Postural control and reaching throughout infancy
Boxum, Anke
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Boxum, A. (2018). Postural control and reaching throughout infancy: In cerebral palsy and in typical
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In cerebral palsy and in typical development
Stichting Beatixoord Noord-Nederland, Noord Negentig, Chipsoft B.V. ©2018 Anke G. Boxum
No parts of this thesis may be reproduced, stored or transmitted in any form or by any means without permission of the author or the publishers holding the copy-right of the published articles.
ISBN (printed version) 978-94-034-0802-6 ISBN (electronic version) 978-94-034-0801-9 Cover design: Koen Bos
throughout infancy
In cerebral palsy and in typical development
Proefschrift
ter verkrijging van de graad van doctor aan de
Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken
en volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op
woensdag 19 september 2018 om 16.15 uur
door
Anke Geertje Boxum
geboren op 04 oktober 1991
Copromotores
Dr. H.A. Reinders-Messelink
Dr. S. la Bastide-van Gemert
Beoordelingscommissie
Prof. dr. G.J.P. Savelsbergh
Prof. dr. B. Steenbergen
Prof. dr. O.F. Brouwer
Chapter 1 9
General introduction
Chapter 2 29
Postural adjustments in infants at very high risk for cerebral palsy before and after developing the ability to sit independently
Early Human Development 2014 Sep; 90:435–41
Chapter 3 51
Are postural adjustments during reaching related to development of walking in typically-developing infants and infants at risk of cerebral palsy?
Infant Behavior and Development 2017 Dec; 50:107–115
Chapter 4 69
Postural control during reaching while sitting and general motor behaviour when learning to walk
Developmental Medicine and Child Neurology 2018 Jun; epub ahead of print
Chapter 5 91
Development of postural control in infancy in cerebral palsy and cystic periventricular leukomalacia
Research in Developmental Disabilities 2018 May; 78:66–77
Chapter 6 117
Development of the quality of reaching in infants with cerebral palsy: a kinematic study
Developmental Medicine and Child Neurology 2017 Nov; 59:1164–1173
Chapter 7 137 General discussion Chapter 8 155 Summary Nederlandse samenvatting Dankwoord 166 Over de auteur 169 List of publications 171
1
“Every single brain is absolutely individual, both in its development and in the way it encounters the world”, is what Gerald Edelman wrote, cell biologist and physician. In his books on the biological theory of consciousness, he presents the theory of Neuronal Group Selection (NGST). Using the framework of the NGST to describe human motor development, this thesis sheds light on the development of postural control in typically developing infants and infants at very high risk of cerebral palsy.
Motor development
The NGST is one of many theories describing motor development. In the theories, the contribution of nature and nurture to motor development remains an ongoing debate. Outdated neuromaturational theories assume that the normal sequences of motor development are the consequence of genetically determined structural changes in the central nervous system.1–3 On the contrary, the Dynamic Systems Theory emphasizes the importance of interaction with the environment and con-siders motor development as a non-linear process. Motor behaviour is considered to be the product of multiple interacting sub-systems within the body with dif-ferent tasks and environments. Spontaneous self-organization of the sub-systems produces the most efficient motor strategy for specific tasks.4–6 The NGST meets both theories halfway by emphasizing a complex interaction between nature and nurture: the theory acknowledges the genetically determined organization of vari-able networks in the central nervous system, while also endorsing the effect of interaction with the environment.
Gerald Edelman argued that the formation of the cortical and subcortical structures into networks is determined by genetic factors, in which development and growth determine the formation of individual synaptic connections between neurons and determine their organization in functional neuronal groups. This pro-cess induces a tremendous amount of variation in neural circuitries between indi-viduals. The functional plasticity of the neuronal groups and the abundant neuro-nal connections facilitate the organization of complex and adaptable ‘networks’ of neuronal groups. Within these primary networks, neurons are stronger connected to each other than to neurons in other networks. After forming the initial primary networks, development continues by the process of selection. Selection of specific neuronal groups for specific behaviour is modulated by afferent signals providing information on the success of behaviour, thereby changing the strength of synap-tic connections between neurons and neuronal groups. The process of selection results in the formation of secondary networks with altered connectivity, in which
specific neuronal groups will be selected for different situations. Edelman draws similarities with Charles Darwin’s Theory of Natural Selection, accordingly he refers to his theory as Neural Darwinism.7–9
When human motor development is described according to the framework of the NGST,10,11 two phases of variability can be distinguished.10,11 In the phase of primary variability, young infants first explore the many possibilities of the central nervous system. This phase is characterized by abundant variation in motor activi-ties: a large repertoire of motor actions. The output of the self-produced motor behaviour gives rise to afferent information, which will in turn provide information on selection of the best motor strategy for a specific situation: the phase of second-ary variability. The selection process of the motor strategy is based on the selection of specific neuronal groups.11
An early brain lesion may cause damage to the different primary neuronal networks, leading to less possibilities for exploring motor actions of the central nervous system. Clinically it will result in less variation: a poor repertoire of motor actions. As motor impairments due to brain lesions are often associated with other impairments such as visual problems, the selection process in the secondary vari-ability is often also hampered. The development of secondary neuronal networks is therefore presumably delayed and the secondary networks will remain limited in infants with brain lesions.10
Cerebral palsy
Cerebral palsy (CP) is caused by a lesion to the developing brain and is one of the most common developmental motor disorders in children, with an incidence around 2 on 1000 live births.12,13 According to the definition of Bax et al. (2005), Cere-bral palsy is “a heterogeneous group of motor disorders. CP describes a group of disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing fetal or infant brain. The motor disorders of cerebral palsy are often accompanied by disturbances of sensation, cognition, communication, perception, and/or behav-iour, and/or by a seizure disorder.” 14
As the definition proposes, CP can be caused by different lesions to the brain during pregnancy, delivery or the first months of postnatal life. For instance parenchymal infarctions or haemorrhages can result in CP. Also periventricular leu-komalacia is a well-known cause of CP, it occurs most often in premature infants. Actually, cystic periventricular leukomalacia (cPVL) is one of the most severe lesions to the developing brain, in which cyst formation is the result of focal periventricular
1
necrosis. Around the cysts, generally a more diffuse damage of the cerebral white matter is present, including the cortical subplate.15 The variety in brain lesions caus-ing CP lead to different and heterogeneous appearances of CP. Spastic CP is the most common type, in which a hypertonic muscle tone is most prominent. Ataxic CP is mainly characterized by problems in balance and loss of normal muscle coordi-nation and dyskinetic CP by a fluctuating muscle tone and involuntary stereotyped movements. In addition, CP can be classified according to the distribution of the limbs involved: the symptoms can be uni- or bilateral.16 Also severity of CP varies: children with Gross Motor Function Classification System (GMFCS) level I are least affected and are able to walk independently, while children with GMFCS level V are not able to move around independently, or use electric wheelchairs with extensive adaptations.17
The clinical diagnosis of CP requires serial examinations, as clinical signs can evolve or resolve when the nervous system matures.18 The diagnosis is often made in the first two years of life, but when symptoms are mild, the diagnosis can be delayed.19 In terms of motor development, infants who are later diagnosed with CP are delayed in the development of milestones, and show a reduced variation in movements in different positions.
Postural control
Assessment of postural control
As the definition of CP indicates, a major motor problem in CP is postural dysfunc-tion. Every motor activity requires proper postural control; the body needs to main-tain its balance and keep the centre of mass within the support surface.20 Postural control is essential for virtually all daily life activities, yet most of the time we are not aware of using the postural control system, until it is challenged or damaged. Postural control is a highly complex task, in which almost all parts of the central nervous system are involved.21,22 The complexity ensures a long-lasting develop-ment, at least until adolescence. It can be assessed in different ways.
Some researchers focus on the assessment of postural sway: the body is never able to stand perfectly still, it continuously ‘sways’ due to everlasting cor-rections in posture by the central nervous system. The sway might indicate that the central nervous system searches for the limits of the stability.23 By studying postural sway, centre of pressure (COP) parameters are often used. The COP indi-cates the point of application of the vector of the ground reaction force, in which
the vector of the ground reaction force represents the sum of all forces between the supporting surface and the body. When analysing COP behaviour, multiple parameters can be used, including postural sway area and amplitude, COP velocity and COP travel path. The parameters yield in particular information on the size of postural sway, and little on neural control mechanisms.
Research on postural sway provides information on the net result of the postural control system, but does not include information on the muscular strate-gies of the central nervous system to achieve the stability. Bernstein (1935) real-ized that the central nervous system had to cope with many degrees of freedom in upright stance, induced by a body consisting of multiple joints and muscles. He suggested that the nervous system solved this problem by creating motor syn-ergies. Motor synergies provide supraspinal control centres with the possibility of activating a predefined set of muscles, instead of controlling every singular muscle contraction.24 In 1994, Forssberg and Hirschfeld divided the neural con-trol of postural synergies into two functional levels, the first level was labelled as direction-specificity. It means that when the body sways in a forward direction, the dorsal muscles are activated prior to the ventral muscles in order to maintain bal-ance. When the body sways backward, ventral muscles are activated primarily. At the second level, these directionally appropriate adjustments are adapted to the specifics of the situation.25 The muscular activity can be assessed by means of sur-face electromyography (EMG). In EMG-studies, mainly two types of paradigms are used. In the first paradigm the participants rely on feedback mechanisms (reac-tive neural control) when experiencing external perturbations from e.g., a moving platform. On the other hand, feedforward mechanisms (active neural control) can be assessed. In this case participants rely on anticipatory postural control, for example tested during reaching movements.
Typical postural development
Evidence shows that postural sway decreases with increasing age and experience, in supine,26 sitting27 and upright stance.28,29 Regarding muscular postural control, the principles of the NGST can be applied to its development. In early infancy, the postural activity is highly variable, and not adapted to the situation: the phase of primary variability.30 Secondary variability emerges when the second level of postural control starts to become functional.
Already at the age of one month, infants are able to produce (reactive) direction-specific adjustments in 85% of the testing trials in the dorsal muscles, when placed in sitting position on a moving platform. The presence of the first
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level of postural control at this age suggests an innate origin.31 Direction-specificity in sitting during external perturbations remains around 70–85% until the age of 4–5 months and is consistently present from 7–8 months onwards.32–34 In stand-ing position, direction-specificity on a movstand-ing platform is not consistently pres-ent in infants in the pull-to-stand phase with35 and without support.36 However, infants who are able to stand independently all show consistent direction-spec-ificity during external perturbations.35,37,38 Active – and internally triggered – pos-tural control shows a slightly different development, mostly studied during reach-ing in sittreach-ing or supine position. At the age of 4–6 months, when goal-directed reaching movements emerge, infants show variable direction-specificity of dorsal muscles in about 40–50% of the reaching movements.39,40 Throughout infancy, the percentage increases to 60–80% at 18 months40 and reaches 100% at the age of two years.41 However, no literature is available addressing the question whether the development of direction-specificity during reaching is related to age or to developmental stage such as learning to sit or walk independently.
In the phase of secondary variability, the second level of postural control becomes functional.25 Every situation requires a different postural strategy and muscle activity. For instance, a reaching movement in sitting position demands other postural activities than a reaching movement in standing position. The fine-tuning of the direction-specific adjustments is adapted to the difficulty of the postural task. The development of adaptation to the situation starts for example with the selection of the complete pattern – the pattern in which all the direction-specific muscles are activated in concert. During external pertur-bations in sitting, the complete pattern is present in 5–20% of the perturpertur-bations at 1 month of age, disappears around 3 months and emerges again after 3–4 months. It increases to about 30–50% at 6 months, 75–100% at 9–10 months of age and after the age of 2,5–3 years the preference for the complete pattern disappears again.31,34,42 In standing, the dominance of the complete pattern is present from 2 years onwards, at least until the age of 10 years.35,37,43 During internally triggered postural adjustments while reaching in sitting position, the complete pattern is present in about 50% of the reaching movements at 6 months.39 It becomes the preferred pattern until 18 months,40 but the preference for this pattern disappears again after 18–24 months.41,42 The difference in timing of presence of the complete pattern in different positions and during differently triggered (external or internal) perturbations show that fine-tuning of postural control depends on the situation and difficulty of the postural task. Other ways of adaptation to the situation are changing the order of recruitment of the pos-tural muscles, antagonistic activity, activating the pospos-tural muscle prior to the movement (anticipatory activity) and the most subtle way of adaptation is the
modulation of the muscle contraction.23,25 As postural control is a highly complex neural task, adult levels of the second level of postural control will only be reached after adolescence.41
Atypical postural development
Considering the complexity of postural control, it is not surprising that the pos-tural control system is vulnerable for brain injury, resulting in problems in children with CP. Postural sway data indicates that infants at risk of CP and children with CP show a worse postural stability compared to typically developing infants and children.44–46 Regarding muscular postural control, children with CP are in general able to produce direction-specific adjustments at school-age, but show difficul-ties with the second level of postural control. The degree of dysfunction is related to the severity of CP.47 In the study of van der Heide et al. (2004), children with CP used a stereotyped top-down recruitment order during reaching in sitting position, while typically developing (TD) children showed variation and at the youngest ages a slight preference for bottom-up recruitment. Children with CP also presented with problems in modulating the degree of muscle contraction to sitting position and reaching velocity.47
As the diagnosis of CP cannot be made in the first year of life, research into the development of these problems is mainly restricted to infants at high risk of CP (HR-infants). Van Balen et al. (2015) showed that in early infancy, HR-infants have similar postural strategies as TD-infants, but display a delayed development of direction-specificity at 18 months. HR-infants also had lower rates of anticipa-tory activity, used less often the complete pattern and had longer latencies to recruitment of postural muscles at 18 months, but did not differ from TD-infants early in infancy.48 However, in this study only five of the 23 HR-infants developed CP. Another study described the development of seven infants who were all diag-nosed with CP at 18 months. The five infants with unilateral spastic CP showed direction-specificity and similar features of the second level of postural control as TD-infants from 15 months onwards, with the exception that they were not able to modulate postural muscle contraction. One infant with bilateral CP had a similar postural development as the infants with unilateral spastic CP but the develop-ment was slower. The other infant was diagnosed with bilateral CP and athetosis, she presented with a lack of direction-specificity and a disorganized second level of control.49
Literature on postural control in infants and children with severe CP is scarce. Infants or children with severe CP often use adaptive seating systems with
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support of the trunk, pelvis, head and/or legs to engage in daily life activities,50,51 but it is unknown to what extent the children regulate their own postural control. Follow-up at 4 years of the infant lacking direction-specificity revealed that she was not able to sit independently.49 Another 4-year-old child with CP from a different study also lacked direction-specificity during perturbation experiments and was not able to sit independently.52 These two case reports of children with CP function-ing at GMFCS level V suggest that the absence of the basic level of postural control precludes the development of independent sitting. Also children with GMFCS level IV require trunk support during sitting,17 and postural control data of 8 children with CP with GMFCS level IV indicated a variable and inconsistent presence of direction-specific muscle activity at neck or leg level.47,53 The latter data complement the sug-gestion of a relation between direction-specificity and independent sitting.
The above indicates that the development of the postural problems in early infancy in CP (instead of in high-risk infants) remains mostly unknown. Also the effect of different types of brain lesions on postural development is lacking.
Reaching
Typical development of reaching
Most of the studies on internally triggered postural adjustments were conducted during reaching in sitting position, as successful reaching is highly dependent on postural control. It requires involvement of the whole body. This is for example demonstrated by research showing that infants who are not able to sit improve in reaching quality when extra pelvic support is provided54 and research showing that more direction-specificity in sitting position was associated with a higher per-centage of reaching movements resulting in successfully grasping or touching the object.39 Reaching is an important milestone, e.g. it offers the possibility to explore the environment, it is involved in many daily life activities like eating and drinking and it is essential for interaction with other infants or adults.55,56 Important neural circuits, including primary motor and somatosensory cortices and frontal and pari-etal areas are involved in reaching movements. Learning to reach is challenging, not only in view of the neural complexity, but also considering the biomechanical complexity.
Newborn infants are not able to reach and grasp objects. Soon after birth, they start to follow objects or persons with their eyes. As soon as interest in the environment emerges, the infant starts to move the arms in response to an
attrac-tive object more often than might be expected by chance.57 These are so-called pre-reaching movements.58 Around the age of 4 months, infants accomplish to grasp the presented object, although the reaching movement is not yet smooth and fluent.59 Reaching movements are variable in speed, duration, trajectory and amplitude.5,60 During the next few months, they become rapidly more smooth and fluent.59,61 Ini-tially, infants use both hands for reaching and grasping movements. Around the age of 6–8 months it changes to a preference for unilateral reaching, although the preference for uni- or bilateral reaching remains dependent on the position of the infant and the size and shape of the object.62,63
Kinematically, reaching movements can be described using the number of corrections in the movement trajectory: movement units (MUs). One MU consists of one acceleration and one deceleration in the velocity profile of the reaching movement.61,64 In adults the reaching movements usually involve one MU; it indi-cates that reaching movements are programmed in advance. Infants who just mastered the ability to reach towards an object around the age of 4–5 months, produce reaching movements with several MUs.61,64 It suggests that infants at this age mainly rely on feedback mechanisms and continuously adapt the trajectory of the reaching movement. The number of MUs decreases rapidly until the age of 6 months.59,61,65 After this age, development of reaching continues to improve until adolescence.59,66,67 Also in other reaching parameters the major part of the improve-ment is seen between 4 and 6 months.59,61,65 Parameters that rely on feedforward control are for example the relative size of the transport MU – the first MU that covers most of the transport of the hand – and the curvature index describing the straightness of the movement. Reaching parameters that rely on a mix of feedfor-ward and feedback mechanisms are reaching duration, average speed and length of the movement.68
Atypical reaching development
Van der Heide et al. (2005) showed that at school-age, children with CP have a worse kinematic reaching quality of the dominant arm compared to TD-children, expressed as longer reaching durations, lower average speed and less often reaching move-ments consisting of one MU. The transport MU appeared to be smaller in children with bilateral CP compared to TD-children, but the transport MUs of children with unilateral CP were similar to those of TD-children. Performance on kinematic parameters was associated with severity of CP: infants with severe CP scored worse than infants with mild or moderate CP. The detailed kinematic reaching parameters were also associated with scores on the Pediatric Evaluation of Disability Inventory
1
(PEDI), indicating that better kinematic reaching quality was associated with better functional performance in daily life.69 Also other studies revealed that children with CP show a worse kinematic reaching quality than TD-children.70,71
Research into the development of these problems is again restricted to infants at risk, as neurological outcome is difficult to predict at early age. Heteroge-neous groups of preterm infants have been studied. Compared to full-term infants not at risk, the kinematics of reaching in low-risk preterm infants show signs of slightly advanced development at 4 months CA – probably due to more extrauter-ine experience.72 At 6 and 8 months CA, low-risk preterm infants use less efficient reaching strategies compared to term-aged peers.73,74 However, high-risk preterms, i.e., infants with an Apgar score < 3 after 5 minutes or with respiratory problems, do not have an advantage in kinematic characteristics of reaching compared to full-term infants at any age, presumably because the negative effects of prefull-term birth overshadow the advantages of additional extrauterine experience. At 6 months, high-risk preterms show less optimal reaching movements compared to full-term and low-risk infants, as expressed by a combined measure of peak velocity and number of MUs.72 The study of Fallang et al. (2005) showed that this worse kinematic reaching quality at 6 months was related to the development of complex minor neurological dysfunction and fine manipulative disability at the age of 6 years.75 It suggests that already at early age, the subtle measure of kinematic reaching quality is associated with neurological outcome. However, in these studies, infants who later developed CP or infants with a very high risk of CP were excluded. There-fore the development of the kinematic reaching problems in CP remains largely unknown.
Early intervention
Promoting postural control is incredibly important, considering its involvement in virtually every daily life activity. Therefore, postural problems, but also other motor impairments, are frequently addressed in early intervention programs. Early intervention is likely to be most beneficial early in infancy, in light of the consid-erable plasticity of the brain in early life. Neuroplasticity refers to the ability of the central nervous system to mature, structurally and functionally change and adapt to experiences or injury throughout the life of an individual. Considering the many developmental changes and the formation and adaptation of the neuronal networks based on experiences at a young age, neuroplasticity seems to be more extensive early in life, creating opportunities for early intervention in infants with brain lesions.10,18,76–78 The efficacy of different early intervention programs
on neuro-logical and motor outcome however, is largely unknown. Studies evaluating differ-ent forms of early intervdiffer-ention programs are often of low quality, with small sample sizes, and they vary widely in intervention approaches, length of intervention and outcome measures.79–82 The indistinct effect of different early intervention programs was the inspiration for the development of an early intervention program based on the principles of the NGST: COPing with and CAring for infants with special needs (COPCA).83 The effects and working mechanisms of COPCA were compared to tra-ditional infant physiotherapy (TIP) in the Netherlands in a randomized controlled trial: LEARN 2 MOVE 0–2 years (L2M 0–2).84 To understand working mechanisms of an intervention program and evaluate whether intervention has an effect on postural development, it is essential to know typical and atypical developmental patterns of postural control. Thus, within L2M 0–2, data were collected on reaching and pos-tural control throughout infancy.
Study groups of the thesis
LEARN 2 MOVE 0–2 years
LEARN 2 MOVE is a Dutch national research program evaluating the effects and working mechanisms of age-specific intervention programs for infants, children and adolescents with CP.85 The national program is divided into four age cohorts, with the youngest cohort being L2M 0–2 years.84 As the diagnosis CP can only reli-ably be made after 18 months, L2M 0–2 deals with infants at high risk of CP.
In L2M 0–2 years, the effects of two types of early intervention are assessed in infants at very high risk of CP. The infants were included before the corrected age of 9 months, based on a severe brain lesion around birth, or neurological dysfunc-tion suggestive for the development of CP. The infants received 1 year of intervendysfunc-tion: either traditional infant physiotherapy (TIP) or COPCA.84 TIP is in the Netherlands mainly based on the principles of neurodevelopmental treatment (NDT). Tradition-ally, Karel and Berta Bobath – the founders of NDT – aimed at inhibiting spasticity and abnormal reflexes by using handling techniques to facilitate normal movement patterns and muscle tone.86 As neuroscience and paediatric physiotherapy devel-oped and the Bobaths gained more experience through the years, NDT evolved into a living concept: the treatment principles changed according to additional
under-1
standing of the central nervous system and its associated disorders. The goal is nowadays to enhance daily function of the individual by teaching the infant typical movement patterns. Direct handling techniques are used to provide the infant with sensorimotor experiences of typical movements. The physical therapist teaches the parents treatment techniques to incorporate the intervention into daily life.87,88
COPCA is a family centred program with two components. The first compo-nent is the family: COPCA focusses on family autonomy, responsibility and parent-ing specific for the family. A coach observes and helps the family to challenge the infant in different daily life activities, within the family’s own perspective on raising a child. The second neurodevelopmental component is based on the principles of the NGST. COPCA is aimed at functional mobility of the individual, and accepts atypical motor patterns if they do not hamper but promote participation in daily life activities. COPCA acknowledges the importance of variation in motor develop-ment, and intends to promote the exploration of means to enlarge the reduced motor repertoire. In addition, the child is challenged to explore and select within his available motor strategies. Facilitation techniques are avoided, the infant learns and develops by means of trial-and-error experiences during self-produced motor behaviour.83
The postural control and kinematic data of reaching in this thesis were col-lected as additional explorative data on the working mechanisms of intervention in the 43 infants at very high risk of CP participating in L2M 0–2.
Pocowalk
During the course of postural control and kinematic data collection and analysis in L2M 0–2, a gap in knowledge of postural control data of typically developing infants became evident. The ultimate goal of human postural control is aimed at standing and walking on a narrow support base. Yet, no study had addressed the relationship between muscular postural control and the development of indepen-dent walking. To this end, the POCOWALK study was designed. Twenty-eight typically developing infants were included when they were at the verge of being able to walk independently. Longitudinal postural control and kinematic data in sitting position while reaching were collected at 3 points in time: 1) when the infant could pull to stand but was not able to walk independently; 2) within one week after the infant had mastered to take his first steps; 3) one month after the second session.
Aim and outline of the thesis
This thesis focuses on postural control and reaching in typically developing infants and infants at very high risk of CP. The aim is to explore and increase understanding on the development of postural control and reaching in typically developing and high-risk infants, which may in turn provide knowledge and clues for early interven-tion. Insight in developmental trajectories of postural control during the develop-ment of milestones and in infants with different types of brain lesions or severity of symptoms may for example guide early intervention towards early postural training or the early provision of external support.
Chapter 2 comprises a study investigating whether muscular postural parameters change when typically developing infants and infants at very high risk of CP develop the ability to sit independently. Since case-reports from the literature suggested that direction-specificity could be a prerequisite for the development of independent sitting, we hypothesize that postural parameters would improve when learning to sit independently.
Chapter 3 evaluates differences in postural control of the high-risk infants of L2M 0–2 and typically developing infants before and after the infants develop the ability to walk independently. We hypothesize that if the postural parameters are related to independent walking, postural control will improve after learning to walk independently.
Chapter 4 deals with a more detailed look into the development of postural muscle activity in typically developing infants during the emergence of learning to walk – the POCOWALK study. We hypothesize that developing the ability to walk independently requires a reorganization in postural control. We assess whether infants who just mastered to take their first steps differ in postural control from infants who are not able to walk and those who have more walking experience.
Chapter 5 consists of a study evaluating the longitudinal development of postural control in VHR-infants throughout infancy. The effects of the diagnosis of CP and presence of cystic periventricular leukomalacia on development of pos-tural control are explored. Corresponding to prior research, we expect that infants developing CP would ‘grow into a postural deficit’ with increasing age. However, we also predict that infants with cystic periventricular leukomalacia – one of the most severe brain lesions – will show postural problems from early age onwards.
1
Chapter 6 describes the longitudinal development of kinematic reaching quality in VHR-infants throughout infancy. Again, the effects of presence of cystic periventricular leukomalacia and diagnosis of CP are taken into account. Corre-sponding to chapter 5, we hypothesize that infants with CP 'grow into a deficit', while infants with cystic periventricular leukomalacia show difficulties with reach-ing from early age onwards.
Chapter 7 provides a general discussion on the results and contents of this thesis and provides clinical implications and prospects for future research.
References
1. Gesell A, Amatruda C. Developmental diagnosis. Normal and abnormal child development. 2nd ed. Harper & Row: New York, 1947.
2. McGraw MB. Later development of children specially trained during infancy, Johnny and Jimmy at school age. Child Dev 1939; 10: 1–19.
3. McGraw MB. The neuromuscular maturation of the human infant. Reprinted: Classics
in Devel-opmental Medicine No. 4. Mac Keith Press: London, 1989.
4. Thelen E. Developmental origins of motor coordination: leg movements in human infants. Dev
Psychobiol 1985; 18: 1–22.
5. Thelen E, Corbetta D, Kamm K, Spencer JP, Schneider K, Zernicke RF. The transition to reaching: mapping intention and intrinsic dynamics. Child Dev 1993; 64: 1058–98.
6. Ulrich BD. Dynamic systems theory and skill development in infants and children. In: Connolly K, Forssberg H (eds). Neurophysiology and neuropsychology of motor development. Clinics
in Developmental Medicine No 143–144. Mac Keith Press: London, 1997, pp 319–345.
7. Edelman GM. Neural Darwinism. The theory of neuronal group selection. Oxford University Press: Oxford, 1989.
8. Edelman GM. Neural Darwinism: selection and reentrant signaling in higher brain function.
Neuron 1993; 10: 115–25.
9. Sporns O, Edelman GM. Solving Bernstein’s problem: a proposal for the development of coor-dinated movement by selection. Child Dev 1993; 64: 960–81.
10. Hadders-Algra M. The neuronal group selection theory: promising principles for understand-ing and treatunderstand-ing developmental motor disorders. Dev Med Child Neurol 2000; 42: 707–15. 11. Hadders-Algra M. The neuronal group selection theory: a framework to explain variation
in normal motor development. Dev Med Child Neurol 2000; 42: 566–72.
12. Himmelmann K, Uvebrant P. The panorama of cerebral palsy in Sweden. XI. Changing patterns in the birth-year period 2003–2006. Acta Paediatr 2014; 103: 618–24.
13. Sigurdardóttir S, Thórkelsson T, Halldórsdóttir M, Thorarensen O, Vik T. Trends in prevalence and characteristics of cerebral palsy among Icelandic children born 1990 to 2003. Dev Med
Child Neurol 2009; 51: 356–63.
14. Bax M, Goldstein M, Rosenbaum P, Leviton A, Paneth N, Dan B et al. Proposed definition and classification of cerebral palsy, April 2005. Dev Med Child Neurol 2005; 47: 571–6.
15. Volpe JJ. Neurology of the Newborn. WB Saunders: Philadelphia, 2008, pp 359–379.
16. Surveillance of Cerebral Palsy in Europe. Surveillance of cerebral palsy in Europe: a collabora-tion of cerebral palsy surveys and registers. Surveillance of Cerebral Palsy in Europe (SCPE).
Dev Med Child Neurol 2000; 42: 816–24.
17. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child
1
18. Hadders-Algra M. Early diagnosis and early intervention in cerebral palsy. Front Neurol 2014; 5: 185. 19. Paneth N. Establishing the diagnosis of cerebral palsy. Clin Obstet Gynecol 2008; 51: 742–8. 20. Massion J. Postural control system. Curr Opin Neurobiol 1994; 4: 877–87.
21. Dietz V. Human neuronal control of automatic functional movements: interaction between central programs and afferent input. Physiol Rev 1992; 72: 33–69.
22. Massion J, Alexandrov A, Frolov A. Why and how are posture and movement coordinated? Prog
Brain Res 2004; 143: 13–27.
23. Hadders-Algra M. The development of postural control. In: Hadders-Algra M, Brogren-Carlberg E (eds). Postural control: a key issue in developmental disorders. Mac Keith Press: London, 2008, pp 22–73.
24. Bernstein N. The problem of the interrelation of co-ordination and localization. Reprinted
in Human Motor Actions. Bernstein Reassessed. Elsevier: Amsterdam, 1984.
25. Forssberg H, Hirschfeld H. Postural adjustments in sitting humans following external pertur-bations: muscle activity and kinematics. Exp brain Res 1994; 97: 515–27.
26. Fallang B, Saugstad OD, Hadders-Algra M. Goal directed reaching and postural control in supine position in healthy infants. Behav Brain Res 2000; 115: 9–18.
27. Cignetti F, Kyvelidou A, Harbourne RT, Stergiou N. Anterior-posterior and medial-lateral con-trol of sway in infants during sitting acquisition does not become adult-like. Gait Posture 2011; 33: 88–92.
28. Hallemans A, De Clercq D, Van Dongen S, Aerts P. Changes in foot-function parameters during the first 5 months after the onset of independent walking: a longitudinal follow-up study. Gait
Posture 2006; 23: 142–8.
29. Verbecque E, Vereeck L, Hallemans A. Postural sway in children: A literature review. Gait
Pos-ture 2016; 49: 402–10.
30. Hadders-Algra M. Development of postural control during the first 18 months of life. Neural
Plast 2005; 12: 99–108–72.
31. Hedberg A, Forssberg H, Hadders-Algra M. Postural adjustments due to external perturbations during sitting in 1-month-old infants: evidence for the innate origin of direction-specificity.
Exp brain Res 2004; 157: 10–7.
32. Harbourne RT, Giuliani C, Neela JM. A kinematic and electromyographic analysis of the devel-opment of sitting posture in infants. Dev Psychobiol 1993; 26: 51–64.
33. Hadders-Algra M, Brogren E, Forssberg H. Ontogeny of postural adjustments during sitting in infancy: variation, selection and modulation. J Physiol 1996; 493 (Pt 1): 273–88.
34. Hedberg A, Carlberg EB, Forssberg H, Hadders-Algra M. Development of postural adjustments in sitting position during the first half year of life. Dev Med Child Neurol 2005; 47: 312–20. 35. Sveistrup H, Woollacott MH. Longitudinal Development of the Automatic Postural Response
in Infants. J Mot Behav 1996; 28: 58–70.
36. Hedberg A, Schmitz C, Forssberg H, Hadders-Algra M. Early development of postural adjust-ments in standing with and without support. Exp brain Res 2007; 178: 439–49.
37. Forssberg H, Nashner LM. Ontogenetic development of postural control in man: adaptation to altered support and visual conditions during stance. J Neurosci 1982; 2: 545–52.
38. Woollacott M, Debu B, Mowatt M. Neuromuscular control of posture in the infant and child: is vision dominant? J Mot Behav 1987; 19: 167–86.
39. de Graaf-Peters VB, Bakker H, van Eykern LA, Otten B, Hadders-Algra M. Postural adjustments and reaching in 4- and 6-month-old infants: an EMG and kinematical study. Exp brain Res 2007; 181: 647–56.
40. Van Balen LC, Dijkstra LJ, Hadders-Algra M. Development of postural adjustments during reaching in typically developing infants from 4 to 18 months. Exp Brain Res 2012; 220: 109–119. 41. van der Heide JC, Otten B, van Eykern LA, Hadders-Algra M. Development of postural
adjust-ments during reaching in sitting children. Exp brain Res 2003; 151: 32–45.
42. Hadders-Algra M, Brogren E, Forssberg H. Postural adjustments during sitting at preschool age: presence of a transient toddling phase. Dev Med Child Neurol 1998; 40: 436–47.
43. Sundermier L, Woollacott M, Roncesvalles N, Jensen J. The development of balance control in children: comparisons of EMG and kinetic variables and chronological and developmental groupings. Exp brain Res 2001; 136: 340–50.
44. Kenis-Coskun O, Giray E, Eren B, Ozkok O, Karadag-Saygi E. Evaluation of postural stability in children with hemiplegic cerebral palsy. J Phys Ther Sci 2016; 28: 1398–402.
45. Donker SF, Ledebt A, Roerdink M, Savelsbergh GJP, Beek PJ. Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children. Exp brain Res 2008; 184: 363–70.
46. Kyvelidou A, Harbourne RT, Willett SL, Stergiou N. Sitting postural control in infants with typi-cal development, motor delay, or cerebral palsy. Pediatr Phys Ther 2013; 25: 46–51.
47. van der Heide JC, Begeer C, Fock JM, Otten B, Stremmelaar E, van Eykern LA et al. Postural control during reaching in preterm children with cerebral palsy. Dev Med Child Neurol 2004; 46: 253–66.
48. Van Balen LC, Dijkstra LJ, Bos AF, Van Den Heuvel ER, Hadders-Algra M. Development of pos-tural adjustments during reaching in infants at risk for cerebral palsy from 4 to 18 months.
Dev Med Child Neurol 2015; 57: 668–676.
49. Hadders-Algra M, van der Fits IB, Stremmelaar EF, Touwen BC. Development of postural adjust-ments during reaching in infants with CP. Dev Med Child Neurol 1999; 41: 766–76.
50. Rigby PJ, Ryan SE, Campbell KA. Effect of adaptive seating devices on the activity performance of children with cerebral palsy. Arch Phys Med Rehabil 2009; 90: 1389–95.
51. Angsupaisal M, Maathuis CGB, Hadders-Algra M. Adaptive seating systems in children with severe cerebral palsy across International Classification of Functioning, Disability and Health for Chil-dren and Youth version domains: a systematic review. Dev Med Child Neurol 2015; 57: 919–30. 52. Hadders-Algra M, Brogren E, Katz-Salamon M, Forssberg H. Periventricular leucomalacia and
preterm birth have different detrimental effects on postural adjustments. Brain 1999; 122 (Pt 4): 727–40.
1
53. Brogren E, Forssberg H, Hadders-Algra M. Influence of two different sitting positions on pos-tural adjustments in children with spastic diplegia. Dev Med Child Neurol 2001; 43: 534–46. 54. Hopkins B, Rönnqvist L. Facilitating postural control: effects on the reaching behavior of
6-month-old infants. Dev Psychobiol 2002; 40: 168–82.
55. Lobo MA, Galloway JC. The onset of reaching significantly impacts how infants explore both objects and their bodies. Infant Behav Dev 2013; 36: 14–24.
56. Bakeman R, Adamson LB. Coordinating attention to people and objects in mother-infant and peer-infant interaction. Child Dev 1984; 55: 1278–89.
57. Bower TG, Broughton JM, Moore MK. Demonstration of intention in the reaching behaviour of neonate humans. Nature 1970; 228: 679–81.
58. Trevarthen C. How control of movements develops. In: Whiting HTA (ed). Human motor actions.
Bernstein reassessed. Elsevier: Amsterdam, 1984, pp 223–261.
59. Konczak J, Borutta M, Topka H, Dichgans J. The development of goal-directed reaching in infants: hand trajectory formation and joint torque control. Exp brain Res 1995; 106: 156–68. 60. von Hofsten C, Rönnqvist L. The structuring of neonatal arm movements. Child Dev 1993; 64:
1046–57.
61. Hofsten C von. Structuring of early reaching movements: a longitudinal study. J Mot Behav 1991.
62. Rochat P. Self-sitting and reaching in 5- to 8-month-old infants: the impact of posture and its development on early eye-hand coordination. J Mot Behav 1992; 24: 210–20.
63. Newell KM, Scully DM, McDonald P V, Baillargeon R. Task constraints and infant grip configura-tions. Dev Psychobiol 1989; 22: 817–31.
64. Hofsten C von. Development of visually directed reaching: The approach phase. J Hum Mov
Stud 1979; 5: 160–178.
65. Mathew A, Cook M. The control of reaching movements by young infants. Child Dev 1990; 61: 1238–57.
66. Fetters L, Todd J. Quantitative assessment of infant reaching movements. J Mot Behav 1987; 19: 147–66.
67. Kuhtz-Buschbeck JP, Stolze H, Jöhnk K, Boczek-Funcke A, Illert M. Development of prehension movements in children: a kinematic study. Exp brain Res 1998; 122: 424–32.
68. Angsupaisal M, Dijkstra L-J, la Bastide-van Gemert S, van Hoorn JF, Burger K, Maathuis CGB
et al. Best seating condition in children with spastic cerebral palsy: One type does not fit all. Res Dev Disabil 2017; 71: 42–52.
69. van der Heide JC, Fock JM, Otten B, Stremmelaar E, Hadders-Algra M. Kinematic characteristics of reaching movements in preterm children with cerebral palsy. Pediatr Res 2005; 57: 883–9. 70. Aboelnasr EA, Hegazy FA, Altalway HA. Kinematic characteristics of reaching in children with
hemiplegic cerebral palsy: A comparative study. Brain Inj 2017; 31: 83–89.
71. Jaspers E, Desloovere K, Bruyninckx H, Klingels K, Molenaers G, Aertbeliën E et al. Three-dimensional upper limb movement characteristics in children with hemiplegic cerebral palsy
72. Fallang B, Saugstad OD, Grøgaard J, Hadders-Algra M. Kinematic quality of reaching move-ments in preterm infants. Pediatr Res 2003; 53: 836–42.
73. Toledo AM, Tudella E. The development of reaching behavior in low-risk preterm infants.
Infant Behav Dev 2008; 31: 398–407.
74. Grönqvist H, Strand Brodd K, von Hofsten C. Reaching strategies of very preterm infants at 8 months corrected age. Exp brain Res 2011; 209: 225–33.
75. Fallang B, Øien I, Hellem E, Saugstad OD, Hadders-Algra M. Quality of reaching and postural control in young preterm infants is related to neuromotor outcome at 6 years. Pediatr Res 2005; 58: 347–53.
76. Ismail FY, Fatemi A, Johnston M V. Cerebral plasticity: Windows of opportunity in the develop-ing brain. Eur J Paediatr Neurol 2017; 21: 23–48.
77. Kolb B, Mychasiuk R, Muhammad A, Gibb R. Brain plasticity in the developing brain. Prog Brain
Res 2013; 207: 35–64.
78. de Graaf-Peters VB, Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when? Early Hum Dev 2006; 82: 257–66.
79. Morgan C, Darrah J, Gordon AM, Harbourne R, Spittle A, Johnson R et al. Effectiveness of motor interventions in infants with cerebral palsy: a systematic review. Dev Med Child Neurol 2016; 58: 900–9.
80. Hadders-Algra M, Boxum AG, Hielkema T, Hamer EG. Effect of early intervention in infants at very high risk of cerebral palsy: a systematic review. Dev Med Child Neurol 2017; 59: 246–258. 81. Spittle A, Orton J, Anderson PJ, Boyd R, Doyle LW. Early developmental intervention
pro-grammes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane database Syst Rev 2015; : CD005495.
82. Blauw-Hospers CH, Hadders-Algra M. A systematic review of the effects of early intervention on motor development. Dev Med Child Neurol 2005; 47: 421–32.
83. Dirks T, Blauw-Hospers CH, Hulshof LJ, Hadders-Algra M. Differences between the family-centered "COPCA" program and traditional infant physical therapy based on neu-rodevelopmental treatment principles. Phys Ther 2011; 91: 1303–22.
84. Hielkema T, Hamer EG, Reinders-Messelink HA, Maathuis CGB, Bos AF, Dirks T et al. LEARN 2 MOVE 0–2 years: effects of a new intervention program in infants at very high risk for cerebral palsy; a randomized controlled trial. BMC Pediatr 2010; 10: 76.
85. http://cp-research.nl/LEARN2MOVE/.
86. Bobath K, Bobath B. The neurodevelopmental treatment. In: Scrutton D (ed). Management of
the Motor Disorders of Children with Cerebral Palsy. JB Lippincott: Philadelphia, 1984, pp 6–18.
87. Howle JM. Neuro-Developmental Treatment Approach: Theoretical Foundations and Principles of Clinical Practice. Laguna Beach, CA: Neuro-Developmental Treatment Association, 2002. 88. Bly L. Baby Treatment based on NDT principles. Pro-Ed Inc: Austin, TX, 1999.
Postural adjustments in infants at
very high risk for cerebral palsy
before and after developing the
ability to sit independently
Anke G. Boxum
Lieke C. van Balen
Linze-Jaap Dijkstra
Elisa G. Hamer
Tjitske Hielkema
Heleen A. Reinders-Messelink
Mijna Hadders-Algra
Early Human Development 2014 Sep; 90:435–41
Abstract
Background: Children with cerebral palsy (CP) have impaired postural control. Pos-ture is controlled in two levels: specificity, and fine-tuning of direction-specific adjustments, including recruitment order. Literature suggests that direc-tion-specificity might be a prerequisite for independent sitting.
Aim: To study development of postural adjustments in infants at very high risk for CP (VHR-infants) during developing the ability to sit independently.
Method: In a longitudinal study surface electromyograms of the neck-, trunk- and arm muscles of 11 VHR-infants and 11 typically developing (TD) infants were recorded during reaching in sitting before and after developing the ability to sit unsupported (median ages: VHR 8.0 and 14.9 months; TD 5.7 and 10.4 months). Ses-sions were video-recorded.
Results: In VHR- and TD-infants the prevalence of direction-specific adjustments and recruitment order did not change when the infant learned to sit independently. In VHR-infants able to sit independently more successful reaching was associated with a higher frequency of bottom-up recruitment (Spearman’s rho = 0.828, p = 0.006) and a lower frequency of simultaneous recruitment (Spearman’s rho = - 0.701, p = 0.035), but not with more direction-specificity. In TD-infants not able to sit inde-pendently, more successful reaching was associated with higher rates of direction-specific adjustments at the neck level (Spearman’s rho = 0.778, p = 0.014), but not with recruitment order.
Conclusions: In VHR- and TD-infants postural adjustments during reaching in terms of direction-specificity and recruitment order are not related to development of independent sitting. Postural adjustments are associated with success of reaching, be it in a different way for VHR- and TD-infants.
2
Introduction
Infants at high risk (HR) for cerebral palsy (CP), such as infants born preterm or with perinatal asphyxia, often show a delay in the development of motor milestones like sitting, walking, reaching and grasping.1 These motor activities are highly dependent on postural control.2 However, little is known on the organization of postural adjust-ments in HR-infants.
Postural control is a complex neural task involving activity of many muscles. In terms of muscle activity two levels of control can be distinguished. The first level consists of direction-specificity, implying that if balance is compromised by a for-ward body sway, the muscles on the dorsal side of the body are primarily activated and in case of a backward sway the muscles on the ventral side. At the second level of control the direction-specific postural pattern is fine-tuned to the specifics of the situation by means of e.g. adaptation of the recruitment order of the direction-specific muscles.2,3
Typically developing (TD) infants aged 1 to 3 months show pre-reaching movements accompanied by postural activity without direction-specificity.4 Four-month-olds, who just have mastered the ability to reach for a toy, show direction-specific postural adjustments during 40% of reaching movements.5 The study of de Graaf-Peters et al. (2007) showed that infants aged 4 to 6 months, who demon-strated direction-specific adjustments during at least half of their reaches, were more successful in reaching and had reaches with a better kinematic quality than infants whose reaches were less often accompanied by direction-specific postural activity.6 This suggests that direction-specificity is not a prerequisite for reaching, but that it is associated with better reaching. During infancy the rate of direction-specific adjustments during reaching gradually increases to about 60% at 18 months5 and 100% at 2 years of age.7 Throughout infancy direction-specific adjust-ments are characterized by variation, for instance variation in recruitment order.5 Despite the large variation, a developmental trend in recruitment order is observed. At 4 months, a mild preference for top-down recruitment (the neck muscle is acti-vated prior to the trunk muscles) is present, which changes into a preference for bottom-up (trunk muscle activated prior to the neck muscles) at 18 months.5
Relatively little is known on the organisation of postural adjustments of infants at high risk for CP. The data of van Balen et al. indicated that the devel-opment of direction-specificity during reaching in high risk infants is delayed.8 But at preschool age, most children with CP do show consistent direction-specific adjustments during reaching while sitting.9 The limited data available suggest that only children with CP functioning at Gross Motor Function Classification System (GMFCS)10 level V – who do not develop the ability to sit independently – show
a total lack of direction-specificity.9,11 This might mean that direction-specificity is a prerequisite for the development of sitting ability. But direction-specificity is not the only factor involved in the development of the ability to sit without support, as the study of Hedberg et al. (2004) showed that one-month-old TD-infants virtu-ally always showed direction-specific postural adjustments in response to external perturbations of balance, while they were unable to sit independently.12
Others studied the development of reaching and postural control using the theoretical framework of the dynamic systems theory.13 For instance, the lon-gitudinal data of Thelen and Spencer indicated that in typical development stable head control precedes the emergence of reaching.14 Harbourne and Stergiou15 , who applied non-linear dynamics to study centre of pressure (COP) behavior of sitting infants, reported that infants decreased the degrees of freedom in body motility when the ability to sit emerged, to return to increased levels of degrees of freedom when they could sit properly without help – a flexibility allowing them to adapt to the environment. Kyvelidou et al.16 noted that COP behavior of infants with CP and infants born preterm with motor delays at the emergence of early sitting differed from that of TD-infants. The data suggested that the infants with CP had a severely limited repertoire of adjustments, those with developmental delay a moderately reduced repertoire, while TD-infants had a large and flexible repertoire.
Non-linear measures, such as used in the above mentioned studies on COP-behavior,15,16 do not provide information on the muscular strategy to achieve the stability needed to sit without support. Therefore we wondered whether in infants at very high risk for CP (VHR-infants) and TD-infants the development of the abil-ity to sit without help (requiring active neural control instead of reactive neural control) is related to the development of direction-specific postural adjustments during reaching (also requiring active control). Thus, the aim of this longitudinal study is to increase the understanding of postural development in VHR-infants, during the phase of the development of sitting ability. To this end, postural control during reaching was studied in infants participating in the LEARN2MOVE 0–2 years project (L2M 0–2). L2M 0–2 aims to evaluate whether intervention with the newly developed COPCA-program (Coping with and Caring for infants with special needs – a family centred program [Dirks et al. 2011])17 results in a better outcome in terms of functional capabilities of the VHR-infant and developmental potential of the family, compared to traditional infant therapy.18 Similar data on postural control of TD-infants were available from a previous project.5
2
We addressed the following questions: (1) Does postural control in terms of direction-specificity and recruitment order of VHR-infants change when the infant develops the ability to sit independently? (2) Does postural control in terms of direction-specificity and recruitment order of VHR-infants before and after devel-opment of the ability to sit independently differ from that of TD-infants? (3) Is pos-tural control in terms of direction-specificity and recruitment order in VHR-infants associated with reaching performance, and with the presence of CP at 21 months corrected age?
Method
Participants
This study comprised 11 VHR-infants (nine boys, two girls), and 11 TD-infants born at term without perinatal complications (seven boys, four girls). The VHR-infants were included in the L2M 0–2 project before 9 months corrected age based on one of the following criteria (Hielkema et al. 2010)18: 1) cystic periventricular leukoma-lacia; 2) parenchymal lesion of the brain (uni- or bilateral); 3) brain lesions on MRI with Sarnat 2 or 319 caused by term/near-term asphyxia; 4) neurological dysfunc-tion which might lead to the development of CP. Infants were excluded in case of presence of a severe congenital disorder, or presence of an inadequate under-standing of the Dutch language by caregivers. For the present study, VHR-infants who fulfilled the following additional criteria were included: a) they developed the ability to sit independently, and b) they had two postural electromyography (EMG) recordings: one when they were not able to sit independently (EMG recording 1: E1), the other when they could sit without support as noted during the Touwen Infant Neurological Examination20 (EMG recording 2: E2). Clinical details of the par-ticipants are summarized in Table 1. The ethics committee of the University Medical Center Groningen approved the protocol (L2M 0–2 is registered under trial number NTR1428) and informed consent was given by the parents.
Table 1. Participant’s characteristics
VHR-infants TD-infants
Gestational age (wk), median (range) 36.3 (26.3–41.1) 40.5 (37.6–42.0)* Birth weight (g), median (range) 2375 (1070–5400) 3463 (3000–4000)* Corrected age E1 (mo), median (range) 8.0 (4.7–9.6) 5.7 (3.8–6.5) Corrected age E2 (mo), median (range) 14.9 (11.4–22.4) 10.4 (9.6–11.4)* Type of brain lesion, n (%)
Posthaemorrhagic porencephaly Basal ganglia/thalamic lesion Cortical infarction Other lesions ◊ 6 (55) 2 (18) 1 (9) 2 (18) Not applicable
g: grams, E1: Electromyography recording 1 (not able to sit unsupported), E2: electromyography recording 2 (able to sit unsupported), mo: months corrected age, TD: typically developing, VHR: very high risk, wk: weeks
* Mann-Whitney: p < 0.01
◊ Other brain lesions: arachnoid cyst with hydrocephalus and bilateral intraventricular haemorrhage grade 3
Procedure
Postural control in VHR-infants was assessed at inclusion (T0), 6 months after inclusion (T2), 12 months after inclusion (T3) and at the corrected age of 21 months (T4). For this study, two assessments were selected: 1) the first assessment available when the infant was able to reach but unable to sit unsupported (E1); and 2) the first assessment available when the infant could sit unsupported (E2).
Similar data of 11 TD-infants were present at the ages of 4, 6 and 10 months.5 According to the Touwen Infant Neurological Examination (TINE)20, six of the TD-infants could not sit independently at 6 months (E1 for the present study); in the remaining five infants who could sit independently at 6 months, the data recorded at 4 months, when the infants could not sit independently were used for E1. All TD-infants were able to sit independently at 10 months; these 10 months data were used for E2.
The infants were examined while seated in an infant chair providing pos-tural support at the back and front or while sitting on the floor with the parent providing back support. The latter occurred in both assessments of one VHR-infant. Reaching was elicited by presenting a small toy at arm length distance. The aim was to elicit at least ten reaching movements with the preferred arm, but if less than ten reaching movements were available – in order to minimize loss of data – data were included if a minimum of three adequate trials were present. The reaching session lasted about 30 minutes. If less than three reaching movements per position were present, the data of this session were excluded from further data
2
analysis. Data of two sessions could not be used (data of a non-sitting VHR-infant who was interested in the toy but did not reach, and data of a sitting VHR-infant due to technical problems).
EMG recording
EMG of the neck, trunk and arm muscles was continuously recorded on the right side of the body (unless the infant preferred the left arm to reach: n = 2 VHR-infants) with bipolar surface electrodes (interelectrode distance: 14 mm). The electrodes were placed on postural muscles, i.e., the sternocleidomastoid (neck flexor, NF), neck extensor (NE), rectus abdominis (RA), thoracal extensor (TE), lumbar extensor (LE), and on arm- and shoulder muscles, i.e., the deltoid (DE), pectoralis major (PM), biceps brachii (BB) and triceps brachii (TB). In most infants, an additional elec-trode was placed on the sternum to facilitate detection of cardiac activity. The EMG signal was recorded at a sampling rate of 500 Hz with the software program Portilab (Twente Medical Systems International, Enschede, The Netherlands).
Video recording
The entire EMG-session was recorded on video. The video was used to select reach-ing movements with the preferred arm, to classify the success of the movements (percentage of reaching movements resulting in actual grasping of the object) and to select trials in which the infant was in an alert and calm behavioural state. The video was also used to identify and exclude trials with evident trunk or head move-ments which were not related to the reaching movement.
Data analysis
EMG analysis was carried out using the PedEMG software (Developmental Neurol-ogy, University Medical Center Groningen, The Netherlands).5 PedEMG allows for synchronous analysis of video and EMG data. The software used for EMG analysis includes the computer algorithm of Staude and Wolf.21 This algorithm uses a model based statistical decision method to determine onsets of phasic EMG activity. Before determining the onsets the signal was filtered for 50 Hz noise using 5th order band Chebyshev filter. Signal artifacts and cardiac activity were identified to take
into account when appropriate. Clear signal artifacts were identified manually. Car-diac activity (QRS-complexes) was identified using a pattern recognition algorithm based on a linear derivative approximation of the signal using the combination of the repeating pattern and specific shapes of the QRS-complexes.
The activity of the postural muscles was considered to be related to the arm movement when increased muscle activity was found within a time window starting 100 ms before activation of the prime mover, i.e., the arm muscle that was activated first, until the duration of (or the first 1000 ms of) the reaching movement (for details see van Balen et al.).5 The choice of the 100 ms time window instead of the 500 ms window used by Witherington et al.22 to determine postural muscle activity related to a reaching movement was based on a) the video recordings revealing that the longer time window was associated with a high rate of ‘false positives’, i.e., muscle activity related to other spontaneous movements of the infant and not to reaching; b) a preliminary analysis of the data in which we compared the results of the 100 ms and 500 ms time window. This analysis revealed that the rates of direc-tion-specificity and specific forms of recruitment order were not affected by the duration of the analysis window; and c) the 100 ms window allows for comparison of the infant data with the data of older children in which the 100 ms window was used (van der Heide et al.).7,9,23
For each infant at each assessment the following parameters were calcu-lated: 1) percentage of direction-specific trials at the neck and/or trunk level; direc-tion-specificity means that the direction-specific dorsal muscle is activated prior to or in the absence of ventral muscle recruitment. The other EMG-parameters were only calculated if direction-specific activity at trunk level was present: 2) latencies to recruitment of the direction-specific muscles after onset of the prime mover; and 3) percentage of trials with top-down, bottom-up or a simultaneous recruitment order. Recruitment order was classified as top-down when NE was the direction-specific muscle which was recruited first (or in case the NE signal was missing, TE was recruited first), and as bottom-up when LE was recruited first (or in case that the LE signal was missing, TE was recruited first). If all recruited direction-specific muscles were activated within a time frame of 20 ms, recruitment order was clas-sified as simultaneous.
