Nutritional evaluation and growth of infants in a Rwandan neonatal follow‐up clinic

Abstract Children born preterm, low birth weight (LBW) or with other perinatal risk factors are at high‐risk of malnutrition. Regular growth monitoring and early intervention are essential to promote optimal feeding and growth; however, monitoring growth in preterm infants can be complex. This study evaluated growth monitoring of infants under 6 months enrolled in Paediatric Development Clinics (PDCs) in rural Rwanda. We reviewed electronic medical records (EMR) of infants enrolled in PDCs before age 2 months with their first visit between January 2015 and December 2016 and followed them until age 6 months. Nurse classification of anthropometric measures and nutritional status were extracted from the EMR. Interval growth and length‐for‐age, weight‐for‐length, and weight‐for‐age z‐scores were calculated using World Health Organization anthropometry software as a ‘gold standard’ comparison to nurse classifications. Two hundred and ninety‐four patients enrolled and had 2,033 visits during the study period. Referral reasons included prematurity/LBW (73.8%) and hypoxic ischemic encephalopathy (28.2%). Nurses assessed interval growth at 58.7% of visits, length‐for‐age at 66.4%, weight‐for‐length at 65.6% and weight‐for‐age at 66.4%. Nurses and gold standard assessment agreed on interval growth at 53.3% of visits and length‐for‐age at 63.7%, weight‐for‐length at 78.2% and weight‐for‐age at 66.3%. At 6 months, 46.5% were stunted, 19.9% were wasted and 44.2% were underweight. There were significant challenges to optimizing growth and growth monitoring among high‐risk infants served by PDCs, including incomplete and inaccurate assessments. Developing tools for clinician decision support in assessing growth and providing specialized nutritional counselling are essential to supporting optimal outcomes in this population.


| INTRODUCTION
Globally, under-five mortality has decreased substantially over the past few decades as countries worked towards Millennium Development Goals (MDGs) and now the Sustainable Development Goals (SDGs; You et al., 2015). Although decreases in neonatal mortality have lagged behind improvements in under-five mortality, more and more high-risk infants are surviving the neonatal period. It is well known that infants born with perinatal complications due to prematurity, low birth weight (LBW), hypoxic ischemic encephalopathy (HIE) or other problems may have ongoing challenges requiring follow-up.
These infants are at-risk for developmental delays, poor nutrition, increased mortality during childhood and non-communicable diseases later in life (Lawn et al., 2014). However, in resource-limited settings, few programmes exist to meet the ongoing developmental, nutritional and healthcare needs of infants born premature, LBW, with HIE, or with congenital problems, increasing the risk of morbidity and mortality.
Infants born with perinatal complications are at increased risk for developing undernutrition, in both the acute and chronic forms (Christian et al., 2013;Danaei et al., 2016). Research among these populations of children in sub-Saharan Africa has shown high rates of stunting, wasting and underweight that are often at least double national prevalence Tann et al., 2018;Van den Boogaard et al., 2017). Although optimal weight gain in healthy, term infants has been studied and defined, there are no currently accepted international standards of how to monitor growth in premature infants, with a variety of methods used, including grams per day, grams per kilogram per day and z-scores (Fenton et al., 2017). Additionally, there is no single currently accepted standard growth chart for use in infants born prematurely. World Health Organization (WHO) standard growth charts require use of corrected age when used for preterm infants. There are also a variety of other charts specific for preterm infants; however, they are normed on different populations (Villar et al., 2018). In all cases, the use of these charts well relies on accurate gestational age, which is a major limitation in low-and middle-income countries. The tools and assessments for monitoring growth in infants <6 months present many challenges, particularly for infants born premature and LBW infants. Routine monitoring of growth in infants <6 months is left out of many national screening programmes (Lopriore, Dop, Solal-Celigny, & Lagnado, 2007) despite evidence of malnutrition among children in this age range (Kerac et al., 2011 perinatal risk factors such as prematurity, low birth weight or neonatal encephalopathy, which may require specialized guidelines for low-resource settings.
• Despite training and mentorship, nurses were unable to correctly and consistently monitor growth among highrisk infants in this context, including challenges in the correct plotting of anthropometrics using standard World Health Organization growth charts.
• Children born preterm, low birth weight or with other perinatal risk factors showed high rates of malnutrition and early growth failure even when enrolled in a clinic designed especially for their routine nutritional follow-up and intervention. This early growth failure contributes to the burden of wasting, stunting and underweight in older children.
• The follow-up care of preterm infants and other infants with perinatal risk requires greater attention for feasibility in low-resource settings and specialized tools to aid healthcare workers in growth monitoring and early identification of growth failure are needed.

| Study design and population
This was a descriptive retrospective cohort study on the nutritional status of infants under 6 months enrolled in PDC. We included in our analysis patients who were enrolled in PDCs between January 1, 2015 and December 31, 2016 with age less than 2 months at enrolment and who remained in care through 6 months of age (age at each PDC visit adjusted for prematurity days when gestational age was <37 weeks). The PDC follow-up period included visits that occurred from January 1, 2015 through September 30, 2017. All infants who met these inclusion criteria were included in this study, regardless of the diagnostic criteria that led to the infant's enrolment in PDC.

| Data collection
Data on socio-economic and clinical characteristics and anthropometric measurements recorded at PDC enrolment and each visit were extracted from the PDC's routine electronic medical record (EMR) for analysis. The EMR is an OpenMRS (Seebregts et al., 2009) system that stores data for the PDCs. PDC data are first recorded on paper forms at every visit before a team of permanent trained data collectors enter those data into EMR within 1 week of a visit.

| Definition of variables
'Small for gestational age (SGA)' was defined as birth weight < 10th percentile for gestational age using the INTERGROWTH-21st preterm growth charts (Villar et al., 2014Re).
'Age at each PDC visit/chronological age' was calculated by taking the date of visit minus the child's date of birth.
'Corrected age' was defined as a premature (born <37 weeks gestational age) infant's chronological age minus the number of weeks born early, where weeks born early is defined as 40 weeks minus gestational age.
'Interval growth' at each PDC visit was calculated by taking the child's weight at the most recent visit and subtracting the weight at the previous visit from it and dividing by the number of days in between those two weights to have an average weight gain in grams per day. Adequate interval growth for infants 0-3 months is 20 g/day and 15 g/day for infants from 3 to 6 months (Ministry of Health, 2017).
'Gold standard assessments' were defined as using Stata software to calculate interval growth, z-scores and corrected age based on date of birth and date of visit, as well as documented anthropometric measurements on each PDC visit.

| Data analysis
We used descriptive statistics to summarize data on sociodemographic and clinical characteristics of infants using frequencies and percentages for categorical data and median and interquartile ranges for continuous data.

| Ethical considerations
This study received ethical approvals from the Rwanda National Ethics Committee and the Ministry of Health.  were not wasted and 47.2% were not underweight.

| DISCUSSION
Our study highlights a number of challenges in monitoring growth and nutritional status in this population of high-risk infants, despite training and mentorship of nurses in this specific aspect of care.
There were gaps in completeness of assessment at PDC visits, in documentation of key patient history information and in accuracy of nutritional assessments compared with the gold standard. Rates of malnutrition in this population were high particularly at 6 months of age, at which time the global recommendation is to transition infants from exclusive breastfeeding to complementary feeding (see Figure 1).
Interval growth and z-scores were not documented by nurses in one third or more visits. This incomplete documentation of assessments is of concern because the primary aim of the PDC is to be able to identify growth and other challenges early for appropriate intervention. By not completing the full assessments, early signs of growth failure may be missed. Lack of completed nutrition assessments and documentation were also gaps observed in national nutrition programs implemented in Brazil and Bangladesh (Abud & Gaíva, 2015;Saha et al., 2015). This is also a common barrier identi- In addition to challenges with the way that growth is monitored, our study showed high numbers of children who are not meeting growth targets, even very early in infancy. Nearly half of infants were stunted and underweight at 6 months, and 20% were wasted, and both wasting and underweight increased from the rates observed at 3 months of age. The highest rates of malnutrition were seen among infants born preterm or LBW. The nutritional vulnerability of infants <6 months is unique in that they rely often exclusively on the mother to provide all of their nutritional and fluid needs through breastfeeding; the nutritional changes that take place in the first 6 months (mechanical, physiological, biochemical and protective) are very rapid, more than changes during other periods of life (Lucas & Zlotkin, 2003). Among those born LBW, these differences may have even greater impact on their nutritional status (Kerac et al., 2010). We were not able to determine from our data why there was an in increase in wasting from 3 to 6 months. Exclusive breastfeeding rates are high in Rwanda, with 87% of infants under 6 months reported to be exclusively In Rwanda, only 58% of infants 6-8 months are fed complementary foods (National Institute of Statistics, 2015). With the high rates of malnutrition in PDC patients already observed when they reach 6 months, this vulnerable period of transitioning complementary feeding will require additional support and specialized interventions for children with feeding difficulties to prevent further growth failure (Kerac et al., 2014 (Kerac et al., 2011). The high rates of malnutrition during toddler years that is seen among infants born preterm and LBW in other studies Van den Boogaard et al., 2017) may be related to nutrition and growth challenges that begin at an early age, as we have identified in this study. Additionally, this study supports prior studies that infants born SGA continue to lag behind those born appropriate for gestational age in terms of nutritional outcomes. For these infants, continued nutritional support is important, but prevention is essential for infants to reach their optimum growth potential.
However, the prevention of malnutrition is reliant on early identification of growth failure, quality growth monitoring and appropriate health and nutrition interventions that encompass the motherinfant dyad. Poor maternal mental health can contribute to child undernutrition (Ruel et al., 2013) and neurological impairments can lead to feeding difficulties and increased risk of aspiration and subsequent illness and early mortality (Kerac et al., 2014;Olusanya & Nair, 2019 (Beck et al., 2018).
This study has some limitations to note. We relied on data available within the EMR system, and so missing data could overestimate the lack of growth monitoring occurring during visits. In addition, the gold standard assessments were conducted post hoc using measurements taken and documented by the nurse during clinic visits. The accuracy of measuring height or taking weight was not assessed in this study; however, the observed differences in nurse classification of poor growth and gold standard using the same input measurements still provide very valuable information about the quality of growth monitoring in neonatal follow-up. This study shows ongoing issues early in infancy with poor growth among infants with medical vulnerabilities following discharge from neonatal units, despite being enrolled in PDCs. It highlights the need for improvements in early nutritional support among these patients, and strategies to improve quality of care delivery in the PDC around nutrition are ongoing. Adequate recognition of poor growth is needed for problems to be addressed. In addition, strategies to prevent prematurity, intrauterine growth restriction, and feeding difficulties that may arise in the first days of life for preterm infants are needed alongside interventions like the PDC to provide essential early intervention and follow-up care for high risk infants. Further research is also needed to help develop more appropriate tools and global guidance for the assessment of growth in infants born prematurely. Abbreviations: HIE, hypoxic ischemic encephalopathy; LBW, low birth weight.

ACKNOWLEDGMENTS
a Adequate interval growth defined as ≥20 g/day for 0-3 months or ≥15 g/day for 3-6 months of age.
F I G U R E 1 Factors that contribute to poor growth in infants enrolled in the Paediatric Development Clinic (PDC)