What assessments evaluate use of hands in infants? A literature review

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1 DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY ORIGINAL ARTICLE What assessments evaluate use of hands in infants? A literature review LENA KRUMLINDE-SUNDHOLM LINDA EK ANN-CHRISTIN ELIASSON Department of Women s and Children s Health, Astrid Lindgren Children s Hospital, Karolinska Institutet, Stockholm, Sweden. Correspondence to Lena Krumlinde-Sundholm, Neuropediatric Unit, Department of Women s and Children s Health, Astrid Lindgren Children s Hospital Q2:07, Karolinska Institutet, Stockholm, Sweden. Lena.Krumlinde.Sundholm@ki.se PUBLICATION DATA Accepted for publication 5th September Published online ABBREVIATIONS BSID-III Bayley Scales of Infant and Toddler Development version III GRAB Grasping and Reaching Assessment of Brisbane HAI Hand Assessment for Infants IMP Infant Motor Profile MAI Movement Assessment of Infants PDMS-2 Peabody Developmental Motor Scales version 2 PFMAI Postural and Fine Motor Assessment of Infants TIME Toddler and Infant Motor Examination AIM To identify assessments, applicable to infants aged 3 months to 12 months, measuring hand function, and to discuss their usefulness in assessing infants at risk of developing unilateral cerebral palsy (CP). METHOD Instruments described in two previous systematic reviews were scrutinized for inclusion of fine motor components. Additionally, a new literature search was performed in Medline, PsychInfo, PubMed, and Cinahl ( ) to identify newly developed assessments of infant motor functioning. RESULTS Five assessments from the two previous systematic reviews included fine motor components but only three provided separate measures of fine motor performance: the Peabody Developmental Motor Scales version 2 (PDMS-2), the Bayley Scale of Infant and Toddler Development version III, and the Posture and Fine Motor Assessment of Infants, each of which provided measures of the preferred hand only. From 531 papers retrieved, 10 new assessments were found, three of which met our inclusion criteria: the Infant Motor Profile (IMP), the Grasping and Reaching Assessment of Brisbane (GRAB), and the Hand Assessment for Infants (HAI). Only the GRAB and the HAI provide measures relevant for assessing infants at risk of developing unilateral cerebral palsy; however, both measures are still under construction. INTERPRETATION currently available assessment for infants aged 3 to 12 months old measures aspects of hand function suitable for quantifying asymmetry between hands or quality of bimanual performance. Early infancy is a period of rapid motor development and is possibly the best period for therapeutic interventions addressing motor outcomes, owing to the period s great neural plasticity. 1,2 In infants developing unilateral cerebral palsy (CP), asymmetric segmental spontaneous upper limb movements can be observed as early as at 3 months of age after thorough video-based observation. 3 Commonly, the first signs of asymmetric hand use are noticed later during the first 6 months of life. The possibility of measuring the extent of this asymmetry at an early age could offer an important method for diagnosis, predicting outcome, following development, and evaluating early intervention approaches. To provide valid and reliable quantifications, appropriate assessment tools are essential. Many assessment tools developed for use with infants include fine motor components. The question at issue is whether currently available tests could be useful in measuring fine motor performance in infants at risk of developing unilateral CP. It is well known that fine motor performance is complex and influenced by many components. From the aim of finding appropriate tools from an integrative and developmental approach to unilateral CP, the aspects of perception action cognition environment (PACE) should be considered also when expressed by an infant s fine motor performance, namely when infants use their hands to act on an age-appropriate stimulus. The searched-for assessment should quantify possible differences between the two hands and the quality of bilateral hand use as well as be able to evaluate change over time. Consequently, normative assessments of developmental milestones will not be able to detect change 4 and neurological examinations have a poor relationship with perception, action, cognition, and environmental stimulation. Two systematic reviews of assessment instruments for neuromotor function in infants during the first year of life were published in ,6 Heineman and Hadders-Algra 5 investigated the psychometric properties of instruments evaluating neuromotor function and motor behaviour in infancy, whereas Spittle et al. 6 focused on instruments for preterm infants in their first year of life. These reviews did not, however, specifically address hand function, and since their publication new scales might have been developed The Authors. Developmental Medicine & Child Neurology 2015 Mac Keith Press, 57 (Suppl. 2): DOI: /dmcn

2 Therefore a new review was justified. Because our special interest was in hand use in children at risk of developing unilateral CP, we took these two reviews as a starting point. The aims of the present review were (1) to identify whether any new clinical tools for assessing hand use in infancy had been developed, (2) to investigate how new and previously identified assessment tools describe and measure the hand function components, and (3) to discuss the suitability of these assessment tools for use with infants aged 3 months to 12 months at risk of developing unilateral CP. METHOD Previous reviews of instruments for infants below 1 year old Heineman and Hadders-Algra 5 found 15 instruments, which they divided into four categories: (1) comprehensive neurological examinations: Active and Passive Muscle Power, Amiel-Tison neurological examination, Hammersmith Infant Neurological Examination, and Touwen Infant Neurological Examination; (2) procedures with standardized scoring: Bayley Scales of Infant and Toddler Development version III (BSID-III), 7 Infant Neurological International Battery, 5 Movement Assessment of Infants (MAI), 8 Neuromotor Behavioral Inventory, 5 Peabody Developmental Motor Scales version 2 (PDMS- 2), 9 Primitive Reflex Profile, 5 and Toddler and Infant Motor Examination (TIME); 10,11 (3) observation of milestones: Alberta Infant Motor Scale and Structured Observation of Motor Performance; and (4) quality of motor behaviour: Prechtl s Assessment of General Movements and the Test of Infant Motor Performance. 5 Spittle et al. 6 sought assessments used to discriminate, predict, or evaluate the motor development of preterm infants in the first year of life, identifying nine assessments, only two of which were not mentioned by Heineman and Hadders-Algra 5 : the Neuro-Sensory Motor Development Assessment (NSMDA) 12 and the Postural and Fine Motor Assessment of Infants (PFMAI). 13,14 Seven assessments were evaluated in both studies: Alberta Infant Motor Scale, BSID-III, Prechtl s Assessment of General Movements, MAI, PDMS- 2, Test of Infant Motor Performance, and TIME. The assessment tools identified in the reviews by Heineman and Hadders-Algra 5 and Spittle et al. 6 were scrutinized to determine whether they met all of the following inclusion criteria: (1) include fine motor performance; (2) cover an age range of 3 months to 12 months; (3) can be used continuously throughout the age range. The assessments were excluded if they met any of the following exclusion criteria: (1) intended for screening; (2) evaluate developmental milestones; (3) neurological examination; (4) the original article was not in English; (5) developed for specific non-western cultural contexts; (6) developed for specific diagnoses with clearly differing pathogenesis from that of our group of interest. Only five of the assessment tools met all the inclusion and exclusion criteria: BSID-III, PDMS-2, MAI, PFMAI, What this paper adds available assessment provides a measure of asymmetry between hands in infants. Only three assessments include discrete fine motor scales for infants of 3 to 12 months. New assessments designed for infants with unilateral cerebral palsy are needed. and TIME. An overview of excluded instruments and the reasons for exclusion are presented in Table I. Search for new instruments developed since 2007 The search strategy was developed using the reviews of Heineman and Hadders-Algra 5 and Spittle et al. 6 as a starting point. As the searches for both of these reviews were performed in 2007, we designed our search to find any new assessment tools developed since Relevant terms and medical subject headings (MeSH terms) were identified from the two earlier reviews. Some search terms used were developmental disabilities, psychomotor performance, assessment, evaluation, neuropsychological test, and intervention. The Medline, PsychInfo, PubMed, and Cinahl databases were searched by two librarians on 10 December 2013, after discussions with the authors, and the searches were limited to studies covering infants 0 to 23 months old and to articles published since The search initially identified 531 articles. One of the authors (LE) scanned the abstracts for age information and identified 348 articles covering children younger than 24 months old. Table I: Reasons for assessment exclusion Reason excluded Does not include fine motor performance Does not cover the 3 10mo age range Cannot be used at any given time Observation of developmental milestones Neurological examination Original article not in English Developed for non-western culture Developed for different diagnosis Assessments GM, TIMP, AIMS, PRP, NBI Mini-AHA, SOMP NSMDA CUE, HINE Muscle-Power, Infanib, Amiel-Tison, Touwen NPED HK-PFMDA, KDI BISCUIT, CHOP INTEND GM, Prechtl s Assessment of General Movements; 5 TIMP, Test of Infant Motor Performance; 5 AIMS, Alberta Infant Motor Scale; 5 PRP, Primitive Reflex Profile; 5 NBI, Neuromotor Behavioral Inventory; 5 Mini-AHA, Mini-Assisting Hand Assessment 23 SOMP, Structured Observation of Motor Performance; 5 NSMDA, Neuro-Sensory Motor Development Assessment; 12 CUE, Continuous Unified Electronic Diary Method; 24 HINE, Hammersmith Infant Neurological Examination; 5 Muscle-Power, Active and Passive Muscle Power; 5 Infanib, Infant Neurological International Battery; 5 Amiel-Tison, Amiel-Tison neurological examination; 5 Touwen, Touwen Infant Neurological Examination; 5 NPED, Neuropediatric Development; 25 HK-PFMDA, Hong Kong Preschool Fine-Motor Developmental Assessment; 26 KDI, Kilifi Developmental Inventory; 27 BISCUIT, Baby and Infant Screen for Children with Autism Traits; 28 CHOP-INTEND, Children s Hospital of Philadelphia Infant Test of Neuromuscular Disorders Developmental Medicine & Child Neurology 2015, 57 (Suppl. 2): 37 41

3 All articles were scanned for assessment tools by one of the authors (LE) and 10 assessment tools developed since 2007 were identified. Seven of the assessments were excluded owing to the exclusion criteria (Table I); three of the new assessment tools met all our inclusion and exclusion criteria (as mentioned above): the Infant Motor Profile (IMP), 15 Grasping and Reaching Assessment of Brisbane (GRAB), 16 and Hand Assessment for Infants (HAI), 16 although the last two are under construction. Analysis of fine motor function components of selected assessment tools We collected available articles and manuals for the five relevant assessment tools selected from Heineman and Hadders- Algra 5 and Spittle et al. 6 as well as all the information we could find about the three new assessment tools. We evaluated the content of the assessments with a focus on hand function and their relevance for assessing children with clinical signs of unilateral CP using the following parameters: includes fine motor performance, has separate fine motor subscales, each separately, contains bimanual tasks, outcomes show presence or magnitude of asymmetry. RESULTS Assessments including fine motor components The five assessments previously identified by Heineman and Hadders-Algra 5 and Spittle et al. 6 and the three newly developed instruments meeting our inclusion and exclusion criteria were scrutinized for their fine motor components (Table II). BSID-III was developed in 1969 and most recently revised in It aims to identify children with developmental delay. There is a separate fine motor scale with the outcome presented as both raw scores and age-related scaled scores (i.e. norm referenced). Both bimanual and unimanual items are included, the latter to be performed with the preferred hand. The test does not provide information about side differences between hands or the ability to use both hands together. IMP was published in 2008 and is a video-based assessment tool for motor behaviour. 15 It aims to enable early detection of developmental motor disorders, was developed for infants 3 to 18 months old, and contains five subscales: movement variation, variability, fluency, symmetry, and performance. IMP can assess motor behaviour and identify developmental motor disorders. However, IMP does not have a specific fine motor subscale, the hand-function-related items being incorporated into each subscale. This makes IMP unsuitable for evaluating fine motor performance. MAI was developed in Fine motor items are included in the volitional movement subscale, although this also includes several other components, such as vision and hearing. 8 Since there is no specific fine motor scale, MAI is unsuitable for evaluating fine motor performance. PDMS-2 was developed in 1983 with a second version released in It aims to measure motor development and includes a separate and fairly extensive fine motor scale with two subscales: (1) grasping and (2) fine motor integration. Both unimanual and bimanual tasks are included and Table II: Characteristics of reviewed assessment tools; instruments reviewed in Heineman and Hadders-Algra 5 and Spittle et al. 6 (n=5) and instruments developed after 2007 (n=3) Short name Criterion or norm referenced? Age range Includes fine motor performance? Separate fine motor subscale? Each separately? Contains bimanual tasks? Outcomes show presence or magnitude of asymmetry? BSID-III rm 1mo 3y 6mo, preferred GRAB a,b Criterion >4mo and norm HAI a,c Criterion and norm 3 10mo, different scores for right and left hand shows an asymmetry IMP a Criterion 3 18mo, asymmetry scored for three items MAI Criterion 0 12mo, different scores for right and left hand shows an asymmetry PDMS-2 rm 1mo 5y, preferred PFMAI Criterion 2 12mo, preferred TIME rm 4 42mo, preferred a Published after b A Guzzetta, personal communication 26 January c L Krumlinde-Sundholm, personal communication 27 January BSID-III, Bayley Scale of Infant and Toddler Development version III; 7 GRAB, Grasping and Reaching Assessment of Brisbane; HAI, Hand Assessment for Infants; IMP, Infant Motor Profile; 15 MAI, Movement Assessment of Infants; 8 PDMS-2, Peabody Developmental Motor Scales version 2; 9 PFMAI, Posture and Fine Motor Assessment of Infants; 13 TIME, Toddler and Infant Motor Evaluation. 10 Assessments of Infants Hand Function Lena Krumlinde-Sundholm et al. 39

4 unimanual tasks are scored based on how they are performed with the preferred hand. From the raw scores for each subscale, age-equivalent and standard scores are derived, so the information provided is norm referenced; for the two fine motor scales, quotient centiles are also provided. PDMS-2 can be used to measure age-related fine motor development but it does not provide information about side differences between hands or the ability to use both hands together. PFMAI is an evaluative criterion-referenced test developed in 1991 comprising a posture section and a fine motor section, variables stated to be of special interest for identifying cerebral palsy. 13,14 The fine motor section measures the quality of reaching and grasping as well as of isolated hand and arm movements in relation to three objects. Since the tasks are performed with the preferred hand, the scale does not provide a measure for the non-preferred hand or a separate measure for the two hands. TIME was developed in 1994 (Miller and Roid 10 ) to identify children with motor delay. It uses an observational, play-based approach for assessing movement quality. Fine motor tasks are included in the motor organization subtest together with balance and general motor planning items. Since there is no specific fine motor scale, TIME is unsuitable for evaluating fine motor performance. Instruments under development GRAB is an assessment tool under development, described by Guzzetta et al. 16 In GRAB, video-recorded sessions are analysed in fragments to determine the number and types of hand toy contacts and bilateral actions in an experimental setting. It will be both norm and criterion referenced and will show both presence and magnitude of asymmetry. GRAB can be used with infants from 4 months. It seems to be a promising tool for assessing fine motor performance at early age in a research context (A Guzzetta, personal communication 26 January 2014). The HAI is another assessment tool not yet published; it is briefly described by Guzzetta et al. 16 in the methods protocol for an upcoming intervention study of upper limb function, in the study protocol of Eliasson et al., 17 and in conference abstracts (L Krumlinde-Sundholm, personal communication 26 January 2014). HAI aims to evaluate goal-directed manual actions in infants, 3 to 12 months old, at risk of developing unilateral CP. HAI provides measures of unilateral hand use and bimanual performance. It aims to detect and quantify possible asymmetry between hands by providing scores for each hand separately, and to provide a measure of bimanual hand use both on criterionand on norm-referenced scales. DISCUSSION Most of the reviewed assessments include fine motor performance items incorporated into general developmental scales. These scales do not aim to measure fine motor performance per se, but rather general motor development. It may be questioned whether fine motor performance needs to be measured separately at all. Over the past decade, there has been mounting evidence that hand function can be improved both by unimanual and by bimanual training in children over 18 months old. 18,19 There has also been increasing interest in various early intervention approaches. 16,17,20 22 To evaluate the effects of interventions to improve upper limb function, assessments specifically measuring fine motor performance are essential. Children at risk of developing unilateral CP are in the special situation of having one well-functioning and one affected upper limb. Our literature search identified only three published assessment tools providing a separate fine motor scale: PDMS-2, BSID-III, and PFMAI. All three have reported adequate psychometric properties. The assessment tools include several unimanual test items but in which only the preferred hand is to be used. A child with unilateral CP will naturally use their well-functioning hand for these tasks. PDMS-2 and BSID-III are norm referenced, so children with unilateral CP, who prefer to use their well-functioning hand, will presumably score within the normative reference values, regardless of the severity of problems with the affected hand. Some test items are bimanual in nature. These are typically scored on the basis of whether or not the task is performed, with no indication of performance quality or of how well the hemiplegic hand is used with the well-functioning hand to complete the task. ne of these tests will capture or measure the specific hand function characteristics of children with signs of unilateral CP. On the basis of our special interest in finding tests that can be used for evaluating fine motor performance in infants at risk of developing unilateral CP, we identified the hand function items that we believe an appropriate assessment tool should include, beyond evidence of proper psychometric properties: (1) a measure of how the infant uses each hand separately that can quantify any possible asymmetry; (2) a measure of how the infant uses both hands together to perform bimanual tasks (that is, a measure of bilateral hand use); and (3) enough items/qualifiers to separate different ability levels with high enough precision to be sensitive to change. Moreover, (4) because hand use is just emerging and rapidly changing in the 3 month to 12 month age range, the scale should also be norm referenced. One test, the Mini-Assisting Hand Assessment, fulfilled many of the above requirements, but was excluded because it cannot be used with infants under 8 months old. 23 The newly developed IMP includes an asymmetry scale and several hand-related test items, although it does not provide a subscore for fine motor performance. Two other assessments that seem relevant for assessing infants at risk of developing unilateral CP, namely HAI and GRAB, appear promising, 16 but are not yet available. A possible limitation of this study is that we based our review on the results of other reviews. There is a risk that some relevant assessment tools might have been overlooked as our main interests and aims differed from those 40 Developmental Medicine & Child Neurology 2015, 57 (Suppl. 2): 37 41

5 of the previous reviewers. Our special interest concerned hand use in infants at risk of developing unilateral CP, which differs from the foci of the reviews by Heineman and Hadders-Algra 5 and Spittle et al. 6 There might also be additional assessment tools under construction that are missing because we did not include abstract reviews in the search strategy. In conclusion, only three available tests include a separate fine motor scale; however, these scales include tasks to be performed with the preferred hand only. published assessment has separate scales for each hand to quantify asymmetry or investigate bimanual performance. The new assessment tool HAI, which is under development, seems to be the only one to consider these important aspects for measuring hand function in infants at risk of developing unilateral CP. ACKNOWLEDGEMENTS This study was supported by La Fondation Motrice and Sodiaal (Paris), and the Strategic Research Programme in Care Sciences and the Health Care Sciences Postgraduate School at Karolinska Institutet, Stockholm. The authors have stated that they had no interests which might be perceived as posing a conflict or bias. REFERENCES 1. Martin JH, Chakrabarty S, Friel KM. Harnessing activity-dependent plasticity to repair the damaged corticospinal tract in an animal model of cerebral palsy. Dev Med Child Neurol 2011; 53(Suppl. 4): Al-Whaibi R, Eyre J. Environmental cues influence hand movement from 1 month of age: implications for therapy following perinatal stroke. [Abstract.] Paper presented at the Annual Meeting of the European Academy of Childhood Disability, 5 7 June 2008; Zagreb, Croatia. Dev Med Child Neurol 2008; 50: Guzzetta A, Pizzardi A, Belmonti V, et al. Hand movements at 3 months predict later hemiplegia in term infants with neonatal cerebral infarction. 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