asymmetry score of 85% (IQR 74%–87%) at 6 months of age. The second trajectory group, the moderate-functioning group, had a steady increase in hand function scores over time. This group had a median EaHS on the affected hand of 11.5 (IQR 9–14) at 6 months of age, increasing to 13 (IQR 12–15) by 12 months of age. The median asymmetry score at 6 months of age was 48% (IQR 36%–61%). The third trajectory group, the high-functioning group, had a more rapid acquisition of hand function ability to 6 months of age but continued to steadily improve until 12 months of age. This highest-functioning group had a median EaHS on the affected hand of 17 (IQR 14–18) at 6 months, which increased to 18.5 (IQR 17–20) at 12 months of age. Median asymmetry scores were 25.5% (IQR 22%–39%) at 6 months of age. Demographic characteristics of each trajectory group are summarized in Table 1. No associations between trajectory group membership and gestational age, brain lesion, side of hemiplegia, prematurity, sex, country of origin, or intervention were found using multinomial logistic regression (Table 4). Separate trajectories were plotted for those infants who did not and those who did receive an intensive motor training intervention, which demonstrated little difference in trajectory profiles (Figure S1, online supporting information). This study identified significant heterogeneity in the developmental trajectories of hand function in infants with unilateral CP during the first year of life; however, three distinct groups were identified. There was a group of infants who demonstrated a more rapid and continuous acquisition of skills, a second group had slower but steady gains, and a third group showed a much slower improvement which plateaued. Neonatal history and access to intensive intervention were not associated with trajectory group membership as we showed that different types of neonatal history and children receiving intervention were represented in all trajectory groups. Results highlight three different pathways of hand development for infants with unilateral CP. At 3 months and 4 months of age, there was some overlap of confidence levels for trajectory groups, but by 6 months of age these were more clearly delineated. The large variations at 3 months and even 4 months of age show that the HAI score was less indicative of later functioning compared with results at 6 months of age. The large variation of HAI scores at an early age is similar in typically developing children (L Ek, E Sicola, and A-C Eliasson, personal communication).21 Trajectory group membership seems to be related to the ability to grasp. Scores on the HAI for both the moderate-functioning and high-functioning trajectory groups demonstrate that these two groups of infants score highly on items related to grasping objects by 6 months of age. Grasping ability was also distinguished between groups of children at 18 months in a previous study which investigated later development in children with unilateral CP.10 The outcome measures used, however, are not directly comparable. Children above 18 months were investigated using the Assisting Hand Assessment, measuring only the use of the affected hand in bimanual activities, while the HAI measures each hand separately and both hands together.4, 22 The low-functioning trajectory is of concern, as it represented the largest proportion of infants, with very small improvement over the first year of life. This large proportion is different to previous longitudinal studies of older children with unilateral CP10 and may reflect differences in recruitment. The group in this study was a hospital-based cohort, which included infants with a known neonatal event placing them at risk of unilateral CP, therefore potentially missing some infants who did not have early identified risk factors. It is known that a group of children with unilateral CP has no known early neurological events and will be detected at later ages. There was also an over-representation of infants who had perinatal stroke, while periventricular white matter lesions are the dominant pattern even for unilateral CP.23 A second suggestion is that some children may improve hand function at a later age, when cognitive skills and understanding the advantage of the use of the hand become clearer. The low-functioning group in older children continued to develop at a slow rate up to 8 years of age.10 Membership in a trajectory group was not associated with early intensive motor intervention, or the type of brain lesion characteristics. The lack of significant association between brain lesion and trajectory group membership might be explained by our reporting of the predominant type of brain lesion characteristics, which did not account for the complexity of the brain lesion. Findings of a lack of association between trajectory group membership and access to intensive motor training interventions show that children in all severity levels were included in intervention, that it may be difficult to move infants from one trajectory group to another, and that intervention does not prevent infants from being in the low-functioning group. This was also shown in a recent study investigating constraint-induced movement therapy, whereby the lowest-functioning infants seemed to respond less to treatment.6 To what extent early intervention influences the shape of each trajectory needs to be further investigated with a larger cohort with defined time points for intervention. Gestational age, sex, side of impairment, and country were also not associated with trajectory membership. Heterogeneity was large, as some children had good development, independent of brain lesion characteristics, gestational age, and intervention, while it was the opposite for others. Several limitations of the study need to be acknowledged. Data were drawn from different research and clinical programmes; therefore, assessment time points were not uniform and available clinical and demographic information was diverse. Therefore, there may be other possible covariates such as genetic variation, size of lesion, and socio-economic status, which may account for trajectory membership. Additionally, it is unclear what proportion of the whole population attending these services in each country this sample represents. This study aimed to determine whether there were distinct developmental trajectories of hand function in infants with unilateral CP. The group-based approach to analysis is ideally suited to this purpose.20 Previous studies investigating trajectories of development of self-care and gross motor function of children with CP have used assignment rules on the basis of categorization according to classification systems (e.g. the Gross Motor Function Classification System and the Manual Ability Classification System) or other predefined groups10, 24-27 and then modelled trajectories on the basis of these predefined groupings. The current GBTM approach creates trajectory groups based on formal statistical modelling, rather than on subjective classification rules. Previous approaches using subjective classification rules have made a priori assumptions that there are distinct developmental trajectories, potentially limiting the ability to actually test for their presence.20 Additionally, this could lead to creation of trajectory groups that reflect random variation due to over-fitting or underfitting of data.20 The GBTM approach aims to summarize the average development of hand function of a group of infants who follow similar outcome trajectories over time. Infants assigned to specific trajectories, however, may not perfectly follow the overall trajectory pattern.20 This method also accommodates missing data, which is ideally suited in this study as data were drawn from clinical and research studies across four countries, with variability in the timing of assessments. Although this is the largest study of its kind, given the heterogeneity of the population, a greater sample size may identify additional trajectories not determined with the current sample. Clinically, the functional ability of the low-functioning trajectory group approximately represented the development from minor movements of the affected arm that occasionally were goal directed (3mo of age) to inconsistent ability to contact objects and ‘hold easy to hold objects’ (12mo of age). In the moderate-functioning trajectory group, initial ability was similar to the low-functioning group, but by 5 months of age children in this group demonstrated a slow and steady improvement, and started to do grasping actions. By 12 months of age, children in the moderate-functioning trajectory group were able to use their affected hand for easy grasping but with reduced quality, which affected the bimanual use of the hands. The high-functioning trajectory group started somewhat higher than the other two groups. The infants could initiate movements of their affected arm, contact but inconsistently attempted to grasp easy to hold objects close to the hand. Their development was good but the quality of grasping and the amount of use was somewhat reduced, affecting bimanual use of the hands. Forearm movements of the affected hand were reduced. The high-functioning group did not reach the maximum score on the HAI, compared with typically developing children who reached the ceiling on the HAI between 8 months and 10 months of age with only very few children demonstrating a small difference between hands (L. Ek, E. Sicola, & A.-C. Eliasson, personal communication). This is the first study to identify and describe trajectories of development of hand function in infants with unilateral CP. GBTM identified three distinct patterns of change in hand function over time with distinctly different clinical profiles. The measure at 6 months of age demonstrated that grasping seems to be a key clinical feature, found in infants in both high- and moderate-trajectory groups. The low-trajectory group failed to make any substantive progress in the acquisition of hand skills over the first year of life. Further modelling of a larger data set, with clearly defined time points of intervention, is probably required to discern associations between neonatal and intervention factors and trajectory group membership. We thank Cathy Morgan for sharing some of her data with us. Likewise, we thank Lena Sjöstrand who collected and analysed most of the data from Sweden; she had regular contact with families in Sweden. We acknowledge Mark Chatfield for his statistical advice. LS was supported by a National Health and Medical Research Council of Australia Early Career Research Fellowship (1090828) and Foundation Frimurarna Barnhuset. ACE was supported by the Swedish Research Council (grant numbers 521-211-2655 and 521-2011-456), Stockholm City Council (2011-2117), Foundation Olle Engkvist Byggmästare, and Foundation Frimurarna Barnhuset. The authors have stated that they had no interest that could be perceived as posing a conflict or bias. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article." @default.
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• W2899948557 title "Development of hand function during the first year of life in children with unilateral cerebral palsy" @default.
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