The Journal of Nutrition Vol. 128 No. 5 May 1998, pp. 860-864

Fortified Foods Contribute One Half of Recommended Vitamin A Intake in Poor Urban Guatemalan Toddlers^1,2,3

Vivian M. Krause⁴, Helene Delisle, and Noel W. Solomons^*

Département de Nutrition, Université de Montréal, C.P. 6128 Succursale Centre-ville, Montreal, QC, Canada, H3C 3J7 and ^* Center for Studies of Sensory Impairment, Aging and Metabolism, Hospital de Ojos y Oidos, "Dr. Rodolfo Robles V," Ciudad Guatemala, Guatemala

	ABSTRACT

Abstract Introduction Methods Results Discussion References

Vitamin A intake from food sources, not including breast milk, was determined from seven consecutive 24-h recalls for 55 children (mean age 20.8 mo, SD 8.9) from two poor communities of Guatemala City. Not including vitamin A derived from fortified sugar or breast milk, the median daily vitamin A intake was 194 retinol equivalents (RE). Including vitamin A derived from fortified sugar but not including that derived from breast milk, the median total vitamin A intake (25th and 75th percentiles) was 338 RE (146 and 617 RE) of which 78% was preformed retinol and 22% provitamin A. More than 90% of total vitamin A intake from non-breast milk food sources was derived from only 10 items; over half came from three fortified foods: fortified sugar, Incaparina and margarine. Sugar samples from 91 households in 1991 had a median of 3.3 RE/g (range, 0.0-29.9 RE/g), <25% of the target level (13-17 RE/g); nevertheless, fortified sugar provided 25% of these children's total vitamin A intake (81 RE/d) from non-breast milk food sources and their intake approached the level recommended by the FAO/WHO (400 RE/d). These results show that fortified foods make an important contribution towards vitamin A intake in this sample of poor urban Guatemalan toddlers.

	INTRODUCTION

Abstract Introduction Methods Results Discussion References

Historically, vitamin A has been recognized as playing an important role in vision, maintenance of epithelial membranes, hematopoiesis, growth, reproduction and immunity (Underwood 1984, West 1991). In the 1980s, it was shown that vitamin A capsule distribution reduces child mortality rates by as much as 30% (Beaton et al. 1993). Since then, politicians and public health specialists have become more sensitized to eradicating vitamin A deficiency as part of child survival strategies (West et al. 1989). The three main intervention approaches to control vitamin A deficiency are dietary behavioral change through communications strategies, periodic supplementation with high dose capsules and fortification. Of these three, fortification has great potential but has been the least employed strategy due to cost and technical problems. Another reason for hesitancy to invest in food fortification is the concern that some fortified foods do not reach the target populationsnoteably, the poor. The purpose of this paper is to address this concern by assessing vitamin A intake and the importance of fortified foods and other sources of vitamin A in a sample of poor urban Guatemalan toddlers.

The National Nutrition Survey of Guatemala in 1965 showed that 26% of preschool age children suffered vitamin A deficiency as indicated by a plasma retinol concentration of <0.35 µmol/L (10 mg/dL; INCAP 1969). The fortification of sugar with vitamin A (retinyl palmitate) was subsequently developed by the Institute of Nutrition of Central America and Panama (INCAP) as a means to control vitamin A deficiency in Guatemala. Sugar, the lowest cost food source of energy in Guatemala, was chosen as the vehicle for fortification because it is centrally produced, consumed in relatively constant quantities by the majority of the population, and its organoleptic properties are not changed with fortification (Arroyave et al. 1981). In 1974, legislation was passed requiring that all table sugar for domestic consumption be fortified with 15 retinol equivalents (RE) per gram of sugar. For various reasons, including lack of enforcement of the law, fortification was discontinued from the late 1970s until 1987 (UNICEF 1995). The prevalence of vitamin A deficiency in preschool children decreased from 26% in 1967 to 10% in 1977 (when harvested sugar was fortified), and rose again to 25% in rural areas in 1987 during the period when sugar fortification was disrupted (Arroyave et al. 1981). The National Micronutrient Study of Guatemala in 1995 found that with the renewal of sugar fortification, the percentage of children age 1-5 y with plasma retinol <0.70 µmol/L (20 mg/dL) fell to 15.8% in 1995 (Ministerio de Salud Publica y Asistencia Social 1996).

Vitamin A intake and status of poor periurban populations are growing concerns, especially in Latin America where many cities are expanding rapidly (Sanchez-Castillo et al. 1992). The urban poor suffer both the malnutrition and infectious diseases associated with underdevelopment as well as the chronic and social diseases of industrialization (Rossi-Espagnet 1987, Solomons and Gross 1987). Solomons and co-workers (1989) reported that less than half of the preschool children in poor areas of Guatemala City attained 350 RE daily as recommended by FAO/WHO (1991).

	SUBJECTS AND METHODS

Abstract Introduction Methods Results Discussion References

Communities.  This study was undertaken late in the dry season (April and May of 1990) in two neighboring periurban communities of Guatemala City (Jocotales and Buena Vista of Zone 6). Approximately 30% of the population of Guatemala City is considered to live in extreme poverty (UNICEF 1994). With respect to household income, community infrastructure, social services and access to education and health care, the two communities selected for this study are typical of the poor areas of Guatemala City (UNICEF/SEGEPLAN 1992, UNICEF 1994). Both communities have public schools at the elementary level and they share a health center, but the coverage of these services is incomplete. Most families frequent the local market and purchase staple items in one of the 15-20 small food stores in the area.

Participants.  A random sample of 60 of the 659 households in Jocotales and 40 of the 471 in Buena Vista was identified by using maps made by the local health promoters and personnel from the health center. After a random start, every sixth house in Jocotales and every fourth in Buena Vista, was identified. Of these 100 households, 60 had a child within the target age group (6-36 mo). The mother or female caregiver of each of these 60 children was asked to participate in the study. Of them, 58 agreed and 55 completed seven 24-h recalls for one child per household. All of these women spoke Spanish. If two or more children in the same household fell into the target age-group, the child closest to 24 mo of age was selected. The mean age (±SD) of the 55 children studied was 20.8 ± 8.9 mo. Participants included 30 boys and 25 girls; all were free of congenital defects and apparent illness.

The 24-h recalls.  On seven consecutive days, a 24-h recall was conducted for each child. The recall consisted of asking the respondent to name all items the child ate or drank during a 24-h period, beginning from the time he or she first awoke on the day before the interview. Recipes were collected for prepared foods, although these were few due to the nature of the children's diets. For bottle feedings (e.g., milk, coffee or Incaparina), mothers were asked to estimate how much of each of the ingredients was used to prepare the amount given in the bottle. Quantities were estimated with the aid of plastic spoons, cups and bowls commonly used in these communities. Each recall took ~20 min to complete. None of the women reported giving their children vitamin supplements during the study period and none had received a high dose vitamin A capsule within the past 15 mo.

The 24-h recalls were done by an experienced nutritionist or one of four health promoters who had received extensive training before the commencement of the study. The interviewers were trained specifically in the use of the model dishes to estimate portion size, and when and how to probe for more information. Corrective feedback and retraining throughout the study enhanced standardization in the interviewing procedures. The information collected by the health promoters was reviewed daily. For a given child, all seven 24-h recalls were conducted by the same interviewer.

Data processing and analysis.  Dietary data collection sheets were coded by one person and doubly entered using Lotus 123. Standard range edits were performed using SAS for microcomputers, to identify invalid coding or keying.

Intakes of retinol, -carotene and other carotenoids, expressed as retinol equivalents (RE) were calculated using a modified version of a program written for SAS by Humberto Mendez of the Institute of Nutrition of Central America and Panama (INCAP). Results presented here do not include vitamin A intake from breast milk. To calculate nutrient intakes from food sources, the INCAP food composition database was used. This database for 751 foods is derived from the Central American food composition tables (Flores et al. 1971). Nutrient values for 24 additional foods were added to the original data base. These values were taken from label information for four commercial products, from hand calculations of 13 recipes, from scientific literature (Portocarrero et al. 1992) and from the Canadian food composition tables (Ministry of Supply and Services Canada 1987) for five foods (hard candy, bubble gum, wheat germ, cornmeal and blackberries) for which the values for the local food were not available. To estimate the amount of vitamin A derived from sugar, the median value of assayed samples was used (3.3 RE/g sugar). For 11 types of broths (corn, fried steak, beef liver, carrot, beef stomach, potato, plantain, rice, summer squash, tortilla and fish), a value of zero was given for their vitamin A content because suitable nutrient composition data could not be found. These broths consisted of the cooking water in which the food was prepared, but not the food itself. Each of these broths was mentioned only once except for the cooking water from dark green leaves which accounted for 27 (0.4%) of the 7114 items mentioned in the total of 385 24-h recalls.

For each nutrient, intake was summed over the 7 d and then divided by seven to obtain an estimate of average daily intake. Vitamin A intake per 4182 kJ (roughly normally distributed) was also calculated for each of the seven individual days; these values were then used in a repeated-measures ANOVA to check for a time-sequence effect.

To assess the importance of specific foods as sources of vitamin A, the data were analyzed in two ways. First, the percentage of total vitamin A intake contributed by a given item at the level of the whole group was assessed when all observations were included. Subjects who had not consumed the food had an intake of 0 RE from that food. Second, the contribution of each item was determined for consumers only.

Sugar collection and analysis.  After a random start in each community, every 10th household was identified for inclusion in the sugar study. In 95 of the 100 identified households, an adult female representative agreed to complete a short interview on sugar use. Two of the identified 100 households could not be reached on any of three visits and three refused to participate. Four did not have any sugar at the time the sample was to be collected. In total, 91 sugar samples of ~100 g were individually collected into clean, black, plastic bags, protected from direct sunlight and maintained at room temperature.

Three weeks after collection, the sugar samples were analyzed spectrophotometrically in Guatemala, in duplicate, using a modification of the method of Arroyave and Funes (1974). Sugar (0.5 g) was dissolved in 10 drops of hot, distilled water in a 13 × 100 mm test-tube. The solution was shaken for 30 s. The reactive chromogen (3 mL) was added and then mixed carefully with the sugar solution. The reactive chromogen was prepared with 60.0 g trichloroacetic acid dissolved in 40.0 g dichloromethane and protected from direct light in a darkened bottle. Samples were read on a Beckman spectrophotometer (model 2400) within 24 h of preparation of the reactive chromogen.

This study was approved by the Ethics committees of the department of Nutrition of the Université de Montréal and the Hospital Rodolfo Robles V, Ojos y Oidos of the National Committee for the Blind and Deaf of Guatemala.

	RESULTS

Abstract Introduction Methods Results Discussion References

General characteristics of the diet.  The 10 items mentioned the greatest number of times as foods or ingredients were as follows, in descending order: sugar, coffee, white-maize tortilla, cooking oil, a type of hard "sugar cookie" (pan dulce), tomato, white bread, Incaparina, banana and chicken egg. These 10 items accounted for nearly 60% of the 7114 items mentioned in the total of 385 24-h recalls. Of these 10 foods, three (sugar, coffee and tortilla) accounted for one third of all items mentioned.

Daily intakes (mean ± SD) were 3994 ± 1972 kJ, 29 ± 16 g protein, 24 ± 15 g fat and 162 ± 77 g carbohydrate. Fat represented 22% of total energy intake, protein accounted for 12% and carbohydrates for the remaining 66%. Average intake of calcium and iron was 394 ± 293 and 9.0 ± 5.4 mg/d, respectively. Mean daily vitamin intakes included 0.7 mg thiamin, 0.6 mg riboflavin, 6.9 mg niacin and 38 mg ascorbic acid.

Total vitamin A intake.  Frequency distributions (not shown) indicated that vitamin A intake was highly skewed to the left. The median total vitamin A intake from food sources, including sugar but not including breast milk, was 162 RE in breast-fed children and 597 RE in weaned children (Table 1). Of the median daily total vitamin A intake for all children (338 RE) from food sources not including breast milk, the median percentage of preformed vitamin A was 78% (57-90%) whereas provitamin A accounted for 22% (10-43%). Not including fortified sugar, 64% came from preformed sources and 36% from provitamin A. 

Due to colinearity between age and breast-feeding status, dividing the children by age (with 18 mo as a cut-off point) gave similar estimates of average intake, as did grouping them by breast-feeding status. As Table 1 shows, median vitamin A intake from food sources (457 RE) was >100% greater in the older, weaned children than in those <18 mo of age (190 RE). When expressed per 4182 kJ, mean protein and total vitamin A intakes did not differ in boys and girls; mean preformed vitamin A intake tended to be slightly higher in boys and -carotene intake tended to be higher in girls but neither difference was significant.

Distributions of energy intake and of nutrients other than vitamin A were roughly normal. For both preformed and provitamin A, the distribution approached normality when intake was expressed per 4182 kJ. Over the 7 d studied, repeated-measures ANOVA did not show a time-sequence effect for energy, protein, preformed vitamin A per 4182 kJ or provitamin A per 4182 kJ.

Vitamin A intake from specific foods.  In the whole sample of 55 children, 10 food items contributed a mean of 87% and a median of 91% to total vitamin A intake from non-breast milk food sources (Table 2). These 10 items are fortified sugar, Incaparina (a locally made protein-, vitamin- and mineral-fortified beverage mix), margarine, chicken egg, cow's milk, ripe mango, carrot, tomato, beef liver and an instant infant cereal (Cerelac). A mean percentage of 55 ± 25 was contributed by three fortified foods: sugar, Incaparina and margarine. When individual items were combined into traditional food groups, the group that included fruits, vegetables and dark green leaves provided 19 ± 10%, milk, cheese and egg provided 11 ± 10% and organ meats, 5 ± 15% of vitamin A intake from non-breast milk sources. The distributions were skewed to the left so that median percentage contributions were close to zero except for sugar.

When only the consumers of a particular food item were included, the foods that provided the largest amounts of vitamin A were, in order: beef liver, Incaparina, sugar, chicken liver, carrots, margarine, ripe mango, cow's milk, dark green leaves, chicken egg, pumpkin, beef stomach, cheese and tomato (Table 2).

Vitamin A intake from sugar.  The mean (±SD) retinyl palmitate concentration in the 91 sugar samples was 4.5 ± 4.7 RE/g sugar. The median concentration was 3.3 RE/g and the range was 0.0-29.9 RE/g. Twenty-four percent of the sugar samples did not have a detectable amount of vitamin A, whereas one sample had almost double (29.9 RE/g) the target concentration (13-17 RE/g).

The median (25th and 75th percentiles) and mean (±SD) daily amounts of vitamin A derived from sugar were 81 RE (40 and 143 RE) and 99 ± 77 RE, respectively. This corresponds to daily intakes of sugar of 24 g (11 and 43 g) and 30 ± 23 g, respectively. If the sugar had contained the legally stipulated level of 15 RE/g, the mean ± SD vitamin A intake of these children would have been 793 ± RE (327 and 1135 RE).

	DISCUSSION

Abstract Introduction Methods Results Discussion References

These children's diets have little diversity, consisting basically of grains and legumes (corn, black beans and rice), and are scarce in animal products except chicken egg. In terms of fruits and vegetables, mainly tomato and banana, both low in vitamin A, are the most frequently consumed.

The median daily intake of the weaned children was 597 RE, based on the following assumptions: 1) the children received an average of 3.3 RE vitamin A per gram sugar consumed; 2) the nutrient composition values of the INCAP data base represent the true content of the corresponding foods; 3) Incaparina and margarine are fortified as described by their manufacturers; and 4) reported types and quantities of food consumed are valid. Adequacy of vitamin A status cannot be inferred from this level of intake, especially in this population in which parasitic and other infections may impair vitamin A absorption and increase physiological requirements (Filteau et al. 1993, Salazar-Lindo et al. 1993, Solomons and Bulux, 1993). In the breast-fed children in this sample, total vitamin A intake could not be estimated because quantitative data on breast milk intake were not collected. The data represent the situation in the late dry season when provitamin A-containing fruits such as mango are less plentiful.

Average vitamin A intake of the weaned children attained the FAO/WHO recommended level (400 RE/d) with the contribution from fortified foods. Ten items provided 90% of vitamin A from non-breast milk food sources. Of these, three fortified foods (sugar, margarine and Incaparina) contributed more than half. In those children who consumed the food in question, the daily mean vitamin A intake provided by fortified sugar, Incaparina and margarine was 81, 94 and 61 RE, respectively.

Sugar intake and the effect of its fortification.  Fortified sugar contributed 25-29% of vitamin A intake from non-breast milk food sources. If sugar had contained 15 RE/g, the total vitamin A intake of poor urban toddlers in this study would have been 793 RE/d, almost twice the daily intake recommended by the FAO/WHO (400 RE), but still far from levels associated with low dose toxicity in children as reported by Hathcock et al. (1990).

Since the collection of these sugar samples in 1991, the association of sugar manufacturers of Guatemala (ASAZGUA) with technical support from the Institute of Nutrition of Central America and Panama (INCAP) has strengthened quality control measures. The National Micronutrient Survey in 1995 found the vitamin A concentration in sugar as follows: 41% had <4 µg/g; 21% had 4-6 µg/g; 24% had 6-10 µg/g and 14% had >10 µg/g (Ministerio de Salud Publica y Asistencia Social 1996). These results are better than those found in 1991 but indicate that scope for improvement still exists.

Per capita sugar consumption appears to have increased over the past 20 y. When the fortification level was established at 15 µg/g sugar in the 1970s, an average daily intake of 40 g per person was assumed; this would permit a daily average of 600 RE per person (Arroyave et al. 1979, Zarate-Zarate 1978). Alarcon and Adrino (1991) found a mean sugar intake in 1990 of 61 and 85 g in rural and urban populations, respectively. The National Micronutrient Survey of Guatemala in 1995 found an average daily per capita consumption of 67.5 g sugar (Ministerio de Salud Publica y Asistencia Social 1996). In this study, the mean daily amount of sugar purchased per week was 500 ± 227 g, or 71 g per person; waste and nondietary use of sugar is unknown but is thought to be small.

The fortification level was set at 15 RE/g sugar to provide 300 RE/d for children consuming 24 to 30 g sugar/d (Arroyave et al. 1979). Sugar intake in this study of poor urban toddlers was estimated at 24 g, but true intake may have been higher when discretionary sugar plus that hidden in prepared foods (e.g., candies, carbonated beverages or cakes) was included. On the other hand, because sweetened beverages given in a baby bottle are a major vehicle by which sugar is served to infants and young children, sugar intake may be lower in rural children in remote areas where the duration of breast-feeding is longer and bottle-feeding may begin at an older age or not at all.

The cost of the vitamin A fortificant alone accounts for more than 95% of the cost of sugar fortification, exceeding two million U.S. $ per year (UNICEF 1995). Thus, a reduction in the required level of fortification could substantially reduce the cost of sugar fortification. Potential savings to the manufacturers would likely outweigh the costs of periodic assessment of sugar intake. More information is needed on 1) postfortification losses over time in varying climatic and storage conditions, 2) sugar intake by age group and socioeconomic status across the rural-urban gradient, and 3) vitamin A status of at-risk groups.

Food composition values for vitamin A.  More valid data on the vitamin A content of foods would permit a better estimation of the percentage of total nutrient intake that is contributed by fortified foods but would not bear on the conclusion that in this sample, fortified foods provided approximately half of the Recommended Nutrient Intake (RNI). In the INCAP database, values for foods from animal sources are similar to those given in other food composition tables, such as the one for Canada (Ministry of Supply and Services Canada 1987). For vitamin A from plant sources (ripe mango, oranges, cantaloupe, papaya, green string beans and pumpkin), the values in the INCAP database are within the range reported by West and Poortvliet (1993). However, this range is up to five-fold in some cases. The apparent variation in vitamin A content of foods likely reflects both the laboratory methods used in analysis as well as true differences associated with climatic and soil conditions, stage of ripeness, storage and processing (Mangels et al. 1993). As mentioned previously, vitamin A content was considered zero for 11 types of cooking water, including that of some important sources of vitamin A such as liver and carrots. Although these broths were rarely consumed, analytical data on their nutrient composition would permit more accurate estimations of the vitamin A intake of infants and young children.

In conclusion, fortified foods, particularly fortified sugar, Incaparina and margarine, make an important contribution to vitamin A intake in this sample of poor urban toddlers. Clearly, breast milk is also a vital source of vitamin A and other nutrients. We are reminded of the importance of quality assurance, technical support to the food industry, political will to enforce fortification and surveillance of consumption patterns.

	ACKNOWLEDGMENTS

The authors thank Omar Dary and the Institute of Nutrition of Central America and Panama (INCAP) for their generosity in facilitating the analysis of the sugar samples. We also appreciate the collaboration of The Commission for Attention to Precarious Areas (COINAP) of the Secretary General for Economic Planning (SEGEPLAN), the Basic Urban Services Program of UNICEF, and the health center of San Julian, Nueva Chinautla for facilitating the field work. Jesus Bulux and Julieta Quan de Serrano, and other members of the investigative team at CeSSIAM are acknowledged for providing preliminary information on vitamin A status and intake in Guatemala. We are also very grateful to Humberto Mendez of INCAP who wrote the SAS program for the nutrient analysis.

	FOOTNOTES

Manuscript received 11 March 1997. Initial reviews completed 11 May 1997. Revision accepted 20 January 1998.

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