Original Article

European Journal of Clinical Nutrition (2010) 64, 468–474; doi:10.1038/ejcn.2010.23; published online 10 March 2010

Influence of carotene-rich vegetable meals on the prevalence of anaemia and iron deficiency in Filipino schoolchildren

Contributors: CCM coordinated the implementation of the study, participated in data analysis and writing of the manuscript; JDR-M was principal investigator, participated in the study design and writing of the manuscript; PR-S contributed to data analysis and writing of the manuscript; JAAS contributed to the writing of the manuscript; LWT coordinated the implementation of the study; JBB coordinated the procedure at Tufts University; FSS participated in the study design and was overall coordinator of procedures in the Philippines. The authors critically reviewed the manuscript.

C C Maramag1, J D Ribaya-Mercado2, P Rayco-Solon1, J A A Solon3, L W Tengco1, J B Blumberg2 and F S Solon1

  1. 1Research Division, Nutrition Center of the Philippines, Taguig City, Philippines
  2. 2Jean Mayer US Department of Agriculture, Human Nutrition Research Center at Tufts University, Boston, MA, USA
  3. 3Department of Parasitology, College of Public Health, University of the Philippines, Ermita, City of Manila, Philippines

Correspondence: Professor CC Maramag, Nutrition Center of the Philippines, 2322 Chino Roces Avenue Extension, Western Bicutan, Taguig City 1630, Philippines. E-mail: cmaramag@ncp.org.ph

Received 22 February 2009; Revised 22 January 2010; Accepted 27 January 2010; Published online 10 March 2010.

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Abstract

Objective:

 

To determine the effects of eating carotene-rich green and yellow vegetables on the prevalence of anaemia, iron deficiency and iron-deficiency anaemia in schoolchildren.

Subjects and methods:

 

Schoolchildren (n=104), aged 9–12 years, received standardized meals containing 4.2mg of provitamin A carotenoids/day (mainly β-carotene) from yellow and green leafy vegetables and at least 7g dietary fat/day. The meals were provided three times/day, 5 days/week, for 9 weeks at school. Before and after the dietary intervention, total-body vitamin A pool size was assessed by using the deuterated-retinol-dilution method; serum retinol and β-carotene concentrations were measured by high-performance liquid chromatography; and whole blood haemoglobin (Hb) and zinc protoporphyrin (ZnPP) concentrations were measured by using a photometer and a hematofluorometer, respectively.

Results:

 

After 9 weeks, the mean total-body vitamin A pool size increased twofold (95% confidence interval (CI): −0.11, −0.07μmol retinol; P<0.001), and serum β-carotene concentration increased fivefold (95% CI: −0.97, −0.79μmol/l; P<0.001). Blood Hb (95% CI: −1.02, −0.52g per 100ml; P<0.001) and ZnPP increased (95% CI: −11.82, −4.57μmol/mol haem; P<0.001). The prevalence of anaemia (Hb<11.5g per 100ml) decreased from 12.5 to 1.9% (P<0.001). There were no significant changes in the prevalence of iron deficiency or iron-deficiency anaemia.

Conclusions:

 

Ingestion of carotene-rich yellow and green leafy vegetables improves the total-body vitamin A pool size and Hb concentration, and decreases anaemia rates in Filipino schoolchildren, with no effect on iron deficiency or iron-deficiency anaemia rates.

Keywords:

β-carotene; vitamin A; anaemia; iron deficiency; iron-deficiency anaemia; schoolchildren; Philippines

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Introduction

Anaemia remains a public health problem affecting 818 million women and young children worldwide (McLean et al., 2007). Among the most vulnerable groups are schoolchildren, 53% of whom in developing countries are anaemic (ACC/SCN, 2000). In the Philippines, 37.4% of 6- to 12-year-old children are anaemic (FNRI-DOST, 2006). Cognitive performance, behaviour, physical growth and immunity of these schoolchildren are likely to be impaired (UNICEF/UNU/WHO, 2001).

The interactions between vitamin A and iron metabolism have been described in animal and human studies. Vitamin A repletion in vitamin A-deficient rats enhanced optimum erythropoiesis and iron mobilization from iron stores (Roodenburg et al., 1996). A number of studies among children, aged 1–13 years, showed significant improvement in mean haemoglobin (Hb) concentrations and a decrease in anaemia prevalence after supplementation with vitamin A capsules (Bloem et al., 1989, 1990; Smith et al., 1999; Zimmermann et al., 2006). Greater improvements in iron status were also seen among anaemic 1- to 8-year-old (Mejia and Chew, 1988) and 9- to 12-year-old children (Mwanri et al., 2000) and in pregnant women (Panth et al., 1990; Suharno et al., 1993; Kolsteren et al., 1999; Muslimatum et al., 2001) when iron and vitamin A supplements were given simultaneously rather than when iron or vitamin A were supplemented alone. In addition, iron absorption from iron-fortified foods was enhanced when vitamin A in the chemical form of either retinol or β-carotene was added (Garcia-Casal et al., 1998); improvements in iron status were also seen when vitamin A-fortified foods (Mejia and Arroyave, 1982; Muhilal et al., 1988) and β-carotene-rich foods such as gac (Momordica cochinchinensis) fruit (Vuong et al., 2002), amaranth, spinach, cabbage, colocasia and radish leaves (Agte et al., 2006) and papaya and carrot (Ncube et al., 2001) were consumed.

In contrast, a study conducted by de Pee et al. (1998) designed to compare the bioavailability of carotenoids from orange fruit and from leafy vegetables and carrots among anaemic schoolchildren showed that Hb concentration did not change among those fed green leafy vegetables and carrots despite significant improvements in their serum carotenoid concentrations. A study among anaemic preschoolers fed dark-green, leafy vegetables showed similar results in that there was no improvement in Hb concentration despite an increase in serum retinol concentration (Takyi, 1999).

A low blood Hb concentration (<11.5g per 100ml) is most commonly used to detect anaemia, and an elevated blood zinc protoporphyrin (ZnPP) concentration (ZnPP>70μmol/mol haem) is deemed to be indicative of iron deficiency, with or without concurrent anaemia. In this study, our objective was to evaluate the effects of ingesting carotene-rich green and yellow vegetable meals for 9 weeks on whole blood Hb and ZnPP concentrations of generally healthy, free-living schoolchildren.

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Methods

Subjects

Schoolchildren, 54 girls and 65 boys, aged 9–12 years, from two elementary schools located in the adjacent rural communities of Banawang and Atillano Ricardo in Bagac, Bataan province, Philippines, were recruited in June 2004 to participate in a food-intervention study to investigate the influence of amounts of dietary fat on the bioavailability of plant carotenoids (Ribaya-Mercado et al., 2007). All the subjects were in generally good health, with no chronic or acute illnesses, febrile conditions or gastrointestinal problems; they had no overt diagnostics clinical signs of vitamin A or iron deficiency, and they did not take any nutritional supplements or medications during the time of study.

Approval to conduct the study was obtained from the National Ethics Committee of the Philippine Council for Health Research and Development, and from the Human Investigation Review Committee of Tufts University-New England Medical Center. Written informed consent was obtained from the children and their caregivers.

Study protocol

The details of the dietary intervention have already been described (Ribaya-Mercado et al., 2007). Briefly, the children were fed standardized meals three times daily (that is, before the start of morning class, at lunch time and after the last afternoon class) on school days (5 days/week) for 9 weeks at their schools. Nutritionists recorded food intakes and any plate wastes after every feeding session. No dietary restrictions were imposed on the study participants; their intakes of self-selected foods that were not provided by the dietary intervention were recorded daily by them and their caregivers, and were validated by nutritionists through daily interviews.

Trained nutritionists measured each child's weight and height using a platform weighing scale (Detecto, Webb City, MO, USA) and a microtoise (Body Care Height Meter, 200cm, Chasmors, London, England), respectively. Weight-for-age z-scores, height-for-age z-scores and body mass index-for-age z-scores were determined using the 2000 Centers for Disease Control and Prevention growth reference data (Kuczmarski et al., 2000).

Stool samples were collected from each child and analysed for presence of soil-transmitted helminths using the Kato-Katz technique (Martin and Beaver, 1968). Those found to have parasitic infections were given an anthelmintic treatment of 400mg of albendazole tablets (Kopran, Worli, Mumbai, India) 1 month before the start of the feeding period. Stool analysis was repeated at midway and at the end of the feeding period for all subjects; those found to be re-infected with helminths were given a repeat anthelmintic treatment at the end of the study.

Tests for vitamin A and iron status, and other biochemical measurements were done at baseline and at the end of the 9-week intervention period as described below.

Study meals

The intervention was the standardized meals that contained the following sources of provitamin A carotenoids: carrots, squash fruit, pechay (bok choy; Brassica chinensis) and kangkong leaves (swamp cabbage; Ipomea batatas aquatica). The ingredients in these meals were based on three non-consecutive 24-h food recall (2 weekdays and 1 weekend) that was conducted before the intervention. This was done in order to give meals that were customary to the subjects. The meals provided 1.4mg of provitamin A carotenoids/meal (or ~4.2mg/day), mainly as β-carotene. Also included in each meal were small amounts of either chicken or pork meat that provided ~4.2μg of preformed retinol/meal (or ~12.6μg/day). The choice of vegetables and meals were based on a food frequency survey.

There were different portion sizes for vegetables given to the children, the amount of which depended on the menu and the specific vegetables given. An example of a daily menu (with the accompanying vegetable portions) would have sotanghon (30g of pechay and 5g carrots); ginataan (70g squash, 50g stringbeans and 5g carrots); and chicken tinola (25g pechay, 30g sayote and 5g carrots). The aim was to give ~400 retinol activity equivalents/day, with most of the vitamin A coming from vegetables.

Because the goal of the dietary intervention was to determine the influence of amounts of dietary fat on the bioefficacy of plant provitamin A carotenoids in improving vitamin A status (Ribaya-Mercado et al., 2007), the children were divided into three treatment groups, and their meals provided different amounts of dietary fat from refined coconut oil, that is, either 2.4, 5 or 10g fat/meal, which are equivalent to fat intakes of 7, 15 or 29g/day. By adjusting their carbohydrate content, the meals provided similar amounts of energy. The energy and nutrient contents of all foods eaten during the 9-week intervention period were computed by using the Philippine Food Composition Tables (FNRI, 1997).

Biochemical measurements

Venous blood for biochemical analysis was drawn at baseline and at post-intervention. Estimation of the total-body vitamin A pool size was carried out using the deuterated-retinol-dilution technique, whereas serum retinol and carotene concentrations were analysed using a gradient reversed-phase high-performance liquid chromatography procedure (Ribaya-Mercado et al., 2007). Whole blood Hb was measured on-site using a HemoCue B-Hemoglobin photometer (HemoCue, Angelholm, Sweden), and anaemia was defined as Hb concentration <11.5g per 100ml (UNICEF/UNU/WHO, 2001). Whole blood ZnPP was determined on-site using a hematofluorometre machine (AVIV Biomedical, Lakewood, New Jersey, USA), and iron deficiency was defined as ZnPP concentration >70μmol/mol haem (UNICEF/UNU/WHO, 2001). Serum C-reactive protein was measured in all children at baseline and at endline. Serum C-reactive protein was analysed at the Bureau of Research Laboratories, Department of Health, Manila, by solid-phase sandwich immunometric assay with a NycoCard READER II System (Axis-Shield Group, Oslo, Norway). Children with serum C-reactive protein level of greater than or equal to10mg/l indicative of an active acute phase response with which serum retinol may decrease transiently (Stephensen and Gildengorin, 2000) were excluded from the analysis.

Statistical analysis

Biochemical measurements at baseline and at post-intervention were compared by Student's paired t-test. The prevalence of anaemia, iron deficiency and iron-deficiency anaemia at baseline were compared with those at post-intervention using an Exact McNemar's χ2-test. Analyses were conducted at the P<0.05 level using Stata version 9.2 (Stata, College Station, TX, USA).

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Results

A total of 116 schoolchildren (62 boys and 54 girls) completed the dietary intervention phase of the study; however, only 104 (56 boys and 48 girls) have complete data for both vitamin A and iron measurements. Their mean age was 10.6 years; mean weight was 26.3kg (Table 1). Among them, 47.8% were underweight, 38.1% were stunted and 13.3% were wasted.


Analysis of the children's total food intake during the intervention period (that is, from standardized meals provided at school 5 day/week, and from self-selected foods during schooldays and weekends) showed that the children assigned to the three treatment groups ate similar amounts of energy, protein, retinol and provitamin A carotenoids, and differed only in their intakes of fat and carbohydrates (Ribaya-Mercado et al., 2007). The dietary iron intakes of the three treatment groups on schooldays (11.4, 11.1 and 11.0mg/day) and on weekends (6.5, 6.5 and 6.7mg/day) were not different. The usual food sources of iron were meat, fish and vegetables.

There were no significant differences among the three treatment groups in total-body vitamin A pool size, in serum β-carotene and retinol concentrations, and in the changes in these measurements in response to the dietary intervention, thus indicating that the dietary fat requirement for optimal utilization of plant provitamin A carotenoids is minimal (Ribaya-Mercado et al., 2007). Similarly, there were no significant differences among the three groups in blood Hb and ZnPP concentrations and in changes in these measurements, in response to the dietary intervention. Thus, in this report, pooled data from the three treatment groups are given.

The dietary intakes of vitamin A and iron of the schoolchildren were greater during schooldays when study meals were provided than during weekends when no study meals were provided and the children ate their usual self-selected diets (Table 2). The mean total vitamin A intake during schooldays was 94% adequate, and on weekends it was 41% adequate based on the recommended nutrient intake of 400μg retinol activity equivalents/day for this age group (FNRI, 2002).


The usual (weekend) dietary iron intakes of all children aged 9 years were 66% adequate, and those of boys and girls aged 10–12 years were 48 and 34% adequate based on the Philippine recommended nutrient intake (11mg/day for 7- to 9-year-old and 13 and 19mg/day for 9- to 12-year-old boys and girls, respectively) (FNRI, 2002). When study meals were provided on schooldays, the dietary iron intakes of 9-year-old children fully met the recommended nutrient intake for iron of 11mg/day; however, the iron intakes of 10- to 12-year-old boys and girls were only 85 and 58%, respectively, of the recommended intakes of 13 and 19mg/day for boys and girls in this age range.

The weekend dietary intake for vitamin C is 85% adequate for children 7–9 years and 41% adequate for those 10–12 years. During study intervention days, the adequacy was at 177 and 152% for ages 7–9 and 10–12 years, respectively (FNRI, 2002).

After 9 weeks of dietary intervention, the children's total-body vitamin A pool size increased twofold (P<0.001), and their serum β-carotene concentration increased fivefold (P<0.001); there was no significant change in serum retinol concentration (Table 3). At post-intervention, the mean blood Hb concentration increased by 0.8g per 100ml (P<0.001); whereas ZnPP concentration increased by 8.2μmol/mol haem (P<0.001). There was a significant reduction in anaemia prevalence from 12.5 to 1.9% (P=0.001) and no change in iron deficiency or iron-deficiency anaemia (Table 3).


At baseline, the cumulative prevalence of soil-transmitted helminths was 48%, with 9% of the children infected with Ascaris lumbricoides, 43% with Trichuris trichiura and 3% with hookworm. After treatment with albendazole, the cumulative prevalence of helminthic infections was reduced to 20% after 2 months, and then increased to 33% after 3 months. Helminthic infections, particularly hookworms, have adverse effects on Hb levels and iron status in both children and adults (Olsen et al., 1998). In this study, the intensity of all the helminth infections at baseline, midline and at post-intervention were light. Reanalysis of the results excluding subjects with any of the helminths at the three time points at which helminth load was measured showed the same results as with all the subjects included (data not shown).

All the children had serum C-reactive protein levels of less than 10mg/l at baseline and at endline.

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Discussion

We have previously reported that a 9-week diet of carotene-rich yellow and green leafy vegetables resulted in increases in serum β-carotene and other carotenoids, total-body vitamin A pool size and liver vitamin A concentration, with no significant change in serum retinol concentration in Filipino school-aged children (Ribaya-Mercado et al., 2007, 2008). We now report that the vegetable diet intervention also increased the mean Hb concentration and reduced the prevalence of anaemia in this population, without significantly affecting iron stores and the prevalence of iron-deficiency anaemia.

These findings are significant at two levels. First, it provides evidence for a simple food-based intervention that may contribute to the reduction of anaemia in developing countries. Second, it raises the possibility that carotenoids may have compartmentalized effects on iron metabolism by facilitating the incorporation of iron into Hb.

We have previously reported that poor intakes of bioavailable iron and vitamin C, low maternal education, and low socioeconomic status are independent risk factors for anaemia in preschool-aged Filipino children (Tengco et al., 2008). To address inadequate iron intakes in Filipino schoolchildren and pregnant women, we have demonstrated that the provision of iron supplements (Risonar et al., 2008a, 2008b), multiple micronutrient-fortified beverage (Solon et al., 2003) and iron-fortified bread (Cabalda et al., 2009) can improve their iron intakes and status.

In this report, the ingestion of vegetable meals for 9 weeks by school-aged children resulted in a 0.8g per 100ml increase in mean Hb concentration and an 84% reduction in the prevalence of anaemia. As a comparison, the provision of weekly iron supplements to Filipino schoolchildren for 27 week resulted in a mean increase in Hb of 0.4g per 100ml and a reduction of anaemia prevalence by 53.7% (34). Studies in other countries have likewise shown that carotenoid-rich diets or β-carotene supplements can increase Hb concentrations (de Pee et al., 1998; Ncube et al., 2001; Vuong et al., 2002; Agte et al., 2006). The type of carotene-rich foods may have an influence on the magnitude of Hb increase, with fruits being more effective than dark-green leafy vegetables (de Pee et al., 1998). The expected improvement in Hb, however, may be tempered by the presence of infections such as malaria (Takyi, 1999).

The study meals, which consisted mostly of carotene-rich vegetables, displaced some of the animal foods that the children normally ate, resulting in a reduction in the amounts of preformed retinol and of bioavailable haem iron consumed during the intervention days. Nonetheless, there was a significant improvement in their Hb concentration after consuming the study diet for 9 week. This improvement in Hb may be attributed to the relatively high sufficiency of dietary plant provitamin A carotenoids that resulted in improved vitamin A stores (Ribaya-Mercado et al., 2007), without improvement of iron stores. The high proportion of β-carotene in the diets may have contributed to the absorption of iron from the meals and its subsequent utilization in haematopoiesis. It has been reported that among adult humans, β-carotene fortificant was more effective than vitamin A fortificant in improving iron absorption when added to high-phytate iron-fortified cereals such as rice, corn and wheat (Garcia-Casal et al., 1998). An in vitro study using Caco-2 cells showed that addition of β-carotene increased the absorption of iron even when tannin or phytate was present, whereas a similar effect was not seen when vitamin A was added (Garcia-Casal et al., 2000).

It should be noted that there was also a significant increase in intake of iron and vitamin C from the intervention. These may have resulted in improved Hb levels. However, the ZnPP levels did not improve and there was no effect on iron deficiency and iron-deficiency anaemia rates. Improvement of iron deficiency with iron supplementation have been seen in interventions as short as 8 weeks (Schultink et al., 1995). Therefore, we are less inclined to suppose that the effect was due to increased intake or absorption of iron.

Food-intervention studies conducted either among anaemic children or non-anaemic adults gave varied results. In general, studies in which carotene-rich fruits were given as the food intervention for 30–60 days showed significant improvements in Hb concentrations by 0.5–1.1mg per 100ml (de Pee et al., 1998; Ncube et al., 2001; Vuong et al., 2002). No significant increase in Hb concentration was observed by feeding dark-green, leafy vegetables for 9–12 weeks to anaemic children (de Pee et al., 1998; Takyi, 1999), a result attributed to the high phytate content of dark-green, leafy vegetables that may have inhibited iron absorption (de Pee et al., 1998) and to the presence of other probable causes of anaemia in the study area such as malaria infection and gum bleeding (Takyi, 1999). However, a study among non-anaemic adults showed a significant increase from 6.4 to 11.1% in Hb concentration after consuming green leafy vegetables for only 3 weeks (Agte et al., 2006). The inconsistencies among studies regarding the effect of carotene-rich meals on Hb concentration may be due to differences in the food provided and the biological characteristics of subjects.

The significant increases in Hb and ZnPP concentrations and nonsignificant increase in prevalence of iron deficiency imply that consumption of carotene-rich vegetables contributed to the improvement of Hb but had no beneficial effect on iron stores. This raises the question of how this may have occurred. Our participants were healthy schoolchildren, most of whom had Hb and ZnPP concentrations that were within normal levels before the start of the feeding period. We hypothesize that the improved vitamin A status of the subjects, through ingestion of carotene-rich yellow and green vegetables, may have led to an enhanced use of iron from body stores for the production of blood cells (Semba and Bloem, 2002) resulting in an increased Hb concentration. The study by Muslimatum et al. (2001) among pregnant women showed a significant increase in Hb and a significant decrease in serum ferritin from baseline levels among those provided with weekly iron and vitamin A supplements, whereas no significant change was observed among those provided with weekly iron supplements only, suggesting that vitamin A improved the use of iron from body stores and increased erythropoiesis.

The interaction of iron and infection has been reviewed (Doherty, 2007). The relevance of a food-based intervention and a compartmentalized effect on iron metabolism can be seen in the light of the effects of iron supplementation in children in a malaria-endemic setting (Sazawal et al., 2006). The study by Sazawal et al. (2006) raised the issue of the effect of iron supplementation on susceptibility to infection. Recently, it has been shown that in malaria-endemic settings, iron-deficient pregnant women were protected from malaria (Kabyemela et al., 2008). Thus, the findings of our vegetable-intervention study may be especially relevant for areas with malaria because this intervention can improve Hb concentrations without increasing iron stores.

In summary, our findings suggest that daily consumption of carotene-rich, yellow and green vegetables with minimal dietary fat improves both vitamin A status and Hb concentration and decrease the prevalence of anaemia, but has no effect on iron-deficiency anaemia, in this population of schoolchildren. We recommend the promotion of vegetables in a well-varied diet, including haem or non-haem sources of iron, to improve dietary nutrient absorption.

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Conflict of interest

The authors declare no conflict of interest.

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Acknowledgements

We thank the children who participated in this study and their caregivers; and the staff of the Nutrition Center of the Philippines, and of the Bureau of Research and Laboratories, Department of Health, Manila, for their contributions during the field work.

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