Construction and validation of the Oxford Neurodevelopment Assessment (OX-NDA) in 1-year-old Brazilian children
BMC Pediatrics volume 22, Article number: 733 (2022)
Over 250 million children under 5 years, globally, are at risk of developmental delay. Interventions during the first 2 years of life have enduring positive effects if children at risk are identified, using standardized assessments, within this window. However, identifying developmental delay during infancy is challenging and there are limited infant development assessments suitable for use in low- and middle-income (LMIC) settings. Here, we describe a new tool, the Oxford Neurodevelopment Assessment (OX-NDA), measuring cognition, language, motor, and behaviour, outcomes in 1-year-old children. We present the results of its evaluation against the Bayley Scales of Infant Development IIIrd edition (BSID-III) and its psychometric properties.
Sixteen international tools measuring infant development were analysed to inform the OX-NDA’s construction. Its agreement with the BSID-III, for cognitive, motor and language domains, was evaluated using intra-class correlations (ICCs, for absolute agreement), Bland-Altman analyses (for bias and limits of agreement), and sensitivity and specificity analyses (for accuracy) in 104 Brazilian children, aged 12 months (SD 8.4 days), recruited from the 2015 Pelotas Birth Cohort Study. Behaviour was not evaluated, as the BSID-III’s adaptive behaviour scale was not included in the cohort’s protocol. Cohen’s kappas and Cronbach’s alphas were calculated to determine the OX-NDA’s reliability and internal consistency respectively.
Agreement was moderate for cognition and motor outcomes (ICCs 0.63 and 0.68, p < 0.001) and low for language outcomes (ICC 0.30, p < 0.04). Bland-Altman analysis showed little to no bias between measures across domains. The OX-NDA’s sensitivity and specificity for predicting moderate-to-severe delay on the BSID-III was 76, 73 and 43% and 75, 80 and 33% for cognition, motor and language outcomes, respectively. Inter-rater (k = 0.80-0.96) and test-rest (k = 0.85-0.94) reliability was high for all domains. Administration time was < 20 minutes.
The OX-NDA shows moderate agreement with the BSID-III for identifying infants at risk of cognitive and motor delay; agreement was low for language delay. It is a rapid, low-cost assessment constructed specifically for use in LMIC populations. Further work is needed to evaluate its use (i) across domains in populations beyond Brazil and (ii) to identify language delays in Brazilian children.
In 2015, Early Child Development (ECD) was, for the first time, included in the Sustainable Development Goals as indicator 4.2.1: “the proportion of children under 5 years of age who are developmentally on track in health, learning and psychosocial well-being, by sex” . Nevertheless, over 250 million children, globally, are at risk of not achieving their developmental potential due to poverty and stunting alone . A disadvantaged start in life limits children’s abilities to benefit from education leading to lower productivity and social consequences that affect not only present but also future generations [3,4,5,6,7]. Moreover, brain stimulation interventions during the first 2 years of life have been to have enduring positive effects if children at risk are identified , using standardized assessments, and receive such interventions, within this window. One of the key challenges in the ECD landscape, therefore, is the early and accurate identification of children at risk, using standardized methodologies, to target interventions and to enable cross-population comparisons [5, 7, 8].
Many developmental batteries assess ECD outcomes during the first year of life  (Additional file 1: Table S1). However, only a few can be administered reliably by non-specialists and be applied across population groups from high-, middle- and low-income settings at relatively low costs [9,10,11,12]. Between 2013 and 2018, a WHO commissioned team identified only 3 initiatives that attempted to address these technical and logistical challenges : (i) the WHO Gross Motor Milestones [13, 14], (ii) the Ages and Stages Questionnaires (ASQ) , and (iii) the Guide for Monitoring Child Development (GMCD) [16, 17]. Two of these (the ASQ and GMCD) were caregiver-reports; and the WHO milestones, although observer-rated, focussed exclusively on measuring gross motor skills.
Previous ECD research has shown that a mixed-methodology approach, combining direct-assessments with observer- and caregiver-reports, provides advantages over either method alone. This approach has been successfully applied in several developmental tests including the Batelle Developmental Inventory (BDI) [18, 19], the Test de Aprendizaje y Desarrollo Infantil (TADI)  and the INTERGROWTH-21st Neurodevelopment Assessment (INTER-NDA; www.inter-nda.com) . The latter is a rapid, standardized, psychometrically valid 37-item international ECD instrument measuring cognition, fine and gross motor, language and behaviour outcomes in children aged 22 to 30 months [21, 22]. It can be administered reliably by non-specialists to identify children at risk of delay, and its norms are international ECD standards constructed according to the WHO’s prescriptive approach .
The adoption of the INTER-NDA - for the identification of children at risk of delay and for cross-population comparisons - by the clinicians and researchers, internationally, prompted demand for a tool, similar in conceptual and technical constructs, for the comprehensive and reliable assessment of outcomes in younger children . The objective of this study is (i) to describe the rationale and methodology leading to the construction of a novel infant development assessment meeting the aforementioned specifications (the Oxford Neurodevelopment Assessment; OX-NDA) and (ii) to evaluate its performance against the Bayley Scales of Infant Development III edition (BSID-III) . The specific aims of the current study were to: (i) examine agreement between OX-NDA and BSID-III domain scores; (ii) evaluate the OX-NDA’s sensitivity and specificity in predicting moderate-to-severe developmental delay on the BSID-III; and (iii) determine the OX-NDA’s internal consistency and rater reliability.
Participants and procedures
Infants enrolled in the 2015 Pelotas Birth Cohort Study , were consecutively recruited to participate in the OX-NDA validation study. Children with known severe hearing or vision impairments, and non-singleton children, were excluded from participation.
The 2015 Pelotas Birth Cohort is a large epidemiological study of child health, growth and development in the city of Pelotas in Southern Brazil. The cohort included 4275 newborns born between 1 January and 31 December 2015. Mothers and children were assessed at birth, and at 3, 12, 24 and 48 months post birth. Details of the cohort have been previously published . The cohort is registered at clinicaltrials.gov [NCT03271723].
Participating children were evaluated on the OX-NDA and the BSID-III between 10 and 14 months by separate assessors, blinded to each other results. Assessments were conducted in Brazilian Portuguese in the children’s homes, in the presence of a primary caregiver over two consecutive days. In half the sample, the BSID-III was administered first; in the remaining sample, the OX-NDA was administered first. We did not evaluate children on both instruments in a single sitting to avoid children’s underperformance due to fatigue from repeated testing and because of the BSID-III’s long administration time (60-90 minutes). The reliability of the OX-NDA was determined for four non-specialist field assessors across 10 assessments.
The design, development and evaluation process of the OX-NDA is summarised in Fig. 1.
The BSID-III: The BSID-III measures cognition, language, motor, social-emotional, and adaptive behaviour outcomes in children aged 1-42 months [25, 27]. The thresholds for moderate and severe delay on its composite scores (Mean 100, SD 15) are 71-85 and ≤ 70, respectively . Its latest norms were developed from 1700 US children recruited in 2004 and selected to match the 2000 United States census population of children . The cost of the BSID-III kit, at the time of writing this paper, is GBP 1521.64, the cost per form per child is GBP 4.89 . In this study, the adaptive behaviour subscale of the BSID-III was not included in the cohort’s protocol.
The OX-NDA: The OX-NDA is a novel multi-dimensional ECD assessment for children aged 10-14 months  consisting of 37 items grouped into cognition, motor, language, and positive and negative behaviour domains (Table 1). Of these items, 21 are directly assessed, 13 are concurrently observed and 3 are caregiver reported. Item scores range from 4 (highest) to 1 (lowest) with ‘unable to assess’ being scored as ‘X’: items scored ‘unable to assess’ are excluded from the calculation of mean domain scores. Its kit (Fig. 2) costs GBP 100.00 in the UK, but sourcing items locally can substantially reduce costs. There is no fee per child for use. The OX-NDA items were created in English and were translated into Brazilian Portuguese according to the WHO Mental Health Initiative translation guidelines which includes processes of translation, back translation and cultural customization .
The construction of the OX-NDA involved five stages:
A landscape analysis of widely used tools measuring child development at 12 months across populations (Additional file 1: Table S1)
An analysis mapping the conceptual basis of the constituent items within each tool onto a ‘neurodevelopment domain’ matrix (Additional file 2: Table S2).
Selection, by a panel of regional and international experts in ECD measurement, of the most appropriate ECD elements (n = 41) for inclusion in the prototype OX-NDA and construction of a 5-point performance reporting scale for each item (Table 1), similar to that of the INTER-NDA, to objectively measure a child’s level of achievement for the respective item (Additional file 3: Table S3).
Initial piloting and assessment of internal consistency (Table 3) resulted in excluding 4 items. The OX-NDA format for further psychometric testing and validation against the BSID-III therefore consisted of 37 items (Additional file 3: Table S3).
Sample size and statistical analysis
Statistical analysis was conducted in Stata 15 software (Stata Corp., College Station, TX, USA). Accounting for attrition, a sample size of 104 was estimated to detected associations at a confidence level of 95% and significance level of < 0.05. Raw mean OX-NDA domain scores were calculated and converted to standardised scaled scores (Mean 50, SD 25, range 0 to 100; Table 1), and distributions explored. The following analyses were carried out:
Continuous correlations (Pearson) to determine whether children who scored high on the OX-NDA also scored high on the BSID-III;
Single measure intra-class correlation coefficients (ICCs) for absolute agreement between each domain, using a two-way mixed effects model (to quantify the strength of the association between OX-NDA and BSID-III scores);
Bias and limits of agreement statistics; and
Bland-Altman plots to identify whether the OX-NDA scores differed systematically across different levels of the BSID-III.
Sensitivity and Specificity Analyses: OX-NDA scores were compared between children scoring ≥85 (to assess OX-NDA sensitivity) and < 85 on BSID-III composites (to assess specificity). Cut-offs with highest sensitivity and specificity for each OX-NDA domain were determined using Receiver Operating Characteristics (ROC) analyses. Positive and negative predictive values and positive and negative likelihood ratios for each OX-NDA cut-off threshold were calculated.
Inter-rater and Test-re test Reliability: was determined using Cohen’s kappa coefficients .
Our study was approved by the Research Ethics Committee of the Medical School (No 1.400.585) and the School of Physical Education at the Federal University of Pelotas, Brazil (CAAE registration number: 26746414.5.0000.5313). Mothers provided written informed consent on behalf of their children.
Of the cohort’s 4018 children followed-up at 12 months, a sub-sample of 104 was randomly selected to participate in the OX-NDA study. Other than age at weaning, there were no significant differences in socio-demographic and health characteristics between the OX-NDA sample and the cohort (Table 2). Children were assessed at a mean age of 367.6 (SD 8.4) days, 55 (53%) were male, and 84 (80.7%) were born at or near term. Mean birth weight was 3.2 (SD 0.5) kg. At the time of the assessment, children weighed 10.1 (SD 1.2) kg (corresponding to the 75th-85th centiles for girls and 50th-75th centiles for boys on the age-specific WHO child growth standards), and measured 75.1 (SD 3.1) cm in length (corresponding to the 50th-75th WHO centiles for girls and 25th-50th centiles for boys). The mean OX-NDA assessment time was 20.0 (SD 5.0) minutes.
For the final OX-NDA (consisting of 37 items), Cronbach’s alpha values (Table 3) were satisfactory (≥0.70) for the cognition, motor and positive behaviour; acceptable (0.40) for language, and weak (< 0.4) for negative behaviour .
Concurrent validity between the OX-NDA and BSID-III
Strong positive correlations were observed between cognition and motor scores of the BSID-III and the OX-NDA (Table 3, Pearson’s r = 0.50-0.52, p < 0.001). The ICCs for the BSID-III and OX-NDA domains showed similarly strong associations for cognition and motor outcomes (ICCs 0.63-0.68, p < 0.001), and low associations for language outcomes (ICC 0.30, p = 0.04).
The Bland-Altman analysis (Table 4) indicated no, or very low, bias in the subscales, suggesting little to acceptable difference between OX-NDA and BSID-III scores . The Bland-Altman plots (Additional file 4: Fig. S4) and the linear regression analyses (Table 4) of difference scores (BSID-III minus OX-NDA) revealed positive associations between the measures.
Sensitivity and specificity analysis
Fewer than 10% of the study’s children obtained BSID-III composite scores < 85, no children scored < 70. Children scoring low (< 85) on the BSID-III composites also scored low on the OX-NDA across all domains (Table 4). The sensitivity and specificity of the OX-NDA cognition and motor scores in predicting moderate to severe delay on the BSID-III (composite scores < 85) was strong (Additional file 5: Table S5) at cut-offs of ≤60 (sensitivity 76%, specificity 75%), ≤73 (sensitivity 73%, specificity 80%), and ≤ 71 (sensitivity 70%, specificity 25%), respectively. This was low for the OX-NDA language score at a cut-off of ≤60 (sensitivity 43%, specificity 33%) [34, 35].
The inter-rater and test-retest reliability was high (Cohen’s k = 0.80-0.96, 95% CI: 0.78-0.97 and Cohen’s k = 0.85-0.94, 95% CI: 0.80-0.95) across all OX-NDA domains (Table 5).
VI. Feasibility Analysis for Use Across Populations and Settings.
The OX-NDA was assessed against three international guidelines for measuring ECD in low- and middle-income settings (Table 6): the World Bank’s Toolkit for Measuring ECD ; Fischer et al’s feasibility criteria for use of developmental screening tools at primary healthcare level in low- and middle-income settings  and Boggs’ et al’s rating of ECD measurement tools for routine health programme use . The OX-NDA met all but one World Bank and Fischer criteria, and scored 19 (of a maximum total of 24) on Boggs et al’s rating.
The OX-NDA is a multi-dimensional, mixed methodology instrument for measuring cognitive, motor and behaviour outcomes in children aged 10 to 14 months: its psychometric validity was low for the language domain. The rationale for its construction was to provide a comprehensive neurodevelopmental assessment that can be administered reliably and rapidly to young children by non-specialists in low-resource settings at relatively low costs. The preliminary evidence obtained from this study supports the OX-NDA’s use as a valid and reliable measure of early cognitive, motor and behaviour outcomes in Brazilian infants.
Across cognitive and motor domains, the OX-NDA demonstrated good concurrent validity with the BSID-III, satisfactory psychometric properties and high levels of inter-rater and test-retest reliability. Importantly, its sensitivity and specificity in predicting moderate-to-severe cognitive and motor delay in 1-year-olds was satisfactory. The OX-NDA’s concurrent validity with the BSID-III for the language domain was low. It is possible that this may reflect the observation that language, as a construct, is highly influenced by culture and it was, as such, not possible for us to ascertain from our dataset whether it is the OX-NDA or the BSID-III that have limited function in this context.
Across domains, the OX-NDA’s reliability, when administered by non-specialists, was high and its administration time was shorter and cost per child was lower than comparable measures. Previous studies have shown that ECD assessments for older ages and constructed using similar approaches, such as the INTER-NDA  and TADI , have yielded similar results.
Our study was limited in that all children were Brazilian, recruited from the city of Pelotas, and that the comparison of the OX-NDA’s behaviour domain with the BSID-III was not ascertained. Its agreement with the BSID-III language composite was limited and further work is needed to ascertain why this was the case and how its performance in the language domain may be improved. Moreover, its ability to predict severe delay could not be determined as no children in our study scored < 70 on the BSID-III composite scores. Additionally, the OX-NDA’s age range is narrow (10 to 14 months). Finally, item selection was guided by the expert panel, initial piloting and assessment of internal consistency: we did not conduct a factorial analysis for item selection which limited our ability to scrutinise relations between observed and latent variables.
Nevertheless, the study’s strengths lie in the detailed validation of the OX-NDA, using multiple statistical techniques, in a population-based sample from a low-and-middle-income setting against the BSID-III , a well-established measure of ECD, considered, by some, to be a gold-standard ECD assessment. Our study design controlled for child fatigue and contamination of results during sequential developmental testing sessions.
The OX-NDA offers several practical and conceptual advantages over other infant developmental assessments (Table 6, Additional file 1: Table S1). First, it reliably measures multiple domains of infant development (cognition, motor, and behaviour). For each domain, outcomes are reported on a 5-point scale characterising the child’s performance across a spectrum and offering a level of granularity beyond that provided by many infant development batteries. Second, it was designed to be free from cultural biases and is based upon objective reporting (rather than subjective judgement) of the child’s performance. Its rigorous standardization protocol ensures children are assessed uniformly and reliably. Moreover, it can be administered reliably by non-specialist assessors in a short assessment time and at relatively low costs. Third, because it is a mixed-methodology assessment, it applies the advantages of direct assessment as well as caregiver- and observer-reports. It assesses cognitive processing by presenting children with new tasks and captures previously demonstrated abilities while being minimally affected by reporter and recall biases.
Nevertheless, although the OX-NDA fulfilled most requirements for a population-level ECD measure when assessed against the World Bank’s , Fischer et al’s  and Boggs’ et al’s criteria  (Table 6); the findings of this study may not be generalizable to culturally and linguistically disparate LMICs and further research is needed to evaluate its adaptability and applicability in screening for infant development delay in populations beyond Brazil. Additionally, further work is needed to examine (and improve) its performance in the language domain. Currently, such studies are on-going in the West Indies, Indonesia, India, and Senegal.
Identifying children at risk of delay during early childhood and comparing outcomes across populations are essential prerequisites for achieving indicator 4.2.1 of the Sustainable Development Goals. The OX-NDA measure presented here contributes an important component to the care of young children: a unique, standardized developmental tool that can be applied by non-specialists in low-resource settings to measure neurodevelopmental outcomes in infants reliably, rapidly and at relatively low costs and to identify those children at risk of delays.
The evidence presented here shows the OX-NDA to be a psychometrically sound measurement tool for the assessment of cognitive, motor and behaviour outcomes in Brazilian infants. Its mixed-methodology, multidimensional approach; relatively low costs; and reliability when administered by non-specialists make it an attractive candidate ECD measure for research and clinical efforts aimed at identifying infants at risk of delay in low-resource settings. Its ability to identify language delay in Brazilian infants was low and further work is needed to examine (and improve) its performance in the language domain. Research efforts, focusing on its adaptation and application in LMIC settings beyond Brazil, are on-going.
Availability of data and materials
The data that support the findings of this study are available from the DOVE research centre (email@example.com) but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors/corresponding author upon reasonable request and with permission of the DOVE research centre (firstname.lastname@example.org).
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We are grateful to the mothers and children who have contributed to the study. We gratefully acknowledge the contribution of Hua-Fang (Lily) Liao, Executive Director of the Chinese Association of Early Intervention Professional for Children with Developmental Delays for providing information on the Comprehensive Developmental Inventory for Infants and Toddlers.
The Wellcome Trust (grant number 095582/Z/11/Z) supports the 2015 Pelotas Birth Cohort. This study was funded by the Brazilian National Council for Scientific and Technological Development (CNPq) (Grant N° 401732/2015-0) and Bill & Melinda Gates Foundation (B&MGF) (Grant N° OPP 1142172). IS Santos, A Matijasevich and PC Hallal receive support from the Brazilian National Council for Scientific and Technological Development (CNPq). M Fernandes receives support from the Medical Research Council in the UK. None of the funding bodies had a role in the design of this study, data analysis, collection, interpretation or writing of the manuscript.
Ethics approval and consent to participate
Our study was approved by the Research Ethics Committee of the Medical School (No 1.400.585) and the School of Physical Education at the Federal University of Pelotas, Brazil (CAAE registration number: 26746414.5.0000.5313) and complies with the principles of the Declaration of Helsinki. Mothers provided written informed consent on behalf of their children.
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Fernandes, M., Bassani, D., Albernaz, E. et al. Construction and validation of the Oxford Neurodevelopment Assessment (OX-NDA) in 1-year-old Brazilian children. BMC Pediatr 22, 733 (2022). https://doi.org/10.1186/s12887-022-03794-1