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Community and International Nutrition

Children's Consumption of Dark Green, Leafy Vegetables with Added Fat Enhances Serum Retinol¹

Nutrition Unit, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana

²To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A randomized, double-blind, controlled study was conducted to determine whether the consumption of leafy vegetables by preschool children would enhance their serum vitamin A concentration to acceptable levels. Preschool children (n = 519; 2.5–6 y) in Saboba, northern Ghana, were randomly assigned to five feeding groups, differing essentially in the amount of fat and ß-carotene, fed once per d, 7 d per wk, for 3 mo. Serum retinol levels, anthropometric measurements, hemoglobin, rapid turnover proteins (pre-albumin and retinol-binding protein), worm infestation (stool examinations) and level of acute and chronic infection (serum C-reactive protein and acid glycoprotein) were determined before and after study. Relative to the baseline serum retinol values, consumption of dark green, leafy vegetables (Manihot sp. and Ceiba sp.) with fat (10 g/100 g) significantly (P < 0.05) enhanced serum retinol; consequently, the percentage of children with adequate retinol status increased from 28.2–48.2% after feeding (P < 0.05). There were no significant differences among groups, ages or pre- versus post-anthropometric measurements, hemoglobin concentration, or levels of worm infestation. The importance of these findings in alleviating and/or controlling vitamin A deficiency in developing countries is discussed.

KEY WORDS: • carotenoids • leafy vegetables • vitamin A status • preschool children • vitamin A deficiency

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Vitamin A (retinol) is a fat-soluble vitamin that is involved in many physiological processes, including vision, growth, reproduction, cellular differentiation, mucus secretion and immune responses (Kaplan and Pesce 1984 ). It is one of the few vitamins of which both deficiency and excess could cause serious health problems (SCN News 1988 ). Vitamin A deficiency (VAD)³ is a nutritional disorder, primarily caused by inadequate intake of vitamin A or its plant-based precursors and often aggravated by low absorption from the intestine (SCN News 1988 ).

In humans, especially children, vitamin A deficiency most commonly and prominently affects the eyes, leading to xerophthalmia (WHO 1976 ), a term used to denote all ocular manifestations of vitamin A deficiency. Vitamin A deficiency, usually accompanied by protein-energy malnutrition, is closely linked with an increased incidence of acute respiratory disease and diarrhea (Mamdani and Ross 1989 , Sommer et al. 1984 ) and probably with defective immunological defense mechanisms (Bang 1972 , Dresser 1968 , Major 1969 ). Indeed, recent studies have shown that vitamin A is important in maintaining children's health and reducing infant mortality (Muhilal et al. 1988 , Rahmethnllah et al. 1990 , Sommer et al. 1986 , Tarwatjo et al. 1987 ). Specifically, it was shown that improving the vitamin A status of a vitamin A-deficient population reduces child mortality by an average of 23% (Beaton et al. 1993 ), decreases the duration and severity of illness episodes (Ghana Vast Study Team, 1993 ), prevents xerophthalmic lesions (Sommer 1994 ) and reduces the prevalence of anemia, when it coexists with vitamin A deficiency (Sommer 1994 ).

In most developing countries, like Ghana, the main source of vitamin A for the majority of population is provitamin A from plant sources because the relatively rich animal sources are usually outside the purchasing power, on sustained basis, of the majority because of socio-economic constraints.

At present even in developed countries, because of increasing scientific evidence linking meat consumption and heart diseases, the focus seems to be on the consumption of more plant materials as substantial sources of many nutrients, including micronutrients (FAO/WHO, 1988 ). Plant constituents, such as ß-carotene, tocotrienols and tocopherols, besides having antimutagenic and hypocholesterolemic potentials, have the capacity to retard peroxidation and to scavenge dangerous free radicals (Rukmini 1994 ). Apart from these advantages, the dietary approach to reducing vitamin A deficiency is being advocated because it is sustainable, provides nutrients other than vitamin A and/or ß-carotene, and adds variety to the diet (de Pee et al. 1995 ).

The major drawback of using plant sources to meet vitamin A requirement is their bioavailability. Hume and Krebs (1949) found that the bioavailability of ß-carotene in carrots and other vegetables was, on the average, only a third of that in oil. The low bioavailability of ß-carotene in dark green, leafy vegetables may be due to several factors. In the green leaves, ß-carotene molecules are organized in pigment-protein complexes located in the chloroplasts (de Pee et al. 1995 ). It may, therefore, be difficult to free ß-carotene molecules from its matrix. In addition, plant components, such as carotenoids, fiber, phytic acid and polyphenls, may have inhibitory effects on ß-carotene absorption (de Pee et al. 1995 ).

This present research was undertaken to explore the possibility of using cassava (Manihot sp.) and kapok (Ceiba sp.) leaves as the main sources of provitamin A to enhance the retinol status of preschool children to an adequate level.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Materials.

ß-carotene (ß,ß-carotene; provitamin A) (purity of >97% (uv); 1600 U/mg: 1 U corresponds to 0.6 µg all-trans ß-carotene) was purchased from Fluka Chemie AG, Buchs, Switzerland.

Study areas.

The study was carried out in the northern region of Ghana, which lies in the sub-Sahelian savanna zone and is characterized by frequent food shortage as a result of climatic and ecological conditions. Malnutrition (<80% National Council on Health and Statistics median of weight for age) among preschool children is estimated at >50%, with severe or clinical cases at 20% (Armar-Klemesu et al. 1995 ). There is also general micronutrient deficiency. VAD was documented as a public health problem in the region (Ghana Vast Study Team 1993 ), and endemic goiter is recognized as such. There are indications that anemia is prevalent (Ghana Vast study Team 1993 ).

Human/animal ethical treatment statement.

The project was approved by the Ethical Committee of the Ministry of Health, Accra, Ghana.

Sample size determination.

Using a confidence level of 95%, a power of 80 and allowing a difference of 14% in carotenoid absorption between fat-supplemented and unsupplemented diets, sample size was 88 children/group. Allowing a dropout rate of 15%, initial sample size was 100/group.

Cassava (Manihot sp.) and kapok (Ceiba sp.) leaves.

Cassava and kapok plants, rich sources of ß-carotene, are able to withstand the climatic conditions all year. Analyses in our laboratory revealed a level of 1700 RE/100g for cassava leaves and 1620 RE/100g for kapok leaves boiled for 10 min each. Values in raw leaves were 1000 RE/100 g and 3850 RE/100 g, respectively.

Feeding groups.

Group 1: Cereal/yams + dark green, leafy vegetable (400 RE/child) + dry roasted fish (anchovies) + fat (shea butter, 20 g/child).

Group 2: Cereal/yams + dark green, leafy vegetable (400 RE/child) + dry roasted fish.

Group 3: Cereal/yams + dark green, leafy vegetable (10 RE) + dry roasted fish (negative control group).

Group 4: Cereal/yams + ß-carotene (400 RE) + dry roasted fish + fat (positive control group).

Group 5: Cereal/yams + dark green, leafy vegetable (400 RE/child) + dry roasted fish + fat + mebendazole (40 mg/d x 3 d/child).

In each group, the leafy vegetables were made into stews with onion, pepper, tomatoes, powdered roasted dry fish, iodinated salt to taste, and minimum groundnut oil for preparing the stews. The fish contained no vitamin A, revealed from analyses prior to use. Home-cooking practices were used for preparing the stews. The stews were served with rice, yams, gari/beans or gari. Those children who were served with vegetables (groups 1, 2 add 5; 400 RE/child) were fed stews made from either cassava or kapok leaves, on alternate days. The leaves were harvested fresh, washed in clean water, weighed, pounded using a wooden mortar and pestle, homogenized in a blender and used for preparing the stews. Children in group 5 who had worm infestation, revealed by stool examination in baseline studies, were given mebendazole for 3 consecutive days prior to feeding.

The nutrient composition of the various stews fed to the children are shown in Table 1 . The important differences in the stews were in the levels of fat and ß-carotene. Home stew (group 3) contained the least amount of both fat (1.3%) and ß-carotene (10.5 RE), whereas the other stews (except group 2) were designed to contain ~400 RE of ß-carotene/50 g stew and 10% fat. The fat content of stew fed to group 2 was also low (2.6%) because of the exclusion of shea butter (a local fat), whereas shea butter was added to each stew in groups 1, 4 and 5. Children in group 5 were fed the same stew as in group 1, but these children were first dewormed with mebendazole.

There were differences in the stew with respect to energy and carbohydrate levels, but these were not important because the stew was not a substantial sources of energy and carbohydrate. The bulk of energy and carbohydrate came from the main carbohydrate food served with the stew, cereal.

General aspects of feeding/compliance.

There were five feeding centers to ensure that the children did not walk >150 m before reaching their respective centers. At each center, the five different stews were served. Two assistants were employed at each center to ensure that children always ate their respective diets and to check the attendance of the children. Any child who was absent was traced to the house and urged to cooperate. This ensured that the children who did not drop out ate the foods and took their supplements most of the time (>98%) they were scheduled to do so. Those who dropped out did so either because their parents moved or were cut off from the feeding centers because of flooding.

Food was served by two other assistants at each center. Each child was given the same quantity of stew dished out by a 50 g/ portion ladle . The carbohydrate meal was served separately, and children ate as much of this meal as they desired. At intervals of 1 wk, B-complex vitamin syrup was administered to the children to enhance their appetites.

Recruitment of children/field studies.

After the details of the project were explained to parents and other leaders of public opinion, the children were recruited. Baseline studies were conducted. One week later, feeding commenced and lasted for 3 mo, at the end of which baseline studies were repeated as described below.

    Age and anthropometric measurement of weight and height. Age was obtained from birth/baptismal certificates; weight was obtained by using an electronic bathroom scale (Precision health scale UC-300, A & D, Tokyo, Japan) and height by using stainless steel stadiometer. The bathroom scale was calibrated each day by using a 1-kg stainless steel standard weight.

    Stool examination. Morning stool samples were collected from each of the children and examined by direct smear technique (in physiological saline). Part of each sample was examined by Kato method (Bailey 1987 ) to identify and quantify helminthic worm infestation.

    Biochemical measurements. Venous blood (3 mL) was withdrawn by venipuncture by using a needle fitted unto a 5-mL polypropylene syringe. Part of the blood was introduced into a capillary tube and centrifuged in a hematocrit centrifuge (Kokusan, Tokyo, Japan) at 900 x g for 5 min to determine hematocrit. Another portion of the blood was used to determine hemoglobin by using HemoCue microcuvettes and blood hemoglobin photometer (HemoCue AB, Angelholm, Sweden).

The rest of the blood was introduced into 5-mL vacutainer Plus tubes containing gels for serum separation. The tubes were allowed to stand at room temperature for 1 h and centrifuged at 900 x g for 10m. The serum was decanted into labeled cryostatic tubes, capped, wrapped in aluminum foil and stored at -30°C until used for biochemical analyses.

    Laboratory/biochemical Analyses. Serum samples were removed from storage and allowed to thaw to room temperature and used for the following analyses: retinol analyses were done using HPLC (Shimadzu UV-Vis spectrophotometer SPD-6AV, with Shimadzu C-R6A/Chromatopac Recorder, Tokyo, Japan) after isolation and extraction in methanol and n-hexane, respectively (Takyi et al. 1994 ). Retinol-binding protein (RBP) and pre-albumin were determined by radial immunodifusion technique (Takyi et al. 1994 ) with kits supplied by The Binding Site (Birmingham, UK). C-reactive protein and acid-glyco-protein were determined by using Automated Clinical Super Z chemistry analyzer (Kyoritsu Radio, Kyoritsu, Japan) according to the manufacturer's instruction manual with kits from Bayer (Tarrytown, NY).

    Food analyses. Samples of the stew from each group were analyzed by using routine methods. Fat was analyzed by Soxhlet extraction with petroleum ether; total protein by Kjeldahl; carbohydrate by difference; and energy, by calculation as the sum of energy values using the factor 37.656 kJ/g for fat and 16.736 kJ/g for protein and carbohydrate. Ash was measured by dry-ashing at 550°C for 4 h in a muffle furnace (Automatic Precision Muffle Furnace ST Type, Thomas Scientific, Swedesboro, NJ). Moisture was determined by lyophilization overnight in a freeze-dryer (Eyela Freeze dryer FD-1, Rikakikai, Tokyo). ß-carotene was analyzed using the following method established in our laboratory: stew (0.3g), a pinch each of pyrogallol, sodium carbonate, anhydrous sodium sulfate, and 0.3g acid-washed (and neutralized) sand were ground together to a very smooth powder by using a mortar and pestle. Distilled water (3 mL) was added and the mixture was ground again to obtain a very smooth slurry. An aliquot (0.5 mL) was put into a 10-mL brown test tube and extracted three times with 4 mL of an ethanol:diethylether (1:1, v/v) mixture on a vortex mixture for 2 min each time, followed by centrifugation each time at 800 x g for 10 min. All the extracts were pooled into a 20-mL brown test tube. Ten mL of 0.36 mol/L potassium hydroxide in methanol (alcoholic potash) was added, and after inverting the tube gently three times, the solution was left to saponify overnight in the dark. The next morning, the contents of the tube were poured into a separatory funnel. Hexane (10 mL) was added and the mixture shaken gently three times. After removing the aqueous layer, the hexane layer was repeatedly washed with distilled water (~150 mL each) until the last wash was neutral. The neutral extract was run into a 10- or 15-mL volumetric flask, and the volume was adjusted with hexane and stored at -70°C until used for assay.

HPLC was used for the analyses. Hexane (10%) in methanol was used as the mobile phase, and a Vydac 218 TP54 (C18), 5 µmol/L, 250 mm column was used as the stationary phase. Detection was at 450 nm. Standard reference carotenoids were used to identify and quantify the carotenoids in the test samples.

For vitamin A, the same extraction procedure was used except that plastic Eppendorf tubes were used with dichloromethane as the solvent. Extraction was, therefore, on a microscale, and detection was at 350 nm, with methanol as the mobile phase.

Statistical analyses of data.

All data were entered into computer in D-base, edited and analyzed either with Epinfo or SPSS statistical package. Age or group differences for all variables were verified using ANOVA with the Duncan's test option for multiple comparisons. Values expressed as percentages were compared using the chi squared test. Paired t tests were also used to compare data in baseline and post feeding studies. P < 0.05 was regarded as significant in all tests.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Stunting was the most predominant form of growth faltering, at 26.3% at baseline (Table 2 ) and 20% after dietary intervention (Table 3 ). Stunting was followed by wasting, with wasting and stunting, together, affecting the fewest children. Baseline and post feeding values did not differ.

Based on serum vitamin A concentration, children were classified into four groups labeled deficient, low, adequate and high. At baseline, 19.6% of the children were classified as deficient, 52.9% as low and 27.5% as adequate (Table 4 ). After dietary intervention, 5.9% were classified as deficient, 44.3% as low, 48.2% as adequate and 1.6% as high (Table 5 ).The differences in the percentages of children with deficient, low and adequate status before and after feeding were significant (P < 0.05). The efficiency of each of the five stews in enhancing the vitamin A status of the children was determined by subtracting retinol concentration at baseline from the level after feeding and dividing the difference by retinol concentration at baseline. The efficiencies were 26.5% (group 1), 23.4% (group 2), 4.8% (group 3), 44.1% (group 4) and 38.8% (group 5).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The present study was designed to determine whether consumption of dark green, leafy vegetables would enhance the retinol status of preschool children to acceptable levels. The dark green, leafy vegetables cassava (Manihot sp.) and kapok (Ceiba sp.) leaves that were investigated were chosen because they are rich sources of provitamin A, especially ß-carotene, and are readily and widely used by the inhabitants. The leaves are also common in many African and developing countries.

The project site, Saboba, was chosen because, in terms of infrastructure, it represents a typical tropical village. Previous studies indicated there was a generally high level of malnutrition, including micronutrient deficiencies (Armar-Klemesu et al. 1995 , Ghana Vast Study Team, 1993 ).

During feeding, the main meal (rice, yam, gari and beans, or gari alone) was the same for all five groups, but the stews were different (Table 1) .We ensured that home-cooking practices and ingredients were used so that the program could be readily implemented, if successful.

Because carotenoids are usually located in protein-chloroplast matrixes within plant tissues (de Pee et al. 1995 ), there was a need to liberate these molecules by using appropriate means. We achieved this by first pounding the leaves in wooden mortars using wooden pestles, followed by high-speed homogenization in a blender. In a village setting, milling on flat-surfaced stone or grinding in earthenware would be substituted for homogenization in a blender.

Iodine deficiency (WHO 1976 ) and type as well as the amount of fat (Jalal et al. 1998 ) can affect the bioavailability of carotenoids. We, therefore, used iodized salt and a local fat in the diet preparation to boost the iodine status and fat intake.

The incidence of iron deficiency anemia, at 92%, was very high. There was no significant difference between incidence of anemia before and after feeding (Tables 2 and 3) . The exact causes of anemia were not investigated, but they could be due to a combination of factors, including malaria, general infection, hookworm infestation and gum bleeding caused by inadequate vitamin C intake. Gum bleeding was found to be common (80% in one nursery school), but this was corrected during our studies period by vitamin C supplementation by the Assemblies of God Development and Relief Services. Malaria infection was the most important single cause of morbidity in this community, representing ~34% of all hospital cases in 1998. (Unpublished Health Centre records)

Before feeding (baseline), as many as 19.6% of the children were classified as deficient for vitamin A (<0.35 µmol/L). It is clear that Saboba was a vitamin A-deficient community according to the WHO definition (Takyi et al. 1994 ) because >5% of the children had retinol levels <0.35 µmol/L.

These results indicate that the leafy vegetable diets significantly (P < 0.05) enhanced the retinol status of the children, albeit to different degrees. There were significant differences (P < 0.05) between post feeding and baseline retinol concentrations in all groups, except group 3 (Table 6 ). The efficiency of enhancement of retinol status for the groups can be ranked as follows: group 4 (44.1%) > group 5 (38.8%) > group 1 (26.5%) > group 2 (23.4%) > group 3 (4.8%). Because group 4 was the positive control group (400 RE ß-carotene), it is apparent that pure ß-carotene was the most effective in enhancing serum retinol status. This group was followed by group 5 in which the children were dewormed with mebendazole prior to feeding. This indicates the beneficial effects of deworming on the bioavailability of carotenoids.

These results are generally in agreement with those obtained by Jalal et al. (1998) , who studied the factors that may influence the success of using ß-carotene as a vitamin A source in food-based programs. They found that the incorporation of ß-carotene (mainly in the form of red sweet potatoes) into meals significantly increased serum vitamin A levels. Furthermore, the greatest rise in serum retinol occurred when added ß-carotene was given with fat to children who had been dewormed.

We agree with the recommendation of Jalal et al. (1998) that food-based intervention in vitamin A-deficient areas could be successful, but other interventions, such as increasing dietary fat concentrations and anthehelmintic treatment, should be considered along with increasing the consumption of ß-carotene-rich foods.

Our work has unequivocally demonstrated the ability of some leaves to enhance serum retinol levels to acceptable levels. This supports other research findings (Jalal et al. 1998 , for reviews see FAO/WHO 1988 ), while it is at variance with some others, notably that of de Pee et al. (1995) , who conducted similar studies and concluded that vitamin A status did not improve with increased consumption of dark green, leafy vegetables.

The work of de Pee et al. (1995) is different from the present study in many respects. First, the subjects were adult women who were breastfeeding children 3–17 mo, whereas preschool children were used in the present study. Second, de Pee et al. stir-fried the leaves compared to the pounding followed by homogenization employed in the present study. It is unknown whether stir-frying will liberate ß-carotene from the pigment-protein complex in the chloroplast. Stir-frying could also lead to partial destruction and/or isomerization of ß-carotene, producing species with lower vitamin A activity. Indeed, they reported that the cis-isomers (13-cis ß-carotene and 9-cis ß-carotene) of ß-carotene in the supplement was 30–35% compared to the raw tissue level of 15%. Third, supplements were given 5 d/wk for 12 wk compared to feeding for 7 d/wk for 12 wk in the present study. Fourth, we increased the fat content of the supplement stews to 10% (by weight), whereas de Pee et al. used a lower fat level of 7.5%.

It is not certain whether our results can be extrapolated to other leaves because the bioavailability of dietary carotenoids is influenced by many interacting factors (de Pee et al. 1995 ). However, because cassava and kapok leaves are common in most of the developing world, which lie in tropical or subtropical areas, increased consumption of these leaves could provide affordable and sustainable means of reducing or controlling the incidence of VAD in these areas.

	ACKNOWLEDGMENTS

 
I thank F. Owusu, E. Addo, J. W. Asaku, J. Fenteng, H. Kpo and Mary Osafo for their technical assistance; G. Mensah and E. Amanquador for the analyses of the data; and Justine Kosivi for secretarial services. Special mention must be made of the Assemblies of God Church based in Accra and Saboba for their assistance in placing their facilities at the disposal of the project.

	FOOTNOTES

 
^{1 1}This work was funded by USAID/OMNI Research, Washington, DC.

³ Abbreviations used: C-rp, c-reactive protein; RBP, retinol- binding protein; VAD, vitamin A deficiency.

Manuscript received September 21, 1998. Initial review completed October 28, 1998. Revision accepted April 7, 1999.

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