Review

A systematic review of the clinimetric properties of neuromotor assessments for preterm infants during the first year of life
Alicia J Spittle* MSc BPhysio, Victorian Infant Brain Studies; Lex W Doyle MD FRACP , Department of Obstetrics and Gynecology, University of Melbourne; Roslyn N Boyd PhD MSc (Physiotherapy) BAppSc BSc Pgrad (Biomechanics), Victorian Infant Brain Studies, Murdoch Childrens Research Institute, Melbourne, Australia. *Correspondence to first author at Victorian Infant Brain Studies, Murdoch Childrens Research Institute, 2nd Floor, Royal Childrens Hospital, Flemington Road, Parkville, Melbourne, Australia 3052. E-mail: alicia.spittle@rch.org.au DOI: 10.1111/j.1469-8749.2008.02025.x Published online 8th January 2008 This systematic review evaluates assessments used to discriminate, predict, or evaluate the motor development of preterm infants during the first year of life. Eighteen assessments were identified; nine met the inclusion criteria. The Alberta Infant Motor Scale (AIMS), Bayley Scale of Infant and Toddler Development Version III, Peabody Developmental Motor Scales Version 2, Test of Infant Motor Performance (TIMP), and Toddler and Infant Motor Examination have good discriminative validity when examined in large populations. The AIMS, Prechtls Assessment of General Movements (GMs), Neuro Sensory Motor Development Assessment (NSMDA), and TIMP were designed for preterm infants and are able to detect more subtle changes in movement quality. The best predictive assessment tools are age dependent: GMs, the Movement Assessment of Infants, and TIMP are strongest in early infancy (age 4mo or less) and the AIMS and NSMDA are better at older ages (812mo). The TIMP is the only tool that has demonstrated a difference between groups in response to intervention in two randomized controlled trials. The AIMS, TIMP, and GMs demonstrated the highest levels of overall reliability (interrater and intrarater intraclass correlation coefficient or >0.85). Selection of motor assessment tools during the first year of life for infants born preterm will depend on the intended purpose of their use for discrimination, prediction, and/or evaluation.

See end of paper for list of abbreviations.

With survival rates of preterm and low-birthweight infants improving, there is an increase in the number of these infants with motor impairments later in life, ranging from developmental coordination disorder to cerebral palsy (CP).1 In 2006, the American Academy of Pediatrics published guidelines for the follow-up of preterm infants and recommended that all children with a very low birthweight (birthweight <1500g) should have a structured, age-appropriate neuromotor examination at least twice during the first year of life.2 Infant neuromotor examinations are performed for a variety of purposes, including discriminating between infants who have motor dysfunction and those who are developing typically (discriminative tool), predicting which infants will have future motor problems from current performance (predictive tool), and evaluating changes over time (evaluative tool).3 There is a growing body of evidence that the first year of an infants life is a critical period of brain development.4 The process of neuronal differentiation, which includes the formation of dendrites and axons, and the production of neurotransmitters and synapses, is particularly active in the few months before and after term.5 Myelination begins during the second trimester and is most rapid in the first year of life, and the process continues up to 30 years of age.4 It is, therefore, important that infants with motor dysfunction are identified early so that appropriate interventions can be implemented. Early neuromotor assessments can be challenging because motor development in the first year of life is rapid and extensive and is influenced by biological, environmental, and social factors.6 Repeated assessments may reveal widely different

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scores that represent random variation in performance across testing sessions, rather than real change in performance.7

Furthermore, preterm infants have been shown to have different motor trajectories from those of infants born at term,

Table I: Characteristics of infant motor assessments

Assessment tool (y) AIMS (1994) BSITD-III (2005) GMs (2004) MAI (1980) movement NSMDA (1989) Primary purpose Discriminative Other purposes Predictive, evaluative Predictive, evaluative Evaluative Age range 018mo Type of test Norm Normative sample 2202 infants from Alberta, Canada 1700 infants from USA NA Domains tested Gross motor Components tested

Weight bearing, posture, and antigravity movement Gross motor and fine motor tasks

Discriminative

142mo

Norm

Gross motor, fine motor Gross motor

Discriminative, predictive Discriminative

Preterm birth to 4mo 012mo

Criterion

Spontaneous movement and neurological integrity Muscle tone, reflexes, automatic reactions, and volitional

Predictive, evaluative

Criterion

NA

Gross motor, fine motor

Discriminative, predictive

Evaluative

1mo6y

Criterion

NA

Gross motor, fine motor

Gross motor, fine motor, neurological, primitive reflexes, postural reactions, and motor responses to sensory input Reflexes, stationary, locomotion, object manipulation, grasping, and visual motor integration Posture and fine motor control and function Observation of movement and elicited items to assess postural control and function

PDMS-2 (2000)

Discriminative, predictive, evaluative Discriminative Evaluative

05y

Norm

2003 infants from USA and Canada

Gross motor, fine motor

PFMAI (2000) TIMP (2005)

212mo

Criterion

NA

Gross motor, fine motor Gross motor

Discriminative, evaluative

Predictive

32wks PMA to 4mo

Norm

990 infants at risk of poor neurological outcome from USA

TIME Discriminative, (1994) evaluative social/emotional abilities, functional performance,

442mo

Norm

731 typically Gross motor, Mobility, stability, motor developing and fine motor organization, and 144 motor-delayed children from USA and atypical movement

AIMS, Alberta Infant Motor Scale;15 BSITD-III, Bayley Scales of Infant and Toddler Development Version III;37 GMs, General Movements Assessment;23 MAI, Movement Assessment of Infants;38 NSDMA, Neuro Sensory Motor Development Assessment;24 PDMS-2, Peabody Developmental Motor Scale Version 2;25 PFMAI, Posture and Fine Motor Assessment of Infants;26 TIMP , Test of Infant Motor Performance;39 TIME, Toddler and Infant Motor Examination;28 PMA, post-menstrual age; NA, not applicable.

Table II: Excluded infant motor assessments

Reason excluded Neonatal developmental assessment Assessment tool Dubowitz Neurological Assessment of the Preterm and Full-term Newborn Infant40 Neonatal Intensive Care Unit Network Neurobehavioral Scale41 Revised Gesell Developmental Schedules42 Griffith General Cognitive Index,43,Denver II44 Pediatric Evaluation of Disability Inventory45 Battelle Developmental Inventory46 Neurological assessment Manual not published Infant Neurological International Battery47 Structured Observation of Motor Performance48

Infant developmental assessment

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which may result in the motor development of preterm infants incorrectly being labeled as abnormal.8 These variations in motor development over the first year can be for a variety of reasons, including behaviours learned during long periods in neonatal intensive care and alterations to brain development caused by exposure to the ex utero environment during critical periods of brain development. This results in infants who have less flexed postures and are more extended than infants born at term.1 A standardized assessment tool appropriate for preterm infants that has a consistent set of

procedures for administering and scoring an assessment should, therefore, be used to ensure that all individuals are assessed under similar conditions. Longitudinal assessments, rather than a single assessment, are more predictive because they give information on developmental progression including monitoring peaks, plateaux, and, in some cases, regression of infants.9,10 For this reason, it is important to ensure that assessment tools can be used at more than one time point in the infants development. The major types of standardized test are norm-referenced

Table III: Clinical utility of included infant assessment tools

Assessment tool AIMS Time to administer (min) 1030 Test procedure Manual/equipment

Observation of infant in prone, supine, sitting, and standing

Comprehensive manual and score sheets (US $80) No special equipment

BSITD-III

2060

Therapist administers items in standardized procedure

Comprehensive manual/kit (US $300) Test kit provides most equipment

GMs

1030

Infants spontaneous movements with no stimulation are filmed and scoring completed from videotape

Comprehensive manual with DVD (US $80) Special equipment (video)

MAI

3060

Therapist observes and administers items Therapist observes and administers items

Manual No special equipment Basic manual (US $20) Specific toys required but easily accessible

NSMDA

1030

PDMS-2

3060

Therapist administers items in standardized procedure

Comprehensive manual/test kit (US $945) Test kit provides most equipment

PFMAI

2530

Therapist administers elicited items in standardized procedure

Manual (US $63) No special equipment

TIMP

2040

Therapist observes infant and then administers elicited items in standardized procedure

Comprehensive manual/test (US $60) Test provides equipment

TIME

1555

Therapist observes infant and parent/caregiver is used to encourage movement

Comprehensive manual/test kit (US $417) Test kit provides most equipment

AIMS, Alberta Infant Motor Scale;15 BSITD-III, Bayley Scales of Infant and Toddler Development Version III;37 GMs, General Movements Assessment;23 MAI, Movement Assessment of Infants;38 NSDMA, Neuro Sensory Motor Development Assessment;24 PDMS-2, Peabody Developmental Motor Scale Version 2;25 PFMAI, Posture and Fine Motor Assessment of Infants;26 TIMP , Test of Infant Motor Performance;39 TIME, Toddler and Infant Motor Examination.28

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and criterion-referenced measures.11 Norm-referenced tests measure the performance of a person in relation to a specific population. Raw scores from these tests are meaningless by themselves and need to be compared with a population. When using norm-referenced assessments it is important to consider the characteristics of the reference population, as motor development may vary across different social and ethnic populations.12 Criterion-referenced tests have criteria or a minimum competence that must be reached to score an item or pass the test. The criterion test contrasts the childs

performance with the test content rather than a population. Some tests are referenced both by norm and by criterion. Infant motor examinations vary with the age of the child and the theoretical construct of the assessment tool.13 Some assessment tools involve observation of the infants movement repertoire with minimal or no handling, whereas others include neurological examination (assessment of reflexes, muscle tone, postural reactions). Traditionally, motor assessments are based on the neuromaturational framework, which assumes that the rate and sequence of motor development

Table III: continued

Training Scoring Interpretation of scores

Not required

4 subscales prone (21 items), supine (9 items), sitting (12 items), and standing (16 items). Score given to all observed items within window and all items below the window

Raw scores Centile ranks Age equivalent Growth scores Raw scores Composite scores Centile ranks Age equivalent Growth scores Individual developmental trajectory Optimality score

Required unless psychologist (2d course)

Motor scale gross (72 items) and fine motor (66 items) subscales. Binary score for each item with reverse and discontinue rules

Required (45d training with GMs Trust)

Movements classified as normal or abnormal (poor repertoire, cramped synchronized or chaotic) from preterm up to 6wks. During fidgety period from 9 to 20wks movement classified as present, abnormal, or absent Scores development as normal, minimal problems, or specific problems. Risk profiles for 4 and 8mo Criteria given for items in 6 subscales: gross motor, fine motor, neurological, postural control, primitive movement patterns, and sensory motor. Items scored as abnormal, suspicious, normal for age Criteria given for items in 6 subscales: reflexes (8 items), stationary (30 items), locomotion (89 items), object manipulation (24 items), grasping (26 items), visualmotor integration (72 items) PFMAI-I (06mo): 18 posture and 21 fine motor items, PFMAI-II (612mo): 13 posture and 17 fine motor items

Not required

Raw scores Risk scores Raw scores Age equivalents Functional scores

Not required

Not required

Raw scores Age equivalents Centile ranks Standard scores for subtests Raw scores Classification of infants motor development as typical, at-risk, or delayed Raw scores Age equivalent scores Centile ranks Growth scores Raw scores Scaled scores Age equivalent scores Centile ranks Growth scores

Not required

Instructional DVD available for selfeducation

42 items: 13 dichotomous observed items and 29 elicited items on 47-level rating scale

Not required

Subtests include mobility, motor organization, stability, functional performance, and social/emotional abilities. Scoring differs for subtests

Review 257

are invariant and that the acquisition of motor skills reflects the hierarchical order of the central nervous system.14 The environment is considered to have little impact on the performance of motor tasks in this framework.15 More recently, assessment tools have been developed that use alternative theories of motor development such as the dynamic systems theory, in which the development of motor skills is considered to emerge through the interaction of multiple subsystems and is dependent on the context of the task.14 Assessments that incorporate dynamic systems theory measure functional capacity and consider the environmental influences to support the infants best performance. The theoretical framework should be considered when choosing an assessment because it will influence the conclusions that can be made from the results. There have been several reviews of newborn examinations and preschool assessments; however, to our knowledge there have been no recent systematic reviews of the clinimetric properties of infant motor assessment tools.16,17 The aim of this review was to systematically identify and evaluate standardized assessments that are used to discriminate, predict, or evaluate the motor development of preterm infants within the first year of life. For the purpose of this review, motor dysfunction or delay will be referred to as atypical development rather than abnormal development because the latter term is ambiguous and does not always equate to abnormal motor function at a later age.8 Method
SEARCH STRATEGY

A comprehensive search was undertaken of computerized databases including Medline Advanced (1966 to February 2007), CINAHL (1982 to February 2007), PsycINFO (1966 to February 2007), and EMBASE (1988 to February 2007). The search strategy included the MeSH terms and text words for (premature infant OR low-birthweight infant) AND (outcome assessment OR psychomotor performance OR psychomotor disorders OR cerebral palsy OR developmental coordination disorder OR movement disorders OR motor skill disorders). After this search, additional searches were performed using the names of each identified assessment tool and their authors .
INCLUSION CRITERIA

Assessment tools were included if they met all of the following criteria: (1) discriminative, predictive, or evaluative of motor development up to 12 months of age, corrected for prematurity; (2) appropriate for use with preterm infants (less than 37 weeks gestational age); (3) standardized assessment procedure; and (4) criterion-referenced or norm-referenced test.
EXCLUSION CRITERIA

Assessment tools were excluded if they met any of the following criteria: (1) not published in English; (2) did not primarily assess motor development (examination tools and developmental assessments for newborn infants were excluded from this review, because motor development is only one component of these assessments and other comprehensive reviews have been completed); and (3) primarily intended for screening.
DATA EXTRACTION

Two authors (AS, RB) then reviewed one key paper for each measure, selected on the basis that adequate detail was provided for the determination of inclusion. Assessments were included after agreement by both raters, and conflicting viewpoints were discussed until consensus was reached. A modified version of the Outcome Measures Rating Form18 was used to collect information on the characteristics, clinical utility, and psychometric properties of the included assessment tools. Characteristics of the assessment tools that were documented included the primary purpose of the tool, whether it was discriminative, predictive, or evaluative, and age range for use, standardization samples, and domains tested.17,19 Psychometric properties included information on the validity and reliability of the assessment tools. Validity is the extent to which an assessment is measuring what it is intended to measure.20 There are several different aspects to validity, including content, construct, criterion and discriminative validity, and responsiveness.3,20,21 Content validity refers to the extent to which measurement covers all the important aspects or domains it is supposed to measure and is usually dependent on a panel of experts and literature reviews.11 Construct validity is considered when there are no criteria against which to evaluate the measure; instead the measure is compared with current theories and models of the construct. Criterion validity examines the agreement between the assessment tool and a gold standard tool used to evaluate the same construct. Criterion validity is usually divided into concurrent validity (correlation between the measurement tool and an alternative, equivalent measurement used at the same time) and predictive validity (accuracy of a measurement tool to predict future outcome, such as CP), depending on whether the criteria refer to current or future assessment. Evaluative validity or responsiveness refers to the ability of an evaluative measure to detect minimal clinically important change over time.19 Sensitivity refers to the ability for a test to detect someone with a condition (e.g. motor delay) when it is present. Specificity refers to the ability of a test to correctly identify those infants without a condition (e.g. normal motor development).19 Reliability describes the extent to which a test is dependable, stable, and consistent when repeated under identical conditions.21 Testretest reliability refers to the relative stability of the assessment over time. Intrarater reliability is a component of testretest reliability because it assesses the degree to which an assessment yields similar results when the same rater scores the examination at different times in the absence of growth or interventions. Interrater reliability assesses the degree to which an assessment yields similar results for the same individual at the same time with more than one rater. Internal consistency is defined as the extent to which the items of a test work together to measure a specific variable.20 Appropriate statistics for measuring inter- and intrarater reliability are intraclass correlation coefficient (ICC) or , not percentage of agreement between raters or Pearsons correlation.21 Studies in which only the percentage of agreement was reported were excluded. Measures of 0.80 or above were considered excellent, 0.6 to 0.79 as adequate, and less than 0.60 as poor for reported ICC and statistics.18 Results Eighteen motor assessment tools were identified by the search strategy, of which nine met all the predefined inclusion criteria

The titles and abstracts were screened by the first author.

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on further examination. The nine included studies are the Alberta Infant Motor Scale (AIMS),15 Bayley Scale of Infant and Table IV: Evidence of content, construct, and concurrent validity
Assessment tool AIMS Content

Toddler Development Version III (BSITD-III),22 Prechtls Assessment of General Movements (GMs),23 Movement

Construct Multidimensional scaling, item response theory and Guttman scaling15 Scores increase with age49 Rasch analysis demonstrated items ordered by increasing difficulty50 Preterm infants have lower scores than term infants12 Discriminates between normal, suspect, and abnormal development (n=60)51 Factor analysis22 Scores increase with age Children with cerebral palsy and high risk of motor problems have lower mean scores than controls Theory supported by ultrasound studies23 Discriminates between infants with cerebral lesions and controls (n=22)53 Discriminates between normal and abnormal movements in term and preterm infants (n=130)54 Discriminates between normal and abnormal development in preterm infants (n=35)38 Does not discriminate between normal and atypical development in healthy term infants (n=50)58 Factor analysis 60 Consistency of results over time24 Discriminates between normal and abnormal development (n=148)60 Preterm infants with IUGR score lower than normal-birthweight preterm infants (n=198)61 Factor analysis25 Sensitive to age-related change Infants with disabilities score lower than infants with no motor problems (n=65) Rasch analysis26 Sensitive to age-related change Discriminates between term and preterm infants Rasch analysis39 Sensitive to age-related change63 Infants with medical risk factors score lower than peers Discriminates between infants with low and high risk of motor problems63

Concurrent Typically developing infants (n=103) 013mo: BSID-II r=0.97 013mo: PDMS r=0.99 At-risk infants (n=68) 013mo: BSID-II r=0.93 013mo: PDMS r=0.9515 Preterm infants (n=41) 6mo: BSID-II r=0.78 12mo: BSID-II r=0.9052 Typically developing infants (n=102) 142mo: BSID-II r=0.6022 Typically developing infants (n=81) 242mo: PDMS-2 Total Motor r=0.55

Literature review15 Expert panel Mailout to 291 members of Canadian Physiotherapy Association Pilot study to test feasibility

BSITD-III

Literature review22 Expert panel Pilot, national try-out, and standardization studies

GMs

Experts in field23

Term infants with HIE (n=58) 04mo: neurological exam %agree=788355 Preterm infants (n=66) 04mo: neurological exam %agree=8056 Preterm and term infants (n=246) 4mo: BSID r=0.6359

MAI

Literature review57 Risk scores based on at risk infants57

NSMDA

Literature review24 Developed by experts in field

Low-birthweight infants (n=148) 24mo: No significant difference between NSDMA and paediatricians classification 2=0.0860

PDMS-2

Literature review25 Hierarchical sequence

Typically developing infants (n=30) 111mo: PDMS-1 Gross Motor r=0.84, Fine Motor r=0.9025

PFMAI

Based upon literature26 Criterion-referenced cut-off scores based on term infants (n=185) Expert panel39 Literature review Elicited items occurred during caregiver interactions62 Pilot studies and revision of content

Typically developing infants (n=32) 26mo: PDMS Gross Motor r=0.83, Fine Motor r=0.6726

TIMP

Term and preterm infants (n=90) 3mo: AIMS r=0.6464

BSID, Bayley Scales of Infant Development Version I;65 BSID-II, Bayley Scales of Infant Development Version II;66 %agree, percentage agreement; HIE, hypoxicischemic encephalopathy; r, Pearsons correlation coefficient; Sens, sensitivity; Spec, specificity; IUGR, intrauterine growth retardation; AIMS, Alberta Infant Motor Scale;15 BSITD-III, Bayley Scales of Infant and Toddler Development Version III;37 GMs, General Movements Assessment;23 MAI, Movement Assessment of Infants;38 NSDMA, Neuro Sensory Motor Development Assessment;24 PDMS-2, , Test of Infant Motor Peabody Developmental Motor Scale Version 2;25 PFMAI, Posture and Fine Motor Assessment of Infants;26 TIMP Performance;39 TIME, Toddler and Infant Motor Examination.28

Review 259

Table IV: continued

Assessment tool TIME Content Literature review28 Expert panels 2 pilot and try-out studies Construct Factor analysis28 Sensitive to age-related change Rasch analysis Discriminates between children with and without motor delays Concurrent Typically developing (n=731) and delayed infants (n=153) 4m3.5y: physician/therapist classification of development (%) Mobility Scale Sens=94, Spec=86; Stability Scale Sens=91, Spec=90; Atypical Scale Sens=97, Spec=99

Table V: Evidence of predictive validity

Assessment tool AIMS Outcome assessment Sample characteristics Preterm and term infants (n=164) Preterm infants (n=41) Age at outcome 18mo Age at initial assessment 4mo (10th centile)a 8mo (5th centile)a 6mo Sensitivity (95% CI) 77.3b 86.4b Specificity (95% CI) 81.7b 93.0b 0.56 (BSID-II PDI) 59.1 (38.579.6) Correlation (Pearsons r)

Paediatrician classification of normal/suspicious (n=142) vs abnormal development (n=22)67 BSID-II PDI52

12mo

BSITD-III GMs

Cerebral palsy (n=19) or mental retardationc (n=2)10 Cerebral palsy or DQ<85)(n=60)54 Cerebral palsy or DQ<85(n=18)55 Cerebral palsy or DQ<85(n=31)56 Cerebral palsy or DQ<85(n=11)68

100 (NA)

Preterm infants 1236mo 2662wks PMA (n=29) Preterm and term infants (n=130) Term infants (n=58) Preterm infants (n=65) IUGR and term control (n=62) 24mo 4660wks PCA

0.95 (89.491.00)

0.96 (90.96100)

24mo 3842wks PCA 4347wks PCA 4856wks PCA 24mo 2837wks 3842wks 4365wks 24mo Term 4951wks PCA 5456wks PCA 38y 4mo (8 total risk score)a

0.94b 0.94b 0.94b 90.6b 100 (NA) 96.2100b 83.33 (62.241.00) 1.00d (NA) 1.00d (NA) 73.5 (58.788.4)

0.59b 0.86b 0.83b 57.6 b 64.5b 74.298.8b 80.00 (68.991.09) 1.00d (NA) 93.0d (84.91.00) 62.7 (53.971.4)

MAI

Cerebral palsy (n=34)69 Cerebral palsy or DQ <70 (n=27)32

Preterm and term infants (n=152) Preterm and term infants (n=160) Preterm and term infants (n=164)

Paediatrician classification normal/ suspicious (n=142) abnormal development (n=22)67 BSID PDI59

18mo 4mo (10 total risk score)a 8mo (10 total risk score)a 18mo 4mo (>9 total risk score)a 8mo (>9 total risk score)a 4mo

83.3 (68.498.4) 96.0 (88.8100) 72.7b 95.5b

78.2 (90.699.8) 64.5 (55.473.7) 93.0b 80.3b

0.67 (BSID PDI) 0.68 (BSID PDI)

BSID MDI70

Preterm and 1224mo term infants (n=246) Term infant at 24mo at social risk (n=134)

0.360.37 (BSID PDI)

4mo (>9 total risk score)a

0.63b

0.53b

aCut-off score for normal versus atypical motor development; bvalue cannot be calculated from published data; cUK usage: learning disability; dabnormal and absent fidgety movements were combined. DQ, Developmental Quotient; PDI, Psycho Motor Index; MDI, Mental Development Index; BOTMP , BruniniksOseretsky Test of Motor Proficiency; PDMS GMQ, Peabody Developmental Motor Scales Gross Motor Quotient; PMA, post-menstrual age; CA, corrected age; , no study identified; NA, not applicable; AIMS, Alberta Infant Motor Scale;15 BSITD-III, Bayley Scales of Infant and Toddler Development Version III;37 GMs, General Movements Assessment;23 MAI, Movement Assessment of Infants;38 NSDMA, Neuro Sensory Motor Development Assessment;24 PDMS-2, Peabody Developmental Motor Scale Version 2;25 PFMAI, Posture and Fine Motor Assessment of Infants;26 TIMP , Test of Infant Motor Performance;39 TIME, Toddler and Infant Motor Examination.28

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Assessment of Infants (MAI), Neuro Sensory Motor Development Assessment (NSMDA),24 Peabody Developmental Motor Scales Version 2 (PDMS-2),25 Posture and Fine Motor Assessment of Infants (PFMAI),26 Test of Infant Motor Performance (TIMP)27 and Toddler and Infant Motor Examination (TIME).28 The characteristics of all nine included assessments are summarized in Table I. Two neonatal assessments and seven infant assessments were excluded because they did not primarily measure motor development or had no published manual. The reasons for exclusion are listed in Table II.
CHARACTERISTICS OF INCLUDED STUDIES

but they can only be used up to approximately 4 months after term. Many of the other assessment tools are appropriate for use from 1 to 12 months of age, but their validity varies depending on the age of the infant at assessment.
CLINICAL UTILITY

All the assessment tools included discriminate the motor development of infants as being normal or atypical, with the AIMS, BSITD-III, PDMS-2, TIMP , and TIME comparing development with a norm-referenced group. The standardization samples for the norm-referenced tools consisted of infants born in the USA and/or Canada. The age ranges of the tests were variable; no assessment tool was able to assess a preterm infant from birth to 12 months after term. The TIMP and GMs are the only tools appropriate for use before term,

Clinical utility is summarized in Table III. The time to administer assessments varied both between assessments and within assessments depending on the age of the infant, with most assessments being longer as the infant grew older, with the exception of GMs. The shortest assessments were the AIMS and GMs; the BSITD-III, PDMS-2, and TIME were more complex and time-consuming. The AIMS and GMs assessments involve minimal handling in comparison with other assessments. The TIME involves interaction and handling by the primary caregiver, which may lead to a more accurate performance of the childs abilities. Most assessment tools can be used by a variety of health professionals; however, it is important for these professionals to have an understanding of preterm motor development and handling of infants, and, when appropriate, of test statistics. Some assessments require specific training, such as GMs and the BSITD-III,

Table V: continued
Assessment Outcome assessment tool NSMDA Paediatrician classification of development60 Sample characteristics Low-birthweight infants (n=148) Age at outcome 24mo Age at initial assessment 1mo (25% below average)a 4mo (25% below average)a 8mo (25% below average)a 12mo (25% below average)a 4mo (6th centile)a 8mo (6th centile)a Sensitivity (95% CI) 68.8b 80.0b 82.4b 58.8b Specificity (95% CI) 72.6b 56.9b 83.7b 93.3b Correlation (Pearsons r)

PDMS-2

Paediatrician classification of normal/suspicious (n=142) vs abnormal development (n=22)67

Preterm and term infants (n=164)

18mo

36.1b 91.7b

93.8b 52.3b

PFMAI TIMP AIMS scores below 5th centile (n=19 at 6mo, 14 at 9mo, and 12 at 12mo)71

Preterm and term infants (n=96)71

6mo

32wk PMA 4mo CA (z score 0.5SD)a

62.5 (43.181.9) (AIMS centile) 91.7 (76.0100) 4592 (b)

77.4 (67.087.8)

0.370.67

9mo 12mo centile) Motor delay on BOTMP (n=8)72 Gross motor delay (PDMS DQ>70) (n=12)73 Preterm and term infants (n=35)72 Preterm and term infants (n=61) 5.75y 32wks PMA 4mo CA (z score 1.6SD)a 45y 1mo (z score 0.5SD)a 2mo (z score 0.5SD)a 3mo (z score 0.5SD)a

75.7 (65.785.8)

0.200.56 (AIMS centile) 6878 (b) 0.320.55 (AIMS 100 (b) 0.36 (BOTMP score)

50.0 (15.685.7)

33 (1947) 50 (3565) 72 (5983)

94 (87100) 86 (7696) 91 (8399)

0.43 (PDMS GMQ) 0.42 (PDMS GMQ) 0.65 (PDMS GMQ)

TIME

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which require both time and expense.

VALIDITY

The primary purpose of the assessment tool needs to be considered when examining validity. Evidence of content, construct and concurrent validity is summarized in Table IV . All assessment tools had adequate content validity and construct validity. However, the the BSITD-III reports that infants born at less than 37 weeks gestational age do not score significantly lower than term infants on the gross motor scale, which may limit its use in detecting minimal motor problems with preterm infants. The concurrent validity of the AIMS, BSITD-III, GMs, MAI, NSMDA, PDMS-2, PFMAI, TIMP , and TIME has been reported in relation to

another motor assessment or paediatrician classification of normal or atypical development. The predictive validity of the assessment tools is summarized in Table V . The predictive validity is dependent on the age of assessment: GMs have the greatest combination of sensitivity and specificity in the first months of life, and the AIMS and NSDMA in the later months.
RESPONSIVENESS

All tools report that they are appropriate for assessing change over time or in response to intervention. However, there have been few validation studies. TIMP has been used in two randomized controlled trials of intervention and has demonstrated a significant difference between groups.29,30 The AIMS and GMs have also been used as outcome assessments in trials of

Table VI: Reliability of assessment tools

Assessment tool AIMS Testretest Intrarater Interrater Internal consistency (Cronbachs ) 018mo (n=unclear) r2 = 0.9949

018mo (n=210) ICC=0.9915

018mo (n=195) ICC=0.9915 318mo (n=45) ICC=0.980.9952

018mo (n=253) ICC=0.99715 318mo (n=41) ICC=0.970.9952 012mo (n=14) ICC=0.989974

BSITD-III

24m (n=50) FM r=0.67, GM r=0.77 913m (n=50) FM r=0.86, GM r=0.8622 NA

112mo norm. pop. (n=1700) FM r=0.770.89, GM r=0.8694 112mo atypical (n=688) FM r=0.900.92, GM r=0.930.96 NA

GMs

326wks (n=20) =1.0023

Term (n=30) =0.8475 020wks (n=19) =0.9276 020wks (n=27) =0.8477 020wks (n=16) =0.9178 4mo (n=53) r=0.7279 124mo (n=NR) r=0.8024 336mo (n=60) FMQ r=0.98, GMQ=0.97, TMQ=0.9625 45y (n=6) TMC ICC=0.91673 26mo (n=13) posture =0.97, FM=0.99 612mo (n=18) posture =0.98, FM=0.9626 Age not specified (n=21) ICC=0.9530 242mo (n=31) r=0.899928

MAI NSMDA PDMS-2

4mo (n=53) r=0.7679 211mo (n=20) FMQ r=0.73, GMQ r=0.84, TMQ r=0.8925

011mo FMQ =0.96, GMQ = 0.97, TMQ= 0.9825

PFMAI

06mo (n=59) posture scale=0.97, FM =0.9926 612mo (n=126) posture=0.95, FM =0.9626

TIMP

34wk PCA4mo (n=108) r=0.8980 441mo (n=33) r=0.960.9928

Age not specified (n=21) ICC=0.989930 441mo (n=33) r=0.960.9928 835mo (n=10) r=0.981.0081

TIME

06mo (n=NR) =0.799328 712mo (n=NR) =0.889728

PMA, post-menstrual age; NA, not applicable; ICC, intraclass correlation coefficient; FM, fine motor; GM, gross motor; TM, total motor; Q, quotient; , no study identified; NR, not reported; AIMS, Alberta Infant Motor Scale;15 BSITD-III, Bayley Scales of Infant and Toddler Development Version III;37 GMs, General Movements Assessment;23 MAI, Movement Assessment of Infants;38 NSDMA, Neuro Sensory Motor Development Assessment;24 PDMS-2, Peabody Developmental Motor Scale Version 2;25 PFMAI, Posture and Fine Motor Assessment of Infants;26 TIMP , Test of Infant Motor Performance;39 TIME, Toddler and Infant Motor Examination.28

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intervention; however, no difference was reported between groups.23,31 It is unclear from these studies whether the intervention was not effective or whether the tool was not sensitive enough to detect change.
RELIABILITY

Studies of the reliability of the assessment tools are summarized in Table VI. Studies of the BSITD-III, MAI, NSMDA, PDMS-2, and TIME reported correlations only (Pearsons r), which does not take into account systematic differences between assessors. The testretest reliability of the AIMS is reported to be excellent with the use of appropriate statistical methods. Intrarater reliability for the AIMS, GMs, and TIMP is excellent, as is the interrater reliability of the AIMS, GMs, MAI, and TIMP . Internal consistency has been studied with the AIMS, BSITD-III, PDMS-2, and PFMAI. Rasch analysis has been used to examine consistency of items for the TIMP . Discussion The nine assessment tools identified in this systematic review are all appropriate for measuring motor development of preterm infants, although each tool has its advantages and disadvantages. The most important step in identifying the best tool is for the clinician or researcher to identify the purpose of the assessment and then choose a test that has been validated as a discriminative, predictive, or evaluative tool. Many assessments report that they are appropriate to use for more than one purpose; however, they do not have the validity studies to support their claims. The clinical utility of assessment tools should be taken into account with the validity and reliability of the tool. Some tools such as GMs and the BSITD-III require standardized training and may be costly, although this may improve the reliability and validity of the assessments. This may be particularly important in research when one intervention is being compared with another. GMs have the best predictive validity for CP and are considered to be a quick, inexpensive, and nonintrusive assessment; however, the cost of initial training needs to be considered because the trainer may have to travel overseas to attend a course. Some clinicians may require an easily accessible tool that requires little training. The AIMS has the advantage of being easily administered in the clinical setting, which may make the instrument more feasible for therapists to use in follow-up clinics because of the minimal handling and time needed to conduct the assessment, while having strong correlation with the BSID-II and PDMS. Norm-referenced tools are useful for comparing an infants motor development with that of a large sample. Traditionally, these tools have examined the ability of an infant to achieve a task and compare the childs achievement with a large sample representative of a population. All the assessments in this review take into account the way in which the infant performs the task to varying degrees, and the tasks are both qualitative and quantitative in nature. However, some tools, such as the BSITD-III, are more quantitative and may not be sensitive enough to detect the subtle changes in quality of movement that are seen with preterm infants. These subtle changes in movement quality may lead to enhanced balance and coordination at later ages. Preterm infants have been shown to have different patterns of motor development from those of term infants, but the long-term implications of altered patterns of development are

not fully understood. This is demonstrated in the study by van Haastert and colleagues, in which preterm infants (gestational age <32wks) had significantly lower scores at all ages on the AIMS.12 Although these preterm infants do not have typical motor development, they have variation in motor development that may not necessarily be abnormal.8 For this reason, criterion-referenced tools designed specifically for preterm infants to discriminate between typical and atypical development or tools that have normative data for infants at risk of developmental problems may be more appropriate, depending on the purpose of assessment. GMs, the NSDMA, MAI, and PFMAI are all criterion-referenced tests which seek to discriminate between normal and abnormal motor development. The NSMDA has the advantage of discriminating between normal motor function and minimal, mild, moderate, and severe motor dysfunction. The PDMS-2, TIMP , and TIME have a larger than normal proportion of infants at risk of developmental problems in their normative samples. Although discriminative assessments are designed to classify current motor performance, knowledge of their predictive value and stability over time is useful in determining which infants require early intervention and informing caregivers of assessment results. Both the AIMS and MAI have shown that up to 30% of healthy term infants perform outside the cut-off for normal development at one point in time, despite having a normal outcome. Longitudinal assessments are recommended to improve the validity of assessments, because no assessment correctly identifies all children as having normal or atypical motor development with a single assessment. Multiple assessments are also recommended because infants with transient neuromotor abnormalities during the first year are at greater risk of developmental coordination disorders at school age.32 Variation in development over the first year of life is inherent in normal development, but it can make prediction difficult.33 Many assessment tools have improved predictive value as the child gets older, because children may be free from neurological signs of dysfunction at an early age but when the complexity of neurological function increases with age, deficits may become apparent.34 However, it may not be appropriate to wait, because intervention is thought to be most beneficial when begun as early as possible.6 The plasticity of the infants brain, particularly in the first years of life, can lead to changes in brain function and may explain why we can never predict outcome with 100% accuracy. The prediction of later problems early in life tends to be most effective for severe disabilities such as CP . More subtle developmental problems can be difficult to predict early in life because environmental, social, and biological interactions may have more of an influence on long-term outcome than for infants with more severe disabilities.35 For example, a preterm infant who has been in hospital for many months may have delayed motor development as a result of lack of experience to move in the hospital environment rather than as a result of a neurological deficit. The concurrent and predictive validities for some assessments were not measured with a criterion standard tool. Many studies used physicians judgments of developmental delay to establish validity, despite the greater accuracy of standardized assessment tools.36 However, it is not clear which motor assessment tool should be considered the criterion standard.

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It is important for outcome measurements to be sensitive to measure change; however, there is no consensus on how this should be assessed.21 Individual changes in the rate of motor development cannot necessarily indicate the success of intervention because change may be due to the natural history and variability of the rate of development of motor skills, and, therefore, large randomized controlled trials are needed in the research of interventions.7 One of the most important considerations when assessing the effects of interventions is whether the sample is large enough to allow a clinically important effect size to be detected. From a clinical viewpoint, individuals and organizations will need to decide what they consider to be acceptable levels of change when assessing an infants response to an intervention, and they should be encouraged to use multiple longitudinal assessments. Research on infant assessment tools has focused on discriminative and predictive validity, with limited evidence on the ability of the measurement tool to evaluate change. Future research should focus on validating assessment tools that document change so that the efficacy of intervention programmes in the first year of life can be evaluated. Many studies have looked only at the prediction of CP or of abnormal motor development up to 2 years of age, with very few studies looking at the long-term correlation with standardized motor assessments. Although long-term follow-up studies can be timely and costly, further studies are needed for preterm infants that correlate early motor assessments with later motor outcome at school age to improve our knowledge of what is a significant variation in motor development for a preterm infant. Conclusion Preterm infants develop differently from infants born at term. However, this does not mean that all preterm infants will have motor problems but rather that assessments appropriate for preterm infants are needed. There is no assessment tool that can take into account all the multiple variables that influence motor development, such as social, environment, and health factors. Norm-referenced tools can be useful to compare the infants development with other infants of the same age. The AIMS demonstrated the best psychometric properties and clinical utility of these tools. However, because preterm infants have different gross motor developmental trajectories on the AIMS from those of term infants in the first 18 months of life, it is useful to also have a criterion tool designed specifically for predicting abnormal motor development, such as the NSMDA or TIMP .12 GMs have the best combination of sensitivity and specificity for predicting CP in the early months, whereas the AIMS and NSMDA are the best predictors of atypical motor development in the later months. The TIMP is the only tool to demonstrate adequate evaluative validity, and along with the AIMS has demonstrated the best reliability. The TIMP and GMs are the only tools appropriate for use before term. In clinical practice, we would recommend using more than one assessment tool to meet the needs of an assessment. For example, in the period before term and in early infancy the use of both GMs and the TIMP , and for the period from 4 to 12 months corrected age the use of the AIMS and NSDMA, will ensure that one has appropriate predicative, discriminative, and evaluative assessments. Longitudinal motor assessments are recommended, to improve the predictive and discriminative validity.

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List of abbreviations
AIMS BSITD-III GMs MAI NSMDA PDMS-2 PFMAI TIME TIMP Alberta Infant Motor Scale Bayley Scale of Infant and Toddler Development Version III Prechtls Assessment of General Movements Movement Assessment of Infants Neuro Sensory Motor Development Assessment Peabody Developmental Motor Scales Version 2 Posture and Fine Motor Assessment of Infants Toddler and Infant Motor Examination Test of Infant Motor Performance

Pediatric Developmental Specialist in NeuroMotor Rehabilitation Glenrose Rehabilitation and Stollery Childrens Hospitals Department of Pediatrics, University of Alberta Edmonton, Alberta, Canada
The Section of Pediatric Neurosciences at the University of Alberta invites applications for the academic position in Pediatric Neuromotor Rehabilitation. The successful applicant would join a well-established Developmental Pediatrics Program with comprehensive inpatient and outpatient services for children with complex disabilities. The Department of Pediatrics at the Stollery Childrens and Glenrose Rehabilitation Hospitals, service a complete range of pediatric subspecialties and is the tertiary and quaternary childrens hospital for Northern Alberta, with a population base of over 1.5 million people. Pediatric Neurosciences offers a full range of sub-specialties, and is a particular focus for growth within the Department. Pediatric Physiatrists and Developmental Pediatricians within the division of Neurodevelopmental Pediatrics have strong affiliations, and active clinical and research collaborations with the Department of Physical Medicine and Rehabilitation, Pediatric Neurology, Pediatric Surgery, and the Faculty of Rehabilitation. Substantial infrastructure is currently available to the successful candidate through already established programs within the hospitals and outreaching to the community and schools. Research support is also available through a number of government, foundation and institutional resources, unique to the province of Alberta. These include the Glenrose and Stollery Hospital Foundations, the Alberta Heritage Foundation for Medical Research, the Women and Childrens Health Research Institute, the Integrated Centre for Care Advancement through Research, the Alberta Centre for Child, Family and Community Research. Full-time funded positions are available through the Department of Pediatrics and Child Health, within our current, very competitive, alternate funding program (AFP). Successful candidates will have a clear interest in an academic career with experience in the area of childhood neuromotor and developmental disabilities. Academic responsibilities include resident and medical student education, contributing to the development of the Division of Neurodevelopmental Pediatrics and participating in research activities. Candidates with either a clinical research or basic research background are encouraged to apply. This position is open to Pediatric Physiatrists, Developmental Pediatricians or specialists in rehabilitation medicine with expertise in the care of children. Alberta is the fastest growing province in Canada, with the most rapidly expanding birth rate in the country. It is the only province that is debt free and financially secure. The Department of Pediatrics, the Glenrose Rehabilitation Hospital and the Stollery Childrens Hospital have been rapidly expanding in the last 5 years and continue to recruit to programs of excellence in a host of areas, with the Pediatric Neurosciences a priority. The city of Edmonton has an excellent school system, beautiful river valley and friendly people. Close to mountains and lakes, the city offers numerous outdoor activities and a vibrant arts and cultural scene. Interested applicants should forward their curriculum vitae, along with a cover letter and the names and contact information of 3 references to: Jerome Y. Yager MD Professor and Head Section of Pediatric Neurosciences Department of Pediatrics University of Alberta Room 7317A Aberhart Centre One 11402 University Avenue NW Edmonton, Alberta, Canada, T6G 2J3 Email: jyager@ualberta.ca Fax: (780) 407-8283

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