Contribution of Milk Beverages to Nutrient Adequacy of Young Children and Preschool Children in the Philippines

Editor(s): Tsz-Ning Mak, Imelda Angeles-Agdeppa, Marie Tassy, Mario V. Capanzana and Elizabeth A. Offord .


Malnutrition is a major public health concern in the Philippines. Milk and dairy products
are important sources of energy, protein, and micronutrients for normal growth and development in children. This study aims to assess the contribution of different types of milk to nutrient intakes and nutrient adequacy among young and preschool children in the Philippines. Filipino children aged one to four years (n = 2992) were analysed while using dietary intake data from the 8th National Nutrition Survey 2013. Children were stratified by age (one to two years and three to four years) and by milk beverage consumption type: young children milk (YCM) and preschool children milk (PCM), other milks (mostly powdered milk with different degrees of fortification of micronutrients), and non-dairy consumers (no milks or dairy products). The mean nutrient intakes and the odds of meeting nutrient adequacy by consumer groups were compared, percentage of
children with inadequate intakes were calculated. Half (51%) of Filipino children (all ages) did not consume any dairy on a given day, 15% consumed YCM or PCM, and 34% consumed other milks. Among children one to two years, those who consumed YCM had higher mean intakes of iron, magnesium, potassium, zinc, B vitamins, folate, and vitamins C, D, and E (all p < 0.001) when compared to other milk consumers. Non-dairy consumers had mean intakes of energy, total fat, fibre, calcium, phosphorus, iron, potassium, zinc, folate, and vitamins D and E that were far below the recommendations. Children who consumed YCM or PCM had the highest odds in meeting adequacy of iron, zinc, thiamin, vitamin B6, folate, and vitamins C, D, and E as compared to other
milks or non-dairy consumers, after adjusting for covariates. This study supports the hypothesis that dairy consumers had higher intakes of micronutrients and higher nutrient adequacy than children who consumed no milk or dairy products. Secondly, YCM or PCM have demonstrated to be good dairy options to achieve nutrient adequacy in Filipino children.

Keywords: milk; dairy; nutrient adequacy; Philippines; young children; preschool children

1. Introduction
A double burden of malnutrition exists in the Philippines. The prevalence of undernutrition in children is high, where one in three children under five years are stunted and 7% are wasted [1]. Micronutrient deficiency continues to be a key public health concern; vitamin A deficiency affects one in five children, while 14% and 18% of children < 5 years are anemic and zinc deficient, respectively [2].

A previous study found that children in the Philippines have poor diet diversity, and the
prevalence of inadequate intakes of micronutrients is high [3]. Seventy-eight percent, 75% and 90% of Filipino children aged one, two, and three to four years, respectively, had inadequate intakes in iron; 62%, 66%, and 84% were inadequate in calcium; 52%, 46%, and 47% were inadequate in zinc, 60%, 41%, and 43% were inadequate in vitamin A, respectively. More than 40% of children aged one year were inadequate in B vitamins (thiamine, riboflavin, niacin, B6, folate, and B12), and in children three to four years, 72% were inadequate in folate and 60% in vitamin C [3]. The diet of children in
the Philippines typically composed of refined rice and energy-dense foods such as cookies and sugar sweetened beverages, low in fruit, vegetables, and protein-rich foods [3]. The consumption of milk and dairy products is generally low among children in the Philippines with a decreasing trend with age [3]. At age one year, 37% of Filipino children were having breastmilk, 35% consuming cow’s milk and 23% consuming toddler milk; at two years, only 11% were receiving breastmilk, 38% of children were consuming cow’s milk, and 15% consuming toddler milk; and, at age three to four years, only 32% of children would consume milk on a given day [3]. Milk and dairy are part of an important food group for preschool children, as it greatly contributes to total energy, protein, and calcium in relation to children’s daily requirements for normal growth and development [4]. In the Philippines, powdered milk is the most common type of milk available. It is a milk usually intended for the whole family, and is typically fortified with
calcium and vitamin A. Young children milk (YCM) and preschool children milk (PCM), are milks tailored for children’s nutritional needs at different age stages, fortified with vitamins and minerals, some with DHA and probiotics. A number of observational studies and randomized controlled trials (RCT) in Europe and Australia and New Zealand have demonstrated that, when compared to cow’s milk, YCM improved nutrient intakes among children above 12 months, particularly in iron and vitamin D [5–9]. Several studies have shown that children who consumed YCM had better iron and
vitamin D status than non-consumers [7,10,11], and it had a lower percentage of body fat than children who consumed cow’s milk [12]. This is likely due to the lower protein of YCM than cow’s milk, as evidence supports the early protein hypothesis that high protein intake in early years might promote weight gain and higher risk of obesity in later life [13,14]. Beyond developed countries, there is a lack of studies on the impact of YCM or PCM in children. A RCT on Indian children found that those who consumed fortified milk had improved weight and height gain and iron status than those who consumed unfortified milk [15]. In the Philippines, only one study can be found to measure the impact of fortified milk among young children. The clinical study showed that preschool children (three to five years) from a small town in Philippines, who
consumed two servings of fortified milk a day for 12 weeks significantly increased the intakes of energy, protein, iron, vitamin A, calcium, thiamin, riboflavin, niacin, and vitamin C when compared to baseline [16]. Therefore, more evidence is needed to examine the role of milks in the diet of children across the Philippines, where nutrient inadequacy is highly prevalent. The aim of the current study was therefore to assess the contribution of different milk types to nutrient intakes and nutrient adequacy among young children and preschool children in the Philippines. We hypothesized that children who consumed milk (YCM/ PCM/ other milks) would have higher intakes of micronutrients and higher nutrient adequacy than children who consumed no milk or dairy products. Furthermore, we also hypothesized that YCM/ PCM consumers may have higher nutrient adequacy than other milk consumers, given the high level of fortification of micronutrients in YCM/PCM.

2. Materials and Methods
2.1. Study Population
Dietary intake data of children aged one to two years (n = 1461) and three to four years (n = 1531) from the 2013 National Nutrition Survey (NNS) were analysed. The details of the NNS have been reported previously [17]. The 2013 NNS was a cross-sectional nationally representative health and nutrition survey of the Filipino population. Filipino households (n = 35,825) were sampled with a response rate of 91% [3]. The Ethics Committee of Food Nutrition Research Institute (FNRI) approved
the survey protocol and data collection instruments. All of the surveyed households provided informed consent prior to participation with a registry number FIERC—2013—001 [17].
2.2. Data Collection
Trained dietitians conducted face-to-face 24-h dietary recalls with a parent or caregiver of each child during household visits, wherein the dietitian recorded all food and beverages that the child consumed the previous day. A first 24-h recall was performed on all children and a second 24-h recall was repeated in 50% of randomly selected households, typically two days after the first recall. The amount of each food item or beverage was estimated while using common household measures, such as cups, tablespoons, by size, or number of pieces. The information was then converted to grams while using a portion-to-weight list for common foods compiled by FNRI or through weighing of the food samples. For powdered milk, a conversion factor of 6.7 was multiplied to estimate the gram weight of fluid milk as consumed, based on the preparation instruction of approximately 36 g milk powder reconstituted to approximately 240 g of fluid milk (in line with recommendation from the Philippines Nutritional Guide Pyramid—four tablespoons of milk powder to one glass of water) [18].
All of the reported foods and drinks were reviewed, to ensure that all of the codes and quantities were correctly entered. The food and beverages consumed were converted to energy and nutrient intakes while using the Philippines Food Composition Tables (PFCT) [19]. The energy intake distribution of the full sample (n = 3016) was assessed and the outliers were defined as energy intakes three standard deviations above and below (±3SD) the mean per age group (one to two year and three to four years) and were removed from analyses. A final sample size of 2992 was retained for analysis.
The 888 unique food items reported were categorised into nine major food groups and further subgroups. The food grouping system was adapted from What We Eat in America Food Categories [20] and US Feeding Infants and Toddlers Study (FITS) adjusted for the Philippines local food culture [3].

Demographic characteristics, including dwelling location, wealth quintiles, mother’s education, occupation status, and civil status were collected. Children’s height-for-age and weight-for-age were obtained and the BMI z-scores were calculated to define their nutritional status (wasting, at risk of overweight, and overweight).

2.3. Data Processing
The three consumer groups were defined as follow. Children who reported to have consumed “Formula”, which included subcategories “Toddler/Pre-school formula” and “Infant formula” were considered as “YCM or PCM consumers”. We identified only 6% of children at age 1 year who were still consuming infant formula. Children who had reported to consume “Milk” which included subcategories “Milk, powdered”, “Milk, fluid”, “Other Milk”, and “Dairy products” were categorized as “Other milk consumers”. Dairy products (cheese and yogurt) consumption was only represented by 2.7% of the sample and was therefore grouped together with the milk subcategories. Children who had consumed both YCM/PCM and other milks were considered as “YCM/PCM
consumers”. All of the children who did not consume any of the above (YCM/PCM, other milk or dairy) were considered “non-dairy consumers”. The nutritional compositions of YCM/PCM, milk (fluid), and milk (powdered) considered in the analyses can be found in Supplementary Materials Table S1.

Twenty-seven nutrients were available in the PFCT. After checking for completeness, 22
nutrients, including total energy (kcal), total carbohydrates (g), fibre (g), protein (g), total fat (g), sodium (mg), calcium (mg), phosphate (mg), iron (mg), magnesium (mg), potassium (mg), selenium (mg), zinc (mg), thiamine (mg), riboflavin (mg), niacin (mg), vitamin B6 (mg), folate (µg), vitamin B12 (mg), vitamin C (mg), vitamin D (µg), and vitamin E (mg) were analysed. Vitamin A, total sugars, saturated fat, monounsaturated fat, and polyunsaturated fat, while available in the PFCT, had high percentage of missing values for the food and beverages of interest, which were deemed too incomplete for the current analysis. The total daily intake of each nutrient based on food consumption was calculated per person per day. An average of nutrient intakes over the two days were considered in the subsequent analyses for children who had a second 24 h recall day.

2.4. Statistical Analysis
All analyses were stratified by age groups: one to two years, and three to four years. The relationships between sociodemographic variables (gender, age group, wealth quintiles, dwelling location, mother’s education, civil status, and occupation status, and BMI z-scores) and consumer groups were tested for significance while using chi-squared tests and Kruskal–Wallis tests. The mean intake per nutrient per consumer group was calculated. Non-parametric Kruskal–Wallis tests were used to compare the mean ranks of each nutrient between three consumer groups due to the skewness of the nutrient intake data. Post hoc Dunn’s tests were then performed to compare mean
nutrient intakes between YCM/PCM consumers and other milk consumers, and YCM/PCM consumers and non-dairy consumers.

Inadequate intakes were defined while using the estimated average requirements (EAR) cut-off method. Children with intake below the EAR for a given nutrient were considered to be inadequate. For nutrients that did not have an established EAR cut-off, e.g., vitamin D and vitamin E, adequate intake (AI) values were used. The Philippines Nutrient Reference Intakes (PNRI) table was used to establish EAR/AI for protein, calcium, phosphorus, iron, selenium, zinc, thiamin, riboflavin, niacin, vitamins B6, B12, folate, and vitamins C, D, and E. For macronutrients (except for protein where EAR
is available), Acceptable Macronutrient Distribution Ranges (AMDR) were used to evaluate carbohydrates and total fat, as a percentage of energy. The proportions of inadequate intakes were classified as %E less than the AMDR lower range. The proportion of children with inadequate intakes were calculated per consumer group.
Logistic regression analysis was used to estimate the odds ratios of children meeting the EAR/AI/AMDR of each nutrient with respect to the consumer group, to test the hypothesis that YCM/PCM consumers (reference group) had higher odds of meeting the EAR/AI/AMDR of nutrient when compared to other milk consumers and/or non-dairy consumers. Adjustment of potential confounding factors—wealth quintiles, dwelling location, mother’s education, and mother’s occupation was included in the final model. R version x64.3.6.1 and R-Studio version 1.2.1335 were used for all of the statistical analysis.

3. Results
3.1. Descriptive Statistics
Table 1 shows a description of the sample population by consumption group. There was an equal split in gender within the sample. Eleven percent of children one to two years suffered from wasting, while 13% were at risk of overweight or overweight. The majority came from the rural area and in poor to poorest wealth quintiles. Most mothers were not working, were married, and were largely high school graduates. There were no significant differences between consumption groups and gender, BMI z-scores, and mother’s civil status. However, wealth quintiles, mother’s education, and mother’s occupation status were significantly related to if children consumed YCM/PCM, other milk or no dairy (all p < 0.001). Of the 1461 children aged one to two years, 43% had no dairy (other milk, YCM or other dairy products), 35% were other milk consumers, and 22% YCM consumers. The mean consumption of YCM before reconstitution was 101 g/d (±SD 69 g) and in fluid weight was 641 g/d (±SD 432 g); mean consumption of other milk before reconstitution was 61 g/d (±SD 58 g) and in fluid weight was 354
g/d (±SD 330 g). Among children aged three to four years (n = 1531), the majority (58%) did not consume any dairy, 34% consumed other milks, and 8% of children consumed PCM. Mean consumption of PCM before reconstitution was 85 g/d (±SD 73 g) and, in fluid weight, was 454 g/d (±SD 355 g); mean consumption of other milks before reconstitution was 46 g/d (±SD 53 g) and in fluid weight 224 g/d (±SD 233 g) for this age group. 

3.2. Comparison of Mean Nutrient Intakes by Consumer Group
3.2.1. YCM/PCM Consumers vs. Other Milk Consumers
Table 2 shows the comparison of mean nutrient intakes by consumer group. YCM/PCM
consumers and other milk consumers had similar macronutrient intakes, except for protein (one to two years only), where YCM consumers had lower intake. YCM/PCM consumers had higher total fat (three to four years only) and higher micronutrient intakes than other milk consumers, except for sodium, phosphorus, riboflavin, and selenium (one to two years only). No significant differences were found for calcium intakes in children aged one to two years. No significant differences were found for sodium, magnesium, selenium, and B12 in the older children. YCM/PCM and other milk consumers both had mean intakes of energy, fibre, and potassium lower than the recommended intake levels. In general, YCM/PCM consumers had mean intakes of
micronutrients closer to the recommendations compare to other milk consumers. In children aged one to two years, other milk consumers had mean intakes of iron, magnesium, folate, and vitamins D and E far below the recommendations.
3.2.2. YCM/PCM Consumers vs. Non-Dairy Consumers Non-dairy consumers had significantly lower intakes than YCM consumers in most macro- and micronutrients, except for fibre in children aged one to two years (p < 0.05). No significant differences
were seen for carbohydrates, fibre, and magnesium and selenium between the PCM and non-dairy consumer groups in children aged three to four years. Non-dairy consumers had mean nutrient intakes far below the recommendation. The only nutrients where non-dairy consumers were in line or above the recommended levels were protein, sodium, selenium, and niacin (all ages); magnesium, B6 and B12 (three to four years only).

3.3. Percentage of Children with Inadequate Intakes
Table 3 shows the proportion of children with nutrient intakes below the EAR or AI across the three consumer groups. Among non-dairy consumers aged one to two years, except for carbohydrates and selenium, more than 50% of children had intakes below the EAR/AI. In particular, almost all children in this group were inadequate in calcium, vitamin D, and iron (99%, 97% and 91%, respectively). The highest level of inadequate intakes among other milk consumers (one to two years) were vitamin D (98%), vitamin E (97%), iron (92%), folate (82%), and vitamin B6 (73%). YCM consumers (1 to 2 years) had the lowest percentage of inadequate intakes when compared to the other
groups. The highest levels of inadequacy in this group were vitamin E (68%), phosphorus (55%), vitamin D (52%), and folate (49%).

Among preschool children, the proportions with inadequate intakes were slightly lower than the younger children, except for calcium in PCM (67%) and other milk consumers (65%), and vitamin D (72%) in PCM consumers. Non-dairy consumers still had the highest proportion of children with inadequate intakes across most nutrients.

3.4. Odds of Nutrient Adequacy Per Consumer Group
Table 4 illustrates the odds ratios of other milk consumers and non-dairy consumers meeting nutrient adequacy when compared to YCM/PCM consumers (reference group), after adjusting for potential confounding factors (wealth quintiles, dwelling location, mother’ education level, mother’s occupation). Among children aged one to two years, other milk consumers were significantly less likely to meet the AMDR for carbohydrates, as well as the EARs for iron, zinc, thiamin, niacin, vitamin B6, folate, vitamins C, D, and E (all p < 0.001), and vitamin B12 (p = 0.002), than YCM consumers (reference group). Other milk consumers were more likely to meet the EAR of protein (p = 0.003),
phosphorus, selenium, and riboflavin (p ≤ 0.001) than YCM consumers. Non-dairy consumers had significantly lower odds of meeting the adequacy of all nutrients when compared to YCM consumers, except for carbohydrates and selenium (both non-significant). In preschool children, other milk consumers were less likely to reach nutrient adequacy in iron, folate, vitamins C, D, E (all p < 0.001), zinc, thiamin, and vitamin B6 (all p < 0.05), but were more likely to meet adequacy in phosphorus and riboflavin when compared to PCM consumers. Non-dairy consumers had lower likelihood of meeting adequacy in total fat, calcium, iron, zinc, folate, vitamins
C, D, E (all p < 0.001), and thiamin (p = 0.005) and vitamins B6 (p = 0.024), but more likely of being within AMDR of carbohydrates (p = 0.016) than PCM consumers.
The results also highlight the sociodemographic factors that were significantly related to
increased or reduced odds of meeting nutrient adequacy. In children one to two years, living in urban areas increased the likelihoods of meeting protein, phosphorus, zinc, thiamin, niacin, and vitamin B6 adequacies; being in the richest wealth quintile were associated with adequacy in total fat, calcium, zinc, thiamin, and vitamin B6 (all p < 0.05). On the other hand, being in poor or poorest wealth quintiles, and/or mothers with education at or below high school levels reduced the odds of meeting adequacy in most nutrients, including protein, total fat, calcium, selenium, zinc, B vitamins, and vitamin E (all p < 0.05). Similar trends were also observed in children aged three to four years. The only nutrient that had an opposite trend than the rest of the nutrients was carbohydrate. In children aged one to two years, being in the richest wealth quintile lowered the odds of meeting the AMD for carbohydrates, and similarly among three to four years, those who were the richest, living in urban dwelling, and with mother currently working reduced the likelihood of meeting AMDR for carbohydrates, while being in the poor or poorest wealth quintile increased the odds. None of the sociodemographic factors were associated with iron, vitamins C and D adequacies
in children aged one to two years, and vitamin B6, folate, vitamins D and E adequacies in children three to four years.