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  • This retrospective cohort included children who had been born at less than 29 weeks gestation, between April 1st 2009 and March 31st 2011; had been seen at our regional quaternary care facility at the Children’s Hospital of Eastern Ontario (CHEO), Ottawa, Canada neonatal follow-up (NNFU) clinic for their 18 months assessment. We included children who had been extremely preterm infants, and who had been administered both an ASQ3 and Bayley-III independently at 18 months corrected gestational age; children with an incomplete ASQ3 or Bayley-III assessment leading to missing data were not included in the analysis. Neither were children not seen at their 18 months old corrected age visit as their care had been transferred to the rehabilitation center for treatment of severe handicap prior to that age, or who were being followed in another paediatric clinic as per geographical criteria. The Children’s Hospital of Eastern Ontario Research Ethics Board approved the study. Considering the retrospective design of the study consent was not required, patient records and information was anonymized and de-identified prior analysis. In our region, infants at high risk for developmental delay are usually seen at 4, 10 and 18 months corrected age and at 4 years of age. During these visits children are assessed by a multidisciplinary team including a nurse, one of five paediatricians involved in the clinic, a physiotherapist at the 4 months corrected age visit and a psychologist at the 18 months corrected age visit. At the 18 months corrected gestational age visit the nurse reviews the medical history, and assesses feeding, growth, behavior and socio-familial status through a structured interview. The registered psychologist reviews the nurse's assessment if already completed, reviews the socio-familial status, assesses behavior, and administers and scores the Bayley-III [6]. This tool is used to assess development of children from 1 to 42 months of age. It determines scores for cognitive, language and motor skills through standardized items and scores for social and adaptive abilities through parental questionnaires. Bayley-III provides norm-referenced composite scores for each skill area with a mean of 100 and a standard deviation of ± 15. Independent of the psychologist’s assessment, the physician reviews the nurse’s assessment before seeing the infant and the family, completes a medical assessment that includes a physical and neurological examination, and along with the parent uses the 18 months old questionnaire of the ASQ3 to score the infant’s developmental performance. The ASQ3 is a screening tool composed of 21 age-specific questionnaires covering the range 1 to 66 months of age [7]. Each questionnaire includes 30 developmental items divided into five domains: communication, gross motor, fine motor, problem solving and personal-social. Although the ASQ3 is designed to be completed by parents, the NNFU team members use the tool to guide the interview with parents and to guide the face-to-face observation of the child’s abilities to perform the milestones, such as stacking of 4 or 5 small size blocks. When a child did not perform an item or when the clinic design was not appropriate for a particular task, for example finding a familiar toy or object in another room, parents were invited to mention whether they witnessed their infant performing that ASQ3 item, and the information was included in the final score. Fig 1 illustrates a typical clinical decision making process that would correspond to most of the clinical situations, as per NNFU team members agreement; however in individual cases the sequence of the different examinations and sources of information used in clinic to come to the decisions that are ultimately communicated to the family may have been adjusted. In short, the psychologist used and scored the Bayley-III and the physician scored the ASQ3 as originally designed [6,7]; both independently administered the screening or the developmental assessment tool, before communicating with one another regarding the particular child. The qualitative information that may also influence decisions with regard to developmental resources includes the socio-familial status, and the behavioral, medical, physical and neurological assessments. The combination of the ASQ3 scores and the qualitative information informs the preliminary physician referral decisions as to requirements for developmental resources. Similarly, the Bayley-III results plus the qualitative information inform the preliminary psychologist referral decisions. Both preliminary referral decisions consolidated into a brief written communication between the psychologist and the physician generally achieves consensus for final integrated decision (FID), that is communicated by the physician to the family at the end of the visit. In the case of discrepancies in decisions, these are addressed at a short meeting between the physician, psychologist and the nurse coordinator, to review the scores obtained from the ASQ3 and the Bayley-III and to discuss other qualitative information to achieve a FID between team members. Figure data removed from full text. Figure identifier and caption: 10.1371/journal.pone.0170171.g001 18 months old corrected gestational age decision-making process and analysis.Qualitative information includes information gathered from the medical, behavioral and socio-family environmental assessment and the neurological exam. ASQ, Ages and Stages Questionnaire; Bayley-III, Bayley Scales of Infant Development 3rd edition; FID, Final integrated decision; TRD, Theoretical referral decision. In our clinic, both the ASQ3 and the Bayley-III scores support physicians’ and psychologists’ decisions to refer to services of developmental resources including: early return to the NNFU clinic, physiotherapy; audiology and speech therapy; Ontario Early Years Center (EYC) for education on parenting skills [14]; Infant Development Program (IDP) for early developmental intervention [15]; and Ottawa Children’s Treatment Center (OCTC) [16], a local rehabilitation center, when there is a clear suspicion of developmental delay. Additional NNFU visits (early return), usually within 6 to 12 months, are suggested when the team has concerns and wants to reassess before the routine visit at 4 years of age. Procedures to reconstruct the decision-making process: For the purpose of this study, we conceptualized the decision making into three dimensions: the preliminary professional opinion that is based on the developmental assessment or screening tool plus the qualitative information; the theoretical referral decision (TRD) which is the referral decision based solely on the scores obtained for the developmental assessment tool (Bayley-III) or screening tool (ASQ3); and the final integrated decision (FID) which represents the interdisciplinary team referral decision made in clinic for a particular child. In two one-hour focused ASQ-Bayley project meetings held outside of the clinical NNFU clinic hours, physicians and the psychologist working in the clinic first reviewed and created a model of how the decisions were made during the NNFU clinic visits (Fig 1); and second discussed and obtained consensus on the TRD for every possible array of test results (S1 and S2 Appendices). To reflect the sequence in the decision-making process within our NNFU clinical practice, the study design assumed that both the physician and the psychologist independently formulate preliminary opinions at the end of their respective assessments. These preliminary opinions are based on the medical, behavioral and socio-family environmental assessment and the neurological exam (physician only), complemented by the scores obtained from the ASQ3 and Bayley-III for the physician and the psychologist respectively. Then, these preliminary opinions made by the physician (physician preliminary opinion) and made by the psychologist (psychologist preliminary opinion) are shared and inform the FID (Fig 1). To isolate testing scores from other sources of information and to estimate how the individual scores in each tool (ASQ3 and Bayley-III) influence the clinician’s judgement and preliminary opinion, we created algorithms that represent TRDs for referrals to developmental resources. These algorithms were used solely for this research project, and are not used in clinic. The TRD algorithms captured consensus between participants of the ASQ-Bayley project meetings to predict a referral TRD corresponding to all possible hypothetical combinations of ASQ3 subscale scores based on three cut off values as per ASQ3 design (ASQ-TRD) and Bayley-III subscale scores also based on three cut-off values as per scaled score Bayley-III design (Bayley-TRD). The cut-off values based on the ASQ3 and Bayley-III for TRDs are included in S1 and S2 Appendices. For example, if a score is lower than 1 standard deviation (SD) the norm in communication on the ASQ3 or in expressive or receptive language on the Bayley-III and the other subscales are normal, a referral to audiology and speech therapy is made. Similarly for a score more than 1 SD below the norm in gross motor on the ASQ3 or on the Bayley-III, a physiotherapist should see the child, etc. After the algorithms were created, the 18-month ASQ3 scores and the Bayley-III scores were extracted from the medical charts and interpreted using a computer program created with R version 3.1 software [17]. The R program applied the cut-off ranges for normal, grey zone, and abnormal to the observed ASQ3 and Bayley-III scores. TRDs were obtained by matching these ranges to the algorithmic logic tables. The TRDs were then compared to FIDs to obtain estimates of sensitivity and specificity. The results of the computed TRDs were manually verified for each child. Demographic characteristics of children included in the study and those excluded for missing data were summarized using descriptive statistics. To test for demographic characteristics, differences between the excluded for missing data and included groups, Pearson’s chi-square or Fisher’s exact test and Student’s t-test were applied as appropriate. Holm’s adjustment was used for multiple testing [18]. For each participant we compared the degree of agreement according to Byrt’s definition [19] between the three levels of decisions—ASQ-TRD, Bayley-TRD and FID—by calculating kappa values for referral to each developmental resource. To render kappa values clinically meaningful and to assess whether the ASQ3 was sufficient to inform FID decisions, we compared the three individual decisions—the ASQ-TRD, Bayley-TRD and FID—with referrals to each developmental resource. Every chart reviewed was determined to fit into one of four clinically possible case-scenarios for decisions. The results were classified in case-scenario 1 when ASQ-TRD, Bayley-TRD and FID were all in agreement, in case-scenario 2 when only the ASQ-TRD and FID were in agreement, in case-scenario 3 when only the Bayley-TRD and FID were in agreement and finally in case-scenario 4 when neither the ASQ-TRD or the Bayley-TRD agreed with the FID, irrespective of an agreement between the ASQ-TRD and the Bayley-TRD. McNemar's test was performed to compare the proportion of ASQ-TRD results that corresponded with the FID to the proportion of Bayley-TRD results that corresponded with the FID, taking into account the pairing of the tests for each FID. To evaluate the uncertainty around the estimated difference in performance of the two tests, a 95% paired Wilson score confidence interval was computed. Finally, following the methodology of Schonhaut [12], we computed Pearson’s correlation coefficient between the ASQ3 and Bayley-III as well as the validity properties of ASQ3 scores ≤ - 2SD to predict a score ≤ - 1SD on the Bayley-III in at least one domain.
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