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The infant motor profileHeineman, Kirsten Roselien

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The Infant Motor Pro�leA standardized and qualitative assessment of

motor behaviour in infancy

Kirsten Heineman

ISBN: 978-90-367-4532-1 (digital version)

© 2010, K.R. HeinemanNo parts of this thesis may be reproduced or transmitted in any forms or by any means, electronicor mechanical, including photocopying, recording or any information storage and retrieval system,without permission of the author

Cover: Willeke van der Broek, oktober 2007

Lay-out: Peter van der Sijde, Groningen

Printed by: drukkerij van Denderen, Groningen

ISBN: 978-90-367-4492-8 (printed version)

RIJKSUNIVERSITEIT GRONINGEN

The Infant Motor Pro�leA standardized and qualitative assessment of

motor behaviour in infancy

Proefschrift

ter verkrijging van het doctoraat in deMedische Wetenschappen

aan de Rijksuniversiteit Groningenop gezag van de

Rector Magni!cus, dr. F. Zwarts,in het openbaar te verdedigen op

woensdag 8 september 2010om 16.15 uur

door

Kirsten Roselien Heineman

geboren op 13 november 1978te Nijmegen

Promotores: Prof. dr. M. Hadders-AlgraProf. dr. A.F. Bos

Beoordelingscommissie: Prof. dr. J.G. BecherProf. dr. O.F. BrouwerProf. dr. L.S. de Vries

Paranimfen: Layla Ben-ZviKarin Middelburg

CONTENTS

Chapter 1 General introduction 9

Chapter 2 Evaluation of neuromotor function in infancy – 19a systematic review of available methodsJournal of Developmental and Behavioral Pediatrics 2008;29:315-23

Chapter 3 The Infant Motor Pro!le: a standardized and qualitative 37method to assess motor behaviour in infancyDevelopmental Medicine and Child Neurology 2008;50:275-82

Chapter 4 Development of adaptive motor behaviour in typically 51developing infantsActa Paediatrica 2010;99:618-24

Chapter 5 Construct validity of the Infant Motor Pro!le: 65Relation with prenatal, perinatal and neonatal risk factorsDevelopmental Medicine and Child Neurology 2010, epub ahead of print

Chapter 6 Concurrent and predictive validity of the Infant Motor Pro!le 77Submitted

Chapter 7 General discussion 95

Summary 107

Appendices 111

Appendix I: Summary on the domains and items of the Infant Motor Pro!leAppendix IIa: Validity of the testsAppendix IIb: Reliability of the testsAppendix III: Infant Motor Pro!le

Nederlandse samenvatting 129

Dankwoord 133

Curriculum Vitae 137

List of publications 141

9

General introduction

1CHAPTER

10

GENERAL INTRODUCTION

Theories on motor development

During the �rst two years of life, children show an impressive development of motor skills such

as reaching, grasping, sitting, crawling, standing and walking. Rapidly, they change from supine

infants to walking toddlers who are able to explore the world around them. Motor development is

a complex process in which many factors play a role. The limited knowledge on the exact processes

that are involved in motor development induced a wide range of theories. Traditionally, the process

of motor development was explained by the Neuronal Maturation Theory (NMT). According to this

theory, at birth all programs involved in motor development are present. As a result of maturation

of the central nervous system, motor development is brought about by a gradual unfolding of

these programs1-3. This unfolding process is not dependent on environmental factors and there

is only a limited role for exercise3,4. Because not all parts of the central nervous system mature at

the same time, motor development takes place from proximal to distal and from cranial to caudal

direction1,3-5. Based on these general developmental rules, Gesell and Amatruda described all motor

milestones and the ages at which they emerge in their book ‘Developmental Diagnosis’2.

In the Dynamic Systems Theory (DST)6,7, motor development is considered as a self-organizing

process in which all components are equally involved. Motor behaviour is determined by an

interplay between many subsystems, such as muscle force, muscle tone, the nervous system, body

weight, state and motivation of the infant, context variables and task characteristics. Development

is described as ‘a series of states of stability, instability, and phase shifts in the attractor landscape,

re!ecting the probability that a pattern will emerge under particular constraints’6. Phase shifts are

brought about by changes in one or more of the involved subsystems, leading to a forced transition

of the system to another state. Attractors states are preferred patterns of behaviour, for example

patterns of locomotion such as rolling, crawling or walking. Depending on the characteristics of all

factors involved, one way of locomotion is the most stable attractor in a certain situation and this

attractor has the highest probability of occurring. For example, a child who has been able to walk

independently for some weeks will choose the locomotion pattern ‘walking’ in easy circumstances,

but will probably switch to crawling when the surface is slippery. In this simpli�ed example, the

surface characteristic is regarded as the control parameter, that is the changed factor that makes

the system shift to another state6,7. In contrast with NMT, in which the central nervous system has

a leading role in the process of motor development, in DST the nervous system is only one of the

elements involved.

In the Neuronal Group Selection Theory (NGST)8-12 on motor development both genetic, innate

factors and environmental in!uences play a role. According to NGST, typical motor development is

characterized by two phases of variability. During the phase of primary variability, variation in motor

behaviour is not geared to external conditions. By means of spontaneous, self-generated activity,

the primary neuronal networks that are already present at birth and the corresponding motor

Chapter 1

1


11

repertoires are explored. This can for example be observed in the so-called general movements

(GMs)13. General movements are the most frequent used movement pattern of the fetus and the

young infant until the age of approximately four months post term. They are characterised by

abundant variation and complexity and are not adapted to the environment nor goal-directed. From

three to four months onwards, these general movements are gradually displaced by goal-directed

motility, such as reaching movements.This goal-directed motility is at !rst characterised by abundant

variation, for example variation in reaching trajectories, amplitude of movements and movement

speed. Gradually, this seemingly random variation decreases and the second phase of motor

development, the phase of secondary variability, takes over. In the phase of secondary variability,

the child develops the ability to select out of the extensive motor repertoire the best motor strategy

in a certain situation, which gives motor behaviour a more e"cient impression. Development of this

ability to select adaptive motor strategies is dependent on the a#erent information brought about

by the self-generated activity. In other words, by means of a process of exploration and selection

the child develops the capacity to adapt motor behaviour to environmental constraints. This ability

to select adaptive motor strategies out of the motor repertoire occurs at function-speci!c ages10,11.

The process of typical motor development is disturbed in developmental motor disorders, such

as cerebral palsy (CP) or developmental coordination disorder (DCD). See below for descriptions of

these motor disorders. According to NGST, children with pre or perinatally acquired lesions of the

brain, such as children with CP and some children with DCD, exhibit stereotyped motor behaviour

with reduced variability. This might be related to a reduction of the repertoire of primary cortical-

subcortical neuronal networks. Besides the reduced neural repertoire, motor behaviour of these

children is also a#ected by problems in adaptive selection of the most suitable motor strategies

in a certain situation. This might be due to problems in processing a#erent, sensory information

that are often encountered in children with CP and DCD14,15, as adaptive selection relies on a#erent

feedback11,16.

Developmental motor disorders

Cerebral palsy (CP) is de!ned as a group of disorders of motor function, movement and posture; it

is permanent but not unchanging and is caused by non-progressive lesions or brain abnormalities

in the developing/immature brain17. It is often associated with severe intellectual de!cit (31%),

severe visual impairment (11%) and/or seizures (21%)18. CP is classi!ed as spastic CP, ataxic CP or

dyskinetic CP. Spastic CP is the most frequent form of CP (85-90%)19 and is characterised by at least

two of the following three characteristics: abnormal pattern of posture and/or movement, increased

tone and pathological re$exes. Spastic CP may be unilateral, involving limbs on one side of the

body, or bilateral with involvement of limbs on both sides of the body. Ataxic CP is characterized

by abnormal pattern of posture and/or movement in combination with a loss of orderly muscular

coordination so that movements are performed with abnormal force, rhythm and accuracy. In

dyskinetic CP, abnormal pattern of posture and/or movement is accompanied by involuntary,

12

Chapter 1

uncontrolled, recurring, occasionally stereotyped movements18. Prevalence of CP is 2 to 3 per 1000

live births18. Infants with very low birth weight (below 1500 gram) and/or very preterm birth are at

higher risk for development of CP. Due to improved prenatal and neonatal care, the survival of this

group of vulnerable infants has increased in the last decennia, possibly leading to an upward trend

in the overall prevalence of CP during the 1970s and 1980s. In the recent years trends have been

less clear18,19, but the prevalence seems to have stabilized or even decreased20. CP is caused in more

than 80% by brain lesions that can be visualised by brain imaging with magnetic resonance imaging

(MRI) or neonatal ultrasound scans. Type and localisation of the brain damage determine the clinical

subtype of CP and are related to the presence and severity of associated disabilities20. Often, no

speci!c cause can be identi!ed and it is assumed that a combination of factors is responsible for the

brain damage. For a long time, only complications of labour and delivery were considered causal risk

factors for CP, but current evidence suggests that intrauterine exposure to infection or in"ammation

and coagulation disorders could be more important causes21. At present, knowledge on the precise

contributors to the risk for CP is still not complete.

Compared to CP, developmental coordination disorder (DCD) is a much less disabling

developmental motor disorder, but it still has major impact on daily life and academic achievements.

Diagnosis of DCD can be made according to the following DSM-IV criteria22: performance in daily

activities that require motor coordination is substantially below that expected, given the person’s

chronological age and measured intelligence. This may be manifested by marked delays in achieving

motor milestones, dropping things, clumsiness, poor performance in sports, or poor handwriting.

The disturbance signi!cantly interferes with academic achievement and/or activities of daily living

and is not due to a general medical condition such as CP or muscular dystrophy. If intellectual delay

is present, the motor di#culties are greater than would be expected, given the level of delay22. DCD

is a common condition with an estimated prevalence of 5 to 6%22. It is often associated with the

presence of signs of minor neurological dysfunction (MND)16.

Assessment of neuromotor function in infancy

Infants born very preterm are especially at risk for developmental motor disorders such as CP or

DCD23-26. Due to improved prenatal and neonatal care the group of surviving very preterm infants

has increased in the last decennia23,26. Follow-up of preterm infants aims at the detection of those

infants that could bene!t from early intervention at young age, when the brain is characterised by

high plasticity27,28. In order to detect those infants, clinicians such as physical therapists, occupational

therapists, paediatricians and paediatric neurologists have a wide range of instruments that assess

neuromotor function in infancy at their disposal. In chapter 2, a systematic review of existing

methods and their psychometric properties is presented. We found that instruments that assess

qualitative aspects of motor behaviour, such as the general movement (GM) method13,29 and the

Test of Infant Motor Performance (TIMP)30, are most promising in terms of prediction of future

developmental outcome. However, these two methods are only suitable for infants until the age

13

1


of four months. Therefore, we developed the Infant Motor Pro�le, a qualitative assessment which is

applicable throughout infancy until the age of 18 months.

The Infant Motor Pro�le

In the development process of the Infant Motor Pro�le, we started with precise observation and

analysis of video-recordings of spontaneous motor behaviour of typically developing infants from

three months until 2 years of age. In addition, we observed video-recordings of infants at high

risk for developmental motor disorders such as cerebral palsy. We tried to discern which aspects

of motor behaviour di!ered between typically developing and high-risk infants. With the NGST as

theoretical background, we categorized the observed variables into various domains. We de�ned

the items on these variables as precisely as possible and wrote guidelines for the examiner on how

to perform the assessment. We viewed and assessed a heterogeneous group of video-recordings

of typically and non-typically developing infants at di!erent ages, and step by step we re�ned the

items and the classi�cation into domains. In the end, the Infant Motor Pro�le had been developed

to the form as it is now and the process of validation was started.

The Infant Motor Pro�le is a video-based assessment of motor behaviour of infants aged 3 to 18

months. It consists of 80 items (see Appendix 1). These items constitute �ve domains. Two domains

are based on ideas of the NGST as described above10,11, the �rst one is on size of motor repertoire

(variation) and the second one is on the ability to select adaptive motor strategies (variability). These

domains consist of respectively 25 and 15 items. The other three domains are on movement "uency

(seven items), movement symmetry (10 items) and motor performance (23 items), the last one being

a more quantitative assessment of motor milestones. Details on the scoring of the items and on

calculation of the domain scores are described in chapter 3. The total IMP-score is computed as the

mean of the �ve domain scores. A general principle in calculating the scores on the various domains

is that only items that re"ect observed motor behaviour are taken into account. This means that for

example an item on variability of leg movements during independent walking is only scored if the

child indeed is able to walk independently. If not, the item is not taken into account in computing

the domain-score. An exception to this rule are the items of the performance domain, which can

always be scored. For example, if the child is not able to walk, item 5 of standing and walking is

scored as ‘1 = cannot walk’.

Aim of this thesis

The aim of this thesis was threefold: �rst to review existing methods to assess neuromotor function

in infancy. The second aim was development of the Infant Motor Pro�le and the third aim was to

investigate its psychometric properties. In order to be able to investigate reliability and validity of

the Infant Motor Pro�le, we performed a longitudinal prospective study on a heterogeneous group

of term and preterm born infants from 3 to 18 months. In addition, another group of term born

infants had cross-sectional assessments at the same ages.

Chapter 1

14

Main focus is on:

1. Intra- and interobserver reliability of the IMP.

2. Construct validity of the IMP, operationalized as relations between IMP-scores throughout

infancy and prenatal, perinatal and neonatal risk factors, including the presence of brain

pathology on neonatal ultrasound scans.

3. Concurrent validity of the IMP with the Alberta Infant Motor Scale (AIMS31) and the Touwen

Infant Neurological Examination (TINE32,33).

4. Predictive validity of the IMP-scores throughout infancy for neurological outcome at corrected

age of 18 months.

METHODS

Study group

The study sample consisted of a heterogeneous group of term and preterm infants, which is

a valuable type of sample when assessing validity of a new instrument. Thirty term born infants with

a median gestational age of 40.1 weeks (range 37.6-42 weeks) and a median birth weight of 3588

grams (range 2730-4470 grams) were followed longitudinally and assessed at ages 3,4,5,6,8,10,12,15

and 18 months. These infants were recruited amongst colleagues and acquaintances of the

researchers. A group of 59 preterm infants was followed longitudinally at corrected ages 4,6,10,12

and 18 months. They had all been admitted to the neonatal intensive care unit (NICU) of the Beatrix

Children’s Hospital of the University Medical Center Groningen (UMCG) between December 2003

and January 2005. Inclusion criteria were gestational age below 35 weeks, singleton or twin,

parents with appropriate understanding of the Dutch language and travel distance between the

child’s home and the hospital of approximately less than one hour. Infants with severe congenital

anomalies were excluded from the study. Median gestational age was 29.7 weeks (range 25-34.7

weeks) and median birth weight was 1285 grams (range 630-2180 grams). Another group of 116

term infants was recruited at Well Child Centres. These infants had a median gestational age of 40.1

weeks (range 37-43 weeks) and a median birth weight of 3500 grams (range 1960-4660 grams).

These infants had cross-sectional assessments at one (n=102), two (n=13) or three (n=1) of the ages

of 4, 6, 10, 12 or 18 months. All parents gave informed consent and the project was approved by the

local Ethics Committee.

For all infants, socio-economic, prenatal and neonatal data were collected on standardized

forms by means of an interview with the parents and consultation of NICU discharge certi!cates. For

the preterm infants, neonatal ultrasounds of the brain were assessed with respect to periventricular

leukomalacia (PVL)34 and intraventricular haemorrhages (IVH)35. Details on socio-economic and

neonatal characteristics of the study groups will be presented in the following chapters.

1

15


Assessments

At all ages, the assessment consisted of a video-recording of motor behaviour of approximately 15

minutes. Motor behaviour was assessed in several positions, depending on the age and functional

capacities of the child: supine, prone, sitting, standing and walking and reaching, grasping and

manipulation of objects. Motor behaviour was spontaneous or was elicited by presenting toys to

the infant. On the basis of the video-recording, both the Infant Motor Pro�le and the Alberta Infant

Motor Scale (AIMS)31 were scored at a later time. The assessment consisted further of an age-speci�c

neurological examination that was carried out after the video-recording. At all ages, except at 18

months, this consisted of theTouwen Infant Neurological Examination (TINE)32,33. InTINE, neurological

signs are grouped according to age-speci�c norms into �ve possible clusters of dysfunction,

namely reaching and grasping, gross motor function, brain stem function, visuomotor function and

sensorimotor function (consisting of re!exes and muscle tone). Neurological condition is classi�ed

as abnormal if there is a distinct neurological syndrome, such as a hemisyndrome, irrespective of

number of deviant clusters. Neurological condition is classi�ed as minor neurological dysfunction

(MND) if there are two or more clusters of dysfunction. Neurological condition is considered normal-

suboptimal when one or two clusters are deviant and normal when no clusters are deviant33. At the

age of 18 months, the Hempel assessment36 was used instead of TINE, as TINE is only applicable

until the age of 12 to 15 months. The Hempel examination is suitable for preschool children from

18 months until 4 years of age. Similar to TINE, the Hempel assessment classi�es neurological signs

into clusters of dysfunction, namely �ne motor dysfunction, gross motor dysfunction, dysfunctional

muscle tone regulation, re!ex abnormalities and visuomotor dysfunction. Neurological condition

can be classi�ed as abnormal, complex MND (when there is more than one dysfunctional cluster),

simple MND (when one cluster of dysfunction is present) or normal (no deviant clusters or the

isolated presence of re!ex abnormalities)16.

Outline of the thesis

Chapter 2 consists of a systematic review of available methods to evaluate neuromotor function in

infancy and their psychometric properties. The review forms the background to which the Infant

Motor Pro�le was developed. Chapter 3 presents the pilot study on the IMP with description of the

instrument and �rst data on intra and inter observer reliability and concurrent validity. In chapter

4, a small side step is made, and development of adaptive motor behaviour in typically developing

infants is investigated with the NGST as theoretical background. Chapter 5 examines construct

validity of the IMP, operationalized as the relation of IMP-scores throughout infancy with prenatal,

perinatal and neonatal risk factors. Chapter 6 re-assesses reliability and investigates concurrent

validity of the IMP with the Alberta Infant Motor Scale (AIMS)31 and with Touwen Infant Neurological

Examination (TINE)32,33 and predictive validity for neurological outcome at 18 months. Chapter 7

consists of a general discussion on the IMP and its psychometric properties as presented in this

thesis.

16

Chapter 1

REFERENCES

1. Gesell A. The Embryology of Behavior. New York: Harper & Row, 1945.

2. Gesell A, Amatruda CS. Developmental Diagnosis. Normal and Abnormal Child Development, 2nd ed. NewYork: Harper & Row, 1947.

3. Illingworth RS. The Development of the Infant and Young Child: Normal and Abnormal Development, 3rded. Edinburgh: Churchill Livingstone, 1966.

4. Peiper A. Cerebral Function in Infancy and Childhood. 3rd ed. New York: Consultants Bureau, 1963.

5. McGraw MB. The Neuromuscular Maturation of the Human Infant. Classics in Developmental Medicine, No.4. London: Mac Keith Press, 1989.

6. Thelen E. Motor development. A new synthesis. American Psychologist 1995;50:79–95.

7. Ulrich BD. Dynamic systems theory and skill development in infants and children. In: Connolly KJ, ForssbergH, editors. Neurophysiology and Neuropsychology of Motor Development. Clinics in DevelopmentalMedicine No. 143/144, London: Mac Keith Press, 1997, p 319–45.

8. Edelman GM. Neural Darwinism: selection and reentrant signaling in higher brain function. Neuron1993;10:115-125.

9. Sporns O, Edelman GM. Solving Bernstein’s problem: a proposal for the development of coordinatedmovement by selection. Child Development 1993;64: 960–81.

10. Hadders-Algra M. The Neuronal Group Selection Theory: a framework to explain variation in normal motordevelopment. Dev Med Child Neurol 2000;42:566-572.

11. Hadders-Algra M. The Neuronal Group Selection Theory: promising principles for understanding andtreating developmental motor disorders. Dev Med Child Neurol 2000;42:707-715.

12. Hadders-Algra M. Early brain damage and the development of motor behavior in children: clues fortherapeutic intervention? Neural Plast 2001;8:31-49.

13. Hadders-Algra M. General movements: A window for early identi!cation of children at high risk fordevelopmental disorders. J Pediatr 2004;145:S12-18.

14. Wilson PH, McKenzie BE. Information processing de!cits associated with developmental coordinationdisorder: a meta-analysis of research !ndings. J Child Psychol Psychiatry 1998;39:829-840.

15. Cooper J, Majnemer A, Rosenblatt B, Birnbaum R. The determination of sensory de!cits in children withhemiplegic cerebral palsy. J Child Neurol 1995;10:300-309.

16. Hadders-Algra M. Developmental coordination disorder: is clumsy motor behaviour caused by a lesion ofthe brain at early age? Neural Plast 2003;10:39-50.

17. Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers. Surveillanceof Cerebral Palsy in Europe (SCPE). Surveillance of Cerebral Palsy in Europe. Dev Med Child Neurol2000;42:816-24.

18. Prevalence and characteristics of children with cerebral palsy in Europe. Surveillance of Cerebral Palsy inEurope. Dev Med Child Neurol 2002;44:633-40.

19. Krägeloh-Mann I, Bax M. Cerebral Palsy. In: Aicardi J , ed. Diseases of the nervous system in childhood. 3rdEdition. Clinics in Developmental Medicine. London: Mac Keith Press, 2009:210-242.

20. Krägeloh-Mann I, Cans C. Cerebral palsy update. Brain Dev 2009 Apr 20. Epub ahead of print.

21. Nelson KB, Grether JK. Causes of cerebral palsy. Curr Opin Pediatr 1999;11:487-91.

22. American Psychiatric Association. Diagnosis and Statistical Manual of Mental Disorders. 4th edn, TextRevision. Washington, DC: American Psychiatric Association, 2000.

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23. Wilson-Costello D, Friedman H, Minich N, Fanaro� AA, Hack M.. Improved survival rates with increasedneurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 2005;115:997-1003.

24. Marlow N, Wolke D, Bracewell MA, Samara M; EPICure Study Group. Neurologic and developmentaldisability at six years of age after extremely preterm birth. N Engl J Med. 2005;352:9-19.

25. Davis NM, Ford GW, Anderson PJ, Doyle LW; Victorian Infant Collaborative Study Group. Developmentalcoordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterminfants. Dev Med Child Neurol 2007;49:325-30

26. Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C, Pierrat V, Rozé JC, Messer J, Thiriez G,Burguet A, Picaud JC, Bréart G, Kaminski M; EPIPAGE Study group. Neurodevelopmental disabilities andspecial care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinalcohort study. Lancet. 2008;371:813-20.

27. Kolb B, Brown R, Witt-Lajeunesse A, Gibb R. Neural compensations after lesion of the cerebral cortex.Neural Plast 2001;8:1-16.

28. De Graaf-Peters VB, Hadders-Algra M. Ontogeny of the human central nervous system: what is happeningwhen? Early Hum Dev 2006;82:257-266.

29. Einspieler C, Prechtl HFR, Bos AF, et al. Prechtl’s method on the qualitative assessment of GeneralMovements in preterm, term and young infants. Clinics in Developmental Medicine No. 167. London: MacKeith Press; 2004.

30. Campbell SK, Kolobe TH, Osten ET, Girolami GL, et al. Construct validity of the test of infant motorperformance. Phys Ther 1995;75:585-596.

31. Piper MC, Darrah J. Motor assessment of the developing infant. Philadelphia: Saunders, 1994.

32. Touwen BCL. Neurological development in infancy. Clinics in Developmental Medicine No. 58. London:Mac Keith Press, 1976.

33. Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological dysfunctionin infancy using the Touwen Infant Neurological Examination: strengths and limitations. Dev Med ChildNeurol, in press.

34. De Vries LS, Eken P, Dubowitz LM. The spectrum of leukomalacia using cranial ultrasound. Behav Brain Res1992;31;49:1-6.

35. Volpe JJ. Neurology of the Newborn. 4th ed. Philadelphia PA: WB Saunders, 2001.

36. Hempel MS. The neurological examination for toddler-age. PhD thesis. University of Groningen, 1993.

19

Evaluation of neuromotor function in infancy –a systematic review of available methods

Kirsten Heineman1,2 and Mijna Hadders-Algra1

1Department of Paediatrics, Institute of Developmental Neurology2Department of Neurology

University Medical Center Groningen

Journal of Developmental and Behavioral Pediatrics 2008;29:315-23

2CHAPTER

20

Chapter 2

ABSTRACT

Background: Neuromotor function in infancy can be evaluated in various ways. Assessment

instruments are used for early detection of children with a high risk for developmental disorders.

Early detection enables clinicians to provide intervention at a young age when plasticity of the

nervous system is high. The assessments may also be used to monitor intervention. The present

paper will review the psychometric properties of methods to assess neuromotora function in

infancy.

Methods: A literature search was performed in PubMed, Medline and PsycINFO (1966 to March

2007) on instruments to assess neuromotor functioning of infants.

Results: Fifteen instruments were included and classi!ed into four groups: 1) Comprehensive

neurological examinations (n=4). These techniques are widely used, though little is known about

their reliability. Their validity in predicting major developmental disorders such as cerebral palsy

is good; their predictive validity for minor motor disorders is moderate at best. 2) Procedures with

standardized scoring (n=7). These have good reliability, but only moderate predictive validity for

major developmental disorders. No data available for prediction of minor developmental disorders.

3) Observation of milestones (n=2). Its predictive validity for major developmental disorders is only

moderate, while reliability is good. 4) Assessment of quality of motor behavior or motor patterns

(n=2). These instruments have the best predictive validity for major and minor developmental

motor disorders, but current methods are only useful under the age of four months.

Conclusion: Prediction of developmental outcome at an early age is di"cult. In medical evaluations

of high-risk infants the best predictions are achieved through a combination of multiple,

complementary tools, that is, achieved milestones, neurological examination and assessment of the

quality of motor behavior.

2

21

Evaluation of neuromotor function in infancy

INTRODUCTION

As the chances of survival of preterm and high-risk full-term infants have increased1,2, extensive

follow-up programs have been developed to determine which of these infants need intervention.

Recent studies suggest that intervention may be most e�ective when it is applied during infancy

when there is high plasticity of the brain3,4. A prerequisite for early intervention is early detection of

infants with a high risk for major developmental disorders such as cerebral palsy (CP) and minor motor

disorders such as developmental coordination disorder (DCD) and minor neurological dysfunction

(MND). It appears that parents of children with developmental disorders are concerned signi!cantly

later than physicians are about the developmental status of their children and therefore, in general,

cannot be relied on for early recognition of infants who are likely to bene!t from early intervention5.

Physiotherapists, occupational therapists, pediatricians and other clinicians in primary health care

settings play an important role in early detection. They have a heterogeneous group of instruments

at their disposal for the detection of early evidence of motor dysfunction in high-risk infants. In

general, these instruments are not only used for detection but also for the evaluation of the

e�ectiveness of an intervention. Usually the instruments are chosen based on habit and for practical

reasons, and not on the basis of information regarding test accuracy and utility and theoretical basis6.

In fact, a primary selection criterion should be: “Has the instrument been designed for the task at

hand?” Kirshner and Guyatt7 classi!ed health measure instruments into three categories according

to the goals they served. The !rst one is discrimination. In the !eld of neuromotor assessment this

implies making a distinction between children who show features of a deviant neuromotor function

compared to the general, healthy population. The second purpose is prediction; that is, instruments

are used as a diagnostic tool to predict developmental outcome, for example, the likeliness that

a child will develop CP. The third purpose is evaluation, the measurement of longitudinal change

of an individual or group over time, for example, changes in motor function of infants enrolled in

early intervention programs. Instruments are generally validated for only one of the three goals. This

means that the instruments cannot automatically be used for other purposes6.

The aim of this paper is to present a systematic review of the instruments used for the evaluation

of neuromotor function and motor behavior in infancy.The contents of the methods will be reviewed,

while special attention will be paid to psychometric properties, that is, reliability and validity.

METHODS

Selection procedure

A literature search in the following databases was performed: PubMed, Medline (1966 to March

2007) and PsycINFO (1967 to March 2007). Keywords used were“neuromotor,”“motor development,”

“motor behavior,” “assessment,” “neurological examination,” “evaluation,” “instrument,” “method,”

“infants,” “neonatal,” “preschool” and “review.” All articles with a name of an assessment in the title

and/or abstract and reviews on one or more methods were selected. Further searches with names

22

Chapter 2

of assessments and authors were performed and references to the articles were studied to �nd

information on reliability and validity. Manuals were obtained when available in the Netherlands.

Instruments were included when they could be applied to infants aged three to eighteen

months and also when the age range of application was more extensive. We focused on the age

range from three to eighteen months, as it has been relatively neglected. Reviews on neonatal

neurological evaluation8,9, instruments to assess motor function of children diagnosed with CP6,10

and assessments of motor development and function in preschool children aged eighteen months

to four years11 were available. Methods were selected if they focused on neurological condition

or motor performance, or if they combined items on neuromotor function with items on other

developmental domains such as mental development, speech or behavior. In the latter case, only

data on reliability and validity of the motor subscale were reviewed. Instruments were only included

if they had been described in at least two English-language peer-reviewed papers.

Instruments used only for screening purposes were excluded, since 1) an overview of frequently

used general developmental screening instruments was provided by Glascoe12 and 2) our main

interest was “full” assessment of the infant’s neuromotor functioning. Screening was de�ned as “the

application to all children born of certain procedures that can be carried out in a short time by the

less specialized members of sta! and that will give indication of the presence and absence of certain

disabilities” (WHO 1967)13. Screening is important in clinical practice. This is illustrated, for instance,

by the considerable power of infant motor screening tests to predict CP, such as the Early Motor

Pattern Pro�le14 and Capute’s motor quotient15. Instruments were considered screening instruments

if the words screen or screening were part of the instrument’s name and/or if the authors mentioned

“screening”as the main purpose of the instrument. Fifteen instruments ful�lled the selection criteria

and were included in the review.

Evaluation procedure

The selected instruments were systematically evaluated with a focus on population, age, purpose

of instrument (discrimination, prediction or evaluation), type of instrument, test description, type

of test data (categorical vs. continuous), test construction and standardization, training required

to become an assessor and time needed to administer the test. For the classi�cation of the type of

instrument, the instrument’s dominant features were used.

The various types of validity and reliability were evaluated by the criteria presented in Table I.

Validity is the extent to which an instrument measures what it is intended to measure. We addressed

construct validity, concurrent validity and predictive validity. Construct validity is the extent to which

items re"ect the theoretical construct of interest, in this case neuromotor functioning. For tests of

neuromotor function, it may be assumed, for instance, that relationships of pre-, peri- and neonatal

adversities, such as preterm birth, and results of brain imaging with test scores may contribute

to construct validity. Concurrent validity is the extent to which scores relate to scores on another

measure on the same construct, ideally a gold standard. If there is no gold standard available,

23

2


correlation with other established instruments is assessed. Predictive validity of an instrument is

the extent to which the scores on the instrument now predict future outcome11,17. In the present

review, we concentrated on predictive validity for developmental motor disorders; we distinguished

predictive validity for major motor disorders such as CP from predictive validity for minor disorders

such as DCD and MND. Factors that were taken into consideration in the judgment of the predictive

validity of the various instruments were type of population (typically developing children vs.

high-risk population), age at follow-up and tests used at follow-up. Reliability is the ability of a

Table I: Evaluation criteria

Construct validity

++

+

+

!

nda

very good

good

good

moderate

moderate

poor

no data

Scoring “good” twice, that is, good for relationship between scores and pre, peri- andneonatal adversities, and good for correlation of scores with results of brain imagingindicates very good construct validity

Scores negatively a!ected by pre-, peri- and neonatal adversities such as PT birth,IUGR, other medical complications, or

Scores correlate with visible pathology on brain imaging (US, MRI), or withelectrophysiological parameters of brain function (CFM, EEG)

Scores are correlated with level of motor development or presence of motor delaysnot documented with a reliable assessment tool

Scores show a signi"cant increase with increasing age

Scores are not related to any of the above-mentioned factors

No data available

Concurrent validity and predictive validity

++

+

!

nda

very good

good

moderate

poor

no data

Cohen’s kappa or Spearman’s ρ > 0.80a

Cohen’s kappa or Spearman’s ρ 0.61-0.80

Cohen’s kappa or Spearman’s ρ = 0.40 – 0.60

Cohen’s kappa or Spearman’s ρ < 0.40

no data available

Intra-observer agreement and inter-observer agreement

++

+

!

nda

very good

good

moderate

poor

no data

Cohen’s kappa or Spearman’s ρ > 0.80a

Cohen’s kappa or Spearman’s ρ 0.61-0.80; agreement >80%

Cohen’s kappa or Spearman’s ρ = 0.40 – 0.60; agreement 60-80%

Cohen’s kappa or Spearman’s ρ < 0.40; agreement < 60%

no data available

a Criteria for reliability according to Landis and Koch16, extended to Spearman’s ρ and % agreementPT = preterm, IUGR = intrauterine growth restriction, US = ultrasound, MRI = magnetic resonance imaging, CFM= cerebral function monitor, EEG = electroencephalography and PPV = positive predictive value

24

Chapter 2

measurement to give consistent scores on repeated assessments in the absence of change in the

characteristics being studied18. Intra-observer agreement is the stability of the observer’s ratings on

the same behavior. Often videotapes are used, which are scored twice by the same observer after

a pre-determined time interval. Interobserver reliability is the stability of ratings across di!erent

evaluators8. The ages used in the review imply that preterm infants are assessed at ages corrected

for preterm birth.

RESULTS

Description of instruments

Fifteen methods to assess neuromotor function in infancy ful"lled the inclusion criteria and were

included in the review. Their main characteristics are described in Table II. The age range in which

the instruments can be applied varied between birth to four months and zero to six years. Four

types of instruments were discerned: 1) comprehensive neurological examination, 2) procedures

with standardized scoring (i.e. condensed neurological assessment with or without observation

of motor behavior with standardized scoring), 3) observation of milestones and speci"c aspects

of motor behavior, and 4) quality of motor behavior. Four instruments were classi"ed as

comprehensive neurological examinations with a focus on cranial nerves, posture, muscle tone,

re#exes and reactions19-22. Seven instruments were procedures with standardized scoring24,25,29,31-34.

Two instruments focused on observation of motor milestones and speci"c aspects of motor

behavior35,36. Two instruments focus on assessing the quality of motor behavior, including postural

adjustments40,41,37.

The authors of all the instruments stated that the main purpose of their instrument was to

discriminate between infants with a deviant neuromotor condition and infants falling within

the range of typical development. Additional purposes have been described for six instruments:

three40,41,21,22 aimed at prediction of future neuromotor development and another three29,32,34 at

evaluation of changes in motor function over time or during intervention. Test construction di!ered

considerably for the various methods, but most assessments took elements from pre-existing

methods, adapted these and/or combined them with other test elements. For four instruments test

construction was not described. Data on standardization was available for seven out of the "fteen

instruments. These standardization procedures were carried out in strikingly heterogeneous ways

with respect to sample sizes (ranging from 35 to 2202 children) and types of populations (typically

developing infants, neonatal intensive care unit (NICU) graduates or infants with a high risk for

developmental delay). Assessors were pediatricians, neonatologists, psychologists, occupational

therapists, nurses or other clinicians working in NICU follow-up programs.Time needed to administer

the test varied from a few minutes to one hour.

25

2


Tabl

eII:

Des

crip

tion

ofth

ein

stru

men

ts

Ass

essm

ent

(Aut

hor)

Shor

tna

me

Popu

lati

onA

gegr

oup

Purp

ose

Test

desc

ript

ion

-as

sess

men

tof:

Type

ofva

riab

les

Test

cons

truc

tion

/st

anda

rdiz

atio

nA

sses

sors

/tim

eto

adm

inis

ter

Neu

rolo

gica

lexa

min

atio

ns

Touw

enin

fant

neur

olog

ical

exam

inat

ion

(Tou

wen

19)

Touw

enin

fant

s0

mos

.to

inde

pend

ent

wal

king

DCr

ania

lner

ves,

post

ure,

tone

,re�

exes

and

reac

tions

,tr

unk

coor

dina

tion

and

gros

san

d�n

em

otor

func

tions

cat.

Base

don

trad

ition

alne

urop

edia

tric

conc

epts

(“G

roni

ngen

scho

ol”)

/nd

a

Pedi

atric

ians

and

othe

rsw

ithsp

eci�

cne

urod

evel

opm

enta

ltr

aini

ng/1

5m

inut

es

Am

iel-T

ison

neur

olog

ical

exam

inat

ion

(Am

iel-

Tiso

nan

dG

osse

lin20

)

Am

iel-

Tiso

nat

-ris

kin

fant

s0

to6

yrs.

DAc

tive

and

pass

ive

mus

cle

tone

,cra

nial

nerv

es,m

otor

mile

ston

es,s

pont

aneo

usm

otor

activ

ity,r

e�ex

esan

dre

actio

ns,q

ualit

ativ

eab

norm

aliti

es

cat.

Base

don

trad

ition

alne

urop

edia

tric

conc

epts

(“Fr

ench

scho

ol”)

/nda

Neo

nato

logi

sts,

pedi

atric

ians

with

neur

odev

elop

men

tal

trai

ning

,occ

upat

iona

lth

erap

ists

/10

min

utes

Activ

ean

dpa

ssiv

em

uscl

epo

wer

(de

Gro

ot21

)

Mus

cle

pow

erhi

gh-r

isk

infa

nts

3to

12m

os.

D,P

Spec

iale

mph

asis

onre

latio

nshi

pbe

twee

nac

tive

and

pass

ive

mus

cle

pow

er;

both

com

pone

nts

shou

ldbe

inba

lanc

ein

orde

rto

crea

tea

stab

lepo

stur

ean

d�u

entm

otili

ty

cat.

nda

/nda

nda

/nda

Ham

mer

smith

Infa

ntN

euro

logi

cal

Exam

inat

ion

(Haa

taja

etal

.22)

HIN

Ein

fant

s2

to24

mos

.D

,PCr

ania

lner

vefu

nctio

n,po

stur

e,m

ovem

ents

,ton

e,re

�exe

san

dre

actio

n(2

6ite

ms)

,dev

elop

men

tal

mile

ston

es(8

item

s),s

tate

ofbe

havi

or(3

item

s)

cont

.Ba

sed

onD

ubow

itzan

dD

ubow

itzm

etho

dfo

rne

urol

ogic

asse

ssm

ent

ofth

ene

wbo

rn23

/st

anda

rdiz

edin

alo

w-r

isk

popu

latio

nof

135

infa

nts

atag

e12

and

18m

os.

Rout

ine

clin

ical

prac

tice,

rela

tivel

yin

expe

rienc

edst

a!/n

da

26

Chapter 2

Ass

essm

ent

(Aut

hor)

Shor

tna

me

Popu

lati

onA

gegr

oup

Purp

ose

Test

desc

ript

ion

-as

sess

men

tof:

Type

ofva

riab

les

Test

cons

truc

tion

/st

anda

rdiz

atio

nA

sses

sors

/tim

eto

adm

inis

ter

Proc

edur

esw

ithst

anda

rdiz

edsc

orin

g

Prim

itive

Re�e

xPr

o�le

(Cap

ute

etal

.24)

PRP

infa

nts

0to

2yr

s.D

9pr

imiti

vere

�exe

sco

nt.

Re�e

xes

wer

ese

lect

edfr

omcl

inic

alob

serv

atio

nsof

path

olog

ical

lype

rsis

ting

prim

itive

re�e

xes

inch

ildre

nw

ithCP

/nda

Dev

elop

men

tal

pedi

atric

ians

/nda

Infa

ntN

euro

logi

cal

Inte

rnat

iona

lBa

tter

y(E

lliso

net

al.25

)

Infa

nib

at-r

isk

infa

nts

inN

ICU

follo

w-u

ppr

ogra

ms

1to

18m

os.

D20

item

sgr

oupe

din

to5

cate

gorie

s:sp

astic

ity,

vest

ibul

arfu

nctio

n,he

adan

dtr

unk

cont

rol,

rest

ing

tone

and

desc

riptio

nof

mot

orbe

havi

orof

the

legs

cat.

Base

don

fact

oran

alys

esof

neur

omot

orbe

havi

oron

32ite

ms

sele

cted

from

four

exis

ting

asse

ssm

ents

24,2

6-

28in

308

NIC

Ugr

adua

ted

infa

nts

/st

anda

rdiz

atio

nba

sed

onth

ese

308

infa

nts

Prof

essi

onal

sw

orki

ngin

NIC

Ufo

llow

-up

prog

ram

s/a

few

min

utes

Bayl

eySc

ales

ofIn

fant

Dev

elop

men

t,2nd

/ /3d

Ed.

(Bay

ley29

,30 )

BSID

-II/

IIIch

ildre

n1

mo.

to3.

5yr

s.D

,EM

otor

scal

e(8

1ite

ms,

gros

san

d�n

em

otor

beha

vior

)(in

addi

tion:

men

tals

cale

and

beha

vior

ratin

gsc

ale)

cont

.G

ener

alm

atur

atio

nalis

tpr

inci

ples

/st

anda

rdiz

atio

non

1700

US

child

ren

aged

1to

42m

os.

Psyc

holo

gist

s/1

5-20

min

utes

(mot

orsc

ale

only

)tot

alte

st:2

5-60

min

utes

Peab

ody

Dev

elop

men

tal

Mot

orSc

ales

,2nd

ed.

(Fol

ioan

dFe

wel

l31)

PDM

S-II

child

ren

0to

6yr

s.D

Gro

ssan

d�n

em

otor

scal

essu

btes

ts:r

e�ex

es,

stat

iona

ry,l

ocom

otio

n,ob

ject

man

ipul

atio

n,gr

aspi

ngan

dvi

sual

-mot

orin

tegr

atio

n

cont

.nd

a/s

tand

ardi

zed

on20

03ch

ildre

nO

ccup

atio

nalt

hera

pist

s/4

5-60

min

utes

27

2


Ass

essm

ent

(Aut

hor)

Shor

tna

me

Popu

lati

onA

gegr

oup

Purp

ose

Test

desc

ript

ion

-as

sess

men

tof:

Type

ofva

riab

les

Test

cons

truc

tion

/st

anda

rdiz

atio

nA

sses

sors

/tim

eto

adm

inis

ter

Mov

emen

tA

sses

smen

tof

Infa

nts

(Cha

ndle

ret

al.32

)

MA

Ihi

gh-r

isk

infa

nts

inN

ICU

follo

w-u

pcl

inic

s

0to

12m

os.

D,E

65te

stite

ms

grou

ped

into

4se

ctio

ns:m

uscl

eto

ne,p

rimiti

vere

�exe

s,au

tom

atic

reac

tions

and

volit

iona

lmov

emen

t

cont

.nd

a/a

pro�

lefo

rty

pica

lmot

orbe

havi

orat

4m

os.h

asbe

ende

velo

ped

base

don

35in

fant

s

Phys

ical

ther

apis

ts,

occu

patio

nalt

hera

pist

s,ph

ysic

ians

,nur

ses,

psyc

holo

gist

san

dot

hers

who

have

spec

ializ

edkn

owle

dge

and

expe

rienc

ein

infa

ntde

velo

pmen

t/20

to30

min

utes

Neu

rom

otor

Beha

vior

alIn

vent

ory

(Gor

gaan

dSt

ern33

)

NBI

infa

nts

0to

12m

os.

D12

0ite

ms

grou

ped

into

cate

gorie

son

mus

cle

tone

,dev

elop

men

tal

mot

orab

ilitie

s,qu

ality

ofm

ovem

ent,

re�e

xes

and

reac

tions

,ora

l-mot

orbe

havi

or

cont

.nd

a/n

dand

a/n

da

Todd

lera

ndIn

fant

Mot

orEv

alua

tion

(Mill

eran

dRo

id34

)TI

ME

child

ren

4m

os.t

o3.

5yr

s.D

,EFi

vepr

imar

ysu

btes

tson

mob

ility

,mot

oror

gani

zatio

n,st

abili

ty,

soci

al/e

mot

iona

lab

ilitie

san

dfu

nctio

nal

perf

orm

ance

and

thre

ecl

inic

alsu

btes

ts:q

ualit

yra

ting,

atyp

ical

posi

tions

and

com

pone

ntan

alys

is;

focu

son

tran

sitio

nsbe

twee

nm

ovem

ent

patt

erns

cont

.Su

bdom

ains

deve

lope

dby

apa

nelo

fexp

erts

,�e

ldte

stin

gan

dex

pert

cons

ulta

tion

/sta

ndar

diza

tion

on14

4ch

ildre

nw

ithm

oder

ate

tose

vere

deve

lopm

enta

ldel

ays

and

731

TDch

ildre

n

Phys

ical

and

occu

patio

nalt

hera

pist

sor

othe

rclin

icia

nsw

ithex

pert

ise

inas

sess

men

tof

mot

orsc

ales

/10-

55m

inut

es

28

Chapter 2

Ass

essm

ent

(Aut

hor)

Shor

tna

me

Popu

lati

onA

gegr

oup

Purp

ose

Test

desc

ript

ion

-as

sess

men

tof:

Type

ofva

riab

les

Test

cons

truc

tion

/st

anda

rdiz

atio

nA

sses

sors

/tim

eto

adm

inis

ter

Obs

erva

tion

ofm

otor

beha

vior

Alb

erta

Infa

ntM

otor

Scal

e(P

iper

and

Dar

rah35

)

AIM

Sin

fant

s0

toin

depe

nden

tw

alki

ng

D58

item

sin

four

post

ural

posi

tions

:pro

ne,s

upin

e,si

ttin

gan

dst

andi

ng,

test

item

sar

esc

ored

asob

serv

edor

noto

bser

ved

base

don

draw

ings

cont

.Ev

alua

tion

ofth

ese

quen

tial

deve

lopm

ento

fpo

stur

alco

ntro

lre

lativ

eto

four

post

ural

posi

tions

/st

anda

rdiz

atio

non

2202

sex

and

age

stra

ti�ed

Cana

dian

FTin

fant

s

Pedi

atric

phys

ical

ther

apis

ts/1

5m

inut

es

Stru

ctur

edob

serv

atio

nof

mot

orpe

rfor

man

ce(P

erss

onan

dSt

röm

berg

36)

SOM

P-I

high

-ris

kin

fant

s0

to10

mos

.D

13as

cend

ing

scal

esof

mot

orde

velo

pmen

tfor

each

body

part

insu

pine

and

pron

epo

sitio

nan

din

the

who

lebo

dyw

ithth

ein

fant

sitt

ing,

stan

ding

and

inlo

com

otio

n

cont

.A

sses

smen

tofl

evel

ofm

otor

deve

lopm

ent

and

qual

ityof

mov

emen

ts/n

da

Phys

ical

ther

apis

ts,

neon

atol

ogis

ts,

paed

iatr

icne

urol

ogis

ts/n

da

Qua

lity

ofm

otor

beha

vior

Test

ofIn

fant

Mot

orPe

rfor

man

ce(C

ampb

ell37

)

TIM

Pin

fant

sbi

rth

(32

wks

.PM

A)t

o4

mos

.

D42

item

sgr

oupe

din

totw

ose

ctio

ns:o

bser

ved

and

elic

ited

sect

ions

cont

.So

me

item

sfr

omne

urol

ogic

al,

neur

obeh

avio

ral

and

mot

oras

sess

men

ts23

,37-

39/

nda

Phys

ical

and

occu

patio

nalt

hera

pist

s/n

da

Gen

eral

Mov

emen

ts(E

insp

iele

reta

l.40,

Had

ders

-Alg

ra41

)

GM

sin

fant

sbi

rth

to4

mos

.D

,PA

sses

smen

tofv

aria

bilit

yan

dco

mpl

exity

ofsp

onta

neou

sm

otor

beha

vior

insu

pine

posi

tion

cat.

Neu

rona

lgro

upse

lect

ion

theo

rypr

inci

ples

/nda

No

spec

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29

2


Validity and reliability

In Table III data on the di�erent kinds of validity and reliability of the selected methods are

presented. Extended versions of Table III on validity and reliability can be found in Appendix II or

on the journal’s website. Construct validity, the extent to which the items of the instruments re�ect

neuromotor function, was moderate to very good for most instruments. For three instruments no

data were available. No data were available on concurrent validity with other methods to assess

neuromotor function for eight instruments; for the other seven the range was from moderate to

very good. Studies on the predictive validity of the instruments for CP or minor developmental

disorders showed good predictive validity for six instruments, moderate predictive validity for four

instruments and no data were described for �ve instruments. Data were available on intra-observer

reliability for only four assessments. Two instruments had a very good and two had a moderate

intra-observer reliability. For eleven instruments information on interobserver agreement was

available: it ranged from moderate to very good.

Table III: Validity and reliability of the tests

Assessment(short name)

Constructvalidity

Concurrentvalidity

Predictivevalidity

Intra-observeragreement

Inter-observeragreement

Touwen19,74 nda nda + nda nda

Amiel-Tison20,42-46 + + + nda

Muscle power47-49 ++ nda + nda nda

HINE22,50-52 + nda + nda ++

PRP24,53 ! ! nda nda +

Infanib25,54,55 + nda nda nda

BSID-II29,56 nda nda +

PDMS-II31,56 nda ++

MAI32,57-62 nda nda

NBI54,63 + nda nda nda nda

TIME64 nda nda nda ++

AIMS65-67 ++ ++ ++

SOMP-I68,69 + nda nda +

TIMP37,70-73 + + + nda +

GMs40,41,74-78 ++ + + ++ ++

++ = very good, + = good, = moderate,!= poor, nda = no data available, see Table I for description of evaluationcriteria. Extended versions of Table III on validity and reliability can be found in Appendix II.

30

Chapter 2

DISCUSSION

We will discuss the �fteen instruments according to their classi�cation into 1) comprehensive

neurological examination, 2) procedures with standardized scoring, 3) observation of milestones

and speci�c aspects of motor behavior and 4) assessment of the quality of motor behavior.

Comprehensive neurological examinations19-22 are mainly based on traditional neuropediatric

concepts. They have a good construct validity and a good predictive validity for the development

of major motor disorders such as CP or the prediction of future locomotor function. Virtually no

information was available on the predictive validity of neurological examinations for more subtle,

minor developmental disorders such as MND and DCD. The exception to this rule was the Touwen

examination for which some data were available showing that MND at school age may be predicted

to a limited extent74. It is interesting to note that little information was available on the reliability of

these frequently used assessments.

The second group of instruments consists of procedures with standardized scoring, which are

quite heterogeneous and comprise the assessment of primitive re!exes (Primitive Re!ex Pro�le

(PRP)24), a compilation of tests of pre-existing neurological assessments (Infant Neurological

International Battery (Infanib)25) and more extensive test batteries like the Motor Scales of the Bayley

(BSID-II/III)29,30 and the Peabody Developmental Motor Scales (PDMS-II)31. Three tests, the Movement

Assessment of Infants (MAI)32, Neuromotor Behavioral Inventory (NBI)33 and Toddler and Infant Motor

Evaluation (TIME)34, combine neurological test items with observation of speci�c aspects of motor

behavior. In general, the procedures with standardized scoring have a poor to moderate construct

validity and concurrent validity. Predictive validity was either only moderate25,31,32 or no data were

available. This might be a point of concern, but it should be realized that these tests have not been

developed with the aim of predicting future motor disorders. The Bayley Scales, MAI and TIME can

be used for the evaluation of changes in neuromotor functioning. Another attractive feature of the

Bayley and PDMS-II is their standardization for very large groups of children. Interobserver reliability

of most of these assessments is good to very good.

Two instruments consist mainly of observation of milestones and speci�c aspects of motor

behavior: the Alberta Infant Motor Scale (AIMS)35 and the Structured Observation of Motor

Performance (SOMP)36. Construct validity for both instruments is acceptable. For the SOMP,

additional validity data are lacking. Concurrent validity for the AIMS is good, but predictive validity

for major developmental disorders is only moderate. Reliability of these observational instruments

is satisfactory.

The last two assessments, the General Movement method (GM)40,41 and the Test of Infant Motor

Performance (TIMP)37 share the feature that they both assess quality of motor behavior or motor

patterns. The GM method assesses quality of spontaneous motor behavior in supine position. The

TIMP di"ers from the GM method in that not only does it focus on spontaneous movements but

also mainly assesses quality of postural adjustments elicited by handling the infant. Interestingly,

31

2


both methods have a good predictive validity, the TIMP for major developmental disorders such as

CP, and the GM method for both major and minor developmental disorders such as MND. Construct

and concurrent validity and reliability of the GMs and TIMP are also satisfactory. These last two

assessments are only useful under the age of four months.

CONCLUDING REMARKS

The main issue in choosing a suitable instrument in a certain situation is de!ning the goal that

the instrument needs to serve. If the main goal is discriminating between infants with deviant

neuromotor function and infants falling in the range of typical development, all !fteen reviewed

instruments can be used. However, only three of the instruments (BSID-II29,30, MAI32 and TIME34) can

be used for evaluation of the e"ect of intervention. Data on predictive validity are available for ten

instruments. The predictive validity for most of them is moderate at best. Only the two instruments

that assess qualitative aspects of motor behavior (TIMP37 and GM-method40,41) show good predictive

validity. Prediction of developmental outcome at an early age will never be perfect. This is inherent

in the developmental characteristics of the young brain4. Therefore, in medical evaluation of high-

risk infants, the best prediction is achieved when multiple, complementary clinical tools are used.

A good combination is medical history including achieved milestones, physical and neurological

examination, a speci!c assessment of the quality of motor behavior and results of neuroimaging

such as ultrasound or MRI assessment.

32

Chapter 2

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37

3CHAPTER

The Infant Motor Pro�le:a standardized and qualitative method to assess motor

behaviour in infancy

Kirsten Heineman1,2, Arend Bos3, Mijna Hadders-Algra1


3Department of Paediatrics, Division of NeonatologyUniversity Medical Center Groningen

Developmental Medicine and Child Neurology 2008;50:275-82

38

Chapter 3

ABSTRACT

Background: A reliable and valid instrument to assess neuromotor condition in infancy is a

prerequisite for early detection of developmental motor disorders. We developed a video-based

assessment of motor behaviour, the Infant Motor Pro�le (IMP), on motor abilities, movement

variability, ability to select motor strategies, movement symmetry and �uency. The IMP consists

of 80 items and is applicable from 3 to 18 months. The present study aims at teasting intra and

interobserver reliability and concurrent validity of the IMP with the Alberta Infant Motor Scale and

Touwen neurological examination.

Methods: The study group consisted of 40 low-risk at term born (median gestational age (GA) 40

weeks, range 38-42) and 40 high-risk preterm born infants (median GA 29.6, range 26-33) with

corrected ages 4 to 18 months (31 girls, 49 boys).

Results: Intra and interobserver agreement of the IMP were satisfactory (Spearman ρ=0.9).

Concurrent validity of IMP and AIMS was good (Spearman ρ=0.8, p<0.0005) . The IMP was able

to di"erentiate between infants with normal neurological condition, simple minor neurological

dysfunction (MND), complex MND and abnormal neurological condition (p<0.0005).

Conclusion: The IMP may be a promising tool to evaluate neurological integrity during

infancy –a suggestion which needs con�rmation by means of assessment of larger groups of infants

with heterogeneous neurological conditions.

39

3

The infant Motor pro�le

INTRODUCTION

Assessment of motor dysfunction in young children is still in its infancy. This is regrettable because

a sensitive, reliable and valid instrument is a prerequisite for early detection of infants with

developmental motor disorders, such as cerebral palsy (CP) and developmental co-ordination

disorder (DCD). Early detection is needed to warrant the provision of intervention at young ages,

i.e. at ages when brain development is characterized by high degrees of plasticity1-3. Adequate

assessment techniques are also indispensable for the evaluation of the e!ectiveness of intervention

strategies.

Recently, we reviewed "fteen instruments to assess neuromotor condition in infancy with

respect to their characteristics and psychometric properties (unpublished data). It was concluded

that the traditional forms of neurological examination showed good predictive validity for major

developmental disorders such as CP. However, instruments that assess quality of motor behaviour

(TIMP4, General Movement method5,6) turned out to be most promising in terms of predictive validity,

as they have good predictive value for both major and minor (minor neurological dysfunction

(MND), DCD) developmental disorders.

The "nding that quality of motor behaviour and variation in particular is an essential parameter

to assess the condition of the young nervous system, "ts well to the concepts of the Neuronal Group

Selection Theory (NGST)7-10. According to NGST, normal motor development is characterized by two

phases of variability. During the phase of primary variability variation in motor behaviour is not

geared to external conditions. Next, at function-speci"c ages, the phase of secondary variability

takes over. The child learns to select the best motor strategy for each situation on the basis of

a!erent information resulting from self-generated motor activity, from active trial and error. In other

words, the child develops the capacity to adapt motor performance to environmental constraints.

Children with pre or perinatally acquired lesions of the brain, such as children with CP and some

children with DCD, exhibit stereotyped motor behaviour. This might be related to a reduction of the

repertoire of primary cortical-subcortical neuronal networks. Motor behaviour of these children is

not only a!ected by the reduced size of the repertoire of motor strategies, but also by problems

in the process of selection of the most e#cient strategy for each situation. The latter problems

may be attributed to the absence of speci"c strategies which forces the child to choose in certain

conditions amongst non-optimal strategies and the presence of de"cits in the processing of sensory

information9-11.

Having noticed that application of motor variability as a means to evaluate neuromotor

condition functions so well in early infancy, we embarked on the development of a similar

assessment instrument for neuromotor condition at ages between 3 and 18 months. This resulted

in the development of the Infant Motor Pro"le (IMP).

40

Chapter 3

The Infant Motor Pro�le (IMP)

The IMP evaluates spontaneous motor behaviour of infants aged 3 to 18 months, or rather until the

age at which the child has a couple of months experience with walking independently. This means

that the IMP can be applied in infants with a more or less typical development until approximately

the age of 18 months. In children with moderate to severe developmental motor disorders

the IMP can be used beyond the age of 18 months. The IMP is a video based assessment. Motor

behaviour is evaluated in the following conditions: supine, prone, sitting, standing and walking. In

addition, reaching, grasping and manipulation of objects are evaluated in supine and in supported

sitting conditions, i.e. while sitting on the parent’s lap. The child’s motor activity may be entirely

spontaneous or may be elicited by the presentation of interesting objects. The order in which

the various conditions are evaluated depends on the child’s age, functional capacities, mood and

interest. In the youngest infants, assessment in general starts with an observation of behaviour in

supine condition for 5 minutes. In older children, it is more common to start with a sitting condition,

either on the parent’s lap or in a freely sitting condition.

The IMP consists of 80 items classi!ed into !ve subscales (for details see Appendix). The !rst

subscaleaddressesmovementvariability; itassessesthesizeofthemovementrepertoire.The25items

of this subscale are scored as ‘insu"ciently variable’ denoting the presence of a limited repertoire of

ways in which the child is able to perform the task, or as ‘su"ciently variable’ denoting the presence

of a variable repertoire of motor solutions. The second subscale also addresses movement variability

and comprises 15 items; it evaluates the child’s ability to select adaptive motor strategies from his or

her movement repertoire, an ability which develops during the phase of secondary variability. The

items of this subscale are scored as ‘no selection’ or as ‘adaptive selection’. ‘No selection’ means that

the child does not select from his or her repertoire the movement strategy which !ts the situation

best, but uses various motor strategies. If the child chooses for most of the time the most suitable

motor strategy from his or her motor repertoire for a speci!c situation ‘adaptive selection’ is scored.

The other subscales of the IMP are movement symmetry, #uency, and performance. The subscale

symmetry contains 10 items which address the presence or absence of stereotyped asymmetries.

In fact, movement symmetry may be regarded as a speci!c form of movement variability, but we

decided for a separate subscale on presence and absence of symmetry as it might have speci!c

diagnostic value12. Movement #uency re#ects the ability of the infant to !ne-tune motor output.

The subscale consists of 7 items, including two items on the presence of tremors. Loss of movement

#uency is one of the !rst signs of a non-optimal neurological condition6,13. The subscale performance

of 23 items is a more or less traditional one on achieved motor milestones. This means that the

IMP does not only address quality of motor behaviour but also evaluates what the child is able to

achieve.

Aim of the study

The aim of the present study is to assess psychometric properties of the IMP. First, inter and

3

41


intraobserver reliability of the IMP are addressed. Second, relations between IMP scores and age,

gestational age at birth and ultrasound scans of the brain made during the neonatal period are

evaluated. These relations might shed light on the construct validity of the IMP. We hypothesize

that total IMP scores and scores on the subscales variability-ability to select and performance are

positively correlated with corrected age as these capacities develop with increasing age, whereas

such relationships between corrected age and the subscores variability-size of repertoire, symmetry

and �uency are absent. In addition, we assume that low gestational age leads to lower IMP scores,

especially on the subscales variability-size of repertoire, symmetry and �uency. Infants born

preterm have a higher risk for brain lesions which can lead to a reduced, less variable movement

repertoire, including stereotyped asymmetries. As loss of �uency is one of the �rst signs of a non-

optimal neuromotor condition, we expect preterm infants to have lower �uency scores. We expect

that infants with serious brain lesions on ultrasound scans show lower IMP scores.

Third, concurrent validity of the IMP with the AIMS14 and the neurological examination according to

Touwen15 is assessed. To this end, a group of 80 infants with corrected ages from 4 to 18 months was

evaluated by means of the IMP, the AIMS and the neurological examination according to Touwen.

We expect a signi�cant positive correlation between AIMS and total IMP score and IMP performance

score, and weakly to moderately positive correlations between AIMS and other subscale scores of

the IMP. In addition, we hypothesize that the degree of neurological dysfunction shows a clear

inverse relationship with the total IMP score and IMP subscores.

METHODS

Participants

The study group consisted of 80 infants (31 girls and 49 boys). Forty infants were born at term

(gestational age at birth 40 weeks (median value; range 38 to 42 weeks) without pre or perinatal

complications with a median birth weight of 3550 grams (range 2730 to 4220 grams). Forty infants

were born preterm with a gestational age at birth of 26-33 weeks (median value 29.6 weeks) and

a median birth weight of 1180 grams (range 585 to 2120 grams). The preterm infants had been

admitted to the neonatal intensive care unit (NICU) of the Beatrix Children’s Hospital of the University

Medical Center (UMC) in Groningen during the years 2003 and 2004.

Infants were assessed cross-sectionally at the corrected ages of 4, 6, 10, 12 and 18 months

(Table I). All parents of the infants signed an informed consent form. The project was approved by

the Ethics Committee of the UMC in Groningen.

Procedures

Each assessment started with a video recording of spontaneous motor behaviour in the following

conditions: supine, prone, sitting with or without support, standing with or without support, walking

with or without support and sitting on the parent’s lap. In the supine position and when seated

42

Chapter 3

on the parent’s lap small attractive objects were presented to assess the infant’s ability to reach,

grasp and manipulate objects. Toys were also used to elicit rolling, crawling, standing up behaviour

and trunk rotation during sitting and standing. In the youngest children recording always started

with the infant lying in supine for 5 minutes. The order of the conditions was not �xed but was

adapted to the child’s interest. In general, video recording lasted about 15 minutes. On basis of the

video recording both the Infant Motor Pro�le scores and AIMS14 were determined. Total AIMS scores,

instead of percentiles, were used in the data processing, as Canadian reference values are currently

inappropriate for Dutch children16. O!-line scoring of the IMP took approximately 10 minutes per

video recording. Calculation of IMP scores will be explained in the next paragraph.

After the video recording of motor behaviour, a neurological examination according to

Touwen15 was carried out. The neurological condition of the child was classi�ed as normal, as the

simple or complex form of minor neurological dysfunction (MND) or as de�nitely abnormal. A child

was classi�ed as de�nitely abnormal, when he or she exhibited a clear neurological syndrome such

as a clear hemisyndrome, a marked hypertonia or hypotonia in combination with clearly abnormal

re"exes or a hyperexcitability syndrome. MND denoted the presence of one or more clusters of

mild signs of neurological dysfunction, such as mild abnormalities in muscle tone regulation, mildly

abnormal re"exes, mild visuomotor dysfunction or mild dysfunction in gross motor or �ne motor

performance11. Simple MND indicates the presence of one cluster of mild signs of neurological

dysfunction and can be regarded as a normal, but non-optimal condition of the nervous system.

Complex MND denotes the presence of two or more clusters of dysfunction and is related to early

brain damage17.

Data analyses

IMP scores were separately calculated for each subscale according to the following formula:

Sum of item scores

Score = * 100%

(no. of items of scale or subscale – no. of items NA) * max score of items

‘No’ stands for number and ‘NA’ means not applicable (for instance the item ‘variability of arm

movements during walking’when a child is not able to walk) and ‘max score of items’ is the maximum

Table I: Number and age distribution of infants included in the validity study

Age (months) 4 6 10 12 18 Total

Term 7 7 7 8 11 40Preterm 7 7 7 8 11 40

Total 14 14 14 16 22 80

43

3


score amongst the items of the subscale. For the subscales variability-size of repertoire, variability-

ability to select and �uency the maximum score for each item is two and for the subscale symmetry,

three. Because the performance subscale contains items with di�erent numbers of maximum scores

(see Appendix I), the scores are weighed before computing the performance subscale score. If a

child scores 3 points on the item ‘reaching and grasping of an object in supine position’ where the

maximum score is 7 points, the child is given 3/7 = 0.43 points. For an item with a 4-point scale,

the score would be 3/4 = 0.75 points. This means that all performance items contribute to a similar

extent to the performance subscore and the total IMP score (see Appendix I). The total IMP score is

computed by summing the scores on the �ve subscales and dividing this number by �ve. All scores

on subscales and the total IMP score are expressed as a percentage with a maximum score of 100%.

To assess the interobserver agreement of the IMP, 38 video recordings were scored independently

by two assessors. The sample was created by randomly selecting from each of the age groups

recordings of three preterm and three full-term infants. Both assessors evaluated eight videos

from the 12-month age group (four full term and four preterm infants) and twelve videos from the

18-month group (six full term and six preterm infants) in order to obtain su�cient data on standing

and walking items to determine reliability. One of the assessors (KRH) knew whether an infant was

born preterm or at term, but she was not aware of the details of the infant’s clinical history. The

other observer (MHA) was blind with respect to the clinical status of the infants. In order to establish

intraobserver agreement of the IMP scores, KRH evaluated the same 38 video recordings twice with

an interval of one month. Inter and intraobserver reliability at subscale level were analysed by means

of the Spearman correlation coe�cient ( ). Interpretation of correlation coe�cients was as follows:

< 0.49: weak relationship, 0.50 < < 0.75: moderate relationship and > 0.75: strong relationship18.

The relationships between IMP scores, AIMS scores and corrected age were evaluated with

Spearman rank correlation and associated con�dence intervals. The relation between IMP and

neurological classi�cation and status at birth (preterm or full-term) was assessed with help of the

non-parametric Kruskal-Wallis and Mann Whitney U test, respectively. Mann Whitney U test was also

used to determine di�erences in IMP scores between infants with and without serious brain lesions.

Throughout the analyses di�erences and correlations with a p-value < 0.05 were considered to be

statistically signi�cant (two-tailed testing).

RESULTS

Reliability

Intra and interobserver reliability of total IMP score were strong (Table II). Intraobserver agreement

was strong for subscales variability-repertoire, variability-ability to select and performance and was

moderate for subscales �uency and symmetry. Interobserver reliability of the subscales variability-

ability to select and performance was strong. Interobserver reliability was moderate for subscales

variability-repertoire and �uency and weak for subscale symmetry.

44

Chapter 3

Validity

The IMP total score varied between 66 and 97 (median value 88). No signi�cant di�erences in total

IMP scores and all subscales were found between girls and boys. The IMP total score was signi�cantly

related to corrected age (ρ = 0.68 (95% CI 0.54-0.78), p < 0.0005). The two subscales variability-ability

to select and performance, which on theoretical assumptions were expected to correlate with

age, were signi�cantly related to corrected age (variability-ability to select: ρ = 0.68 (95% CI 0.54-

0.78), p < 0.0005; performance: ρ = 0.91 (95% CI 0.86-0.94), p < 0.0005). Also, a positive correlation

between age and symmetry score was found, indicating that the infants showed less asymmetric

behaviour with increasing age (ρ = 0.40 (95% CI 0.20-0.57), p< 0.0005). The subscales variability-size

of repertoire and �uency were not related to corrected age (ρ = 0.19 and ρ = 0.07 resp.).

Preterm infants had signi�cantly lower total IMP scores than infants born at term (median IMP

score FT 89 vs. PT 82; Mann-Whitney: p < 0.0005). The di�erence was particularly present in the

subscales variability-size of repertoire (p < 0.0005), �uency (p < 0.0005) and symmetry (p = 0.021).

No statistically signi�cant di�erence between the two groups was found for the other two subscales

variability-ability to select (Mann-Whitney: p = 0.064) and performance (p = 0.126). Also, preterm

infants had signi�cantly lower AIMS scores than full term infants (p = 0.046).

Repeated brain ultrasound scans made during the �rst weeks of life indicated serious brain

lesions in each of three preterm infants: one infant had a unilateral periventricular haemorrhage

due to a venous infarction19, one had bilateral periventricular echodensities evolving into extensive

periventricular cysts20 and one infant had middle cerebral artery infarction on the right side.

Compared to the other 37 PT infants with no or milder brain lesions such as transient periventricular

echodensities, these three infants showed signi�cant lower IMP scores (Mann-Whitney: p = 0.006)

and AIMS scores (Mann-Whitney: p = 0.041).

The AIMS scores of the various assessments varied from 8 to 58 with a median value of 46. The

AIMS score showed a high correlation with corrected age (ρ = 0.91 (95% CI 0.86-0.94), p < 0.0005).

The total IMP score was related to the AIMS score (ρ = 0.78 (95% CI 0.68-0.85), p < 0.0005). This

correlation was brought about in particular by the high correlation between the conceptually

Table II: Intra and interobserver reliability of IMP: Spearman correlation coe�cients

IMP-subscale Spearman ρ (95% con"dence interval)

Intraobserver reliability Interobserver reliability

Total IMP score 0.9 (0.8-0.9) 0.9 (0.8-1.0)IMP-subscale:Variability-repertoire 0.8 (0.6-0.9) 0.7 (0.4-0.8)Variability-ability to select 0.8 (0.7-0.9) 0.8 (0.6-0.9)Fluency 0.6 (0.3-0.8) 0.7 (0.4-0.8)Symmetry 0.6 (0.4-0.8) 0.4 (0.0-0.6)Performance 1.0 (0.9-1.0) 0.9 (0.8-1.0)

45

3


similar AIMS score and IMP subscore on performance (ρ = 0.94 (95% CI 0.91-0.96), p < 0.0005). Also

the subscales variability-size of repertoire, variability-ability to select and symmetry were related to

the AIMS (variability-size of repertoire: ρ = 0.42 (95% CI 0.22-0.59), p < 0.0005; variability-ability to

select: ρ = 0.69 (95% CI 0.56-0.79), p < 0.0005; symmetry: ρ = 0.46 (95% CI 0.27-0.62), p < 0.0005),

but the subscale on �uency was not (ρ = 0.20, n.s.). When the e�ect of the confounding factor of age

was partialled out, the correlations between the various IMP scores and the AIMS score remained

statistically signi�cant (ρ-values varying from 0.31 (95% CI 0.10-0.50), p = 0.006 (�uency) to 0.72

(95% CI 0.60-0.81), p < 0.0005 (performance); median ρ-value 0.338).

Twenty-seven of the 80 infants had a normal neurological condition, 19 were classi�ed as

having simple MND, 32 as having complex MND and 2 as neurologically abnormal. Neurological

condition was not related to corrected age. The total IMP score showed a highly signi�cant relation

with neurological condition (Kruskal-Wallis: p < 0.0005, Figure 1). Also the various subscales of the

IMP were related to neurological condition: variability-size of repertoire (Kruskal-Wallis: p < 0.0005),

variability-ability to select (p = 0.013), �uency (p< 0.0005), symmetry (p = 0.023), and performance

(p = 0.024; Figure 2A-E). It is interesting to note that di�erences in IMP total score and in scores on

the subscales of variability and performance are found in particular between infants with complex

MND or an abnormal neurological condition and those with a normal neurological condition or

simple MND.

TotalIMP-score

100

90

80

70

60

normal S-MND C-MND abnormal

-

- -

-

- -

Figure 1: Relationship between neurological condition and total IMP score. The data are presented bymedian values (horizontal bars) and interquartile ranges (boxes) and ranges (vertical lines). N = neurologicallynormal, S-MND = simple MND, C-MND = complex MND. Kruskal Wallis: ** p < 0.0005

46

Chapter 3

Varia

bilit

y-r

eper

toire

100

90

80

70

60


A-

- -

-

- -

Varia

bilit

y–

abili

tyto

sele

ct

100

90

80

70

60


B

–

- -

Flue

ncy

100

90

80

70


C

- -

- -- -

Sy

mm

etry

100

90

80

70

60


D

- -

-

Perf

orm

ance

100

90

80

70

60


50

40

E

Figure 2: Relationship between neurologicalcondition and the �ve subscales of the IMP.A) variability-repertoire, B) variability-ability to selectC) �uency, D) symmetry, E) performance. KruskalWallis: * p < 0.05, ** p < 0.0005

47

3


DISCUSSION

The present study indicates that the IMP can be performed in a reliable way. In addition, the study

suggests that the IMP has a good concurrent validity with the AIMS and with the infant’s neurological

condition.

The intra and interobserver agreement on the total IMP score was high. Agreement on

the subscales variability-repertoire, variability-ability to select, performance and �uency was

satisfactory. Intraobserver reliability on the subscale symmetry was moderate, but the interobserver

reliability on this subscale was only poor. This was probably caused by the virtual absence of serious

asymmetries in the group used for reliability testing: 34 out of the 38 infants obtained symmetry

scores of 100% from both assessors. The other four infants were given somewhat lower symmetry

scores, but the degree of reduction di!ered slightly between the assessors. This suggests that the

population studied suited the purpose of assessing the reliability of the symmetry subscale only to

a moderate extent.

In line with our assumptions, the IMP total score increased signi"cantly with increasing age.

This e!ect was brought about by the relationship between age and the subscores performance and

variability. Our "nding parallels those on the AIMS; the AIMS score is signi"cantly related to age14.

The positive correlation between age and the subscore variability-ability to select underlines the

notion that infants learn to select a preferred strategy from the motor repertoire when they get

older9. In our population, symmetry scores also correlated with age with older infants showing less

asymmetries than younger infants. This is probably due to the fact that in our study group only one

infant had a serious asymmetry. This girl was assessed at 10 months corrected age; later follow-up

assessments revealed that she developed a unilateral spastic cerebral palsy. Young infants quite

often show mild to moderate asymmetries which usually resolve spontaneously with increasing

age21. The low prevalence of serious unilateral disorders in the present sample precludes a proper

evaluation of the e!ect and utility of the symmetry subscale. As expected, movement �uency was

not related to age.

Preterm infants showed lower total IMP scores and lower scores on the subscales variability-

repertoire, symmetry and �uency, as was expected. Infants born preterm are at risk for brain

lesions, which can lead to a reduction of movement repertoire and the presence of stereotyped

asymmetries10,12. Loss of movement �uency is one of the "rst signs associated with non-optimal

neurological condition6,13. Prematurity was not related to the scores on the subscales variability-

ability to select and performance. Infants with serious brain lesions as seen on ultrasound, such as

haemorrhage grade IV or periventricular cystic lesions, indeed showed signi"cantly lower IMP scores

than infants with no or mild brain lesions. Altogether, construct validity of the IMP, operationalized as

relation of IMP scores with age, gestational age and brain lesions on ultrasound, seems satisfactory.

The IMP total score and the "ve subscales of the IMP correlated with the AIMS scores. Especially

the performance subscale showed high correlation with the AIMS, which is not surprising, as both

48

Chapter 3

assess achievements in motor behaviour. Also if correction for age is applied, these correlations

still subsist, which shows that both AIMS and IMP measure the same construct, i.e. integrity of the

brain. Nevertheless, it is interesting to note that the IMP is more sensitive in picking up the e!ect of

preterm birth and serious brain lesions than the AIMS.

Di!erences in total IMP scores and scores on the "ve subscales were found between the four

neurological conditions, with an inverse relationship between IMP scores and degree of neurological

dysfunction. Especially the subscales variability-repertoire and #uency showed clear di!erences.

Di!erences in total IMP scores, scores on variability subscales and on performance subscale were

in particular found between infants with complex MND or abnormal neurological condition and

those with a normal neurological condition or simple MND. Complex MND is the form of minor

neurological dysfunction which in contrast to simple MND has clinical relevance. It probably is

caused by adversities in the pre or perinatal period, and in some cases it might be considered as a

borderline form of cerebral palsy11,22. All in all, concurrent validity of the IMP with the AIMS and with

the neurological examination according to Touwen can be regarded as good.

A limitation of this pilot study is the small sample size of 80 infants of di!erent ages and with

di!erent risk for developmental motor disorders. Present data on reliability and concurrent validity

with AIMS and theTouwen neurological examination are promising, but further research on construct

and predictive validity is necessary. Extrapolation of the di!erence in predictive power of General

Movement-assessment5,6 and the neonatal neurological assessment22 generates the hypothesis

that predictive power of the IMP surpasses that of the AIMS and the neurological examination. The

next step in IMP-development will be the generation of norms and the determination of clinical

applicability.

In conclusion: the Infant Motor Pro"le is a reliable video based assessment of motor behaviour

in infancy which does not only address the child’s motor abilities but also movement variation,

ability to select movement strategies, symmetry and #uency. The current study suggests that the

latter characteristics are promising parameters of neurological integrity – a suggestion which needs

con"rmation by means of assessment of larger groups of infants with a heterogeneous neurological

condition.

ACKNOWLEDGEMENTSWe thank Cornill Blauw-Hospers, MSc , Victorine de Graaf-Peters, MSc and Karin Middelburg, MD, for performinga part of the neurological assessments, and Ms Lidy Kingma-Balkema and Ms Ineke Bakker for skilled technicalassistance. The study was supported by a Junior Scienti"c Masterclass grant of the post-graduate schoolBehavioral and Cognitive Neurosciences (BCN), University of Groningen.

49

3


REFERENCES

1. Kolb B, Brown R, Witt-Lajeunesse A, Gibb R. Neural compensations after lesion of the cerebral cortex.Neural Plasticity 2001;8:1-16.


3. Staudt M. (Re-)organization of the developing human brain following periventricular white matter lesions.Neurosci Biobehav Rev 2007;31:1150-6.

4. Campbell SK, Kolobe TH, Osten ET, Girolami GL, Lenke M. Construct validity of the test of infant motorperformance. Phys Ther 1995;75:585-596.

5. Einspieler C, Prechtl HF, Bos A, Ferrari F, Cioni G. Prechtl’s method on the qualitative assessment of generalmovements in preterm, term and young infants. Clin Dev Med No. 167, London: Mac Keith Press, 2004.

6. Hadders-Algra M. General movements: A window for early identi�cation of children at high risk fordevelopmental disorders. J Pediatr 2004;145:S12-18.


8. Sporns O, Edelman GM. Solving Bernstein’s problem: a proposal for the development of coordinatedmovement by selection. Child Dev 1993;64:960-981.



11. Hadders-Algra M. Developmental coordination disorder: is clumsy motor behaviour caused by a lesion ofthe brain at early age? Neural Plast 2003;10:39-50.

12. Guzzetta A, Haataja L, Cowan F, Bassi L, Ricci D, Cioni G, Dubowitz L, Mercuri E. Neurological examination inhealthy term infants aged 3-10 weeks. Biol Neonate 2005;87:187-196.

13. Hadders-Algra M, Mavinkurve-Groothuis AM, Groen SE, Stremmelaar EF, Martijn A, Butcher PR. Quality ofgeneral movements and the development of minor neurological dysfunction at toddler and school age.Clin Rehabil 2004;18:287-299.

14. Piper MC, Darrah J. Motor assessment of the developing infant. Philadelphia: WB Saunders Company, 1994.

15. Touwen BCL. Neurological development in infancy. Clin Dev Med No. 58. Philadelphia: Lippincott, 1976.

16. Fleuren KM, Smit LS, Stijnen T, Hartman A. New reference values for the Alberta Infant Motor Scale need tobe established. Acta Paediatr 2007;96:424-427.

17. Soorani-Lunsing I, Woltil HA, Hadders-Algra M. Are moderate degrees of hyperbilirubinemia in healthyterm neonates really safe for the brain? Pediatr Res 2001;50:701-5.

18. Portney LG, Watkins MP. Part IV Data analysis: Correlation. Foundations of clinical research. Applications topractice. 2nd ed. Upper Saddle River, NJ: Prentice Hall Health; p. 494, 2000.

19. Volpe JJ. Intraventricular haemorrhage in the premature infant - current concepts. Part II. Ann Neurol1989;25:109-116.


21. Michaelis R, Asenbauer C, Buchwald-Saal M, Haas G, Krageloh-Mann I. Transitory neurological �ndings in apopulation of at risk infants. Early Hum Dev 1993;34:143-153.

22. Hadders-Algra M. Two distinct forms of minor neurological dysfunction: perspectives emerging from areview of data of the Groningen Perinatal Project. Dev Med Child Neurol 2002;44: 561-571.

51

4CHAPTER

Development of adaptive motor behaviour in typicallydeveloping infants

Kirsten Heineman1,2, Karin Middelburg1, Mijna Hadders-Algra1



Acta Paediatrica 2010;99:618-24

52

Chapter 4

ABSTRACT

Aim:During motor development, infants learn to select adaptive motor strategies out of their motor

repertoire. The aim of this study is twofold: �rst, to investigate whether the presence of adaptive

motor behaviour can be observed reliably, and second, to explore the ages at which clinically

observable transition to adaptive motility emerges for four speci�c motor functions: abdominal

progression, sitting motility, reaching, and grasping.

Methods: The reliability part of the study included 38 assessments of term and preterm infants

in the age range of four to 18 months. The longitudinal prospective study included 30 term born

typically developing infants with nine assessments between three and 18 months. On the basis of

standardized video-recordings of spontaneous motor behaviour, the presence of adaptive motor

strategies was scored.

Results: Intra- and interobserver reliability were good. Clinically observable transitions to adaptive

selection started to emerge from six months onwards and peaked between eight and 15 months.

Transitions developed gradually and occurred at speci�c ages for di!erent motor functions.

Conclusion: Transition to adaptive motor behaviour can be observed reliably. Adaptive motor

behaviour develops gradually from six months onwards at function-speci�c ages. Comparison of

our results to literature showed that changes measured by neurophysiologic methods precede

clinically observed transitions.

53

4

Development of adaptive motor behaviour in typically developing infants

INTRODUCTION

During the �rst years of life, children show an impressive development of motor skills like sitting,

crawling, standing, walking, reaching and grasping. Rapidly, the child’s motor repertoire expands,

which enables the child to start exploration of the world. Motor development is a complex

process in which many factors play a role. The limited knowledge on processes governing motor

development induced a wide range of developmental theories. Theories di�er especially with

respect to the roles of ‘nature’ and ‘nurture’. Neuromaturationist theories for instance attribute

major part of development to endogenous, genetic factors, whereas environmental and contextual

factors dominate in the Dynamic Systems Theory1,2. The Neuronal Group Selection Theory (NGST)

is a theory which stresses the complex, continuous and cascadic interaction between information

from the genetic script and environment1,3-5.

According to the Neuronal Group Selection Theory (NGST)1,3-5, motor development is

characterised by two phases of variability. Development starts with the phase of primary variability

which can be observed during fetal life and early infancy. During this phase, all possibilities of the

innate neural networks are explored by means of self-generated activity and movements are neither

adapted to environmental constraints nor dependent on sensory feedback. In the fetus, newborn

and young infant this can be observed in General Movements: movements with great complexity

and variation in which all body parts are involved6,7. These general movements are present until

about four months of age, after which goal-directed motility gradually takes over. The emerging

goal-directed motility such as reaching, grasping and crawling, is characterised by large variability at

�rst. For each motor function all possible motor strategies and their corresponding neural networks

are explored. At function-speci�c ages, infants start to select more adaptive motor strategies.

Motor behaviour becomes more e�cient and adapted to the task requirements and environmental

characteristics. This phase of adaptive selection is called the phase of secondary variability. In this

phase, there is still abundant variability in motor behaviour, which serves the purpose of adaptation

of the movements to speci�c task and environmental characteristics.

Age of transition from primary to secondary variability di�ers for di�erent motor functions.

Sucking patterns, for example, are already adaptive around term age, i.e. at 37 to 40 weeks

gestational age8,9, while transition from primary to secondary variability for postural adjustments

during supported sitting occurs between three and eight months10-12. Reaching movements of

infants aged four months are characterised by large variability in movement trajectories. Around

the age of seven months, infants start to select straighter and more e�cient reaching movements,

indicating that for reaching the transition from primary to secondary variability lies approximately

between four and seven months1,13. These examples illustrate that secondary variability for basic

motor functions emerges during infancy. However, development of secondary variability continues

until adolescence. During this period, the child gains the capacity to �ne-tune motor output to

speci�c requirements and characteristics of task and environment.

54

Chapter 4

The above presented data on ages of transition from primary to secondary variability are based

on exact registration techniques such as electromyography (EMG) and kinematical recordings.

These techniques allow precise measurement of timing of changes in muscle patterns involved in

postural adjustments or straightening of reaching movement trajectories. No research has been

conducted on when transition from primary to secondary variability becomes clinically observable.

We hypothesize that changes measured by neurophysiologic methods precede clinically observable

transitions. Changes in motor behaviour recorded with exact registration techniques represent the

early phases of selection, while clinical observation shows when a certain pattern is selected during

the majority of movements. Knowledge on clinical observable transitions is of clinical relevance.

We recently demonstrated that the assessment of variation and the ability to select adaptive motor

strategies is a useful tool to assess neuromotor integrity (Infant Motor Pro�le14).

Aim of the study

The aim of this study was twofold. First, to investigate whether the presence of adaptive motor

behaviour can be observed reliably (intra- and interobserver reliability). Second, to explore the ages

at which clinically observable transition to adaptive motility emerges in typically developing infants

for four speci�c motor functions: abdominal progression, sitting motility, arm movements during

reaching and hand motility during grasping and manipulation. The four motor functions are part of

the IMP assessment14. The emergence of adaptive motor behaviour in the four motor functions was

studied as part of entire IMP assessments.

METHODS

The reliability part of the study included 38 cross-sectional assessments of term and preterm infants

in the age range of four to 18 months. The longitudinal prospective study included 30 term born

typically developing infants with nine assessments between three and 18 months. The study groups

are described in detail below. On the basis of standardized video-recordings of spontaneous motor

behaviour, the presence of adaptive motor strategies was assessed.

Participants in the reliability study

We studied whether the presence of adaptive motor behaviour can be observed reliably in 19 term

infants and 19 preterm infants. The term group in the reliability study consisted of 6 girls and 13

boys. Median gestational age was 40 weeks (range 38 – 42 weeks) and median birth weight was

3588 grams (range 3070 – 4200 grams). The preterm group consisted of 6 girls and 13 boys, median

gestational age was 29.9 weeks (range 27.1 – 32 weeks) and median birth weight was 1165 grams

(range 585 – 2120 grams). Three of the preterm infants had serious brain lesions on neonatal brain

ultrasound: two had signs of cystic periventricular leukomalacia15 and one had intraventricular

haemorrhage with ventricular dilatation (grade III)16. The preterm infants had been admitted to the

55

4


neonatal intensive care unit (NICU) of the Beatrix Children’s Hospital of the University Medical Center

(UMC) in Groningen between December 2003 and January 2005. The infants were assessed at one of

the following ages: 4, 6, 10, 12 or 18 months. At 4, 6 and 10 months three full term and three preterm

infants were included, at 12 months four full term and four preterm infants and at 18 months six full

term and six preterm infants. The 38 videotapes were scored by two observers independently (KRH

and MHA) to assess interobserver agreement. To determine intra-observer agreement, the sample

was scored twice by one observer (KRH) with an interval of one month.

Participants in the study on emergence of adaptive motor behaviour

Thirty typically developing infants were included in the study on the emergence of adaptive motor

behaviour (12 girls and 18 boys).They were recruited at well baby clinics and amongst acquaintances.

They were born at term (gestational age at birth 40.1 weeks (median value), range 37.6 to 42 weeks)

without pre or perinatal complications with a median birth weight of 3588 grams (range 2730 to

4470 grams). The infants were followed longitudinally and assessments took place at ages 3, 4, 5,

6, 8, 10, 12, 15 and 18 months. Of 19 of these infants one assessment was included in the reliability

study as described above. Attrition rate was very low, only at 5 and 8 months one of the 30 infants

had no assessment, due to minor illness of the child or scheduling problems with the parents. At 6

months arm and hand motility during reaching and grasping could not be assessed for two of the

30 infants due to fatigue of the child. All parents signed informed consent and the research project

was approved by the Ethics Committee of the University Medical Center Groningen.

Procedures

Each assessment consisted of a video recording of in total 15 minutes of spontaneous motor

behaviour in supine, prone, sitting, standing and walking, depending on the child’s age and

functional capacities14. The order of the conditions was not !xed, but was adapted to the child’s

interest. Motor functions were only assessed if the infant was able to perform it independently,

e.g. showed abdominal progression, sat independently, showed successful reaching or showed

successful grasping. Table I shows the four items of the Infant Motor Pro!le and the de!nitions

used for determining whether motor behaviour can be classi!ed as adaptive motor behaviour for

the four speci!c motor functions (abdominal progression, sitting motility, arm movements during

reaching and hand motility during grasping and manipulation)14. Scoring is dichotomous: either the

motor behaviour is scored as ‘no selection’ or as ‘adaptive selection’ (Table I).

Abdominal progression was elicited with toys. Besides crawling, wriggling and pivoting

movements were also considered as forms of abdominal progression. Wriggling movements

are small, quick, twisting and turning movements of the body without speci!c use of arms and/

or legs resulting in spatial displacement, while the abdomen remains in contact with the support

surface17,18. Pivoting movements result in spatial displacement around the centre of the body, i.e.

around a vertical axis through the umbilicus. Older infants who showed crawling were encouraged

56

Chapter 4

to follow a ball or a toy car.

Sitting motility was only assessed if infants were able to sit independently. To observe sitting

motility, reaching movements and rotation movements of the trunk were elicited by presenting

toys at various distances, in various directions and at various heights, e.g. close to the trunk of the

infant, at arm length and a bit further at di�erent heights in front and to the sides of the sitting

infant. Sitting behaviour of children who were able to sit up independently was observed during

spontaneous motor activity while they were moving into various body positions.

To assess the infant’s ability to reach, grasp and manipulate objects, small toys were presented

to the infant seated on the parent’s lap. If the child was able to grasp objects in the midline at arm

Table 1: De�nitions of non-adaptive and adaptive motor behaviour for the four motor functions

Abdominal progression: ability to make an adaptive selection

No selection: The child does not select speci!c crawling strategies out of its motor repertoire. Thechild explores various crawling strategies with variation in movement patterns andmovement ranges. These variations in movements occur in a random way, whichresults in relatively ‘ine"cient’ motor behaviour. Wriggling and pivoting are alwaysassigned ‘no selection’, as these can be considered exploratory and variable precursormovements of crawling.

Adaptive selection: The child selects speci!c, e"cient crawling strategies out of its motor repertoire. Thechild is able to crawl e"ciently with appropriately coordinated movements of armsand legs, allowing for e.g. smooth crawling trajectories while turning a corner.

Sitting motility: ability to make an adaptive selection

No selection: The child does not select speci!c motor strategies out of its motor repertoire. Thechild explores various postural adjustment strategies, with variation in combination ofrecruited muscles, movement direction and movement velocity. Sitting motility is note"cient and there are multiple minor and major swaying movements of the upperbody in all directions with or without balance disturbance.

Adaptive selection: The child selects speci!c, e"cient strategies of postural adjustments out of its motorrepertoire. The child is able to adjust sitting motility e"ciently and does not loosebalance while reaching for objects at various distances and heights.

Reaching movements: ability to make an adaptive selection

No selection: The child does not select speci!c reaching strategies out of its motor repertoire. Thechild explores various reaching movements with variable movement trajectories,movement ranges and movement velocities. Movements are not adapted to distance,position and other characteristics of presented objects.

Adaptive selection: The child selects speci!c, e"cient reaching strategies out of its motor repertoire.Reaching movements are goal-directed with more or less straight and e"cientmovement trajectories.

Hand motility during grasping: ability to make an adaptive selection

No selection: The child does not select speci!c motor strategies out its motor repertoire. The childexplores various grasping and manipulation strategies. The variations in movementsoccur in a random way. Movements are not adapted to the size and shape of thepresented objects.

Adaptive selection: The child selects speci!c, e"cient grasping and manipulation strategies out of itsmotor repertoire. Grasping is adapted to the size and shape of the presented objects.

57

4


length distance, toys were presented in di�erent positions to elicit di�erent reaching and grasping

movements. Type of grasping and variation in grasping were assessed by presenting objects of

various sizes and forms. A small cupboard with drawers with small handles was presented to the

older infants to observe �ne manipulation skills. Toys used were not standardised, but commercially

available small (approximately the size of the infant’s hand) puppets, animals, toy cars and balls (See

�gure 1).

Figure 1: Examples of toys used in the Infant Motor Pro�le assessment.

Statistical analyses

To determine intra- and interobserver reliability, Cohen’s kappa’s were calculated. Criteria of Landis

and Koch19 were used which state that κ > 0.80 is considered very good, 0.61< κ < 0.80 is good, 0.40

< κ < 0.60 is moderate and κ < 0.40 is poor. To explore the ages of transition, i.e., the age at which

motor behaviour changed from no selection to adaptive selection, the non-parametric Sign or

Friedman tests for related samples were used. Throughout the analyses, di�erences with a p-value <

0.05 were considered to be statistically signi�cant (two-tailed testing).

RESULTS

Reliability

For the item on adaptive selection during abdominal progression, intra- and interobserver

agreement were very good (See Table II for Kappa and 95% con�dence intervals). This was also the

case for the item on sitting motility. The item on arm motility during reaching showed good intra-

and interobserver agreement. For the item on hand motility, intra-observer reliability was moderate,

while interobserver agreement was very good.

58

Figure 2: Variability of abdominal progression: presence of adaptive selection.Hatched parts of bars represent percentage of infants showing no selection of crawling patterns and black partsrepresent percentage showing adaptive selection of crawling patterns. White parts represent the percentagesof infants showing no abdominal progression. ** Signi!cant increase in adaptive selection between 8 and 15months (Friedman: p<0.0005). The three developmental steps from 8 to 10, 10 to 12 and 12 to 15 months werealso statistically signi!cant (Sign test: p = 0.03, p = 0.002 and p = 0.001, respectively).

Chapter 4

Emergence of adaptive motor behaviour

In the development of abdominal progression, the transition from variable, non-adaptive behaviour

to adaptive behaviour was observed between 8 and 15 months (Friedman, p < 0.0005). This means

that at the age of 15 months virtually all children selected adaptive crawling strategies (Figure 2).

For sitting motility (Figure 3) transition from exploratory, variable behaviour without selection to

adaptive selection started from 6 months onwards. At 8 months 33% of infants showed adaptive

sitting motility, which increased to almost 90% of infants at 10 months (Friedman test 6 to 10

months: p<0.0005). Transition to adaptive selection of arm movements during reaching occurred

in a majority of infants between 6 and 8 months (Sign test: p < 0.0005). However, in the period from

Table II: Intra- and interobserver agreement

Intra-observer agreement Interobserver agreement

Item Kappa 95% CI Kappa 95% CI

Abdominal progression 0.84 0.69-0.99 0.84 0.69-0.99

Sitting motility 1.0 1.0-1.0 0.90 0.77-1.0

Reaching movements 0.68 0.42-0.94 0.61 0.32-0.89

Hand motility during grasping 0.56 0.23-0.88 0.87 0.71-1.0

CI: con!dence interval

59

Figure 4: Variability of arm movements during reaching: presence of adaptive selection.Hatched parts of bars represent percentage of infants showing no selection of arm movements and blackparts represent percentage of infants showing adaptive selection of arm movements. White parts representthe percentages of infants showing no reaching movements. Asterisks indicate signi�cant increase in adaptiveselection (Sign test): * p = 0.02 and ** p < 0.0005.

4

Figure 3: Variability of sitting motility: presence of adaptive selection.Hatched parts of bars represent percentage of infants showing no selection of sitting motility and black partsrepresent percentage showing adaptive selection of sitting motility. White parts represent the percentagesof infants that are not able to sit independently. * Signi�cant increase in adaptive selection between 6 and10 months (Friedman: p<0.0005). The two steps from 6 to 8 and from 8 to 10 months were also statisticallysigni�cant (Sign test 6 to 8 and 8 to 10 months: p = 0.02).


60

8 to 12 months about 10% to 25% of infants continued to show variable reaching movements. Not

until 15 months, all infants showed adaptive reaching movements (Sign test: p = 0.02; Figure 4). For

hand motility during grasping transition from variable, non-adaptive to adaptive motor behaviour

was observed between 15 and 18 months (Sign test: p < 0.0005; Figure 5).

DISCUSSION

This study illustrated that transition to selection of adaptive motor behaviour can be reliably

observed and that this transition emerges around the age of 6 months and peaks between 8 and 15

months. The transition develops gradually and occurs at speci!c ages for di"erent motor functions.

Findings

Intra and interobserver reliability of all items were good to very good, except intra observer reliability

for the item on hand motility during grasping, which was moderate. The latter may have been an

expression of a learning e"ect.

For abdominal progression, clinically observable transition to selection of adaptive crawling

strategies started at 8 months of age. At 15 months, almost all children showed adaptive crawling

patterns on hands and knees. Adolph et al.20 also found decreasing movement variability with

increasing weeks of crawling experience. More experience with prone position and practice of

crawling accelerates selection of adaptive crawling patterns20-22. Development of crawling continues

Figure 5: Variability of hand motility during grasping: presence of adaptive selection.Hatched parts of bars represent percentage of infants showing no selection of hand motility and black partsrepresent percentage of infants showing adaptive selection of hand motility. White parts represent thepercentages of infants showing no successful grasping movements. ** Signi!cant increase in adaptive selection(Sign test, p < 0.0005).

Chapter 4

61

4


beyond infancy23.

With respect to sitting motility, we know from literature that selection of the complete EMG

pattern, in which all dorsal neck- and trunk muscles are activated synchronously, emerges between

4 and 6 months11,12. The present study showed that transition to adaptive sitting motility is clinically

observable between 6 and 10 months of age. This indicates that selection of a preferred postural

adjustment pattern measured by EMG precedes the clinical observable transition. Development

of postural control is not !nished during infancy; it has a protracted course that lasts at least until

adolescence12.

Our study showed that clinically observable transition from variable, exploratory reaching

movements to straighter, adaptive reaching movements emerged between six and eight months,

but not until 15 months all typically developing children showed adaptive reaching movements.

Kinematic data from literature showed rapid straightening of movement trajectories around the age

of four to six months13, again preceding the clinical observed transition we found. Stable patterns of

temporal coordination start to develop from 12 to 15 months onwards until the age of three years23,

illustrating the long course of development of secondary variability during which !ne-tuning of the

reaching movements to the speci!c task requirements occurs.

For hand motility during grasping, transition to secondary variability occurred for more than

70 percent of children between 15 and 18 months. Corticospinal connections are crucial for the

development of skilled hand and !nger movements. Direct cortico-motoneuronal projections

already develop in the !rst months of postnatal life and allow for voluntary independent !nger

movements25,26. Thereafter, corticospinal projections become !ne-tuned, a process that includes the

disappearance of the majority of ipsilateral connections which is !nished by the age of 24 months27.

During the process of activity-dependent remodeling of the corticospinal connections, adaptive

hand motility emerges from 15 months onwards. But again, !ne-tuning of grasping movements

continues at least until the age of eight to ten years26.

Strengths and limitations of the study

A strength of this study is its longitudinal prospective character. For closer monitoring of

developmental changes, it would have been better to have more frequent assessments, for example

each month. However, time intervals between assessments were especially short during the !rst

year of life when motor development has a rapid course. Another strength was the very low attrition

rate. A limitation of the reliability study is that only two assessors participated. They were not blinded

with respect to term or preterm status of the infant. However, they were unaware of any details of

the child’s clinical history or results of neonatal ultrasounds of the preterm infants. A weakness of the

longitudinal part of the study is the relatively small sample size, especially because variability within

and between typically developing infants can be quite large. Nevertheless, we were able to detect

the ages of transition. In the current study, we compared the clinically observed ages of transition

with data in the literature available on changes measured by neurophysiologic methods. It would

62

Chapter 4

have been interesting and possibly more exact if the same children had had the neurophysiological

assessments and the clinical observations. This could be done in further research.

CONCLUDING REMARKS

During the !rst half year of life, infant motor behaviour is characterised by variation and exploration.

Transition to clinically observable adaptive motor behaviour develops gradually from six months

onwards at function-speci!c ages. By comparing our results to literature, we found that changes

measured by neurophysiologic methods precede the clinically observed transitions. Changes

in motor behaviour recorded with exact registration techniques represent the early phases of

selection, while clinical observation shows when a certain pattern is used during the majority of

movements. It would be interesting to perform further research on ages of transition in infants

with a high risk for developmental motor disorders such as cerebral palsy (CP) or developmental

coordination disorder (DCD). These children can have di"culties with processing a#erent, sensory

information and experience problems in !ne-tuning and adapting motor behaviour5,28-29. This could

possibly be re$ected in delayed or impeded transition to secondary variability. If so, age of transition

could be a useful clinical parameter of neuromotor condition.

ACKNOWLEDGEMENTSWe kindly acknowledge Arend Bos, MD, PhD for critical comments on a previous version of the manuscript. Wethank Nicole Arink and Dineke Dijkhuizen for performing part of the assessments. The study was supported bya Junior Scienti!c Masterclass grant of the post-graduate school Behavioral and Cognitive Neurosciences (BCN),University of Groningen.

63

4


REFERENCES1. Hadders-Algra M. The Neuronal Group Selection Theory: a framework to explain variation in normal motor

development. Dev Med Child Neurol 2000;42:566-572.

2. Thelen E. Motor development. A new synthesis. American Psychologist 1995;50:79–95.






8. Wol� PH. The serial organization of sucking in the young infant. Pediatrics 1968;42:943-956.

9. Bu’Lock F, Woolridge MW, Baum JD. Development of co-ordination of sucking, swallowing and breathing:ultrasound study of term and preterm infants. Dev Med Child Neurol 1990;32:669-678.

10. Hedberg A, Carlberg EB, Forssberg H, Hadders-Algra M. Development of postural adjustments in sittingposition during the �rst half year of life. Dev Med Child Neurol 2005;47:312-320.

11. De Graaf-Peters VB, Bakker H, van Eykern LA, Otten B, Hadders-Algra M. Postural adjustments and reachingin 4- and 6-month-old infants: an EMG and kinematical study. Exp Brain Res 2007;181:647-56.

12. Hadders-Algra M. Development of postural control. In: M. Hadders-Algra and E. Brogren Carlberg, editors.Postural control: a key issue in developmental disorders. Clin Dev Med No. 179. London: Mac Keith Press,2008, pp 22-73.

13. Konczak J, Borutta M, Topka H, Dichgans J. The development of goal-directed reaching in infants: handtrajectory formation and joint torque control. Exp Brain Res 1995;106:156-68.

14. Heineman KR, Bos AF, Hadders-Algra M. The Infant Motor Pro�le: a standardized and qualitative method toassess motor behaviour in infancy. Dev Med Child Neurol 2008;50:275-82.




18. Piper MC, Darrah J. Motor assessment of the developing infant. Philadelphia: WB Saunders Compan, 1994.

19. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159-174.

20. Adolph KE, Vereijken B, Denny MA. Learning to crawl. Child Dev 1998;69:1299-1312.

21. Davis BE, Moon RY, Sachs HC, Ottolini MC. E�ects of sleep position on infant motor development. Pediatrics1998;102:1135-1140.

22. Lagerspetz K, Nygard M, Strandvik C. The e�ects of training in crawling on the motor and mentaldevelopment of infants. Scand J Psychol 1971;12:192-197.

23. Touwen BC, Hempel MS, Westra LC. The development of crawling between 18 months and four years. DevMed Child Neurol 1992;34:410-416.

24. Konczak J, Dichgans J. The development toward stereotypic arm kinematics during reaching in the �rst 3years of life. Exp Brain Res 1997;117:346-354.

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25. Armand J, Olivier E, Edgley SA, Lemon RN. Postnatal development of corticospinal projections from motorcortex to the cervical enlargement in the macaque monkey. J Neurosci 1997;1:251-266.

26. Forssberg H. Neural control of human motor development. Curr Opin Neurobiol 1999;9:676-682.

27. Eyre JA. Development and plasticity of the corticospinal system in man. Neural Plast 2003;10:93-106.

28. Wilson PH, McKenzie BE. Information processing de�cits associated with developmental coordinationdisorder: a meta-analysis of research �ndings. J Child Psychol Psychiatry 1998;39:829-840.

29. Cooper J, Majnemer A, Rosenblatt B, Birnbaum R. The determination of sensory de�cits in children withhemiplegic cerebral palsy. J Child Neurol 1995;10:300-309.

65

5CHAPTER

Construct validity of the Infant Motor Pro�le:Relation with prenatal, perinatal and neonatal risk factors

Kirsten Heineman1,2, Sacha la Bastide-van Gemert3, Vaclav Fidler3,Karin Middelburg1, Arend Bos4, Mijna Hadders-Algra1


3Department of Epidemiology4Department of Paediatrics, Division of Neonatology


Developmental Medicine and Child Neurology 2010; Epub ahead of print

66

Chapter 5

ABSTRACT

Aim: The Infant Motor Pro�le (IMP) is a qualitative assessment of motor behaviour of infants aged

3 to 18 months. The aim of this study was to investigate construct validity of the IMP, through

the relation of IMP scores with pre-, peri- and neonatal variables, including the presence of brain

pathology indicated by neonatal ultrasound imaging of the brain.

Methods: A longitudinal prospective study was performed in a group of 30 term born (12 females

and 18 males; median gestational age 40.1wks, range 37.6-42wks) and 59 preterm infants (25

females and 34 males; median gestational age 29.7wks, range 25-34.7wks). IMP assessments were

performed at (corrected) ages of 4, 6, 10, 12 and 18 months. Socio-economic and perinatal data

were collected, which, in the case of preterm infants, included information on periventricular

leukomalacia and intraventricular haemorrhage based on neonatal cranial ultrasounds. Data were

analysed by �tting mixed-e!ects models.

Results: Gestational age, socio-economic status and 5-minute Apgar score were signi�cant

determinants of IMP scores in the total group of infants (p-values resp. <0.001, 0.002 and 0.042

respectively). In the subgroup of preterms, IMP scores were signi�cantly a!ected by brain lesions on

neonatal ultrasound (p<0.001) and socio-economic status (p=0.001).

Interpretation: The �ndings support the construct validity of the Infant Motor Pro�le: IMP scores

are clearly associated with relevant determinants of neuromotor function.

67

5

Construct validity of the Infant Motor Pro�le

INTRODUCTION

The Infant Motor Pro�le (IMP)1 is a recently developed qualitative assessment of motor behaviour

of infants aged 3 to 18 months. It may be used for early detection and developmental evaluation of

infants with a high risk for developmental motor disorders such as cerebral palsy or developmental

coordination disorder. Infants born very preterm are especially at risk for these developmental

motor disorders2-5. Owing to improved prenatal and neonatal care, the survival of very preterm

infants has increased in the last decennia2,3. Follow-up of preterm infants aims at detection of those

infants that could bene�t from early intervention at young age, when the brain is highly plastic6,7

The IMP is based on ideas of the Neuronal Group Selection Theory (NGST) of motor

development8-10. According to NGST, typical motor development starts with the phase of primary

variability with exploratory, variable motor behaviour. Children with pre- or perinatally acquired

brain damage show more stereotyped motor behaviour with considerably less variation. During

development, infants learn to select adaptive motor strategies out of their motor repertoire and

to adapt motor behaviour to the environment. This phase of adaptive selection is called secondary

variability. Children with developmental motor disorders often have problems in selecting

adaptive motor strategies9,10. Two domains of the IMP are based on the NGST-principles of motor

development; they deal with variation of motor behaviour (size of repertoire) and the ability to

select motor strategies (variability). Three additional domains assess movement �uency, movement

symmetry and motor performance.

The IMP assessment consists of video-recording of approximately 15 minutes of spontaneous

motor behaviour in supine, prone, sitting, standing, and walking condition, depending on age and

functional capacities of the infant. In addition, reaching, grasping and manipulation of objects are

tested in the supine and sitting positions. The 80 items of the IMP are scored based on the video

recording1. The 80 items constitute the subscores on the �ve domains: size of repertoire (variation),

ability to select (variability), movement �uency, movement symmetry and motor performance. The

mean of the �ve subscores is the total IMP score1 (Appendix I).

In our pilot study on the IMP1, we described the theoretical background of the method, its

domains and items, and details of scoring procedures. In addition, we have published �rst data on

the reliability and concurrent validity of the IMP with the Alberta Infant Motor Scale (AIMS)11 and

Touwen neurological examination12. Intra- and interobserver reliability for total IMP score were good

(Spearman’s rho 0.9 for both; 95% con�dence intervals 0.8–0.9 and 0.8-1.0 respectively). Concurrent

validity of the IMP with the AIMS was very high for the performance subscale and moderate for the

total IMP score. Concurrent validity of the IMP with the Touwen examination was very good, with a

clear inverse relationship between IMP scores and the degree of neurological dysfunction1.

The present study focuses on construct validity. Construct validity is the extent to which items

of the instrument re�ect the theoretical construct of interest, in this case neuromotor function13.

Parameters of construct validity with respect to neuromotor function are the relation of test scores

68

Chapter 5

with prenatal, perinatal and neonatal adversities and correlation with results from brain imaging. The

aim of the present study was to investigate construct validity of the IMP, through the relation of IMP

scores with prenatal, perinatal and neonatal variables, including the presence of brain pathology

indicated by neonatal ultrasound imaging of the brain. To this end, we performed a longitudinal

prospective study in a group of term and preterm infants from the age of 4 to 18 months.

METHODS

Participants

We included a longitudinal study group of 30 term and 59 preterm infants. The term infants

(12 females and 18 males) were recruited from amongst colleagues and acquaintances of the

researchers. The preterm infants had been admitted to the neonatal intensive care unit of the Beatrix

Children’s Hospital of the University Medical Center in Groningen between December 2003 and

January 2005. Inclusion criteria were: gestational age below 35 weeks, singleton or twin, parents

with appropriate understanding of the Dutch language, and travel distance between the child’s

home and the hospital of < 1 hour. Infants with severe congenital anomalies were excluded from

the study. During the time interval mentioned above, 148 infants were eligible for inclusion. Owing

to the limited capacity of our department, only a limited number of infants could be included in the

intensive follow-up scheme each month. Therefore, not all of the eligible infants were approached

for inclusion. By approaching parents at random, 59 infants were eventually included. The project

was approved by the local ethics committee. All parents of the infants gave informed consent.

Procedures

Longitudinal assessments were performed at (corrected) ages of 4, 6, 10, 12 and 18 months.

Assessments consisted of a video-recording of approximately 15 minutes of spontaneous motor

behaviour. Motor behaviour was recorded while supine, prone, sitting, standing, and walking,

depending on the age and functional capacity of the infant. Reaching, grasping and manipulation

of objects were evaluated in supine and in (supported) sitting positions. The IMP assessments were

carried out by one of the examiners (KRH or KJM). The examiners knew whether an infant was born

at term or preterm, but were not aware of any of the perinatal and neonatal details. The 80 items of

the IMP were scored on the basis of the video recording. In this paper, only the total IMP scores are

addressed.

Socio-economic, perinatal and neonatal data were collected for all infants on standardized

forms by means of an interview with the parents and by consultating neonatal intensive care unit

discharge certi!cates. Socio-economic status (SES) was de!ned by the sum score of four variables

describing educational and professional level of father and mother, all expressed on a scale from 0

(lowest) through 2 (highest). Neonatal ultrasounds of the brain of the preterm infants were assessed

with respect to periventricular leukomalacia (PVL) and intraventricular haemorrhage (IVH). PVL was

69

5


classi�ed according to De Vries et al.14: grade I; transient periventricular echodensities persisting

for more than 7 days; grade II; transient periventricular densities, evolving into small localised

frontoparietal cysts; grade III; periventricular densities, evolving into extensive periventricular cystic

lesions; and grade IV; densities extending into the deep white matter evolving into extensive cystic

lesions. IVH was classi�ed according to Volpe15:grade I; haemorrhage con�ned to the subependymal

germinal matrix; grade II; haemorrhage into the lateral ventricles without ventricular dilatation;

grade III; IVH with ventricular dilatation; and grade IV; IVH with parenchymal involvement (venous

infarction). PVL grade II or worse and/or IVH grade III or worse were classi�ed as serious brain lesions.

‘Small for gestational age’ was de�ned as birthweight compared to gestational age below the 10th

percentile16.


For comparison of background characteristics of term and preterm groups we used the Mann-

Whitney U test or the Pearson chi-squared test. Analyses to test the association between risk variables

and IMP scores at di!erent ages were performed with the Mann-Whitney U test for categorical

variables and Spearman’s rho correlation for continuous variables. Variables that correlated with

IMP scores with a Spearman’s rho correlation of 0.20 or more at more than one of the �ve assessed

ages, or a Mann-Whitney U test with p-value of 0.05 at one or more of the �ve assessed ages

were entered in a mixed-e!ects analysis17. This analysis makes it possible to describe the change of

the IMP scores over time and in relation to perinatal and neonatal variables. It takes into account

the dependence between observations from the same infant, and it can also take into account

dependence between twins. Children for whom outcomes at some time-points were missing were

still included in the analysis by entering non-missing data at these time-points; the analysis assumes

that missing values do not a!ect the outcome (‘missing at random’ assumption18). The results of

neonatal sonography of the brain were investigated in a separate analysis, as these measurements

were available only in the preterm group. In selecting the best-�tting models, we used 0.05 as the

nominal level of signi�cance.

RESULTS

Table I shows socio-economic and neonatal characteristics of the term and preterm infants. Thirty-

�ve of the preterm infants were singletons and 24 were twins. Nine pairs of twins participated in the

study; the remaining six had lost their twin sibling. The attrition rate was low: in the preterm group

two children missed assessment at two of the �ve time-points and 11 children at one time-point.

Reasons for missed assessments were scheduling problems with the parents or minor illness of the

infant. In the term group no assessment was missed. The preterm infants generally had a higher

chance to be born small for gestational age, to be delivered by Caesarean section, more signs of fetal

distress at birth, and a lower 5-minute Apgar score than the infants born at term. Preterm and term

infants did not signi�cantly di!er in SES and maternal age.

70

Figure 1: Individual Infant Motor Pro!le curves in the term (left) and preterm (right) groups.IMP scores in the preterm group are, in general, lower and show a larger within-participant variability than in theterm group (p<0.001).

Chapter 5

Associations in the total group

Throughout infancy, preterm infants had signi�cantly lower IMP scores than term infants (Mann-

Whitney U; p<0.001). No signi�cant di�erence in IMP scores was found between males and females.

Figure 1 depicts the individual IMP curves in the term and preterm groups. Univariate analyses

showed a signi�cant relation between IMP and SES, gestational age, signs of fetal distress, Ceasarian

Table I: Socio-economic and neonatal characteristics of term and preterm groups

Term Preterm p-value

Number of children 30 59

Males/Females, n 18/12 34/15 0.831

Maternal age (years), mean (SD) 32.8 (4.1) 31.8 (5.2) 0.514

SESa, median (range) 5 (0-8) 4 (0-8) 0.265

Twins, n (%) 0 24 (41) <0.001

Gestational age wks, median (range) 40.1 (37.6-42) 29.7 (25-34.7) <0.001

Birthweight g, median (range) 3588 (2730-4470) 1285 (630-2180) <0.001

Small for gestational ageb, n (%) 2 (6.7) 20 (33.7) 0.005

Caesarian section, n (%) 3 (10) 33 (55.9) <0.001

Signs of fetal distressc, n (%) 5 (16.7) 30 (50.8) 0.002

Apgar score at 5 min,median (range)

10 (9-10) 9 (4-10) <0.001

a SES = socio-economic status, sum score of four variables describing educational and professional level of fatherand mother, all expressed on a scale from 0 (lowest) through 2 (highest).b Small for gestational age is de�ned as birthweight compared with gestational age below 10th centile16.c Presence of at least one of the following factors: meconium staining, cardiotocography abnormalities, acidaemiaduring delivery (arterial umbilical pH below 7.05).

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71

5


section, and 5-minute Apgar score at nearly all �ve time-points. These variables were entered into

the mixed-e�ects model. The data were well described by a model (see Table II) which included,

as �xed e�ects, a quadratic function of age (re�ecting a substantial increase in IMP scores with

increasing age), gestational age, SES and 5-minute Apgar score. A nearly equally well-�tting model

was obtained by replacing gestational age with birthweight or with preterm status. The best-�tting

model also included a random intercept, a random linear age e�ect, and a within-participant

variance that was larger in the preterm group than in the term group (p<0.001). We also �tted a

mixed model including an additional random factor for family to account for dependence of twins.

The results obtained with this multilevel model were rather similar to those obtained without taking

twin status into account. We have decided to present the simpler model that does not take twin

status into account.

Associations in the subgroup of preterm infants

Neonatal ultrasound was available for 57 of the 59 preterm infants. Serious brain pathology was

observed in six infants: one infant had cystic PVL, four infants had IVH grade IV, and one infant had

Table II: Regression analysis of Infant Motor Pro�le scores (term and preterm infants, n = 76a)

Regression coe!cient Standard error p-value 95%-con"dence interval

Intercept 47.6 2.22

Age (mo) 2.16 0.165 <0.001

Age2 (x10-2) -5.70 0.734 <0.001

Gestational age (wks) 0.478 0.068 <0.001 0.34 – 0.61

SESb 0.427 0.131 0.002 0.16 – 0.68

Apgar 5 min 0.535 0.258 0.042 0.02 – 1.05

a For 12 term infants 5-minute Apgar score was missing and for one infant no complete data were available onSES.b SES = socio-economic status, sum score of four variables describing educational and professional level of fatherand mother, all expressed on a scale from 0 (lowest) through 2 (highest).

Table III: Regression analysis of Infant Motor Pro�le scores in the preterm group (n = 56a)

Regression coe!cient Standard error p-value 95%-con"dence interval

Intercept 64.0 1.36

Age (mo) 2.52 0.223 <0.001

Age2 (x10-2) -7.22 0.981 <0.001

Brain lesions -6.33 1.28 <0.001 -8.9 – -3.8

SESb 0.588 0.173 0.001 0.24 – 0.93

a Two preterm infants did not undergo neonatal ultrasonography, and for one infant no complete data wereavailable on SES.b SES = socio-economic status, sum score of four variables describing educational and professional level of fatherand mother, all expressed on a scale from 0 (lowest) through 2 (highest).

72

Chapter 5

middle cerebral artery infarction on the right side. Infants with serious brain lesions had signi�cantly

lower IMP scores at ages 4, 6, 10, and 18 months than infants without serious abnormalities on

neonatal ultrasound (Mann-Whitney U test: p=0.002, 0.003, 0.01 and 0.004 respectively). The mixed-

e�ects analysis revealed that lower IMP scores in the preterm group were associated with serious

brain lesions on ultrasound and with SES (Table III).

DISCUSSION

Our study revealed clear associations between prenatal, perinatal and neonatal adversities and

IMP scores at ages 4 to 18 months in term and preterm infants. In preterm infants serious brain

pathology on neonatal ultrasound was strongly related to lower IMP scores. These �ndings support

the construct validity of the IMP.

The strengths of the study are its longitudinal character and the low attrition rate. The study

group was explicitly heterogeneous with respect to neuromotor function, which is valuable in

assessing validity of a new instrument. The weaknesses of the study are the relatively small sample

size of the term group and the missing Apgar scores for 12 term children. Therefore, we recommend

that the study be replicated with a larger sample of term infants. A further limitation of the study

is that the assessors were not blind with respect to term or preterm status of the infant. However,

the assessors were unaware of any details of the child’s clinical history or results of neonatal

ultrasonography.

To investigate whether the group of preterm infants included in this study was representative

for a Dutch neonatal intensive care unit population in a tertiary referral centre, we compared it with

established reference groups of preterm infants19,20. We found that gestational age, birthweight,

frequency of Apgar score at 5 minutes below 7 (15%) and the need for ventilatory support (68%)

were similar. Our sample showed a relatively high percentage of infants small for gestational age

and of Caesarean deliveries.19,20. The latter could be a result of the increased tendency over the years

to deliver very preterm infants by Caesarean section21.

The IMP scores were most strongly a�ected by preterm birth. Preterm birth is a major risk factor

for major and minor neurodevelopmental disabilities3-5. Both types of disability may largely interfere

with daily activities and academic achievements. The clear in!uence of this important risk factor on

IMP scores contributes to construct validity of the IMP. In the total group of infants, a low 5-minute

Apgar score was associated with low IMP scores. In fact, the Apgar score was never intended to

be used to predict neurodevelopmental outcome, but mainly the risk of neonatal death22. The

Apgar score re!ects the condition of the infant shortly after delivery, and could be interpreted as

an indicator of the infant’s ability to adapt to the novel situation of extrauterine life. In the preterm

group, the presence of a serious brain lesion had a greater e�ect than the Apgar score on later IMP

performance.

Preterm infants showed more individual variations in IMP scores over time than term infants. The

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5


more variable developmental trajectories in preterm infants presumably re!ect that developmental

progress in infants with atypical brain function is less stable than in infants with typical brain

function23. In other words, atypical brain function is expressed di"erently at di"erent ages. The

inconsistent expression of atypical motor behaviour emphasizes the need of repeated assessments

in high-risk infants.

Serious brain lesions on ultrasound, such as cystic PVL or IVH, were associated with lower

IMP scores throughout infancy. According to NGST, brain lesions lead to a reduction of available

neuronal networks, which results, in particular, in reduced variation of motor behaviour and

an impaired ability to select adaptive motor behaviour. The presence of serious brain lesions on

neonatal ultrasound is a strong predictor of later neurodevelopmental disability24.

We found a clear increase in IMP scores with increasing age, which implies that the IMP is able to

detect and re!ect age-related changes in motor development (i.e., higher levels of performance and

better abilities to select adaptive motor behavior). This contributes considerably to the construct

validity of an instrument for assessment of motor development25.

In our study, higher SES was associated with higher IMP scores in the group of infants as a

whole and in the preterm group separately. No relation between maternal education and motor

development in infancy was found in a study on healthy, term born infants26, but lower SES was

clearly associated with the presence of the complex form of minor neurological dysfunction at

school age27. Highly educated parents probably provide both favourable genetic factors and a

healthy and stimulating environment for the child. The latter is especially important for children at

high biological risk of developmental disorders, such as preterm infants28.

In conclusion, this study supports the construct validity of the IMP. IMP scores were clearly

related to relevant risk factors for developmental motor problems. These #ndings support the use

of the IMP in clinical follow-up of high risk infants.

ACKNOWLEDGEMENTSWe thank Nicole Arink, Hylco Bouwstra, Dineke Dijkhuizen and Anne Hoekstra for performing part of theassessments. The study was supported by a Junior Scienti#c Masterclass grant of the post-graduate schoolBehavioral and Cognitive Neurosciences (BCN), University of Groningen.

74

Chapter 5

REFERENCES1. Heineman KR, Bos AF, Hadders-Algra M. The Infant Motor Pro�le: a standardized and qualitative method to

assess motor behaviour in infancy. Dev Med Child Neurol 2008;50:275-82.

2. Wilson-Costello D, Friedman H, Minich N, Fanaro� AA, Hack M.. Improved survival rates with increasedneurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 2005;115:997-1003.


4. Marlow N, Wolke D, Bracewell MA, Samara M; EPICure Study Group. Neurologic and developmentaldisability at six years of age after extremely preterm birth. N Engl J Med. 2005;352:9-19.

5. Davis NM, Ford GW, Anderson PJ, Doyle LW; Victorian Infant Collaborative Study Group. Developmentalcoordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterminfants. Dev Med Child Neurol 2007;49:325-30








13. Heineman KR, Hadders-Algra M. Evaluation of neuromotor function in infancy - A systematic review ofavailable methods. J Dev Behav Pediatr 2008;29:315-23.



16. Kloosterman GJ. On intrauterine growth: the signi�cance of prenatal care. Int J Gynaecol Obstet 1970;8:895-912.

17. Pinheiro JS, Bates DM. Mixed-E�ects Models in S and S-plus. New York: Springer, 2000.

18. Fitzmaurice GM, Laird NM, Ware JH. Applied longitudinal analysis. Hoboken, New Jersey: John Wiley &Sons, Inc., 2004.

19. Stoelhorst GM, Rijken M, Martens SE, Brand R, den Ouden AL, Wit JM, Veen S; Leiden Follow-Up Project onPrematurity. Changes in neonatology: comparison of two cohorts of very preterm infants (gestational age<32 weeks): the Project On Preterm and Small for Gestational Age Infants 1983 and the Leiden Follow-UpProject on Prematurity 1996-1997. Pediatrics 2005;115:396-405.

20. de Kleine MJ, den Ouden AL, Kollée LA, van Baar A, Nijhuis-van der Sanden MW, Ilsen A, Brand R, Verloove-Vanhorick SP. Outcome of perinatal care for very preterm infants at 5 years of age: a comparison between1983 and 1993. Paediatr Perinat Epidemiol 2007;21:26-33.

21. Haque KN, Hayes AM, Ahmed Z, Wilde R, Fong CY. Caesarean or vaginal delivery for preterm very-low-birth weight (< or =1,250 g) infant: experience from a district general hospital in UK. Arch Gynecol Obstet.

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2008;277:207-12.

22. Casey BM, McIntire DD, Leveno KJ. The continuing value of the Apgar score for the assessment of newborninfants. N Engl J Med 2001;15;344:467-471.

23. Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological dysfunctionin infancy using the Touwen Infant Neurological Examination: strengths and limitations. Dev Med ChildNeurol, 2009, e-pub ahead of print.

24. Weisglas-Kuperus N, Baerts W, Fetter WP, Sauer PJ. Neonatal cerebral ultrasound, neonatal neurology andperinatal conditions as predictors of neurodevelopmental outcome in very low birthweight infants. EarlyHum Dev 1992;31:131-148.

25. Campbell SK, Kolobe TH, Osten ET, Lenke M, Girolami GL. Construct validity of the test of infant motorperformance. Phys Ther. 1995;75:585-96.

26. Ravenscroft EF, Harris SR. Is maternal education related to infant motor development? Pediatr Phys Ther2007;19:56-61.

27. Hadders-Algra M, Huisjes HJ, Touwen BC. Perinatal correlates of major and minor neurological dysfunctionat school age: a multivariate analysis. Dev Med Child Neurol 1988;30:472-481.

28. Weisglas-Kuperus N, Baerts W, Smrkovsky M, Sauer PJ. E�ects of biological and social factors on thecognitive development of very low birth weight children. Pediatrics 1993;92:658-665.

77

6CHAPTER

Concurrent and predictive validity of theInfant Motor Pro�le

Kirsten Heineman1,2, Karin Middelburg1, Arend Bos3,Lieke Eidhof1, Mijna Hadders-Algra1


3Department of Paediatrics, Division of NeonatologyUniversity Medical Center Groningen

Submitted

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Chapter 6

ABSTRACT

Background: The Infant Motor Pro�le (IMP) is a qualitative instrument to assess motor behaviour

of infants aged 3 to 18 months. The IMP consists of �ve domains: size of motor repertoire, ability to

select motor strategies (variability), �uency, symmetry and motor performance.

Objective: To assess inter-observer reliability, concurrent validity of the IMP with the Alberta Infant

Motor Scale and the Touwen Infant Neurological Examination, and predictive validity of the IMP for

neurological outcome at 18 months.

Design: A longitudinal prospective study was performed in a group of 30 term born and 59 preterm

infants. For the concurrent validity part of the study, a second group of term infants was added with

cross-sectional assessments.

Methods: Assessments were performed at corrected ages of 4,6,10,12 and 18 months and consisted

of the IMP, AIMS and neurological assessment. Socio-economic and perinatal data were collected.

Non-parametric statistics were used to analyze the data.

Results: Inter-observer reliability was high (intra-class coe!cient 0.95). Correlations between IMP

and AIMS scores varied across IMP domains; they were highest for the performance domain of

the IMP (Spearman’s rho 0.47-0.84). A clear relationship was found between total IMP score and

neurological condition (Kruskal-Wallis p < 0.001). Sensitivity for prediction of abnormal neurological

outcome at 18 months was 86 to 100% with speci�city ranging from 71 to 78%.

Limitations: Assessors were not blinded with respect to term or preterm status of the infants.

Follow-up did not extend beyond the age of 18 months.

Conclusions: Reliability of the IMP is good and concurrent and predictive validity are satisfactory.

These �ndings support the notion that the IMP is a promising and valuable instrument to assess

motor behaviour in infancy.

79

Concurrent and predictive validity of the Infant Motor Pro�le

6

INTRODUCTION

Prediction of neurological outcome in infants with a high risk for developmental motor disorders,

such as cerebral palsy (CP) or developmental coordination disorder (DCD), is di�cult. It appears

that instruments that assess qualitative aspects of motor behaviour, such as the General Movement

method (GM1,2) and the Test of Infant Motor Performance (TIMP3) are most promising as single

clinical neuromotor predictors4. However, the GM method and TIMP are only applicable until the

age of four months. Therefore, we developed the Infant Motor Pro!le5, a qualitative assessment of

motor behaviour that is applicable throughout infancy until the age of 18 months.

The IMP was developed for three purposes: !rst it may be used to detect infants with a high

risk for developmental motor disorders, such as CP or DCD. Infants born very preterm are especially

at risk for these developmental motor disorders6. Early detection of high-risk infants is important

to provide early intervention at young age when plasticity of the brain is still high7,8. Second, the

IMP may be used for evaluation of changes in neuromotor function, e.g. during or after early

intervention. The third aim of the IMP is prediction of future developmental outcome.

The IMP is based on ideas of the Neuronal Group Selection Theory (NGST) on motor

development9,10,11. According to NGST, typical motor development starts with the phase of

primary variability with exploratory, variable motor behaviour. Children with pre- or perinatally

acquired brain damage show more stereotyped motor behaviour with considerably less variation.

During development, infants learn to select adaptive motor strategies out of their primary motor

repertoire and to adapt motor behaviour to the environment. This phase of adaptive selection is

called secondary variability. Children with developmental motor disorders often have problems

in selecting adaptive motor strategies10,11. Two domains of the IMP are based on these principles

of motor development; they assess variation of motor behaviour and the ability to select motor

strategies. Three additional domains assess movement "uency, movement symmetry and motor

performance.

Two types of validity that are important in the development and validation of a new instrument

are concurrent and predictive validity. Concurrent validity is the extent to which scores on the

new instrument relate to scores on another measure of the same theoretical construct, ideally a

‘gold standard’. However, no gold standard for assessment of neuromotor function in infancy is

available. Therefore, concurrent validity of the new instrument with other established instruments is

assessed. Predictive validity is de!ned as the extent to which current scores on the new instrument

predict future developmental outcome. A distinction can be made between prediction of major

developmental disorders, such as cerebral palsy, and prediction of minor developmental motor

problems, such as minor neurological dysfunction and developmental coordination disorder.

In our pilot study5, we described the Infant Motor Pro!le and its theoretical background, its

domains and items, and details on scoring procedures. In addition, !rst data on reliability and some

data on validity were presented. Intra and inter observer reliability of scoring were satisfactory in the

80

Chapter 6

persons who developed the IMP. Concurrent validity of the IMP with the Alberta Infant Motor Scale

(AIMS12) and the Touwen Infant Neurological Examination (TINE13,14) was assessed in a relatively

small sample of infants.

Aim of the present study is threefold: �rst to examine inter-observer reliability of a newly

trained assessor without prior experience with the IMP. The second aim is to investigate concurrent

validity of the IMP with AIMS and TINE in a large sample of infants and assessments. Based on the

idea that the AIMS measures motor performance and the IMP assesses various aspects of motor

behaviour including motor performance, we expect a moderate correlation between the total IMP

score and the AIMS and a high correlation between the performance domain of the IMP and the

AIMS. As the IMP assesses several parameters of neurological integrity, we expect strong association

between IMP scores and neurological condition assessed with TINE. Third aim of this study is to

determine predictive validity of the IMP at 4, 6, 10 and 12 months for neurological outcome at 18

months measured by the Hempel assessment.

METHODS

Participants

We included a longitudinal study group of term and preterm infants and a cross-sectional study

group of only term infants. The longitudinal study group consisted of 30 term born and 59 preterm

infants. The term infants (12 girls and 18 boys) were recruited from amongst colleagues and

acquaintances of the researchers. Median gestational age of the longitudinal term group was 40.1

weeks (range 37.6-42 weeks), median birth weight was 3588 grams (range 2730-4470 grams) and

there had been no pre or perinatal complications. Fifty-nine infants were born preterm (25 girls

and 34 boys) with median gestational age 29.7 weeks (range 25 to 34.7 weeks) and median birth

weight of 1285 grams (range 630 to 2180 grams). The preterm infants had been admitted to the

neonatal intensive care unit of the Beatrix Children’s Hospital of the University Medical Center (UMC)

in Groningen between December 2003 and January 2005. Thirty-�ve of the preterm infants were

singletons and 24 were twins. Nine pairs of twins participated in the study; the remaining six had

lost their twin sibling. Neonatal ultrasound was available for 57 of the 59 preterm infants. Serious

brain pathology was observed in six infants: one infant had cystic PVL15, four infants had IVH grade

IV16 and one infant had middle cerebral artery infarction on the right side. The longitudinal study

group (term and preterm infants) was assessed at corrected ages 4, 6, 10, 12 and 18 months.

For the concurrent validity part of the study, another group of 116 term born infants (62

girls and 54 boys) was added. They were recruited at Well Child Centers and had cross-sectional

assessments at ages 4, 6, 10, 12 or 18 months. Median gestational age was 40.1 weeks (range 37-

43 weeks) and median birth weight was 3500 grams (1960-4660 grams). All parents of the infants

signed an informed consent form. The project was approved by the Ethics Committee of the UMC

in Groningen.

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6


Socio-economic, perinatal and neonatal data were collected for all infants on standardised

forms by means of an interview with the parents and consultation of neonatal intensive care unit

discharge certi�cates. Socio-economic status (SES) was operationalized as the sum score of four

variables describing educational and professional level of father and mother, all expressed on a

scale from 0 (lowest) through 2 (highest). ‘Small for gestational age’ (SGA) was de�ned as birth

weight below 10th percentile17. ‘Signs of fetal distress’ was de�ned as the presence of at least one

of the following factors: meconium staining, cardiotocography abnormalities and acidaemia during

delivery (arterial umbilical pH below 7.05).Table I shows socio-economic and neonatal characteristics

Table I: Socio-economic and neonatal characteristics of study groups

Term Preterm p-value

Number of children 146 59

Male gender, n (%) 72 (49) 34 (58) 0.282

Maternal age at child birth (years), mean SD 32 5.1 31.8 5.2 0.826

SESa, median (range) 6 (0-8) 4 (0-8) 0.002f

Twins, n (%) 2 (1.4) 24 (41) <0.001

Gestational age (weeks), median (range) 40.1 (37-43) 29.7 (25-34.7) <0.001

Birthweight (grams), median (range) 3500 (1960-4660) 1285 (630-2180) <0.001

Small for gestational ageb, n (%) 15 (10) 20 (34) <0.001

Caesarian section, n (%) 16 (11) 34 (58) <0.001

Signs of fetal distressc, n (%) 35 (24)d 30 (51)e <0.001

Apgar score at 5 minutes, median (range) 10 (7-10) 9 (4-10) <0.001

Art�cial ventilation, n (%) 1 (0.7) 40 (68) <0.001

a SES = socio-economic status, sum score of four variables describing educational and professional level of fatherand mother, all expressed on a scale from 0 (lowest) through 2 (highest).b Small for gestational age is de�ned as birthweight compared with gestational age below 10th centile17.c Presence of at least one of the following factors: meconium staining, CTG abnormalities, acidaemia duringdelivery (arterial umbilical pH below 7.05).d Data on signs of fetal distress were available for 144 of the term infants: 107 (73%) infants showed no signs offetal distress, 23 (16%) had meconium staining, 11 (7,5%) had CTG abnormalities and one had arterial umbilicalpH of 6.82. This infant had perinatal asphyxia with meconium aspiration for which ventilation was required. Inaddition, neonatal convulsions occurred. Brain MRI at day 6 was normal.e 30 (51%) of the preterm infants showed signs of fetal distress: 4 (6,8%) had meconium staining, 22 (37%)showed CTG abnormalities, 2 (3%) had acidaemia with low umbilical pH and 2 (3%) showed a combination ofsigns of fetal distress, both as a result of placental dysfunction.f SES of preterm group is lower than term group

of term and preterm groups. As no signi�cant di!erences in characteristics were found between the

longitudinal and cross-sectional term groups, we displayed them as one term group.

Procedures

Assessments were performed at (corrected) ages 4, 6, 10, 12 and 18 months for the longitudinal

82

Chapter 6

term group and the preterm group. The term cross-sectional group was assessed at one (n = 102

infants), two (n = 13 infants) or three (n = 1) of these ages. The actual number of infants assessed at

each age is displayed in Table II. Assessments consisted of a video-recording of approximately 15

minutes of spontaneous motor behaviour in supine, prone, sitting, standing, and walking condition,

depending on age and functional capacities of the infant. Furthermore, reaching, grasping and

manipulation of objects was tested in supine and in (supported) sitting position. The 80 items of the

IMP were scored on the basis of the video recording. These constitute the scores in �ve domains: size

of repertoire (variation), ability to select (variability), movement �uency, movement symmetry and

motor performance. The mean of the �ve domain-scores is the total IMP score5. IMP assessments of

the longitudinal term and preterm groups were carried out by KRH who knew whether an infant

was term or preterm born, but was not aware of any of the perinatal and neonatal details. IMP

assessments of the cross-sectional term group were scored by KRH and LE.

Table II: Number of assessments for term and preterm groups

Group Numberof infants 4 mo 6 mo 10 mo 12 mo 18 mo Number of

assessments

Term longitudinal 30 30a 30 30 30 30 150

Term cross-sectional 116 22 25 26 29 30 131

Preterm 59 58 57b 54 54 57 280

Total 205 110 112 110 113 117 561

mo = monthsa For 1 term infant data of neurological examination at 4 months were missing, only AIMS and IMP were assessed.b For 1 preterm infant AIMS score could not be determined at 6 months, because assessment in prone positionwas not performed.

Reliability assessment

LE, who was involved in this study as a master student, was trained in the assessment of the IMP.

During a training period of �ve weeks, 100 video’s of term and preterm infants at various ages were

assessed. After this training period, inter observer agreement between LE and KRH was investigated

on a sample of another 25 video’s consisting of �ve video’s at each of the �ve assessment ages

(4,6,10,12 and 18 months). The �ve video’s at each age consisted of two randomly selected video’s

of the term infant group and three of the preterm group.

Concurrent validity

At all ages the AIMS12 and Touwen Infant Neurological Examination (TINE13,14) were assessed, in order

to investigate concurrent validity of the IMP with these instruments. The AIMS was scored on the

basis of the video-recording of spontaneous motor behaviour. Total AIMS scores, instead of centiles,

were used in the data processing, as the Canadian reference values seem currently inappropriate

for Dutch children18. Reliability of the AIMS is good, but predictive validity for major developmental

83

6


disorders is only moderate19,20. The Touwen Infant Neurological Examination (TINE13,14) was

performed at (corrected) ages of 4, 6, 10 and 12 months. In TINE, neurological signs are organized

according to age-speci!c norms into clusters of dysfunction. Five clusters are distinguished: reaching

and grasping, gross motor function, brain stem function, visuomotor function and sensorimotor

function (consisting of re"exes and muscle tone). Neurological condition is classi!ed as abnormal

if there is a distinct neurological syndrome, such as a hemisyndrome, irrespective of the number

of deviant clusters. An infant is classi!ed as having minor neurological dysfunction (MND) in case

of presence of more than two clusters of dysfunction. Two forms of typical neurological condition

are distinguished: normal – suboptimal when one or two clusters are deviant and normal when no

clusters ful!l criteria for dysfunction14. Reliability of TINE is good. Predictive validity is good for major

developmental motor disorders such as cerebral palsy and moderate for minor motor disorders4,14.

Predictive validity for major developmental motor disorders such as cerebral palsy is good, but for

minor motor disorders moderate at best4,14.

Predictive validity

For assessment of the predictive validity of the IMP, neurological outcome at the (corrected) age of

18 months was determined with the Hempel assessment21. This method is suitable for children of

pre-school age, from 18 months until four years of age. Similar to the TINE, the Hempel assessment

classi!es neurological signs into clusters of dysfunction, namely !ne motor dysfunction, gross

motor dysfunction, dysfunctional muscle tone regulation, re"ex abnormalities and visuomotor

dysfunction. Neurological condition is classi!ed into four categories: abnormal, complex MND

(denoting the presence of more than one dysfunctional cluster), simple MND (one cluster of

dysfunction) or normal (no deviant clusters or the isolated presence of re"ex abnormalities)22.


To analyze inter-observer reliability, intra-class correlation coe#cients (ICCs) for a two-way mixed

e$ects model with associated 95% con!dence intervals were used. Di$erences in IMP scores

between term and preterm groups and between the four neurological conditions were analyzed

by means of the non-parametric Mann-Whitney U test and Kruskal-Wallis test respectively. Relations

between IMP scores and AIMS scores and correlation between IMP scores throughout infancy and

neurological outcome at 18 months were assessed with Spearman’s rank correlation with associated

con!dence intervals. Interpretation of Spearman’s correlation coe#cient was as follows: rho < 0.50

weak relationship, 0.50 ≥ rho ≥ 0.75 moderate relationship, rho > 0.75 good relationship23. To assess

predictive validity of the IMP scores for the outcome at 18 months, a cut-o$ score below the 5th

percentile was used. Throughout the analyses, di$erences and correlations with a p-value < 0.05

were considered to be statistically signi!cant (two-tailed testing).

84

Chapter 6

RESULTS

At all ages total IMP scores did not signi�cantly di�er between girls and boys. The preterm group

consistently showed lower total IMP scores than the term group (Figure 1, Mann-Whitney U test p

values < 0.001). This was also the case for the scores on the domains size of repertoire (p < 0.001 at

all ages), !uency (p< 0.001 at 4, 6, 12 and 18 months, p = 0.028 at 10 months) and performance (p =

0.001 at 4 months and p < 0.001 at 6, 10, 12 and 18 months). Scores on adaptive selection (variability)

were signi�cantly lower for preterm infants compared to term infants from age 10 months onwards

(4 months p = 0.90, 6 months p = 0.16, 10 months p<0.001, 12 months p = 0.03, 18 months p =

0.001). Symmetry scores were signi�cantly lower for the preterm group at ages 4 and 18 months

(p-values 0.02 and 0.04 respectively), but not at 6,10 and 12 months.

Reliability

Interobserver reliability of the total IMP score yielded an intraclass correlation coe"cient (ICC) of

0.95 (95% con�dence interval 0.89-0.98), indicating good reliability. Reliability of IMP domains was

moderate to good with ICC from 0.74 to 0.99 (Table III).

Concurrent validity

Correlations between AIMS scores and total IMP scores were weak to moderate at all ages

Figure 1: Di!erences in total IMP scores between term and preterm infants at 4, 6, 10, 12 and 18 months.Data are presented as median values (horizontal bars), interquartile ranges (boxes) and ranges (vertical lines).Open circles and asterisks represent outliers. FT = full term group, PT = preterm group. At all ages di�erences intotal IMP scores between the two groups were signi�cant (Mann-Whitney U test p < 0.001).

60

70

80

90

Tota

lIM

P-sc

ore

(%)

100

FT PT4 months

FT PT6 months

FT PT10 months

FT PT12 months

FT PT18 months

60

70

80

90

Tota

lIM

P-sc

ore

(%)

100

FT PT4 months

FT PT6 months

FT PT10 months

FT PT12 months

FT PT18 months

6

85


(Spearman’s rho 0.36 to 0.55, see Table IV). The performance domain of the IMP showed the strongest

correlations with the AIMS scores, especially at the age of 10 and 12 months (Spearman’s rho 0.84

and 0.81 respectively, Table IV). Correlations between the other domains and the AIMS were weak

(Spearman’s rho 0.01-0.41, Table IV). Preterm infants had signi�cantly lower AIMS scores than term

infants at ages 4, 10, 12 and 18 months (Mann-Whitney U test, p-values 0.001, < 0.001, < 0.001 and

<0.001 respectively). No di�erence was found at age 6 months (p = 0.32).

We found a clear relationship between the total IMP score and neurological condition at all

ages: infants with a normal neurological condition had highest IMP scores and infants with an

abnormal neurological condition had lowest IMP scores (Figure 2, Kruskal-Wallis p < 0.001 at all

ages). The domains size of repertoire, �uency, symmetry and performance were highly signi�cantly

related to neurological condition at all ages (p-values for variability, �uency and performance

all < 0.001, except for �uency at 10 months p = 0.008; p-values for symmetry respectively 0.025,

0.006, < 0.001, 0.025 and < 0.001 at 4, 6, 10, 12 and 18 months). Scores on the domain ability to

select (variability) were signi�cantly di�erent between neurological conditions at ages 10 and 12

months (p=0.021 and 0.008 respectively), but not at ages 4, 6 and 18 months (p= 0.49, 0.46 and 0.06

respectively).

Predictive validity

Neurological condition at 18 months was determined with the Hempel examination21. Of the

longitudinal term group, 23 children had normal neurological condition and 7 had simple MND.

None of the term children showed complex MND or abnormal neurological condition at 18 months.

Of the preterm group, eleven children had a normal neurological condition, 7 had simple MND, 31

had complex MND and neurological condition of 8 infants was considered as abnormal (14% of

preterm group), of which four infants had a unilateral spastic CP and four had bilateral spastic CP.

Two preterm children did not have follow-up at 18 months.

For the total longitudinal group of infants, correlation between total IMP scores throughout

infancy and neurological outcome at 18 months was moderate, with Spearman’s rho’s of -0.62

Table III: Inter observer reliability of total IMP score and IMP domains

Intraclass correlation coe!cient (ICC)(95% Con"dence Interval)

Total IMP score 0.95 (0.89-0.98)

IMP domain

Size of repertoire 0.91 (0.81-0.96)

Ability to select 0.79 (0.58-0.90)

Fluency 0.74 (0.49-0.87)

Symmetry 0.99 (0.98-1.0)

Performance 0.98 (0.95-0.99)

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Chapter 6

4 mo

Nn=31

N-subn=34

MNDn=31

An=13

60

70

80

90

Tota

lIM

P-sc

ore

(%)4

mo

Neurological condi on 4 mo

100

-

-

-

-

-

-6 mo

Nn=33

N-subn=46

MNDn=27

An=5

70

80

90

Tota

lIM

P-sc

ore

(%)6

mo


100

-10 mo

Nn=42

N-subn=38

MNDn=26

An=4

70

80

90

Tota

lIM

P-sc

ore

(%)1

0m

o


100

70

80

90

-

100

12 mo

Nn=49

N-subn=38

MNDn=22

An=4

70

80

90

Tota

lIM

P-sc

ore

(%)1

2m

o


100-

18 mo

Nn=62

N-subn=16

S-MNDn=31

An=8

60

70

80

90

Tota

lIM

P-sc

ore

(%)1

8m

o


100

-

--

Figure 2: Relationship between total IMP scoresand neurological condition at the various ages.Data are presented as median values (horizontalbars), interquartile ranges (boxes) and ranges(vertical lines). N = normal neurological condition,N-sub = normal suboptimal neurological condition,MND = minor neurological dysfunction, A =abnormal neurological condition, mo = months, n= number of infants, S-MND = simple MND, C-MND= complex MND. At all ages di�erences in total IMPscores between the four neurological conditionswere signi�cant (Kruskal-Wallis p < 0.001).

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6


Table IV: Spearman’s correlation coe�cients of IMP scores and AIMS scores per age

AIMS 4 mo AIMS 6 mo AIMS 10 mo AIMS 12 mo AIMS 18 mo

Total IMP score 0.43**

(0.26-0.57)0.34**

(0.19-0.52)0.55**

(0.40-0.66)0.43**

(0.27-0.57)0.36**

(0.19-0.51)

IMP domain

Size ofrepertoire

0.39**

(0.22-0.54)0.29**

(0.11-0.45)0.36**

(0.19-0.51)0.37**

(0.19-0.52)0.41**

(0.25-0.55)

Ability toselect

0.07(-0.11-0.26)

0.01(-0.18-0.19)

0.22*

(0.04-0.39)0.11

(-0.07-0.29)0.04

(-0.14-0.22)

Fluency 0.27**

(0.09-0.43)0.24*

(0.06-0.41)0.08

(-0.11-0.26)0.15

(-0.03-0.33)0.23*

(0.05-0.39)

Symmetry 0.23*

(0.05-0.40)0.05

(-0.13-0.24)0.13

(-0.05-0.31)0.12

(-0.07-0.30)0.32**

(0.14-0.47)

Performance 0.56**

(0.42-0.67)0.56**

(0.41-0.67)0.84**

(0.78-0.89)0.81**

(0.73-0.86)0.47**

(0.31-0.60)

Spearman’s correlation coe!cients with associated 95% con"dence intervals between brackets, * p < 0.05, ** p< 0.01.

Table V: Predictive validity of total IMP score at ages 4, 6, 10 or 12 months for neurological outcome at 18months

Total IMP4 mo

Total IMP6 mo

Total IMP10 mo

Total IMP12 mo

Prediction of CP at 18 mo (IMP score < p5)

Sensitivity 100 88 100 86

Speci"city 71 78 78 77

PPV 26 29 26 26

NPV 100 98 100 98

Accuracy 73 79 79 78

Prediction of deviant neurologicaloutcome (complex MND or CP) at 18 mo (IMP score < p5)

Sensitivity 63 55 56 63

Speci"city 85 94 93 98

PPV 77 88 87 96

NPV 75 72 73 78

Accuracy 76 76 77 83

mo = months, p5 = 5th percentileSensitivity = true positives/(true positives + false negatives)Speci"city = true negatives/(true negatives + false positives)PPV = positive predictive value = true positives/all positivesNPV = negative predictive value = true negatives/all negativesAccuracy = (true positives + true negatives)/all subjects

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Chapter 6

(CI -0.74—0.47), -0.57 (CI -0.70—0.41), -0.67 (CI -0.77—0.53) and -0.65 (CI -0.76—0.50) respectively

at ages 4, 6, 10 and 12 months. Predictive validity of total IMP scores (with cut-o� score below 5th

percentile) for abnormal neurological condition (CP) at 18 months varied with age of assessment

and showed sensitivity from 86 to 100% and speci�city from 71 to 78% (Table V). Predictive validity

for deviant neurological outcome (complex MND or CP) at 18 months demonstrated sensitivity from

55 to 63% and speci�city of 85 to 98% (Table V). If instead of 5th percentile the 15th percentile was

used as cut-o� point, sensitivity increased to 68 to 89%, but speci�city decreased to 72 to 87%.

Accuracy was around 80% and did not di�er between level of cut-o� point at 5th or 15th percentile.

DISCUSSION

Our study showed a good reliability of the IMP. Concurrent validity of the IMP with the AIMS met

the a priori theoretical expectations: the IMP performance domain correlated best with the AIMS.

Concurrent validity of the IMP with TINE and Hempel examination was very good. Predictive validity

of the IMP for neurological outcome at 18 months was satisfactory.

Strengths of this study are its predominantly longitudinal character and the low attrition rate

(3.5% over all longitudinal assessments, see Table II). A weakness of the study is that the assessors

were not blind with respect to term or preterm status of the infant. This may have in!uenced

scoring. However, the assessors were unaware of any details of the child’s clinical history or results

of neonatal ultrasounds. Besides, if assessors had been blinded to term or preterm status, it would

have been di"cult to conceal preterm status, because the infant’s appearance usually discloses

preterm birth. A second weakness of this study is the relatively short duration of follow-up. At 18

months, clinical signs of CP often are not yet fully expressed and signs of minor developmental

motor disorders may not be present until school age24,25.

The term group showed a relatively high percentage of infants with signs of fetal distress,

consisting mainly of meconium staining which is fairly common in term deliveries26. The group of

preterm infants included in this study may be considered as a representative sample of a Dutch

neonatal intensive care unit population in a tertiary referral centre with respect to gestational age,

birthweight, frequency of Apgar score at 5 minutes below 7 (15%) and ventilatory support (68%)27,28.

Our preterm sample showed a relatively high percentage of infants small for gestational age and

Caesarean deliveries27,28. The latter could be due to the increased tendency over the years to deliver

very preterm infants by Caesarean section29. The preterm group had lower socio-economic status

than the term group, in accordance with social disadvantage being considered a risk factor for

preterm birth30.

Interobserver reliability of total IMP score and the domains size of repertoire, symmetry and

performance was good to very good. Reliability of the IMP domains ability to select and !uency was

moderate. Interobserver reliability in this study was higher than in our pilot study5, probably as a

result of the more precise de�nitions and descriptions of the IMP items which had been developed

6

89


in the meantime. With good training, IMP scoring can be learnt reliably without prior experience in

infant motor development.

The study showed clear di�erences in IMP scores between term and preterm infants for total

IMP scores and the domains size of repertoire (variability), �uency and performance at all ages.

Preterm birth is a major risk factor for developmental motor disorders6. Preterm infants are at risk

for brain lesions, which according to NGST lead to reduced variability of motor behaviour11. Loss

of �uency of motor behaviour is one of the !rst signs of non-optimal neurological condition1.

Delayed acquisition of motor milestones, in the IMP re�ected as lower performance scores, can be

a sign of developing CP31. For the domain ability to select (variability), scores signi!cantly di�ered

between term and preterm infants from 10 months onwards. In typically developing infants, the

ability to select suitable motor strategies gradually emerges at function-speci!c ages after the !rst

half year of life10. Infants with developmental motor disorders often have problems in processing

a�erent, sensory information and !ne-tuning and adapting motor behaviour11,32,33. This could delay

or hamper development of the ability to select, as adaptive selection relies on a�erent feedback.

Scores on the domain symmetry di�ered between term and preterm infants at ages 4 and 18

months. The asymmetries observed at 4 months could be transitory neurological !ndings that

resolve spontaneously34, whereas the asymmetries observed at later age of 18 months could be

signs of the development of unilateral spastic CP24.

As we expected, the total IMP score only correlated to a moderate extent with the AIMS.

Correlation between AIMS and IMP was highest for the performance domain of the IMP, especially at

the ages of 10 and 12 months. Both the performance domain of the IMP and the AIMS assess motor

achievements in a quantitative way. From the age of 10 months onwards, motor development is

characterized by a rapid gain in motor milestones, which is re�ected in both IMP and AIMS scores.

After the age of 14 months, the discriminative power of the AIMS is diminished12,35. The IMP domain

size of repertoire assesses another aspect of motor behaviour than the AIMS. The !nding that these

parameters were weakly but signi!cantly correlated at all ages indicates that both assess di�erent

aspects of the same underlying construct, being neuromotor integrity. The IMP domain ability to

select was only related to the AIMS score at age ten months, the !rst age in the present study at

which selection of adaptive motor strategies was present to some extent. The IMP domain �uency

was weakly related to the AIMS. Loss of movement �uency is one of the !rst signs of non-optimal

neurological condition1, but it is not speci!c for serious developmental motor disorders that are

associated with low motor performance. The IMP domain symmetry was related to the AIMS score

at the ages of 4 and 18 months, the latter probably representing the infants with a developing

unilateral CP, which besides a low symmetry score also leads to reduced motor performance31.

Concurrent validity of IMP and the age-speci!c neurological examination (TINE and Hempel)

was very good: at all ages infants with normal neurological condition had higher IMP scores than

infants with minor neurological dysfunction or abnormal neurological condition. Di�erences in

IMP scores were especially found between infants with (complex) MND or abnormal neurological

90

Chapter 6

condition and infants with normal or normal – suboptimal neurological condition (or simple MND

at 18 months). Complex MND, in contrast with simple MND, has clinical relevance and is associated

with pre- or perinatal adversities22,25. These di!erences in IMP scores between infants with di!erent

neurological conditions were found at all ages for the domains size of repertoire (variation),

"uency, symmetry and performance, supporting the notion that these are indeed parameters of

neuromotor integrity5. Scores on the domain ability to select were related to neurological condition

at ages 10 and 12 months, but not at 4, 6 and 18 months. This is in analogy with the di!erences we

found between term and preterm infants, except that they did di!er in adaptive selection scores at

18 months. The data indicated that the absence of a relation between neurological condition and

adaptive selection at 18 months was brought about by relatively good scores of infants with an

abnormal neurological condition. Motor behaviour of these children was characterized by a limited

motor performance; nevertheless they demonstrated, within the skills which they had developed, a

relatively good ability of adaptive section out of their limited motor repertoire.

Sensitivity of IMP scores throughout infancy for predicting CP at 18 months was very high.

Positive predictive value of the IMP for neurological outcome at 18 months was low, but negative

predictive value was high, implying that IMP scores above the 5th percentile almost certainly excluded

abnormal neurological outcome at 18 months. It is important to realize that predictive values of a

test strongly depend on the prevalence of the disorder, e.g. CP, in the study population36. Therefore,

predictive values observed in our sample cannot be extrapolated to the general population.

Prediction of developmental outcome at an early age is di#cult and will never be perfect,

because change is one of the main characteristics of the developing brain. To optimize prediction

of neuromotor outcome in children at high risk for developmental motor disorders, it is probably

best to combine multiple, complementary tools, such as neurological examination, assessment of

milestones and assessment of qualitative aspects of motor behaviour4 in addition to neuroimaging

and neurophysiological techniques.

CONCLUSION

The Infant Motor Pro$le is a qualitative assessment of motor behaviour based on the Neuronal Group

Selection Theory on motor development. Interobserver reliability of the IMP is good. Concurrent

validity of the IMP with the Alberta Infant Motor Scale was especially high for the performance

domain of the IMP. Concurrent validity of IMP with Touwen Infant Neurological Examination was

very good. With respect to the three purposes for which the IMP was developed, we can conclude

that the IMP is well able to discriminate between typically developing infants and infants with high

risk for developmental motor disorders. The ability of the IMP to evaluate motor function over time

should be further explored by applying the IMP in intervention studies. Prediction of neurological

outcome is very di#cult, due to change being one of the main characteristics of the developing

nervous system. In our study population, predictive validity of the IMP was satisfactory. Future

studies will aim at generating norm-scores and determining clinical applicability.

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6


ACKNOWLEDGEMENTSWe thank Nicole Arink, Hylco Bouwstra, Dineke Dijkhuizen and Anne Hoekstra for performing part of theassessments. The study was supported by a Junior Scienti�c Masterclass grant of the post-graduate schoolBehavioral and Cognitive Neurosciences (BCN), University of Groningen.

92

Chapter 6

REFERENCES1. Hadders-Algra M. General movements: A window for early identi�cation of children at high risk for

developmental disorders. J Pediatr 2004,145:S12-18.




5. Heineman KR, Bos AF, Hadders-Algra M. The Infant Motor Pro�le: a standardized and qualitative method toassess motor behaviour in infancy. Dev Med Child Neurol 2008;50:275-82.









14. Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological dysfunctionin infancy using the Touwen Infant Neurological Examination: strengths and limitations. Dev Med ChildNeurol, in press.



17. Kloosterman GJ. On intrauterine growth: the signi�cance of prenatal care. Int J Gynaecol Obstet 1970;8:895-912.

18. Fleuren KM, Smit LS, Stijnen T, Hartman A. New reference values for the Alberta Infant Motor Scale need tobe established. Acta Paediatr 2007;96:424-427.

19. Darrah J, M Piper, MJ Watt. Assessment of gross motor skills of at-risk infants: predictive validity of theAlberta Infant Motor Scale. Dev Med Child Neurol 1998;40:485-491.

20. Bartlett DJ, Fanning JE. Use of the Alberta Infant Motor Scale to characterize the motor development ofinfants born preterm at eight months corrected age. Phys Occup Ther Pediatr 2003;23:31-45.


22. Hadders-Algra M. Developmental coordination disorder: is clumsy motor behavior caused by a lesion ofthe brain at early age? Neural Plast 2003;10:39-50.

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23. Portney LG, Watkins MP. Part IV Data analysis: Correlation. Foundations of clinical research. Applications topractice. 2nd ed. Upper Saddle River, NJ: Prentice Hall Health; p. 494, 2000.

24. Krägeloh-Mann I, Cans C. Cerebral palsy update. Brain Dev 2009; Epub ahead of print.

25. Hadders-Algra M. Two distinct forms of minor neurological dysfunction: perspectives emerging from areview of data of the Groningen Perinatal Project. Dev Med Child Neurol 2002;44:561-71.

26. Tran SH, Caughey AB, Musci TJ. Meconium-stained amniotic �uid is associated with puerperal infections.Am J Obstet Gynecol 2003;189:746-50.



29. Haque KN, Hayes AM, Ahmed Z, Wilde R, Fong CY. Caesarean or vaginal delivery for preterm very-low-birth weight (< or =1,250 g) infant: experience from a district general hospital in UK. Arch Gynecol Obstet.2008;277:207-12.

30. Zeka A, Melly SJ, Schwartz J. The e�ects of socioeconomic status and indices of physical environment onreduced birth weight and preterm births in Eastern Massachusetts. Environ Health. 2008;7:60.

31. Allen MC, Alexander GR. Using motor milestones as a multistep process to screen preterm infants forcerebral palsy. Dev Med Child Neurol 1997;39:12-6.



34. Michaelis R, Asenbauer C, Buchwald-Saal M, Haas G, Krägeloh-Mann I. Transitory neurological �ndings in apopulation of at risk infants. Early Hum Dev 1993;34:143-53.

35. Van Haastert IC, de Vries LS, Helders PJ, Jongmans MJ. Early gross motor development of preterm infantsaccording to the Alberta Infant Motor Scale. J Pediatr 2006;149:617-22.

36. Altman DG. Practical statistics for medical research. London: Chapman and Hall, p411-412, 1991.

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7CHAPTER

General discussion

96

Chapter 7

GENERAL DISCUSSION

This thesis presents the Infant Motor Pro�le (IMP), a recently developed qualitative assessment

of motor behaviour in infancy. The IMP is based on ideas of the Neuronal Group Selection Theory

(NGST) which states that motor development is characterised by exploration of the primary variable

motor repertoire and selection of adaptive motor strategies out of this repertoire1,2,3. The IMP

consists of 80 items that are grouped into �ve domains: size of the repertoire (variation), adaptive

selection (variability), movement �uency, movement symmetry and motor performance.

This thesis had three aims: 1) review of existing methods for the assessment of neuromotor

function in infancy, 2) development of the IMP and 3) assessment of the psychometric properties

of the IMP. The �rst two aims are primarily outlined in chapters 1 and 2. The present discussion

will mainly focus on the third aim. First, the �ndings with respect to the psychometric properties

of the IMP will be commented. Next, some methodological considerations with respect to study

group and assessments will be discussed. Last, future research topics and concluding remarks will

be presented.

Psychometric properties of the IMP

To assess the psychometric properties of the IMP, we performed a longitudinal prospective study

on a heterogeneous group of term and preterm born infants aged 3 to 18 months. In addition,

another group of term born infants had cross-sectional assessments at the same ages. Assessments

consisted of the IMP, the Alberta Infant Motor Scale (AIMS4) and an age-speci�c neurological

examination (Touwen Infant Neurological Examination5,6 (TINE) at 4, 6, 10 and 12 months corrected

age and Hempel assessment at 18 months corrected age7).

Intra- and interobserver reliability of the IMP

Intra- and interobserver reliability of the IMP were assessed in the pilot study (chapter 3) and in the

study described in chapter 6. In the pilot study, intra- and interobserver reliability were satisfactory

in the persons who developed the IMP. To test whether it was possible to train a new, inexperienced

assessor, we trained a master student without prior experience in infant motor development.

Reliability of the total IMP score was very good and reliability of the di!erent domains varied from

moderate (ability to select and �uency) to good and very good (size of the repertoire (variation),

symmetry and performance). We found that scoring of the IMP can be learnt reliably after good

training; a typical training course would consist of basic instructions followed by assessment of

about 100 videorecordings with feedback by an experienced supervisor at regular intervals. No prior

experience with developmental assessment of infants is required. The amount of training needed is

comparable to for example the training required for the General Movement method8. Reliability of

the IMP is comparable to that of other methods for assessment of neuromotor function in infancy9,

such as the Touwen Infant Neurological Examination6, Alberta Infant Motor Scale4,10,11 (AIMS), Bayley

Variability in IMP scores at di#erent ages (within-participant variability) was especially large

in the preterm infants. It seems that infants with atypical motor development have less stable

developmental trajectories than typically developing infants, underscoring the need of repeated

assessments especially in high-risk groups, as atypical development can easily be missed with a

single assessment. This "nding is possibly not limited to the IMP assessment, but also valid for other

developmental motor assessments and has consequences for the organization of clinical follow-up

of high risk infants.

In the preterm group, higher socio-economic status was associated with higher IMP scores.

Highly educated parents probably provide both favourable genetic factors and a stimulating

environment. The latter is especially important for children at high biological risk of developmental

problems, such as preterm infants17. Early intervention should therefore especially be targeted at

this group of vulnerable children with both biological and social risk factors for developmental

problems, as these children are most likely to bene"t from it17. Unfortunately, it appears that

especially these children with high social risk are less likely to receive early intervention in practice18.

Figure 1 in chapter 5 shows large di#erences in IMP scores between term and preterm infants,

but even more pronounced di#erences within the preterm group. In general, a small part of the

preterm group has IMP scores comparable to the term infants. This small part is expected to have a

Scales of Infant Development12 and Peabody Developmental Motor Scale13. Intra- and interobserver

agreement of infant motor assessment are not perfect, which could give clinicians the inconvenient

impression of subjectivity. However, it should be kept in mind that other assessments that are used

in daily clinical routine do not have a perfect reliability as well (e.g. assessment of neonatal head

ultrasound scans)14,15 or are subject to an expectancy bias (e.g. interpretation of plantar re!exes in

adults16.

Construct validity of the IMP

Construct validity of the IMP was investigated in chapter 5. Construct validity is the extent to which

an instrument measures the theoretical construct of interest, in this case neuromotor function.

Construct validity was operationalized as the relation of IMP scores with pre-, peri- and neonatal

variables, including the presence of brain pathology on neonatal ultrasound scans of the brain.

A longitudinal prospective study in a group of term and preterm born infants from age 4 to 18

months was performed. Gestational age, socio-economic status and 5-minute Apgar score were

signi"cant determinants of IMP scores throughout infancy in the total group of infants. In the group

of the preterm infants, IMP scores were strongly a#ected by the presence of serious brain lesions on

neonatal ultrasounds and by socio-economic status. We also found a clear increase of IMP scores

with increasing age, which implies that the IMP is able to detect and re!ect age-related changes in

7

97

General discussion

motor development. These !ndings strongly contribute to construct validity of the IMP and make

it more plausible that the IMP indeed measures the construct of interest, namely neuromotor

function.

98

Chapter 7

more or less typical motor development. Many of the preterm infants have lower IMP scores than

the term infants throughout infancy, but they do develop most of the motor skills, though at a

later time, with a less variable repertoire to choose from than the typically developing infants. This

could possibly be the group of children that develops minor motor disorders such as DCD at a later

age, when more complicated �ne motor skills, such as writing or using scissors, and gross motor

skills involving �ne balancing are required in daily and school activities19. Whether these later motor

problems are already re!ected in the IMP scores in infancy has yet to be investigated.

A small number of the preterm infants had clearly low IMP scores from the start and did only

develop some basic motor skills throughout infancy, with IMP scores hardly rising or even lowering

throughout infancy (Figure 1 chapter 5). These are the children with a seriously hampered motor

repertoire due to brain lesions who were diagnosed with CP. It would be interesting to use the IMP in

this group of children during or after application of early intervention, in order to evaluate changes

in neuromotor function. This is currently done in a study on the e"ect of COPCA, a newly developed

physiotherapeutic early intervention programme, in a group of high risk infants20,21.

As mentioned above, the ability to detect age-related changes in motor development

contributes to the construct validity of an instrument for assessment of neuromotor function22.

In chapter 4 the development of adaptive motor behaviour in typically developing infants was

described. For this study, the longitudinal group of term infants had nine assessments between the

ages of 3 and 18 months. The emergence of adaptive selection of motor patterns was investigated

in four speci�c motor functions, namely abdominal progression, sitting motility, arm movements

during reaching and hand motility during grasping and manipulation. We found that transition to

clinically observable adaptive motor behaviour developed gradually from age 6 months onwards,

with a peak between 8 and 15 months. It occurred at speci�c ages for the di"erent motor functions.

It would be interesting to perform further research on ages of transition in infants with a high risk

for developmental motor disorders such as CP or DCD. In these children transition to secondary

variability could possibly be delayed or impeded, as they can have di#culties with processing

a"erent, sensory information and can experience problems in �ne-tuning and adapting motor

behaviour2,23,24. Further research on this subject is needed to make out whether age of transition to

secondary variability could be a useful clinical parameter of neuromotor condition.

Concurrent validity of the IMP

Concurrent validity of an instrument is the extent to which scores on the instrument relate to scores

on another instrument that assesses the same construct. It is important to note that instruments

available for infant motor assessment di"er in focus on the aspects of neuromotor function that

are assessed, depending on the theoretical background of the instrument (see review in chapter 2).

Good concurrent validity of a new instrument with established instruments contributes to the idea

that the new instrument indeed measures neuromotor function, as the established instruments are

supposed to do so. As the focus of the IMP is partly on di"erent aspects of neuromotor function than

99

7

General discussion

established instruments, namely size of repertoire (variation) and selection of motor behaviour,

we did not expect perfect concurrent validity between the IMP and established instruments. In

chapter 6, concurrent validity of the IMP with the Alberta Infant Motor Scale (AIMS), the Touwen

Infant Neurological Examination (TINE) and Hempel neurological examination (at 18 months)

was investigated. The total IMP score correlated to a moderate extent with the AIMS. Correlation

between AIMS and IMP was highest for the performance domain of the IMP, as both the performance

domain of the IMP and the AIMS assess motor achievements in a quantitative way. Concurrent

validity between IMP and neurological examination (TINE or Hempel) was very good: infants

with normal neurological condition had higher IMP scores than infants with minor neurological

dysfunction or abnormal neurological condition. Di�erences in IMP scores were especially found

between infants with complex MND or abnormal neurological condition and infants with normal

or normal - suboptimal neurological condition. Complex MND, in contrast with simple MND, has

clinical relevance and is associated with pre- or perinatal adversities25,26. All in all, the results on

concurrent validity of the IMP are satisfactory and therefore con�rm that the IMP, in line with other

infant motor assessments, is able to measure various aspects of neuromotor function.

In the study on concurrent validity of the IMP with the neurological examination, we noticed

that the total IMP score was not always the most optimal re�ection of the neuromotor functioning

of the child, especially for the infants with an abnormal neurological condition and a very limited

motor repertoire. In these infants, scores on the performance domain were generally low. As a result,

scores on the adaptive selection domain were relatively high, as only the limited motor performance

that the child did show was assessed with respect to adaptive selection. This leads to a relatively high

total IMP score, which is not a good re�ection of the overall poor neuromotor function. In this light,

in future studies for example during application of early intervention, especially in children with a

very high risk for developmental motor disorders such as CP, more attention should be paid to the

individual scores on the di�erent domains and not only to the total IMP scores. Possibly, it is better

to leave the score on the domain on adaptive selection out of the total IMP score during at least

during the �rst six month of age, as adaptive selection of motor behaviour for most of the motor

functions only starts to emerge from this age onwards. We think the studies described in this thesis

were not signi�cantly hampered by this, as only a limited number of infants in the preterm group

developed CP. However, this issue needs further research and it would be interesting to investigate

the development of IMP domain scores throughout infancy and the relation of domain scores with

pre, peri and neonatal variables, including results of brain imaging.

Predictive validity of the IMP

Predictive validity of an instrument is the extent to which the scores on the instrument now predict

future outcome27. Predictive validity of the IMP for neurological outcome at 18 months was described

in chapter 6. We found a very high sensitivity of IMP scores throughout infancy for predicting CP at

18 months. Positive predictive value of the IMP for neurological outcome at 18 months was low,

100

Chapter 7

but negative predictive value was high, implying that IMP scores above the 5th percentile almost

certainly excluded abnormal neurological outcome at 18 months. It is important to realize that

predictive values of a test strongly depend on the prevalence of the disorder, e.g. CP, in the study

population28. Therefore, predictive values observed in our sample cannot be extrapolated to the

general population. In addition, it makes comparison of predictive validity of di�erent infant motor

assessment methods di�cult, as investigations on predictive validity of di�erent tests are generally

done in di�erent study populations.

Prediction of developmental outcome at an early age is di�cult and will never be perfect,

because change is one of the main characteristics of the developing brain. To optimize prediction

of neuromotor outcome in children at high risk for developmental motor disorders, it is probably

best to combine multiple, complementary tools, which focus on di�erent aspects of neuromotor

function, such as neurological examination, assessment of milestones and assessment of qualitative

aspects of motor behaviour, in addition to neuroimaging and neurophysiological techniques9. As

mentioned above, repeated assessments are mandatory, especially in high-risk groups, because of

large variability in expression of neuromotor dysfunction over time6.

Methodological considerations

Study group

The study group consisted of three samples of infants: two longitudinal groups of respectively term

and preterm infants and one group of term infants with cross-sectional assessments.The longitudinal

term group was relatively small with only 30 infants that were assessed nine times between the ages

of 3 to 18 months. In spite of the small sample size, we were able to detect ages of transition for

di�erent motor functions in the study on development of adaptive selection in typically developing

infants (Chapter 4). The very low attrition rate (<1% of assessments were missed) was very valuable

in this respect. But it should be kept in mind that the inclusion procedure may have introduced a

selection bias. The infants were recruited amongst colleagues and acquaintances of the researchers:

socio-economic status was relatively high, neurological condition of the infants was remarkably

good and parents were highly motivated to participate which yielded the very low attrition rate. The

cross-sectional term group consisted of 116 infants who were recruited at several Well Child Centres

in a region were socio-economic living standards were relatively high as well. The percentage of

infants with signs of neonatal distress such as meconium staining (16%) or CTG abnormalities

(7.5%) was somewhat high, possibly because concerned parents of children with a history of minor

perinatal events have a stronger motivation to participate in developmental research.

The preterm group consisted of 59 infants who had been admitted to the neonatal intensive

care unit of the Beatrix Children’s Hospital of the University Medical Center in Groningen between

December 2003 and January 2005. Inclusion criteria were gestational age below 35 weeks, singleton

or twin, parents with appropriate understanding of the Dutch language and travel distance

between the child’s home and the hospital of <1 hour. Infants with severe congenital anomalies

101

7

General discussion

were excluded from the study. During the time interval mentioned above, 148 infants were eligible

for inclusion. Due to the limited capacity of our department for the intensive follow-up scheme,

there was a maximum number of infants that could be included per month for logistical reasons.

Therefore, not all of the eligible infants were approached for inclusion. By approaching parents at

random, 59 infants were eventually included. Unfortunately, it was not well recorded how many

parents of the eligible group actually were approached for the current study, how many refused

to participate and for which reasons. This may have introduced a non-response bias. Therefore,

we compared our sample with established reference groups of preterm infants to investigate

representativeness of the sample retrospectively29,30. We did �nd comparable gestational age, birth

weight, frequency of Apgar score at 5 minutes below 7 (15%) and the need for ventilatory support

(68%). Our preterm sample showed a relatively high percentage of infants small for gestational

age (34%) and Caesarean deliveries29,30. The latter could be due to the increased tendency over the

years to deliver very preterm infants by Caesarean section31. The high percentage of infants born

small for gestational age is common in tertiary referral centres, such as the NICU in the University

Medical Center (UMC) in Groningen. This is due to the preterm birth of intra-uterine growth retarded

children, in whom obstetrical interventions take place on the basis of fetal distress. For our study,

however, this may have induced selection of relatively more vulnerable children.

The preterm group had a lower socio-economic status than the term group, in accordance with

social disadvantage being considered a risk factor for preterm birth32. Attrition rate amongst the

preterm infants was higher than in the longitudinal term group, but still very acceptable (5% of

assessments were missed compared to <1% of assessments for the term group). All in all, strengths

of our study with respect to the study group were the mainly longitudinal character of the data and

the overall low attrition rate. Limitations were a possible selection bias of term infants with relatively

high socio-economic status and a fairly high percentage of small for gestational age preterm infants.

However, the study sample consisted of a heterogeneous group of infants, which is a valuable type

of sample when the study purpose is assessment of validity of a new instrument. We think that our

current study group does suit this goal, but should not be used e.g. to generate reference values for

IMP scores, because of a non-optimal recording of non-response in the preterm group and therefore

a possible bias.

Assessments

An important limitation of the study is that the assessors were not blinded to group allocation

with respect to term or preterm status of the infant. This was mostly for practically reasons, as

recruitment of infants, scheduling appointments and performing the assessments was for the

larger part done by KRH, with help of colleagues and master students. Even so, if assessors would

have been blinded to term or preterm status, group allocation could have become obvious to them

because of the characteristic appearance of preterm infants6. Still, as so many infants were enrolled

in the study, assessors were not aware of details on clinical and developmental history. During the

102

Chapter 7

scheduled assessment, a video-recording was made of spontaneous motor behaviour and an age-

speci�c neurological examination5-7 was carried out. IMP and AIMS were scored on the basis of the

video-recording in di!erent sessions, a long time after the data collection and the large part of

AIMS assessments were scored by master students (with adequate supervision). It is unlikely that

appraisal of the results of neurological examination, IMP and AIMS has mutually in"uenced each

other.

Future research

To date, the IMP has only been used in research settings. The results described in this thesis indicate

that the IMP is well able to discriminate between typically developing infants and infants at high

risk for developmental motor disorders. Predictive validity for neurological outcome at 18 months

was satisfactory in our study group. Due to these characteristics, addition of the IMP to clinical

follow-up of high-risk infants could be valuable. An important requirement for possible clinical

application of the IMP is the generation of norm-scores at di!erent ages in a large, representative

cohort of typically developing infants without relevant pre, peri and neonatal risk factors. Another

requirement is a precise description of all IMP items with corresponding de�nitions, which is also

indispensable for future training courses.

Some issues that need to be addressed in further research were already mentioned in the

earlier sections of this chapter. Two other interesting research topics are described below. First, it

would be of interest to investigate application of the IMP in other groups of infants with a high risk

for developmental motor problems, for example infants with term asphyxia or infants born late

preterm (gestational age between 34 and 36 weeks33). The last group is especially at risk for minor,

more subtle motor problems, which could possibly be detected already at young age with the IMP.

It would also be appealing to study how the IMP performs in other children with an atypical course

of motor development, e.g. children with inborn errors of metabolism34 or children with Prader-Willi

syndrome with related hypotonia35, and to investigate whether IMP scores in infancy can predict

future neurological and developmental outcome.

Second, it would be interesting to unravel the relation of IMP scores with (neonatal) brain

imaging. In the current thesis, the relation of IMP scores with results of neonatal brain ultrasounds

was examined, and we found that serious brain pathology on cranial ultrasound, such as cystic

periventricular leukomalacia (PVL36) or intraventricular haemorrhage (IVH37) grade III or IV was

clearly associated with lower IMP scores throughout infancy. Debate exists on whether magnetic

resonance imaging (MRI) is superior with respect to prediction of future developmental outcome

compared to neonatal cranial ultrasound scanning38. In a large study, abnormal �ndings on

magnetic resonance imaging (MRI) at term age were found to be strong predictors of adverse

neurodevelopmental outcome at two years of age39. Besides identifying di!use white matter injury,

which is common in very preterm infants and clearly associated with impaired motor outcome,

MRI is also able to detect speci�c abnormalities, for example abnormal myelination of the posterior

103

7

General discussion

limb of the internal capsule (PLIC), that are associated with impaired motor development38. Much

research on the relation between term MRI abnormalities and developmental outcome is still in

progress. It would be very interesting to use the IMP as a follow-up tool in this �eld, as we expect

that the IMP will not only be able to detect infants at high risk for major developmental disorders

such as CP, but could possibly also detect infants with minor developmental motor problems. Future

studies should investigate whether speci�c types of MRI abnormalities are associated with lower

IMP scores, especially lower scores on the variation domain. Low scores on the variation domain

might be a re�ection of impaired cerebral connectivity38, but further research is de�nitely needed

to elucidate this issue.

Concluding remarks

This thesis presents the Infant Motor Pro�le (IMP), a recently developed qualitative assessment of

motor behaviour for infants aged 3 to 18 months. Its psychometric properties including reliability,

construct validity, concurrent validity and predictive validity were investigated. With respect to

the three purposes for which the IMP was developed (chapter 6,), we can conclude that the IMP

is well able to discriminate between typically developing infants and infants with high risk for

developmental motor disorders. The ability of the IMP to evaluate motor function over time should

be further explored by applying the method in intervention studies. Prediction of developmental

motor outcome at an early age will always remain di!cult, since change is one of the main

characteristics of the developing nervous system. In our study population, predictive validity of the

IMP was satisfactory. Future studies should be directed at generating norm-scores for the IMP and

determining clinical applicability.

104

Chapter 7

REFERENCES1. 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.


3. Hadders-Algra M. Variation and variability: keywords in human motor development. Submitted forpublication.



6. Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological dysfunctionin infancy using the Touwen Infant Neurological Examination: strengths and limitations. Dev Med ChildNeurol, 2009, e-pub ahead of print.




10. Piper MC, Pinnell LE, Darrah J, Maguire T, Byrne PJ. Construction and validation of the Alberta Infant MotorScale (AIMS). Can J Public Health. 1992;83 Suppl 2:S46-50.

11. Almeida KM, Dutra MV, Mello RR, Reis AB, Martins PS. Concurrent validity and reliability of the AlbertaInfant Motor Scale in premature infants. J Pediatr (Rio J) 2008;84:442-8.

12. Bayley N. Manual for the Bayley Scales of Infant Development: Second Edition. San Antonio: ThePsychological Corporation; 1995.

13. Folio MR, Fewell RR. Peabody Developmental Motor Scales: Examiner’s Manual. 2nd ed. Texas: Pro-ED; 2000.

14. Kuban K, Adler I, Allred EN, Batton D, Bezinque S, Betz BW, Cavenagh E et al. Observer variability assessingUS scans of the preterm brain: the ELGAN study. Pediatr Radiol 2007;37:1201-8.

15. Hintz SR, Slovis T, Bulas D, Van Meurs KP, Perritt R, Stevenson DK, Poole WK, et al. Interobserver reliabilityand accuracy of cranial ultrasound scanning interpretation in premature infants. J Pediatr 2007;150:592-6.

16. Van Gijn J, Bonke B. Interpretation of plantar re�exes: biasing e�ect of other signs and symptoms. J NeurolNeurosurg Psychiatry 1977;40:787-9.

17. Weisglas-Kuperus N, Baerts W, Smrkovsky M, Sauer PJ. E�ects of biological and social factors on thecognitive development of very low birth weight children. Pediatrics 1993;92:658-65.

18. Roberts G, Howard K, Spittle AJ, Brown NC, Anderson PJ, Doyle LW. Rates of early intervention services invery preterm children with developmental disabilities at age 2 years. J Paediatr Child Health 2008;44:276-80.

19. American Psychiatric Association. Diagnosis and Statistical Manual of Mental Disorders. 4th edn, TextRevision. Washington, DC: American Psychiatric Association, 2000.

20. Blauw-Hospers CH, de Graaf-Peters VB, Dirks T, Bos AF, Hadders-Algra M. Does early intervention in infantsat high risk for a developmental motor disorder improve motor and cognitive development? NeurosciBiobehav Rev 2007;31:1201-12.

21. Hielkema T, Blauw-Hospers CH, Dirks T, Bos AF, Hadders-Algra M: Does the type of intervention matter formotor development in infants at high risk for a developmental disorder? Revalidata 2009;151: 29.

22. Campbell SK, Kolobe TH, Osten ET, Lenke M, Girolami GL. Construct validity of the test of infant motorperformance. Phys Ther. 1995;75:585-96.

105

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General discussion



25. Hadders-Algra M. Developmental coordination disorder: is clumsy motor behavior caused by a lesion ofthe brain at early age? Neural Plast 2003;10:39-50.

26. Hadders-Algra M. Two distinct forms of minor neurological dysfunction: perspectives emerging from areview of data of the Groningen Perinatal Project. Dev Med Child Neurol 2002;44:561-71.

27. Tieman BL, Palisano RJ, Sutlive AC. Assessment of motor development and function in preschool children.Ment Retard Dev Disabil Res Rev 2005;11:189-96.

28. Altman DG. Practical statistics for medical research. London: Chapman and Hall, p411-412, 1991.



31. Haque KN, Hayes AM, Ahmed Z, Wilde R, Fong CY. Caesarean or vaginal delivery for preterm very-low-birth weight (< or =1,250 g) infant: experience from a district general hospital in UK. Arch Gynecol Obstet.2008;277:207-12.

32. Zeka A, Melly SJ, Schwartz J. The e�ects of socioeconomic status and indices of physical environment onreduced birth weight and preterm births in Eastern Massachusetts. Environ Health. 2008;7:60.

33. Davido� MJ, Dias T, Damus K, Russell R, Bettegowda VR, Dolan S, Schwarz RH, Green NS, Petrini J. Changesin the gestational age distribution among U.S. singleton births: impact on rates of late preterm birth, 1992to 2002. Semin Perinatol 2006;30:8-15.

34. Bruggink JL, van Spronsen FJ, Wijnberg-Williams BJ, Bos AF. Pilot use of the early motor repertoire in infantswith inborn errors of metabolism: outcomes in early and middle childhood. Early Hum Dev 2009;85:461-5.

35. Festen DA, Wevers M, Lindgren AC, Böhm B, Otten BJ, Wit JM, Duivenvoorden HJ, Hokken-Koelega AC.Mental and motor development before and during growth hormone treatment in infants and toddlerswith Prader-Willi syndrome. Clin Endocrinol 2008;68:919-25.



38. Hintz SR, O’Shea M. Neuroimaging and neurodevelopmental outcomes in preterm infants. Semin Perinatol2008;32:11-9.

39. Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE. Neonatal MRI to predict neurodevelopmentaloutcomes in preterm infants. N Engl J Med 2006;355:685-94.

107

Summary

108108

Summary

This thesis presents the Infant Motor Pro�le (IMP), a video-based qualitative assessment of motor

behaviour of infants between 3 and 18 months. The IMP was developed for three purposes:

discrimination between typically developing infants and infants with high risk for developmental

motor disorders, evaluation of motor function over time and prediction of developmental motor

outcome. The IMP is based on the Neuronal Group Selection Theory (NGST) which states that motor

development is characterised by exploration of the primary variable motor repertoire and selection

of adaptive motor strategies out of this repertoire. The IMP consists of 80 items that are grouped into

�ve domains: size of the repertoire (variation), adaptive selection (variability), movement �uency,

movement symmetry and motor performance.

Chapter 2 describes a systematic review of available methods to evaluate neuromotor function

in infancy and their psychometric properties. This review forms the background against which

the Infant Motor Pro�le was developed. We found that instruments that assess quality of motor

behavior or motor patterns, such as the General Movement method (GM) and the Test of Infant

Motor Performance (TIMP), have the best predictive validity for major and minor developmental

motor disorders. However, these methods are only applicable until the age of four months.

Chapter 3 presents the pilot study on the IMP with a description of the instrument and the �rst

data on reliability and validity. Concurrent validity of the IMP with the Alberta Infant Motor Scale

(AIMS) and with Touwen Infant Neurological Examination (TINE) was assessed in a heterogeneous

study group of low-risk term born and high-risk preterm born infants. Intra and interobserver

reliability of the IMP were satisfactory. Concurrent validity of the IMP with the AIMS was good.

The IMP was able to di!erentiate between infants with normal neurological condition, minor

neurological dysfunction and abnormal neurological condition.

In chapter 4, development of adaptive motor behaviour in typically developing infants is

investigated with the NGST as theoretical background. According to the NGST, infants learn to select

adaptive motor strategies out of their motor repertoire during motor development. This study

explored the ages at which clinically observable transition to adaptive motility emerged for four

speci�c motor functions: abdominal progression, sitting motility, reaching, and grasping in a group

of typically developing infants. In addition, reliability of observation of the presence of adaptive

motor behaviour was investigated. Results indicated that transition to adaptive motor behaviour

could be observed reliably. Clinically observable transitions to adaptive selection started to emerge

from six months onwards and peaked between eight and 15 months. Transitions developed

gradually and occurred at speci�c ages for di!erent motor functions. Comparison of our results to

literature showed that changes measured by neurophysiologic methods precede clinically observed

transitions.

The study described in chapter 5 investigates construct validity of the IMP, operationalized

as the relation of IMP scores throughout infancy with pre-, peri- and neonatal variables, including

the presence of brain pathology on neonatal ultrasound scans. In order to do so, a longitudinal

prospective study was performed in a mixed group of term born and preterm infants. Socio-

109109

Summary

economic and perinatal data were collected, which included for preterm infants information

on periventricular leukomalacia and intraventricular haemorrhage based on neonatal cranial

ultrasounds. Data were analyzed by �tting mixed e�ects models. In the total group of infants

gestational age, socio-economic status and 5-minute Apgar score were signi�cant determinants of

IMP scores throughout infancy. In the subgroup of preterms, IMP scores were signi�cantly a�ected

by brain lesions on neonatal ultrasound and socio-economic status. These �ndings support the

construct validity of the Infant Motor Pro�le: IMP scores were clearly associated with relevant

determinants of neuromotor function.

In chapter 6 reliability, concurrent validity of the IMP with the AIMS and withTINE and predictive

validity for neurological outcome at 18 months are assessed. A longitudinal prospective study was

performed in a heterogeneous group of term born and preterm infants. For the concurrent validity

part of the study, a second group of term infants was added with cross-sectional assessments. Inter-

observer reliability was high. Correlations between IMP and AIMS scores varied across IMP domains;

they were highest for the performance domain of the IMP. A clear relationship was found between

total IMP score and neurological condition. Sensitivity and speci�city for prediction of abnormal

neurological outcome at 18 months were satisfactory in the study sample.

With respect to the three purposes for which the IMP was developed, we can conclude that the

IMP is well able to discriminate between typically developing infants and infants with high risk for

developmental motor disorders. The ability of the IMP to evaluate motor function over time should

be further explored by applying the method in intervention studies. Prediction of developmental

motor outcome at an early age will always remain di!cult, since change is one of the main

characteristics of the developing nervous system. In our study population, predictive validity of the

IMP was satisfactory. Future studies should be directed at generating norm-scores for the IMP and

determining clinical applicability.

111

Appendices

112112

Appendix I

APPENDIX I: SUMMARY ON THE DOMAINS AND ITEMS OF THE INFANT MOTOR PROFILE

The Infant Motor Pro�le consists of �ve domains. The items and scoring methods of each domain

are listed below. IMP scores are calculated for each of the �ve domains according to the following

formula:

Sum of item scores

Score = * 100%

(number of items of domain – number of items not assessed) * maximum score of items

Items are not assessed when a certain motor behaviour is not observed (e.g. the item ‘variation of

arm movements during walking’ is not assessed when a child is not able to walk). ‘Maximum score

of items’ is the maximum score among the items of the domain. For the domains variation-size of

repertoire, variability-ability to select and �uency the maximum score for each item is 2 and for the

domain symmetry the maximum score is 3. Because the performance domain contains items with

di�erent numbers of maximum scores, scores are weighted before computing the performance

domain score. The total IMP score is computed by summing the scores on the �ve domains and

dividing this number by 5. All scores on the domains and the total IMP score are expressed as a

percentage, with a maximum score of 100%.

Domain 1: Variation – size of repertoire

Scoring for variation-items is as follows:

1. Insu!cient variation.

2. Su!cient variation.

Items of this domain:

1) Variation of head movements (Sup)

2 ) Posture, presence of ATNR (Sup) P/F N/Oa

3) Posture, presence of hyperextension of neck and trunk (Sup) P/F N/O

4) Variation of arm movements (Sup)

5) Variation of �nger movements (Sup)

6) Variation of leg movements (Sup)

7) Variation of toe movements (Sup)

8) Variation of reaching or prereaching movements of the arms (Sup)

9) Variation of hand motility during reaching, grasping and manipulation(Sup)

10) Variation of head movements (P)

11) Variation of pre-crawling movements of the legs (P)

12) Variation of wriggling, pivoting or crawling (P)

13) Variation in sitting motility (Sit)

14) Variation in sitting up behaviour (Sit)

15) Bottom shu"ing (Sit) P/F N/Oa

16) Variation in standing up behaviour (S&W)

113113

Appendix I

17) Variation of arm movements (S&W)

18) Variation of trunk movements (S&W)

19) Variation of leg movements (S&W)

20) Variation of placing of feet (S&W)

21) Variation of prereaching or reaching movements of the arms(RGM)

22) Variation of hand motility during reaching and grasping (RGM)

23) Facial expression (Gen)

24) Drooling (Gen) M Nb

25) Presence of stereotyped tongue protrusion (Gen) Yes No

Exceptions to the standard scoring are denoted in the second and third column: a P/F = persistent or

frequent, N/O = no or occasionally, b M = marked drooling, N = no or little drooling

Domain 2: Variability – ability to select

All items of this domain are scored as follows:

1. No selection.

2. Adaptive selection.


1) Variability of head movements: ability to make an adaptive selection (Sup)

2) Variability of reaching or prereaching movements of the arms: ability to make an adaptive

selection (Sup)

3) Variability of hand motility during reaching, grasping and manipulation: ability to make an

adaptive selection (Sup)

4) Variability of head movements: ability to make an adaptive selection (P)

5) Variability of wriggling, pivoting or crawling: ability to make an adaptive selection (P)

6) Variability in sitting motility: ability to make an adaptive selection (Sit)

7) Variability in sitting up behaviour: ability to make an adaptive selection (Sit)

8) Variability in standing up behaviour: ability to make an adaptive selection (S&W)

9) Variability of arm movements: ability to make an adaptive selection (S&W)

10) Variability of trunk movements: ability to make an adaptive selection (S&W)

11) Variability of leg movements: ability to make an adaptive selection (S&W)

12) Variability of placing of feet: ability to make an adaptive selection (S&W)

13) Variability of prereaching or reaching movements of the arms: ability to make an adaptive

selection (RGM)

14) Variability of hand motility during reaching and grasping: ability to make an adaptive selection

(RGM)

15) Facial expression: ability to make an adaptive selection (Gen)

114114

Appendix I

Domain 3: Symmetry

All items of this domain are scored as:

1. Strong asymmetry.

2. Moderate asymmetry.

3. No or mild asymmetry.


1) Position of head (Sup)

2) Reaching, grasping and manipulation of objects (Sup)

3) Position of head (P)

4) Arm posture and motility during activity in prone (P)

5) Position of head during sitting (Sit)

6) Position of trunk during sitting or supported sitting (Sit)

7) Arm posture and motility during sitting or supported sitting (Sit)

8) Arm posture and motility during independent walking (S&W)

9) Leg posture and motility during independent walking (S&W)

10) Reaching, grasping and manipulation of objects (RGM)

Domain 4: Fluency

All !uency items of this domain are scored as:

1. Majority of movements non-!uent.

2. Majority of movements !uent.

All items with presence or absence of tremor are scored as:

1. Frequently tremor present.

2. No or occasionally tremor present.


1) Tremor during reaching or prereaching (Sup)

2) Fluency of motor behaviour in supine (Sup)

3) Fluency of motility during independent walking (S&W)

4) Tremor during reaching or prereaching (RGM)

5) Fluency of motility during reaching or prereaching (RGM)

6) Tremor (Gen)

7) Fluency of motor behaviour (Gen)

115115

Appendix I

Domain 5: Performance

Performance items are not scored in a standard fashion, but are adapted to the speci�c motor

function and range from two to seven options.


1) Control of head movements (Sup)

2) Manipulative behaviour of hands and �ngers (Sup)

3) Tilting of pelvis (Sup)

4) Rolling from supine to prone (Sup)

5) Reaching, grasping and manipulation of objects (Sup)

6) Head lift in prone (P)

7) Functional ability of shoulder girdle (P)

8) Functional ability of hands (P)

9) Rolling from prone to supine (P)

10) Progression in prone: development of crawling (P)

11) Control of head movements (Sit)

12) Sitting ability (Sit)

13) Position of trunk, preference posture (Sit)

14) Need of arm support (Sit)

15) Sitting up (Sit)

16) Standing ability (S&W)

17) Standing up (S&W)

18) Walking (S&W)

19) Balance during independent walking (S&W)

20) Arm posture and motility (S&W)

21) Heel-toe gait (S&W)

22) Reaching, grasping and manipulation of objects (RGM)

23) Type of grasping (RGM)

Sup = supine, P = prone, Sit = sitting, S&W = standing and walking, RGM = reaching, grasping and

manipulation, Gen = general

116116

Appendix II

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essm

ent

(sho

rtna

me)

Cons

truc

tval

idit

yCo

ncur

rent

valid

ity

Pred

icti

veva

lidit

yfo

rCP

orm

inor

deve

lopm

enta

ldi

sord

ers

(e.g

.DCD

,MN

D)

HINE

Goo

dco

rrel

atio

nw

ith�n

ding

son

MRI

scan

50+

nda

Dat

aon

74PT

infa

nts,

asse

ssm

enta

tCA

6-15

mo;

53FT

infa

nts

with

hypo

xic-

isch

emic

ence

phal

opat

hy,

asse

ssm

enta

tage

9-14

mo;

24in

fant

sw

ithcy

stic

PVL,

asse

ssm

enta

tCA

6-9,

5m

o:go

odpr

edic

tion

oflo

com

otor

func

tion

atag

e2

yrs.

and

4yr

s.50-5

2

+

PRP

Theo

retic

alas

sum

ptio

n:se

lect

edpr

imiti

vere

!exe

sar

ere

late

dto

onse

tof

mot

orfu

nctio

nin

norm

alan

dbr

ain-

dam

aged

child

ren;

assu

mpt

ion

notv

alid

ated

.N

ore

latio

nbe

twee

npr

imiti

vere

!exe

san

dm

otor

deve

lopm

entw

asfo

und53

-G

roup

of16

5TD

child

ren:

noco

rrel

atio

nbe

twee

nA

IMS

and

PRP-

scor

eat

ages

6w

ks.,

3m

oan

d5

mo53

-nd

a

Infanib

Clea

rdi"

eren

ces

insc

ores

once

rtai

nne

urom

otor

cate

gorie

sbe

twee

nhe

alth

yFT

and

PTan

dill

PTin

fant

s54

+nd

a20

9PT

LBW

infa

nts:

spec

i�ci

tyof

mot

orev

alua

tion

with

Infa

nib

at7

mo

rega

rdin

gCP

atag

e36

mo

isun

satis

fact

ory,

norm

alne

urom

otor

asse

ssm

enta

t7m

ois

high

lypr

edic

tive

ofsu

bseq

uent

norm

alm

otor

func

tion

(spe

ci�c

ity10

0%(1

11/1

11))55

±

BSID-II

Cons

truc

tsm

ore

di"e

rent

iate

dw

ithag

e29

±G

roup

of44

TDan

dlo

w-r

isk

PTin

fant

s,as

sess

men

tat1

2,15

and

18m

o,co

ncur

rent

valid

ityw

ithPe

abod

ygr

oss

mot

orsc

ores

:r=

.78

tor=

.96

and

with

Peab

ody

�ne

mot

orsc

ores

:r=

.25

tor=

.5756

±nd

a

118118

Appendix II

Ass

essm

ent

(sho

rtna

me)

Cons

truc

tval

idit

yCo

ncur

rent

valid

ity

Pred

icti

veva

lidit

yfo

rCP

orm

inor

deve

lopm

enta

ldi

sord

ers

(e.g

.DCD

,MN

D)

PDMS-II

Subt

ests

core

sco

rrel

ate

with

age56

±G

roup

of44

TDan

dlo

w-r

isk

PTin

fant

s,as

sess

men

tat1

2,15

and

18m

o,co

ncur

rent

valid

ityw

ithBS

ID-II

ofgr

oss

mot

orsc

ores

:r=

.78

tor=

.96

and

of�n

em

otor

scor

es:r

=.2

5to

r=.5

756

±44

FTan

dlo

wris

kPT

infa

nts,

PDM

Sat

12m

o:pr

edic

tion

ofsc

ores

onBS

IDm

otor

scal

esat

18m

or=

.54

(PT)

and

r=.5

6(F

T),P

DM

Sat

15m

o:r=

.59

(FT)

and

r=.6

6(P

T)56

±

MAI

nda

nda

246

high

-ris

kin

fant

sM

AI4

mo,

corr

elat

ion

with

Bayl

eym

otor

scal

eat

age

2yr

sr=

-0.3

7(p

<0.0

01),

75PT

infa

nts

MA

Iat4

mo

CAse

nsiti

vity

and

spec

i�ci

tyfo

rdev

elop

men

talo

utco

me

at18

mo

resp

.61%

(14/

23)a

nd83

%(4

3/52

)57-6

2

77hi

ghris

kin

fant

s,M

AIa

t4m

oan

dgr

oss

and

�ne

mot

orev

alua

tions

(PD

MS

and

Fros

tigEy

eM

otor

Coor

dina

tion

subt

est)

at4,

5yr

s:Sp

earm

an’s

rho

resp

.-0.

12(n

.s.)a

nd-0

.23

(p≤0

.05)

60

±

NBI

Clea

rdis

tinct

ion

insc

ores

betw

een

FTan

dPT

infa

nts54

,63

+nd

and

a

TIME

Child

ren

with

mot

orde

lays

di"e

rfr

omch

ildre

nw

ithou

tdel

ays

inse

quen

ces

ofm

ovem

ents

whe

nas

sess

edfr

omse

vera

lsta

rtin

gpo

sitio

ns64

±nd

and

a

119119

Appendix II

Ass

essm

ent

(sho

rtna

me)

Cons

truc

tval

idit

yCo

ncur

rent

valid

ity

Pred

icti

veva

lidit

yfo

rCP

orm

inor

deve

lopm

enta

ldi

sord

ers

(e.g

.DCD

,MN

D)

AIMS

Ata

ge8

mos

.cle

ardi

�ere

ntia

tion

betw

een

neur

olog

ical

lyno

rmal

,su

spec

tora

bnor

mal

infa

nts65

±12

0TD

and

68de

laye

din

fant

s,co

ncur

rent

valid

ityw

ithBS

IDm

otor

scal

e:r=

.97

and

.93;

with

PDM

Sgr

oss

mot

orsc

ale:

r=.9

9an

dr=

.9566

++17

3hi

gh-r

isk

infa

nts,

pred

ictiv

eva

lidity

ofA

IMS-

scor

eat

4m

ofo

r18

mo

neur

olog

ical

outc

ome:

PPV

=40

%(s

ensi

tivity

77%

,spe

ci�c

ity82

%)

AIM

S-sc

ore

at8

mo:

PPV

=66

%(s

ensi

tivity

87%

,sp

eci�

city

93%

)66

±

SOMP-I

Clea

rdi�

eren

ces

inqu

ality

ofm

otor

perf

orm

ance

betw

een

FTan

dPT

infa

nts68

+nd

and

a

TIMP

TIM

Psc

ores

are

sens

itive

toch

ange

sin

infa

nts’

mot

orpe

rfor

man

cedu

eto

mat

urat

ion

and

med

ical

com

plic

atio

ns37

Goo

ddi

scrim

inat

ion

betw

een

TDin

fant

s,in

fant

sw

ithCP

and

infa

nts

with

deve

lopm

enta

ldel

ay70

+A

sses

smen

tat3

mos

.,TIM

Pid

enti�

ed80

%of

the

sam

ein

fant

sas

the

AIM

S72

+96

infa

nts,

TDan

dhi

gh-r

isk,

pred

ictiv

eva

lidity

ofTI

MP-

scor

eat

3m

ofo

rthe

AIM

S-sc

ore

at12

mo

r=

.5572

61TD

and

risk-

infa

nts,

pred

ictiv

eva

lidity

ofTI

MP-

scor

eat

3m

ofo

rPD

MS-

IIat

4-5

yrs.

r=.6

9,PP

V=

92%

(sen

sitiv

ity62

%,

spec

i�ci

ty97

%)71

+

120120

Appendix II

Ass

essm

ent

(sho

rtna

me)

Cons

truc

tval

idit

yCo

ncur

rent

valid

ity

Pred

icti

veva

lidit

yfo

rCP

orm

inor

deve

lopm

enta

ldi

sord

ers

(e.g

.DCD

,MN

D)

GMs

Pres

ence

ofab

norm

alG

Msi

slin

ked

todi

scer

nabl

ele

sion

sof

the

brai

n40an

dpr

e-,p

eri-

and

neon

atal

adve

rsiti

essu

chas

PTbi

rth

and

IUG

R41

,74

++M

ixed

grou

pof

80hi

ghan

dlo

wris

kin

fant

s,as

sess

men

tsat

0-4

mo,

conc

urre

ntva

lidity

with

neur

olog

ical

exam

inat

ion:

Spea

rman

rho’

s0.

32-0

.5541

58FT

infa

nts

with

HIE

and

66PT

:agr

eem

entb

etw

een

GM

and

neur

olog

ical

exam

inat

ions

80%

75,7

6

+52

low

and

high

risk

infa

nts,

GM

-ass

essm

enta

t2-4

mo,

neur

olog

ical

follo

w-u

pat

4to

9ye

ars:

abno

rmal

GM

sat

�dge

tyag

eha

vese

nsiti

vity

ford

evel

opm

ent

ofCP

88%

(7/8

)and

spec

i�ci

ty10

0%41

,mild

lyab

norm

alG

Ms

are

rela

ted

tode

velo

pmen

tof

MN

D,A

DH

Dan

dag

gres

sive

beha

viou

rat4

-9yr

s(s

peci

�city

58%

)41an

dne

urol

ogic

alco

nditi

on(n

orm

al,s

impl

eM

ND

and

com

plex

MN

D)a

t9-1

2yr

s(r

ho0.

46,p

<0.0

1)78

130

FTan

dPT

infa

nts,

GM

asse

ssm

enta

t6-2

0w

ks,

neur

olog

ical

outc

ome

at2

yrs:

sens

itivi

tyfo

rCP

98%

(43/

44),

spec

i�ci

ty96

%(6

7/70

)40,7

7

+

BSID

=Ba

yley

Scal

esof

Infa

ntD

evel

opm

ent,

CP=

cere

bral

pals

y,H

IE=

hypo

xic

isch

emic

ence

phal

opat

hy,I

UG

R=

intr

aut

erin

egr

owth

reta

rdat

ion,

MN

D=

min

orne

urol

ogic

aldy

sfun

ctio

n,m

o=

mon

th(s

),nd

a=

noda

taav

aila

ble,

PDM

S=

Peab

ody

Dev

elop

men

talM

otor

Scal

e,PP

V=

posi

tive

pred

ictiv

eva

lue,

PVF

=pe

riven

tric

ular

�arin

g,PV

L=

periv

entr

icul

arle

ukom

alac

ia,T

D=

typi

cally

deve

lopi

ng,V

LBW

=ve

rylo

wbi

rth

wei

ght,

yrs.

=ye

ars,

++=

very

good

,+=

good

,±=

mod

erat

e,-=

poor

121121

Appendix II

APPENDIX IIB: EXTENDED VERSION OF TABLE IIIB (CHAPTER 2): RELIABILITY OF THE TESTS

Assessment Intra-observer agreement Interobserver agreement

Touwen nda nda

Amiel-Tison nda Only data available on passive muscle toneitems: reliability excellent to poor for variousmanoeuvres20:

Muscle power nda nda

HINE nda Correlation coe!cient close to 122: ++

PRP nda Agreement 72 to 95%24: +

Infanib nda nda

BSID-II nda r = 0.75 (motor), r = 0.96 (mental)29: +

PDMS-II nda r = 0.9631: ++

MAI Kappa: 10% of items excellentreliability, 42% fair to good, 48%poor reliability61:

Overall score: r = 0.7262 item reliability: kappa: 2%of items excellent reliability, 58% fair to good, 40%poor reliability61:

NBI nda nda

TIME nda r = 0.88 – 0.9964: ++

AIMS r > .9967: ++ r > .9967: ++

SOMP-I Agreement 62%69: Agreement 80%69: +

TIMP nda Agreement 95%73: +

GMs Kappa 0.841,74: ++ Kappa 0.8 – 0.940,41,74: ++

nda = no data available, r = Spearman’s rho

122122

Appendix III

APPENDIX III: INFANT MOTOR PROFILE

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Appendix III

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129

Nederlandse samenvatting

130130


De Infant Motor Pro�le (IMP) is een nieuw meetinstrument voor een kwalitatieve beoordeling van de

motoriek van zuigelingen van 3 tot en met 18 maanden. De IMP werd ontwikkeld met de volgende

drie doelstellingen: onderscheid maken tussen zuigelingen met een hoog risico op motorische

ontwikkelingsproblemen en zuigelingen met een normale motorische ontwikkeling, het evalueren

van motorische functies in de tijd en het voorspellen van motorische ontwikkelingsproblemen. De

IMP is gebaseerd op de Neuronale Groep Selectie Theorie die stelt dat motorische ontwikkeling

gekenmerkt wordt door exploratie van het primaire variabele motorische repertoire gevolgd door

de fase waarin het kind adaptieve motorische strategieën leert kiezen uit het repertoire. De IMP

bestaat uit 80 items die zijn gegroepeerd in 5 domeinen: bewegingsvariatie, vermogen tot selectie

van adaptieve motorische strategieën, vloeiendheid, symmetrie en motorische prestaties. De items

worden beoordeeld aan de hand van een video-opname.

In hoofdstuk 2 wordt een overzicht gepresenteerd van de bestaande methoden voor het

beoordelen van neuromotorische conditie op de zuigelingenleeftijd en de psychometrische

eigenschappen van deze methoden. Dit overzichtsartikel vormde de achtergrond waartegen

de Infant Motor Pro�le werd ontwikkeld. Het bleek dat meetinstrumenten die zich richten op

kwalitatieve aspecten van motoriek, zoals de General Movement methode (GM) en de Test of Infant

Motor Performance (TIMP) de beste voorspellende waarde hebben voor zowel lichte als ernstige

motorische ontwikkelingsproblemen op latere leeftijd. Deze bestaande methoden zijn echter

slechts toepasbaar tot de leeftijd van 4 maanden.

Hoofdstuk 3 bevat de pilot studie over de IMP met een beschrijving van de methode en de

eerste data over betrouwbaarheid en validiteit. Hiervoor werd de IMP toegepast in een heterogene

onderzoekspopulatie van op tijd en te vroeg geboren zuigelingen in de leeftijd van 3 tot en met

18 maanden. Intra- en inter-beoordelaarsbetrouwbaarheid bleken goed te zijn. De soortgenoot

validiteit met de Alberta Infant Motor Scale (AIMS) was goed. Er was een duidelijke relatie tussen

IMP scores en neurologische conditie, beoordeeld met behulp van het neurologisch onderzoek

volgens Touwen.

In hoofdstuk 4 wordt, met als theoretische achtergrond de Neuronale Groep Selectie Theorie,

een studie beschreven die gericht was op het vaststellen van de leeftijd waarop gezonde zuigelingen

het vermogen tot selecteren van adaptieve bewegingsstrategieën ontwikkelen. Er werd gekeken

naar vier speci�eke motorische functies: kruipen, zitten, reiken en grijpen. Ook werd onderzocht of

de deze beoordeling van de aanwezigheid van het selecteren van adaptieve bewegingsstrategieën

betrouwbaar gedaan kon worden. Dit bleek inderdaad het geval. Vanaf de leeftijd van 6 maanden

ontwikkelden zuigelingen het vermogen tot selectie, met een piek tussen de leeftijd van 8 en 15

maanden. Deze transities traden geleidelijk op op functiespeci�eke momenten. Toen we onze

resultaten vergeleken met resultaten in de literatuur van neurofysiologisch onderzoek, bleek dat

deze laatste in de tijd voorafgaan aan klinisch geobserveerde transities.

Hoofdstuk 5 gaat over de construct validiteit van de IMP. Construct validiteit was in deze

studie geoperationaliseerd als de relatie van IMP scores met belangrijke pre-, peri- en neonatale

131131


risicofactoren voor het ontwikkelen van motorische problemen. Om de construct validiteit te

onderzoeken werd een longitudinale, prospectieve studie in een groep op tijd en te vroeg geboren

zuigelingen uitgevoerd. Perinatale data, waaronder gegevens van neonatale schedelecho’s

in termen van intraventriculaire bloedingen en periventriculaire leukomalacie, en gegevens

over de sociaaleconomische situatie werden verzameld en hiermee werden statistische mixed

e�ects modellen gemaakt. In de totale groep zuigelingen bleken de IMP scores het sterkst te

worden beïnvloed door zwangerschapsduur, sociaaleconomische status en de Apgar score na 5

minuten. In de subgroep van de te vroeg geboren kinderen was de aanwezigheid van duidelijke

afwijkingen op de neonatale schedelecho’s de belangrijkste beïnvloedende factor, gevolgd door

sociaaleconomische status. Deze bevindingen ondersteunen de construct validiteit van de IMP: IMP

scores waren duidelijk gerelateerd aan belangrijke risicofactoren voor het optreden van motorische

ontwikkelingsproblemen.

Hoofdstuk 6 is gericht op de betrouwbaarheid, de soortgenoot validiteit met de AIMS en

het neurologisch onderzoek volgens Touwen en de predictieve validiteit van de IMP. Hiervoor

werd een prospectieve, longitudinale studie verricht in een heterogene groep van op tijd en te

vroeg geboren zuigelingen. Voor het deel van het onderzoek gericht op de soortgenoot validiteit

werd een groep op tijd geboren zuigelingen met cross-sectionele beoordelingen toegevoegd. De

inter-beoordelaarsbetrouwbaarheid bleek goed te zijn. De soortgenoot validiteit met de Alberta

Infant Motor Scale was het beste voor de domeinen motorische prestaties en bewegingsvariatie.

Er was een duidelijke relatie tussen IMP scores en neurologische conditie. De predictieve validiteit

van de IMP op de leeftijd van 4 tot en met 12 maanden voor het voorspellen van een afwijkende

neurologische conditie op de leeftijd van 18 maanden bleek redelijk goed te zijn.

Met betrekking tot de drie doelen waarvoor de IMP werd ontwikkeld, kunnen we stellen dat

de IMP goed in staat is om onderscheid te maken tussen zuigelingen met een goede motorische

ontwikkeling en zuigelingen met een hoog risico op motorische ontwikkelingsproblemen. Of

de IMP in staat is om de ontwikkeling van motorische functies in de tijd te evalueren, moet

verder onderzocht worden door de IMP toe te passen in interventiestudies. Het op jonge leeftijd

voorspellen van de motorische uitkomst zal altijd moeilijk blijven, aangezien het zich ontwikkelende

zenuwstelsel veranderlijk is. In onze onderzoekspopulatie was de predictieve validiteit van de IMP

redelijk goed. Vervolgonderzoek dient gericht te zijn op het genereren van normscores en op het

onderzoeken van de klinische toepasbaarheid van de IMP.

133

Dankwoord

134

Dankwoord

Dankwoord

De afgelopen jaren heb ik met veel plezier gewerkt aan mijn promotieonderzoek. Dit is voor een

belangrijk deel te danken aan de mensen die ik hieronder wil noemen.

Allereerst wil ik mijn eerste promotor prof. dr. M. Hadders-Algra bedanken. Beste Mijna, ik

herinner me nog goed dat ik bij je langs kwam om te praten over de mogelijkheden voor een

afstudeeronderzoek. Ik weet nog steeds niet waardoor het precies kwam, maar ik was meteen

geboeid door de ontwikkelingsneurologie en de manier waarop jij erover sprak. Ik ging naar huis

met twee artikelen van jou over de NGST en was meteen verkocht: hier wilde ik mee aan de slag!

Van deze keus heb ik nooit spijt gekregen en dat is grotendeels aan jou te danken. Ik heb veel

bewondering voor jou als wetenschapper: voor je originele ideeën, voor de manier waarop je die

overbrengt en voor je enorme doorzettingsvermogen en gedrevenheid. Ik heb ontzettend veel van

je geleerd en je hebt me steeds op een geschikte manier begeleid bij alle stappen op het pad van de

wetenschap. Het moet voor jou niet ideaal geweest zijn dat ik altijd meerdere dingen tegelijk deed,

eerst tijdens mijn MDPhD-traject en later tijdens het combineren van de opleiding neurologie met

mijn promotieonderzoek. Bedankt dat je me hiervoor de ruimte hebt gegeven. Daarnaast waardeer

ik je persoonlijke betrokkenheid en heb ik bewondering voor de manier waarop je in het leven staat.

Prof. dr. A.F. Bos, beste Arie, als tweede promotor was je voor mij het aanspreekpunt voor alle vragen

betre�ende de neonatologie. Toen ik net begon met mijn onderzoek heb je me rondgeleid over

de NICU en nog steeds ben ik, net als toen, iedere keer als ik daar kom weer onder de indruk van

de complexiteit van jullie vak. Ik ben je zeer dankbaar voor het gedetailleerde beoordelen van de

artikelen en je kritische, klinische blik daarbij.

De leescommissie bestaande uit prof. dr. L.S. de Vries, prof. dr. O.F. Brouwer en prof. dr. J.G. Becher wil

ik bedanken voor het beoordelen van dit proefschrift.

Dr. V. Fidler en dr. S. la Bastide-van Gemert van de afdeling Epidemiologie van het UMCG, beste

Vaclav en Sacha, bedankt voor jullie mooie statistische analyses uit hoofdstuk 5 en de geduldige

uitleg daarbij.

Beste collega’s van de ontwikkelingsneurologie: Cornill Blauw-Hospers, Hylco Bouwstra, Tineke

Dirks, Saskia van Goor, Victorine de Graaf-Peters, Tjitske Hielkema, Corina de Jong, Marjolein

Jongbloed-Pereboom, Hedwig Kikkert en Lieke Peters, een aantal van jullie heeft geholpen met

het �lmen van baby’s die soms in een afgelegen pittoresk Fries dorpje bleken te wonen. Veel dank

daarvoor. Maar vooral bedankt voor de leuke gesprekken over wetenschap en andere zaken en jullie

interesse in het onderzoek.

Loes de Weerd, secretaresse van de afdeling ontwikkelingsneurologie, heel veel dank voor je hulp

en ondersteuning bij duizend-en-één klussen die in de loop van het onderzoek voorbij kwamen.

Michiel Schrier, bedankt voor de mooie lay-out van het IMP scoreformulier en je technische

135

Dankwoord

ondersteuning.

In de loop van de jaren heeft een aantal studenten geneeskunde en bewegingswetenschappen in

het kader van hun afstudeeronderzoek meegewerkt aan het IMP-onderzoek. Nicole Arink, Dineke

Dijkhuizen, Lieke Eidhof, Emilie Groen en Anne Hoekstra: dank voor jullie hulp bij het werven, �lmen

en onderzoeken van de baby’s en vooral bedankt voor jullie vaak actieve meedenken. Ik heb veel

geleerd van jullie kritische vragen!

De Junior Scienti�c Masterclass wil ik bedanken voor de mogelijkheid om dit onderzoek in de vorm

van een MDPhD-traject uit te voeren.

Sta�eden en AIOS van de afdeling neurologie in het UMCG, �jn dat ik bij en met jullie mag werken.

Alle ouders en hun kinderen wil ik bedanken voor de deelname aan dit toch behoorlijk intensieve

follow-up onderzoek. Het is niet makkelijk om een kind te krijgen dat te vroeg geboren is, en ik vind

het dan ook extra bewonderenswaardig dat ouders de moeite wilden nemen om mee te doen.

Het was bijzonder en leuk om hun kinderen te zien opgroeien van baby’s tot pratende peuters van

anderhalf jaar.

Karin Middelburg en Layla Ben-Zvi, wat �jn dat jullie mijn paranimfen willen zijn.

Lieve Karin, je begon als nieuwe collega op de ontwikkelingsneurologie en werd al gauw een

vriendin. Bedankt voor al je hulp bij het �lmen van de baby’s als ik met de co-schappen bezig was

(je moest er voor je eigen onderzoek ook al zo veel…). Maar vooral dank voor je gezelligheid en de

vele winkel- en horeca-uitjes.

Lieve Layla, jij bent een enorm betrokken vriendin die altijd klaar staat met praktische adviezen.

Geweldig dat je zo gezellig om de hoek woont! Misschien moeten we weer eens wat meer gaan

dansen…

Familieleden en vrienden, ook al waren jullie niet betrokken bij de totstandkoming van dit

proefschrift, ik wil jullie toch niet overslaan, want voor allerlei andere leuke en gezellige dingen zijn

jullie heel belangrijk voor mij.

Lieve papa en David, wat hebben wij veel dokters in de familie… Gelukkig kan ik jullie over de

ontwikkelingsneurologie nog wel eens wat nieuws vertellen. Ik vind het �jn dat jullie er zijn.

Van mama heb ik de liefde voor het omgaan met kinderen en hun ouders meegekregen. Zij schreef

haar proefschrift op een bloknootje, op een bankje in de speeltuin waar wij speelden. Ze was erg

geïnteresseerd in mijn onderzoek en is zelfs een keer mee geweest om baby’s te �lmen. Wat jammer

dat ze niet meer bij de afronding van mijn proefschrift kan zijn.

Lieve Cyril, met mijn proefschrift heb je weinig te maken, maar met mij des te meer! Ik ben enorm

blij dat jij er bent en dat we samen van alle grote en kleine dingen in het leven kunnen genieten.

137

Curriculum vitae

139

CURRICULUM VITAE

Kirsten Heineman werd op 13 november 1978 geboren na een zwangerschapsduur van 31+1

weken met een geboortegewicht van 2030 gram. Zij volgde gymnasium klas 1 tot en met 5 aan het

Bernardinuscollege te Heerlen en behaalde in 1997 cum laude haar eindexamen aan het Willem

Lodewijk Gymnasium te Groningen. In 1998 behaalde ze cum laude de propedeuse Pedagogische

Wetenschappen aan de Rijksuniversiteit Groningen. Daarna begon ze met de bovenbouwstudie

Bewegingswetenschappen aan de RUG. In 1999 werd ze ingeloot voor Geneeskunde. In 2004

rondde ze de studie Bewegingswetenschappen af met een afstudeeronderzoek bij de afdeling

Ontwikkelingsneurologie in het Universitair Medisch Centrum Groningen. In datzelfde jaar startte

ze met een MDPhD-traject bij de afdeling Ontwikkelingsneurologie, waarbij ze de coschappen

combineerde met haar promotieonderzoek. Ze deed haar keuzecoschap bij de afdeling

Kinderneurologie in het UMCG en behaalde haar artsexamen in 2007. In december 2007 begon ze

met de opleiding tot neuroloog in het UMCG met als huidige opleider prof. dr. H.P.H. Kremer.

141

List of publications

143

LIST OF PUBLICATIONS

• Heineman KR, La Bastide-van Gemert S, Fidler V, Middelburg KJ, Bos AF, Hadders-Algra M.

Construct validity of the Infant Motor Pro�le: relation with prenatal, perinatal, and neonatal

risk factors. Dev Med Child Neurol 2010, epub ahead of print.

• Heineman KR, Middelburg KJ, Hadders-Algra M. Development of adaptive motor behaviour in

typically developing infants. Acta Paediatr 2010;99:618-24.

• Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological

dysfunction in infancy using the Touwen Infant Neurological Examination: strengths and

limitations. Dev Med Child Neurol 2010;52:87-92.

• Heineman KR, Hadders-Algra M. Evaluation of neuromotor function in infancy-A systematic

review of available methods. J Dev Behav Pediatr 2008;29:315-23.

• Heineman KR, Bos AF, Hadders-Algra M. The Infant Motor Pro�le: a standardized and qualitative

method to assess motor behaviour in infancy. Dev Med Child Neurol 2008;50:275-82.

• Stevens M, Lemmink KAMP, De Jong J, Heineman K. Het e�ect van het GALM-

introductieprogramma op het dagelijkse energieverbruik van senioren van 55 - 65 jaar.

Geneeskunde en Sport 2003;6:170-5.

university of groningen the infant motor profile heineman, … · 2016-03-06 · in the neuronal...

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