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(Journal of Nutrition. 1999;129:2021-2027.)
© 1999 The American Society for Nutritional Sciences


Article

Dietary Vitamin A Intakes of Preschool-Age Children in South India1 ,2

Usha Ramakrishnan3, Reynaldo Martorell, Michael C. Latham* and Rajaratnam Abel{dagger}

Department of International Health, Rollins School of Public Health, Emory University, Atlanta, GA 30322; * Program in International Nutrition, Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853–6301; and {dagger} Rural Unit for Health and Social Affairs Department, Christian Medical College and Hospital, Vellore 632004, India

3To whom correspondence and reprint requests should be addressed.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The vitamin A intake of children aged 1–3 y (n = 683) was assessed using a quantitative food-frequency questionnaire in a vitamin A intervention study in South India. Trained field workers interviewed mothers about their children's usual consumption of common sources of vitamin A and collected information on portion sizes using standard cups. Mothers were asked to state the number of months in a year during which specific seasonal foods were available. Information about current breast-feeding was also obtained. Vitamin A intakes from nonbreast milk sources were extremely low at all ages. The median intake of total vitamin A, ß-carotene and retinol was 121, 100 and 21 retinol equivalents (RE), respectively. Maternal education and socioeconomic status (SES) were positively associated with total vitamin A and retinol intakes. Girls had significantly lower intakes than boys even after adjusting for differences in age, maternal education, SES and breast-feeding status. Breast-feeding was common, but declined to 60% by 24 mo and to 15% by 36 mo. Vitamin A intakes from nonbreast milk sources increased with age only for currently breast-fed children, who tended to be of lower SES. After taking into account the potential contribution of breast milk by using published estimates, nonbreast-fed children met only 60% of the Indian recommended dietary allowance (RDA; 250 RE/d), whereas breast-fed children met ~90% of the RDA during y 2 of life.


KEY WORDS: • preschool children • vitamin A • dietary intakes


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Inadequate diets and high rates of illnesses such as diarrhea are well-recognized causes of vitamin A deficiency among young children in many developing countries. Low dietary intakes of vitamin A may be due to poor socioeconomic status, traditional food beliefs and practices, and the use of exclusively cereal-based complementary foods that contain little vitamin A; in addition, young children may not be fed or may dislike dark green leafy vegetables, a relatively inexpensive and widely available source of ß-carotene. Although dietary surveys have shown that intake of foods rich in ß-carotene and preformed retinol is low among preschool-age children in many developing countries, there are limited data on the actual patterns and determinants of dietary intake of different sources of vitamin A. Some studies have shown that the intake of animal foods, excellent sources of preformed retinol, is low (Backstrand et al. 1995Citation , Shankar et al. 1996Citation , Zeitlin et al. 1992Citation ), but few have examined the relative contributions of the different sources of vitamin A that vary in bioavailability. Another potentially inexpensive and often ignored source of preformed retinol is breast milk. Studies from Bangladesh, Indonesia and Malawi have shown that children who are breast-fed longer have a significantly lower risk for the xerophthalmia and nutritional blindness that result from severe vitamin A deficiency (Mahalabanis 1991Citation , Tarwotjo et al. 1982Citation , West et al. 1986Citation ). Despite current recommendations that promote sustained breast-feeding into y 2 of life (UNICEF 1993Citation ), little is known regarding the contribution of breast milk to total vitamin A intakes in this age group (Institute of Medicine 1991Citation ).

Promoting dietary change to improve vitamin A intakes has been recommended as a feasible long-term strategy in combating vitamin A deficiency among young children (WHO 1994Citation ). However, rigorous evaluation of such interventions depend on the ability to collect good quality dietary data. The assessment of vitamin A intakes is problematic because they are highly variable and are affected greatly by factors such as season and the consumption of specific foods such as liver which are extremely rich sources of retinol (Willett 1998Citation ). In many developing countries in which food processing and storage are limited, fruits such as papaya and mangoes are available for only 2–3 mo in a year. A wide variety of dietary assessment methodologies that range from the qualitative (food-frequency methods) to detailed quantitative methods (24-h food recall; 3- or 7-d food records) are available to assess dietary intakes of vitamin A at the household and community level. More recently, the (semi) quantitative food-frequency questionnaire is being recommended as a useful and simple tool to assess dietary intake of vitamin A in different populations. The International Vitamin A Consultative Group (IVACG)4 developed such an instrument for use in developing countries; it is comprised of a qualitative food-frequency questionnaire combined with semiquantitative estimates of actual consumption using a modified 24-h recall (IVACG 1989Citation ). The Helen Keller International (HKI) Food Frequency Questionnaire, a qualitative 7-d recall of the number of times that a child consumed selected vitamin A rich foods, is simpler and easier to use, but appears to be useful to identify communities and not individuals at risk of vitamin A deficiency (HKI 1992Citation , Sloan and Rosen 1997Citation ). At the time that these methodologies were being developed and tested, the senior author of this paper developed and applied a quantitative food-frequency questionnaire, adapted to local conditions and considering seasonality, to collect dietary data on a large sample of young children, as part of a larger vitamin A intervention study that was conducted in rural South India (Ramakrishnan 1993Citation ). The main objectives of this paper are as follows: 1) to assess and describe the adequacy of dietary intakes of vitamin A (ß-carotene, preformed retinol and total intake) among South Indian children (12–47 mo) using a modified quantitative food-frequency questionnaire in a developing country setting and 2) to identify the determinants of vitamin A intakes from different dietary sources.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study site and experimental design.

This analysis used dietary data from a randomized placebo-controlled vitamin A intervention trial that was conducted during 1989–1991 in 12 villages in South India. Health and nutrition education messages were delivered to mothers by village health workers in all 12 villages; growth monitoring took place in 6 villages. Details of the trial and study population are described elsewhere (Ramakrishnan 1993Citation ). The original study was approved by the Human Subjects Committee at Cornell University, and informed consent was obtained from the parent or guardian of all participating children.

Data collection.

A quantitative food-frequency questionnaire appropriate to the local conditions was developed and pretested by the first author, a native of the region, based on market surveys and interviews with key informants, including field workers and mothers. The instrument was administered once to mothers of all children between 12 and 47 mo of age (n = 683) between January and April 1991 at the end of the vitamin A intervention trial. In most cases, there was only one child per household, but 11% of the 615 households contributed >1 child. Trained female field workers interviewed mothers about the habitual frequency of consumption of common sources of vitamin A by their preschool child. The vitamin A–rich foods included were locally available dark green leafy vegetables (e.g., amaranth or drumstick leaves), yellow and orange fruits and vegetables (e.g., mangoes, papayas, yellow pumpkin or carrots), eggs, milk and meat products. For seasonal foods (e.g., mangoes or yellow pumpkin), mothers were asked to state the number of months in the year during which these foods were available; the frequency of consumption referred only to the period in which they were available. Mothers were also asked to indicate the usual portion size that their child consumed. Commonly used household utensils such as ladles and cups were used to facilitate recall of portion sizes. The volumes and weights of local utensils were estimated and converted by the trained workers using standard plastic measuring cups and spoons. Details of locally used recipes were also obtained. Mothers who were still breast-feeding were asked to report the number of times they breast-fed their child in the previous 24 h. Although the instrument was not formally validated by collecting data over different periods of time and by comparison with other biological indicators of vitamin A deficiency, it is similar to the IVACG method, which has been validated (Abdallah and Ahmed 1993Citation , Nimsakul et al. 1994Citation ).

Sociodemographic information collected included household size and composition, maternal education (number of years of schooling), father's occupation, ownership of land, livestock and other household possessions such as radio, bicycle and television. Details on infant feeding practices such as duration of breast-feeding, timing of introduction of complementary foods and type of complementary foods were also collected using pretested questionnaires. Length or height (in the case of children over 24 mo) and weight were collected for all children using standard measurement techniques (Lohman et al. 1988Citation ). Details of all births that had been monitored prospectively since 1987 were used to determine the ages of all children. All data were collected by trained field workers as part of the original study, entered in the field using DBASEIII and subsequently analyzed using SAS (SAS 1996Citation ).

Data analysis.

Anthropometric data were expressed as Z-scores using the WHO/U.S. National Center for Health Statistics (NCHS) reference values. Stunting and wasting were defined as Z-scores below -2 of the NCHS mean for height/age and weight/height, respectively.

The various responses for the frequency of intake of vitamin A–rich foods were combined into the following categories: 1–3 times per week, 1–3 times per month (including responses such as monthly and bimonthly) and rarely (including frequencies from less than once a month to never). Estimated vitamin A intake from nonbreast milk sources was calculated from the reported frequency of intake, number of months in a year that the food was available, mean serving size and vitamin A content (total, preformed retinol and ß-carotene) of the foods by using the values published by the Indian National Institute of Nutrition (NIN) (1985)Citation . Intakes for seasonal foods were prorated to reflect the number of months they were available. The daily vitamin A intake for a given food source was calculated as follows: daily vitamin A intake [retinol equivalents (RE)] = [(number of times/y) · (vitamin A content of serving)]/365 where number of times/y = (number of times/mo) · (number of mo available/y), and vitamin A content of an average serving = weight per serving (g) · vitamin A content of the food (RE/g)

The vitamin A intakes from the various food sources were then summed and expressed as average daily intake. These calculations was also done separately for ß-carotene and retinol intakes. Because the distributions of intakes were highly skewed, log-transformed values were used in the analysis. The amount of breast milk vitamin A was based on published estimates of average breast milk intake and vitamin A content of breast milk from recent reviews (Newman 1993Citation , WHO 1998Citation ). The estimates of 549 and 320 mL were used for volume of breast milk intake during y 2 and 3 of life, and 309 RE/L and 130 RE/L were used for vitamin A content, respectively. On the basis of the above values, the contribution of breast milk was estimated as 170 and 39 RE/d for breast-fed children during y 2 and 3 of life.

Multivariate analyses were done using the General Linear Models approach (SAS-GLM), in which the dependent variables were the log-transformed values of preformed retinol, ß-carotene and total vitamin A intakes from nonbreast milk sources. The independent variables included age (in months), nutritional status using weight/age Z-score, sex of the child (male/female), whether the child was from a growth monitoring village (Yes/No), current breast-feeding status (Yes/No), maternal education and father's occupation. Although data were available for other indicators of socioeconomic status (SES), father's occupation was found to be the best indicator of SES on the basis of previous correlation analysis (Ramakrishnan 1993Citation ) and was used in the final models. The main occupational groups included coolie laborers, beedi-rollers, semiskilled tradesmen, landed farmers and government employees. Both the beedi-rollers and coolies generally worked for daily wages and owned little or no land. They comprised the lowest socioeconomic groups. Government employees and landed farmers had higher incomes and owned more land, livestock and household possessions.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The description of the study population (n = 683) is presented in Table 1Citation . The prevalence of stunting and wasting among the children was 40.4 and 15.1%, respectively. Agriculture was the mainstay of this population; almost half of the population were landless and worked as coolie laborers for payment in cash and/or kind on others' land and belonged to the socially most deprived castes. Although nearly 70% of the fathers had some education, only 5% of mothers had completed high school and more than half of them had no formal education. The median household size was 5 (range 3–24) and nearly half of the households were either joint or extended families.


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Table 1. Baseline characteristics of the study population1

 
The frequency of intake of foods rich in preformed retinol and ß-carotene and the distribution of the mean serving size for the different foods consumed by preschool children as reported by their mothers are presented in Tables 2Citation and 3, respectively. Although the majority of the children were reported to consume green leafy vegetables such as amaranth and drumstick leaves at least weekly, yellow orange vegetables and fruits such as papaya, mango and pumpkin were consumed less frequently and were available for only part of the year. For example, mangoes were available for only 2–3 mo during the summer. The reported availability of yellow pumpkin and papayas, however, was more variable and ranged from 3 to 8 mo in a year. Animal products such as milk, meat and eggs were consumed less frequently. Less than one third of the children consumed these foods at least once a week, whereas a large proportion rarely or never consumed them. The only exception were children in some villages who regularly attended the government-sponsored preschool creches (balwadis) and received one boiled egg either weekly or every 2 wk. The type of meat consumed was strongly dictated by caste and was commonly beef or goat meat. Specifically, lower caste was associated with increased meat consumption, especially beef, which is taboo for caste Hindus. Poultry and pork, which are more expensive, were consumed less frequently.


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Table 2. Frequency of consumption of common vitamin A–rich foods by preschool children (1–3 y)

 
The mean and median vitamin A intakes from nonbreast milk sources were 137.4 and 121 RE, respectively (Table 4Citation ). Most of this, however, came from plants (ß-carotene). The median contribution of preformed retinol (mainly from animal foods) was only 9.3%. Among the various foods, carrots and eggs were significantly and highly correlated (P < 0.01) with total intakes of vitamin A from nonbreast milk sources. Total vitamin A intake from nonbreast milk sources, i.e., home diet, increased significantly with age until about 2 y of age, beyond which it remained constant (Table 4)Citation . Similar patterns were seen for ß-carotene intakes.


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Table 4. Daily vitamin A intakes of preschool children from nonbreast milk sources by age12

 
Age, sex, maternal education and SES based on father's occupation were highly significant determinants of vitamin A intake from nonbreast milk sources (P < 0.05). The pattern of relationships between determinants and vitamin A intakes was similar across the three dependent variables, ß-carotene, retinol and total vitamin A intakes. Girls had 10% lower dietary intakes of vitamin A (especially retinol) compared with boys (Fig. 1ACitation ); these differences remained significant (P < 0.05) even after controlling for the effects of potential confounders, except for ß-carotene (Table 5Citation ). Vitamin A intakes were the lowest for children whose mothers had no education and the highest for those who had completed high school (Fig. 1Citation B). Higher SES (Fig. 1Citation C), was also positively associated with greater intakes of ß-carotene, retinol and total vitamin A (P < 0.05). The children of beedi-rollers and coolies had the lowest intakes. The effects of maternal education and SES remained significant for total intakes and retinol but not for ß-carotene, after controlling for confounding factors (Table 5)Citation . Age was not significantly associated with retinol intakes when current breast-feeding status was controlled for.



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Figure 1. Mean (unadjusted) daily vitamin A intake expressed as retinol equivalents (RE) from home diets for preschool children by (A) gender, (B) maternal education and (C) paternal occupation.

 

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Table 5. Multivariate model of the determinants of dietary vitamin A intake of preschool children12

 
Breast-feeding was very common in this population. About 95% of all children had ever been breast-fed. Although almost all children were breast-fed in y 1, the prevalence declined to ~60% by the end of y 2 and to 15% at 3 y of age. The mean duration of breast-feeding was 24 mo (range 0–47 mo), and that of exclusive breast-feeding was 3.7 ± 1.6 mo (range 0–8 mo). The most common complementary foods were traditional cereal based gruels of low energy density and micronutrient quality, e.g., ragi kanji, a widely used semisolid-to-liquid gruel prepared from a locally grown millet, ragi. Other common complementary foods included idlis (steamed rice cakes), biscuits, cow's milk and commercially manufactured milk- and cereal-based foods. Although 4 mo of age was widely accepted as the ideal age for introducing complementary foods, most sources of vitamin A were introduced much later. Green leafy vegetables and papayas were introduced toward the end of y 1 of life, whereas mangoes, carrots, eggs and meat were introduced even later.

Vitamin A intake from nonbreast milk sources was significantly lower for children who were currently breast-fed compared with those who were not, especially during y 2 of life (Fig. 2Citation ). These differences were significant even after controlling for other confounding variables (Table 5)Citation . However, vitamin A intake from nonbreast milk sources increased with age among those who were currently breast-fed, whereas that was not the case for those who were not breast-fed. Because the prevalence and frequency of breast-feeding declined with increasing age, we can assume that the volume of breast milk consumed and therefore the contribution of breast milk to total vitamin A intakes most likely declined with age. Using published estimates of breast milk volume and composition, half of the currently breast-fed children met >90% the Indian recommended dietary allowance (RDA) of 250 RE (NIN 1985Citation ) during y 2 of life, but this declined to ~60% of this RDA in y 3 of life.



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Figure 2. Median daily vitamin A intakes expressed as retinol equivalents (RE) of preschool children by current breast-feeding status and age.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Overall, dietary vitamin A intakes were low in this study population and most of the nonbreast milk vitamin A intake was from plant sources. Similar findings have been reported from other developing countries. For example, Zeitlin et al. (1992)Citation used monthly 24-h recalls and found that animal products such as beef, goat, chicken or eggs were rarely consumed (<2%) by preschool-age children in Bangladesh. Although mothers reported that green leafy vegetables were consumed frequently by their children in our study, the actual amounts consumed were extremely small. On the other hand, children tended to consume larger servings of fruits such as papayas and mangoes, which were available for only a few months in the year. This pattern of intake, combined with low fat intakes and worm infestation, and the recent debate on the reduced bioavailability of vitamin A from green leafy vegetables (De Pee and West 1996Citation ), raises important questions on the ability of these diets to meet vitamin A requirements of young children without the inclusion of animal products and consideration of the role of breast milk.

The findings of this study support the importance of breast milk as a major source of preformed retinol in the diets of young children. Although we are limited by the lack of data on the volume and composition of breast milk, our results suggest that breast milk does make a significant contribution to the total vitamin A intake of children during y 2 of life. Using the Indian RDA of 250 RE of vitamin A for children aged 1–3 y (NIN 1985Citation ), our estimates show that children who were not being breast-fed met only 60% of this RDA. The contribution of nonbreast milk sources was even lower (10–40%) among those who were being breast-fed. It should be noted that these estimates would be even lower if the RDA of 400 RE from developed countries was used (NRC 1990Citation ). Zeitlin et al. (1992)Citation concluded that average intakes of preschool age children in Bangladesh were close to or even > 100% of the Indian RDA of 250 RE when the contribution of breast milk was taken into account. More recently, Persson et al. (1998)Citation reported the contribution of breast milk as 164.4 RE/d and 93.6 RE/d during y 2 and 3 of life; this represents 41 and 23% of the recommended safe daily intake of 400 RE for vitamin A, respectively. Although the estimates for the younger children are similar to those reported by Newman (1993)Citation , they are threefold higher for the older children, possibly because it was assumed that breast milk retinol concentrations remained the same. This may not in fact be true because maternal stores become depleted over time in these settings.

An interesting finding of this study that merits special attention is the significant gender-based difference in dietary intakes of vitamin A. Girls were at increased risk for lower intakes of vitamin A, especially preformed retinol even after adjusting for the effects of age, SES, maternal education and current breast-feeding status. Although few studies have demonstrated such differences, these findings are not entirely surprising in light of the evidence of gender-based discrimination against girls in other practices such as female infanticide or reduced access to health care in South Asia (Chen et al. 1981Citation , World Bank, 1994Citation ). In contrast, Backstrand et al. (1997)Citation did not find evidence of gender-based differences in dietary quality and intakes of several micronutrients among preschoolers in Mexico.

Both SES and maternal education were important determinants of vitamin A intakes. Studies from other parts of the world, namely, Mexico and Kenya, using different dietary methods, have also shown that the consumption of micronutrient-rich foods, especially animal foods, was strongly correlated with measures of household wealth (Kennedy and Oniang'o 1993Citation , Zeitlin et al. 1992Citation ). However, in this study, when breast-feeding status was controlled for, SES based on father's occupation was no longer associated with vitamin A intake from plants; this may be explained by the fact that children who were currently breast-fed tended to be of lower SES (P = 0.059) compared with those who were not. Nevertheless, total vitamin A intake from nonbreast milk sources increased significantly with improved SES and maternal education independently of breast-feeding status and was consistently lower for those who were currently breast-fed compared with those who were not, at all levels of SES and maternal education. Children of higher SES, who were not breast-fed, were more likely to meet their requirements (mean intakes were 212 RE/d) compared with those in the lower SES groups. Zeitlin et al. (1992)Citation also found in Bangladesh that vitamin A intake from vegetables was not associated with indicators of SES, but that vitamin A intake from animal sources, which was negligible, was positively associated with maternal education and wealth.

Some of the limitations of these findings are methodological issues related to the estimates of intake. Recall bias may have affected the estimates because mothers were asked to use the past year as the period of recall. This may be more problematic especially for younger children whose diets are constantly changing, and it is likely that mothers were reporting habitual intakes for a more recent period of time, i.e., the past 2–3 mo. Another concern is that differences in the analytical methods, assumptions of bioconversion and the manner in which the food samples were collected may cause systematic errors in the absolute intakes (Booth et al. 1992Citation ). However, these problems are not unique to the Indian database, but are common to use of food composition tables and are less likely to affect the conclusions regarding the patterns of intake.

In conclusion, although food-based approaches are clearly the desirable strategy in eliminating vitamin A deficiency in a sustainable manner, these findings show that a careful understanding of the patterns of intake and their determinants is necessary in planning and implementing the appropriate programs that will be most beneficial and cost effective. Promoting the consumption of animal products may be a viable means of improving dietary quality and child health because the intake of not only vitamin A but also of several other micronutrients such as iron, zinc, and vitamin B-12 could be simultaneously improved (Allen et al. 1992Citation , Demaeyer 1989Citation ). However, this may not be a feasible alternative in some cultures because of socioeconomic, religious and cultural constraints. It is in this context that the importance of breast milk as an inexpensive source of retinol, especially for the poor, cannot be ignored. We must pursue strategies such as the provision of vitamin A supplements to lactating women soon after delivery, which has been shown to improve the retinol content of breast milk (Stoltzfus et al. 1993Citation ), and perhaps multivitamin mineral supplements during pregnancy (Ramakrishnan et al. 1999Citation ).


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Table 3. Distribution of serving size of common vitamin A–rich foods consumed by preschool children (1–3 y) year as reported by mothers1

 

    ACKNOWLEDGMENTS
 
We wish to acknowledge the cooperation of all mothers and children in the 12 villages who participated in this study. We also deeply appreciate the tireless efforts of the village nutrition workers and field workers of the Growth Monitoring Research Project, Rural Unit for Health and Social Affairs Department of the Christian Medical College and Hospital, Vellore, India.


    FOOTNOTES
 
1 Presented at Experimental Biology 95, April 1995, Atlanta, GA [Ramakrishnan, U., Latham, M. C. & Abel, R. (1995) Dietary intake of vitamin A among preschool children in South India using a quantitative food frequency questionnaire. FASEB J. 9: A444 (abs.)]. Back

2 Supported in part by awards from UNICEF and the Ford Foundation. Back

4 Abbreviations used: HKI, Helen Keller International; IVACG, International Vitamin A Consultive Group; NCHS, National Center for Health Statistics; NIN; National Institute of Nutrition (India); RDA, recommended dietary allowance; RE, retinol equivalents; SES, socioeconomic status. Back

Manuscript received January 26, 1999. Initial review completed April 24, 1999. Revision accepted July 19, 1999.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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