Infant feeding, growth monitoring and the double burden of malnutrition among children aged 6 months and their mothers in KwaZulu‐Natal, South Africa

Abstract South Africa has a documented high prevalence of stunting and increasing obesity in children as well as obesity in adults. The double burden of malnutrition, which can be on an individual‐, household‐ or population level, has implications for both health and the economic development of a community and country. This paper describes a large‐scale survey (N = 774) of infant feeding, growth monitoring and anthropometry among mother and child pairs aged 6 months of age in KwaZulu‐Natal (KZN), South Africa, conducted between January and August 2017. Among children, a large increase in the prevalence of stunting and obesity was seen between birth and 6 months of age increasing from 9.3% to 21.7% and 4.0% to 21.0%, respectively. 32.1% of the mothers were overweight [body mass index (BMI): 25.0–29.9] and 28.4% had obesity grade 1 (BMI: 30–<40). Although most mothers (93%; 563/605) initiated breastfeeding, the introduction of other foods started early with 17.6% (56/319) of the mothers having started giving other fluids or food to their child within the first month. At 6 months 70.6% (427/605) children were still breastfed and 23.5% were exclusively breastfed. In addition, we found that length measurements were done less frequently than weight measurements between birth and 6 months, on average 2.2 (SD: 1.3) versus 5.8 (SD: 1.5) times. Moreover, there is a need for improvement of health worker training and understanding regarding anthropometric measurements when assessing malnutrition in children in the clinics. Early detection and improved infant feeding practices are key in preventing both stunting and obesity in children.


| INTRODUCTION
Globally, there are 144 million children under the age of 5 years who are stunted and 47 million who are wasted, while 38.5 million are overweight or obese (World Health Organization, 2020). The term malnutrition encompasses undernutrition (wasting, stunting and underweight), inadequate vitamins or minerals, overweight and obesity according to the World Health Organization (WHO) (World Health Organization, 2020).
When both over-and undernutrition exist at the same time within a country, community or individual, this is referred to as the double burden of malnutrition (DBM) (Popkin et al., 2020). Undernutrition in early life may lead to a higher risk of overweight later in life due to inappropriate or rapid weight gain when the nutritional conditions of the child improve (Martins et al., 2011). Moreover, the risk of DBM is increasing among people with low income in rural areas in low-and middle-income countries (LMIC) due to a new nutrition reality with increasing consumption of ultra-processed food leading to increasing prevalence of overweight and obesity in these communities (Wells et al., 2020).
DBM is a global concern. According to Popkin et al. (2020), this occurs when there is a rapid increase in the prevalence of overweight and obesity in LMIC, at the same time as these countries are experiencing a slower decline in the prevalence of undernutrition. Malnutrition in early life either undernutrition or, particularly obesity, can be the underlying cause of many non-communicable diseases (NCDs) (Abarca-Gómez et al., 2017). NCDs such as cardiovascular diseases, cancers, chronic respiratory disease, and diabetes, kill 41 million people each year, and there is a clear link between severe malnutrition in childhood and later development of cardiovascular disease, hypertension, and impaired glucose metabolism (Grey et al., 2021). In addition, rapid weight gain early in life has been shown to be a risk factor for later insulin resistance, obesity, and cardiovascular disease, particularly among formula-fed infants (Singhal & Lucas, 2004). Therefore, it is important to reduce the risk factors associated with NCDs, which include unhealthy diets, malnutrition in early life and suboptimal breastfeeding practices.
Optimal breastfeeding is important for preventing malnutrition among infants and young children by providing the best source of energy and vitamins and by protecting children from childhood diseases that can adversely affect nutritional status. Infants who have been exclusively breastfed for 6 months have a decreased risk of diseases, such as gastrointestinal infections, pneumonia and hospitalisation compared with non-exclusively breastfed or formula-fed infants (Bahl et al., 2005;Horta et al., 2015;Ogbo et al., 2017). Sustained breastfeeding plays an important role at the time when complementary feeding is introduced, which frequently overlaps with linear growth faltering as children have to adapt to new tastes and textures (Wamani et al., 2006). Therefore, it is important to monitor growth, especially during the period when complementary foods are introduced.
The combination of women with overweight and children with stunting is the most common form of household-level DBM (Popkin et al., 2020). Anthropometric measurements are used to categorise low birthweight, stunting (low height-for-age) or wasting (low weigh-for-height) during infancy or childhood to identify undernutrition (Wells et al., 2020). However, if lengths and weights are omitted or incorrectly measured or interpreted, malnutrition will be missed, and children will not receive the appropriate malnutrition support and management. To prevent long-term morbidity, it is crucial that optimal feeding, particularly breastfeeding, is supported and that malnutrition, including obesity, is identified early through growth monitoring. In this paper, we describe a large-scale survey of infant feeding, growth monitoring and DBM among mother/carer-baby pairs at 6 months of age in KwaZulu-Natal (KZN), South Africa.

| METHODS
This study forms part of a larger study undertaken to estimate exclusive breastfeeding rates among 14 weeks old infants in KZN at two time points, known as KIBS1 (KwaZulu-Natal Initiative for Breastfeeding support) and KIBS2 (Horwood et al., 2018(Horwood et al., , 2020. In this paper, we present the findings of a cross-sectional survey conducted among mothers and caregivers of children aged 6 months (25-31 weeks), which aimed to explore growth monitoring practices, anthropometry and feeding practices among 6-month-old children, and was conducted alongside the KIBS2 breastfeeding survey between January and August 2017.

| Study setting
The study was undertaken in primary health care (PHC) clinics in KZN, one of the largest provinces in South Africa, with a population of over 11 million people (Stats SA, 2019). Free health care services are provided to mothers and children attending public health facilities in South Africa. PHC clinics provide the initial point of contact where maternal and child health services are provided, including antenatal, post-natal and child health, nutrition, immunisation, and curative services.

Key messages
• The double burden of malnutrition is severe in KwaZulu-Natal with high rates of maternal obesity and increasing prevalence of stunting and obesity among infants in the first 6 months of life.
• Breastfeeding and complementary feeding practices are suboptimal and additional support for breastfeeding is required in the post-natal period and in the workplace to address breastfeeding challenges.
• Growth monitoring is inadequate in health facilities leading to many lost opportunities for early identification of malnutrition. Hence, anthropometric practices and interpretation of findings need to be strengthened.

| Sampling
The sample size was calculated based on obtaining valid estimates for breastfeeding rates among children at 14 weeks for the KIBS2 study.
Thirty clinics were randomly sampled, and the sample included clinics in all districts of the province. This survey was conducted alongside KIBS2 and caregivers attending with 6-month-old children were recruited for the duration of the KIBS2 study period but were not part of the KIBS2 study.
All mothers or caregivers aged 15 years or above who attended the participating clinics with a child aged 6 months (25-31 weeks) were eligible to participate in the study. The 6 months age was chosen to coincide with the time when children attend for measles immunisation, which presented an opportunity to reach children in a narrow age band. Non-maternal caregivers answered a subset of relevant questions.

| Data collection
Exit interviews were conducted after completion of the clinic visit by trained fieldworkers in the local language (English or isiZulu) using structured questionnaires (Supporting Information File 1). Background data, such as age, education level and household setting, including access to water and electricity were asked.
Mothers and non-maternal caregivers were asked questions about feeding practices since birth and other feeding practices such as whether any other food or fluids were given to the child together with, or instead of breastmilk. Current feeding practices were assessed using a 24-h food and fluids recall. Moreover, mothers and non-maternal caregivers were asked about their knowledge and attitudes towards breastfeeding with statements and questions. The questions were a series of true/false (T/F) questions constructed in collaboration with the Nutrition Directorate, Department of Health in KZN. These included the following statements: breastfed babies have less diarrhoea (T); a mother who feels the baby is not getting enough breastmilk should top up with formula milk (F); infant formula contains all the ingredients found in breastmilk (F).

Patient-held records for the children [Road to Health Card (RTHC)]
were reviewed by fieldworkers and all anthropometric data (length and weight measurements) recorded on the RTHC since birth until the day of data collection were captured, together with the date of recording.
The mother's current height and weight were measured and recorded at the site.

| Ethical considerations
Ethical approval was obtained from the Biomedical Research Ethics Committee at the University of KwaZulu-Natal (BE064/14) and from the KZN Department of Health. All participants provided written informed consent. Confidentiality and anonymity were assured through the allocation of study numbers. To ensure all mothers of young children were able to participate, ethical approval explicitly allowed the inclusion of younger mothers aged 15-17 years. Permission to undertake the study was obtained from the KZN Department of Health, district managers in all districts, and facility managers in participating clinics.

| Data management and analysis
Data was captured on handheld android tablets and uploaded to a central server in real time. Extensive quality control checks were carried out by trained study staff.
Anthropometric data was cleaned in two stages. First, as anthropometric data was captured from the RTHC, inter-and intra-rater reliability could not be assessed. Therefore, if errors in the recording of the data of children were identified this data was removed from the data set. Errors of recording occurred when the value recorded was incompatible with a child's length or weight. The following numbers of children were removed: seven for birthweight, two for birth length, 14 for weight at 6 months and 45 for lengths at 6 months.
Measurements were set to missing if one or more of these extreme values existed after individually assessing them. The following numbers of children with extreme values were excluded: two for LAZ at birth; seven for LAZ at 6 months; 22 for WLZ at birth; 17 for WLZ at 6 months.
There was a wide variation in the quality and number of measurements across clinic visits from birth to 6 months. The study team's presence at the site is a likely reason for an increased number of weight and length measurements performed at the time of the interview. However, to display the difference in weight and length outcomes, all recorded measurements were included. Therefore, this resulted in different denominators for calculations regarding length and weight, such as LAZ and WLZ.
Descriptive statistical analyses were undertaken to describe the characteristics and distribution of the population. Categorical data are presented as percentages while continuous data are presented as means with standard deviations and confidence intervals.
Multi-variable analysis was used to investigate potential risk factors with the dependent variables LAZ and WLZ with cut-offs at <−2 and >2 z-scores, respectively. LAZ < −2 indicates stunting and WLZ > 2 indicates overweight. Selected variables were based on the UNICEF Conceptual framework on young child malnutrition from 1991 (United Nations Children's Fund, 1991). The selected variables were gender, birthweight, household information, reported breastfeeding practices for the first 6 months and current breastfeeding practices (assessed through 24 h recall), mother's age, mother returning to school, mother's height and HIV status. These were all included in the final model because of potential confounding factors. Only the adjusted OR with 95% CI analysis is presented in the results.

| RESULTS
Seven hundred and seventy-four interviews were conducted with caregivers of children aged 6 months attending PHC clinics between January and August 2017. Most children attended the clinic with their mother (605/774; 78.2%) but some children attended with other caregivers, referred to as non-maternal caregivers (169/774; 21.8%).
Among the non-maternal caregivers, most were relatives of the child.
Non-maternal caregivers reported that the reason for the mother's absence was either because: the mother was at work (102/169; 60.3%), the mother was at school (53/169; 31.4%), the mother was unwell (2/169; 1.1%) or other reasons (not specified) (9/169; 5.3%). Demographic information about all caregivers is shown in Table 1; however, some questions were not asked to non-maternal caregivers. Mothers displayed a positive attitude and good knowledge of breastfeeding with over 75% of the mothers having 9 or more correct answers out of a total of 12 questions/claims about breastfeeding, with 23.1% having 11 or more correct answers.

| Growth monitoring
Among all participants, 772/774 brought the child's RTHC with them on the day of the visit. To assess the coverage of growth monitoring among participants, we determined the proportion of children who had their weight and length measured at each month of age. This was based on recordings of length and weight on the RTHC. The proportion of children who had recorded weight and length measurements at each month is presented in Figure 1 (n = 772).
The average number of weight measurements recorded on the RTHC for each child between birth and 6 months was 5.8 (SD: 1.5), and the average number of length measurements was 2.2 (SD: 1.3).
Most children had their length and weight recorded at birth and at 6 months. The number of length measurements recorded between birth and 6 months was less than the number of weight measurements recorded. In this time period, 70.2% of the children had the recommended 6 weights recorded (i.e. at birth and monthly thereafter) while only 3.8% had more than 6 or more lengths recorded (  Table 3 provides information on LAZ and WLZ at birth and 6 months for the various cut-off points from <−2 to >2. The total numbers differ by column due to inconsistent measurements (children having either no length or no weight at the measurement time point) but also due to the WHO cut-offs explained in the methods.

| Infants' anthropometry
Thus, the denominator changes according to the data available. The reason for keeping the different denominators was to illustrate the difference in measures (lengths and weights) taken at the clinics as shown in Figure 1. Nevertheless, the tables show strikingly large percentages both at birth and at 6 months for the cut-off below −2 and above 2. Moreover, 53/555 (9.5%) of the children were both stunted and overweight in the sample at 6 months. There was one child who was both stunted and wasted at 6 months. Table 4 displays the categories of LAZ (stunting and normal) and WLZ (normal and overweight) at 6 months by birthweight categories.
There were 482 children who had all the information available; birthweight, weight and length at 6 months.
According to the adjusted logistic regression (Table 5), we found that the odds ratio (OR, 95% confidence interval) for low birthweight (below 2500 g) was a risk factor for stunted growth at 6 months (OR: 3.64, 1.92; 6.88). Female sex seems protective with respect to stunting at 6 months Abbreviations: LAZ, length-for-age z-score; WLZ, weight-for-length z-score.
There were no other associations found with stunting at 6 months.
Moreover, no clear factors were associated with obesity at 6 months.

| DISCUSSION
We found that DBM was prevalent in KZN, with the majority of mothers being overweight or obese, and many children developing stunting in the early months of life. Breastfeeding practices were suboptimal and exclusive breastfeeding was uncommon with many mothers adding other food and fluids to the infant's diet even in the first month of life. Although in our study we did not find a significant association between breastfeeding and stunting, other studies support this association and it is likely that inadequate breastfeeding contributed to the high rates of stunting (Black et al., 2013;Campos et al., 2020). Further, our findings suggest that complementary feeding is inadequate at the time of most vulnerability for the development of malnutrition, and children did not get the recommended variety of nutritious complementary food. This occurs against a background of inadequate growth monitoring in clinics, which hinders the early identification of malnutrition so that preventive interventions cannot be implemented. Our findings suggest that there are multiple contributing factors to the high rates of chronic malnutrition and the DBM in SA.
Although most mothers initiated breastfeeding and many were still breastfeeding their children at 6 months, poor infant feeding practices were observed. First, there was a tendency to add other foods or fluids very early. Early introduction of complementary feeds has shown to be a risk factor for faltering growth (Martins et al., 2011), which might lead to overweight and obesity later in life (Ramokolo et al., 2015). Moreover, children who are stunted, wasted or underweight have an increased risk of death from diarrhoea, pneumonia and other infectious diseases (Black et al., 2013). Identification of behavioural and structural barriers to delaying the introduction of other foods is needed to improve exclusive breastfeeding practices in this area. In particular, the common reasons for adding other foods included mothers' experiences with or perceptions about breastfeeding and returning to work or school. Therefore, stronger support is needed for breastfeeding not only at the time of delivery but also for mothers experiencing breastfeeding challenges after returning home or when returning to work or school. Community health workers are deployed in communities in South Africa and are ideally placed to support breastfeeding at the household level. Similar reasons and findings have also been detected in other sub-Saharan countries (Maonga et al., 2016;Masuke et al., 2021). Although there is strong support for breastfeeding provided during antenatal care and most mothers intended to breastfeed, most women fail to breastfeed exclusively or sustain breastfeeding (Horwood et al., 2020;Richard et al., 2021 Household-level DBM is clearly present with high levels of overweight and obesity among mothers, where at the same time high levels of stunted and overweight children were observed. Improved management of moderate malnutrition and identification of malnutrition at the household levels for both mother and child is therefore important, and nutrition advice may need to focus more on the mother-infant dyad rather than a more traditional focus on infants. How mothers may benefit from breastfeeding is often under communicated.

| Strengths and limitations
The major strength of this paper is the large representative sample from KwaZulu-Natal, which is a large province in South Africa. Moreover, according to the SANHANES (South Africa National Health and Nutrition Examination Survey-1), stunting is similar in all provinces and it is therefore likely that these findings are similar across South Africa (Shisana et al., 2013). This cross-sectional study also took advantage of the available operational data to get an overview of monitoring practices.
Of course, it is a weakness in terms of reporting growth that the growth data was not complete and that multiple measurements had to be excluded because the quality was so poor, which suggests that measurements were inaccurate. Given that most participants were from rural areas, it is possible that urban clinics would have performed better. On the other hand, the operational data illudes to a naturalist description of monitoring, which should stimulate further discussion, updated guidelines, and hopefully improved practices.
A limitation of the study was having a long recall period of up to 6 months, which can provide recall bias as mothers and non-maternal caregivers might have difficulty recalling exactly what the infant was fed. There might also possibly have been social desirability bias on how the mothers and non-maternal caregivers answered the questions.

| CONCLUSION
This study highlights that length and weight measurements taken during the first 6 months of a child's life are inadequate in both quantity and quality, based on the number of outlying values. This limits the effectiveness of growth monitoring and assessment of nutritional status. In addition, high rates of both stunting and overweight among children and overweight and obesity in mothers warrants better growth monitoring and detection of malnutrition. Moreover, infant feeding practices, including breastfeeding practices and complementary feeding may need far deeper understanding for improving both guidelines and health services.