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Community and International Nutrition

Vitamin B-12 Status Is Associated with Socioeconomic Level and Adherence to an Animal Food Dietary Pattern in Colombian School Children^1–3,

⁴ Departments of Nutrition and Epidemiology, Harvard School of Public Health, Boston, MA 02115; ⁵ Department of Nutrition, National University of Colombia Medical School, Bogotá, Colombia; ⁶ Nutrition Unit, National Institute of Health of Colombia, Bogotá, Colombia; ⁷ Braun School of Public Health and Community Medicine, Jerusalem, Israel 91120; and ⁸ Department of Community Health, Warren Alpert Medical School of Brown University, Providence, RI 02903

^* To whom correspondence should be addressed. E-mail: evillamo{at}hsph.harvard.edu.

	ABSTRACT

TOP ABSTRACT Introduction Methods Results Discussion LITERATURE CITED

 
Vitamin B-12 is related to neurocognitive function in school-age children, yet sociodemographic and dietary correlates of vitamin B-12 status in this age group are not well characterized. The prevalences of vitamin B-12 or folate deficiencies in Colombia are unknown. We conducted a cross-sectional study in a representative sample of 2800 low- and middle-income children aged 5–12 y from Bogotá's public schools. Plasma vitamin B-12 and erythrocyte folate concentrations (mean ± SD) were 327 ± 106 pmol/L and 858 ± 256 nmol/L, respectively. The prevalence of vitamin B-12 deficiency (<148 pmol/L) was 1.6% and the prevalence of marginal status (148–221 pmol/L) was 15.0%. Only 2 children had folate deficiency (<305 nmol/L). In multivariate analysis, mean vitamin B-12 concentrations significantly decreased with age and were 15 pmol/L higher in girls than boys (95%CI = 8, 23). Vitamin B-12 was inversely related to the mother's parity and positively associated with the amount of money spent on food per person per day at home and the household's neighborhood socioeconomic status (SES) classification. Folate concentrations were lower in girls than in boys and significantly increased with the household's SES. We identified 4 dietary patterns with principal components analysis of a FFQ in a random subsample (n = 972). Plasma vitamin B-12 was strongly, positively associated with a pattern that included frequent intake of beef, chicken, and dairy products in a dose-response manner (P-trend, adjusted, = 0.008). Low vitamin B-12 status is not negligible in Colombian school children and is associated with poverty and marginal intake of animal food sources.

	Introduction

TOP ABSTRACT Introduction Methods Results Discussion LITERATURE CITED

Recent reports indicate that vitamin B-12 could play a significant role on the neurocognitive development of school children (14,15), yet the prevalence and determinants of vitamin B-12 deficiency in this age group have not been widely characterized. We conducted a study to examine the prevalence of vitamin B-12 deficiency in a sample of school children from Bogotá, Colombia, who represent low- and middle-income families. We aimed to determine the sociodemographic and dietary determinants of the plasma concentration of vitamin B-12 in this population.

Colombia adopted folic acid fortification of wheat flour in 1996. The prevalence of folate deficiency in the postfortification era is largely unknown. If folate concentrations have been raised substantially but vitamin B-12 status is low, the consequences of vitamin B-12 deficiency could be aggravated (16). We therefore examined the correlates of folic acid status with the use of erythrocyte folate measurements.

	Methods

TOP ABSTRACT Introduction Methods Results Discussion LITERATURE CITED

 
    Study population. The study was conducted as part of a project on the health and nutritional status of school children from low- and middle-socioeconomic strata in Bogotá, Colombia. Details of the study design have been previously published (17). Briefly, in February 2006, we enrolled 3202 children 5–12 y old from primary schools of Bogotá in a longitudinal study to examine the impact of school health initiatives on their health and nutritional status. The sample was randomly selected from the list of all classes (primary school grades 1–5) for that year in all public schools of the city. We used a cluster sampling technique with classrooms as sampling units. The study population is representative of low- and middle-income families from Bogotá, considering that the public school system enrolls more than one-half of all primary school children in the city and 89% of them are of low- and middle-socioeconomic status (SES) (18).

During wk 1 of classes, we sent a questionnaire to the parents inquiring about their age, marital status, education level, home ownership, socioeconomic characteristics of the household (including income and money spent to purchase food), and food security status. The questionnaire was returned by 2466 households, representing 81% of enrolled children's families, after accounting for siblings. During the next 3 wk, trained research assistants visited the schools to obtain a fasting blood specimen by venipuncture from enrolled children. Approximately 4 mL of blood was placed in an EDTA Vacutainer tube following a protocol to avoid hemolysis. On the same day of collection, the aliquots were transported on ice and protected from sunlight to the National Institute of Health in Bogotá, where all biochemistry analyses took place.

Between May and June, trained dieticians applied a 38-item FFQ to a random sample of 1027 mothers to obtain information on the children's usual dietary intake. The reference period to determine average intake was the month prior to the interview. For each item, we described reference portion sizes in natural units or standard measures for commonly consumed servings in this population and inquired about frequency of intake with a scale comprising 9 options, from 4 to 5 times per day to never. Additional characteristics of the FFQ have been reported (17). Preliminary results of a validation study of this FFQ indicate that it is appropriate to rank individuals according to their dietary vitamin B-12 intake. In a subsample of 110 children, the crude Pearson correlation coefficient between vitamin B-12 intake estimated from the FFQ and vitamin B-12 intake estimated as the mean of multiple-day 24-h recalls was 0.47.

    Laboratory methods. An aliquot of whole blood was hemolyzed by dilution in a hypotonic aqueous solution of 1% ascorbic acid. Another aliquot was centrifuged at 1500 x g for 15 min and plasma was separated. Erythrocyte folate was measured on the RBC lysates and vitamin B-12 on the plasma aliquot with the use of competitive chemiluminescent immunoassay in an ADVIA Centaur analyzer (Bayer Diagnostics).

    Statistical data analyses. Outcomes were plasma vitamin B-12 and erythrocyte folate status. Children were classified as vitamin B-12 deficient when concentrations were <148 pmol/L and marginally deficient if concentrations were 148–221 pmol/L (9). Folate deficiency was defined as erythrocyte folate concentrations < 305 nmol/L (19).

Sociodemographic determinants of vitamin B-12 or folate status included child's age and sex; maternal characteristics, including age, years of formal schooling, marital status, and parity; and indicators of the household's SES, including the amount of money spent on food per person at home every day (the total amount of money spent on food divided by the number of people in the household), home ownership, and the household socioeconomic stratum according to the city's classification of the neighborhood's public services fees. We assessed child food insecurity in the household with the use of an index developed from 5 child-specific questions that were included in a previous food security survey (17). The survey was a modified version of the Spanish language USDA Household Food Security Survey Module (20) and the Community Childhood Hunger Identification project (21). Child food insecurity in the household was considered to be present when 3 of the 5 questions had an affirmative answer.

Dietary determinants of vitamin B-12 and folate status included 4 dietary patterns that we identified with the use of principal component analysis of the 38 items in the FFQ (17). An orthogonal transformation was used to rotate the factors obtained to achieve a simpler structure and facilitate interpretability. To determine the number of factors to retain, we considered eigenvalues > 1, the Scree test, and interpretability. We multiplied the standardized frequencies of intake for each food group by the factor score coefficients and the sum of these products was the score for each derived factor. The patterns identified were: animal protein (e.g. beef/pork/veal/lamb, chicken/turkey, milk, cheese), cheaper protein (e.g. cow tripe/liver, spleen, chicken giblets), traditional/starch (e.g. rice, potato, plantain), and snacking (e.g. candy, ice cream, packed fried snacks, soda, fruit punch). We also examined whether frequency of intake of individual foods or food groups and vitamin supplements were significant correlates of vitamin B-12 or folate status. Analyses of dietary determinants were restricted to the subsample of children from whom we collected the FFQ.

In univariate analyses, we estimated circulating vitamin B-12 and erythrocyte folate concentrations (means ± SD) by categories of each determinant. We tested the significance of the associations between ordinal determinants and nutrient serostatus with the use of tests for trend. These tests were derived from linear generalized estimating equation (GEE) models in which vitamin B-12 or folate was the outcome and the determinant was a covariate representing the ordinal categories of the correlate, introduced as a continuous variable. For dichotomous determinants, we used the Wald test. We specified an exchangeable correlation matrix in the models to account for within-household correlations among siblings in the sample. We estimated adjusted differences in vitamin B-12 or folate concentrations by categories of determinants by fitting multivariate models with the correlates that were significant in univariate analyses at P < 0.10. We retained in the models the determinants that remained associated with each outcome at P < 0.05 or were considered to be biologically relevant. CI were built around the adjusted differences with the use of robust variances, which do not rely on the multivariate normality assumption (22). The effect of clustering by classroom was negligible and was excluded from the models for parsimony. All statistical tests were double-sided. A P-value of <0.05 was considered significant. Analyses were carried out with the use of the Statistical Analysis Software SAS version 9.1 (SAS Institute).

The parents or primary care providers of all children gave written informed consent prior to enrollment. The study protocol was approved by the Ethics Committee of the National University of Colombia Medical School and the Humans Subjects Committee at the Harvard School of Public Health.

	Results

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Among the 3202 children recruited, we collected a biological specimen in 2816 (88%). Results of vitamin B-12 or folate analyses were available in 2800 children, and this constituted the final sample for the present report. Dietary data were available in 972 of these children. Children who did not provide a blood sample were more likely to be female than those who provided a sample (Supplemental Table 1). Among children who provided a sample, those with dietary information were slightly younger and more likely to live in lower SES neighborhoods than children without dietary information. There were no other differences between these groups.

Children's age was 8.7 ± 1.8; 49% were girls. Sixty-eight percent of the children's households had a daily per capita income <2 USD and 75% spent <1 USD on food per person each day. Plasma vitamin B-12 concentration was 327 ± 106 pmol/L and erythrocyte folate was 858 ± 256 nmol/L. The prevalence of vitamin B-12 deficiency (<148 pmol/L) was 1.6% and marginal status (148–221 pmol/L) was 15%. Only 2 children had erythrocyte folate concentrations <305 nmol/L.

    Sociodemographic correlates of vitamin B-12 and folate status. The prevalence of marginal or deficient vitamin B-12 status was 17.2, 15.7, 15.6, and 23.5% in age groups 5–6, 7–8, 9–10, and 11–12 y, respectively. Marginal or deficient status was more prevalent in boys than in girls between 7 and 12 y of age (Fig. 1). In multivariate analysis, plasma vitamin B-12 was significantly higher in girls than boys and was inversely related to the child's age and mother's parity and positively associated with the amount of money spent on food in the household and the household's socioeconomic stratum (Table 1). There was evidence for dose-response associations between these sociodemographic determinants and vitamin B-12 concentrations. Child food insecurity was not significantly related to vitamin B-12 status after adjusting for other socioeconomic indicators. Maternal age, marital status, and home ownership were not associated with the children's vitamin B-12 concentrations.

View larger version (14K): [in this window] [in a new window]   FIGURE 1  Prevalence of marginal and deficient vitamin B-12 status in low- and middle-income school children from Bogotá, Colombia, according to sex and age group. Values are percentages, n = 2660.

View larger version (21K): [in this window] [in a new window]   FIGURE 2  Plasma vitamin B-12 concentrations in low- and middle-income school children from Bogotá, Colombia, according to their adherence to 4 dietary patterns. Bars represent means + SEM, n = 237, 240, 235, and 234 for quartiles 1–4, respectively. Quartile 1 represents the lowest quartile of pattern adherence and quartile 4 the highest quartile of pattern adherence. The P-trend values are derived from linear regression models in which a term representing the quartiles of each pattern was introduced as a continuous variable.

Erythrocyte folate concentrations were not significantly associated with dietary patterns or with the frequency of intake of individual food items, including bread, breakfast cereal, legumes, or supplements.

	Discussion

TOP ABSTRACT Introduction Methods Results Discussion LITERATURE CITED

 
We examined the status and correlates of plasma vitamin B-12 and erythrocyte folate in school children from low- and middle-income families from Bogotá, Colombia. Although folate deficiency was not documented, we found a nonnegligible 17% prevalence of marginal or deficient vitamin B-12 status.

A number of sociodemographic factors were significant determinants of vitamin B-12 status in this population. Vitamin B-12 concentrations were lower in boys than in girls and appeared to decrease with age. A similarly negative, cross-sectional association between plasma vitamin B-12 and age was reported among school children from rural Kenya (23). In older adults, an impairment of vitamin B-12 status with age has been explained through declined gastric acidity, athrophic gastritis, and bacterial overgrowth that lead to lower absorption of protein-bound vitamin B-12 (24); however, these factors do not appear to play a significant role in the vitamin B-12 status of school-age children (25). Instead, the inverse relation between male gender or age and vitamin B-12 status in our study could be interpreted in light of greater requirements for more rapid growth in boys than in girls and in older than in younger children that are not being met with adequate intake of the vitamin. The estimated average requirements are greater for children 9–13 y old (1.5 µg/d) than for those aged 4–8 y (1.0 µg/d) (26). Age differences in plasma vitamin B-12 could be due in part to dietary intake variability in our study, because we found that older children were less likely to adhere to an animal protein intake pattern.

Vitamin B-12 concentrations were strongly associated with indicators of SES, including maternal parity, the amount of money spent on food at home, and a general ranking of the household's stratum according to the neighborhood. These associations have not been consistently found in other settings. In Guatemalan school children, for example, parental income was lower in children with plasma vitamin B-12 < 162 pmol/L than among children with higher concentrations, but this difference was not significant (P > 0.05) (25) and there were no associations with other SES indicators. Large household size was inversely related to vitamin B-12 status in Guatemalan infants, but an index of economic status or the level of maternal education were not (23). Among Venezuelan children, vitamin B-12 concentrations were not related to SES (11). The socioeconomic gap in the vitamin B-12 status of our population is likely to represent high levels of inequity in access to animal food sources. Meat is an expensive food item in this setting and the imposition of cost constraints has been shown to decrease meat intake (27). In support of this explanation are the strong, positive, linear associations we found between adherence to an animal food intake pattern and indicators of SES such as the daily amount of money spent on food per capita and the household's neighborhood socioeconomic classification. Furthermore, the associations between SES indicators and vitamin B-12 concentrations were attenuated when we introduced them in a model with the animal protein food pattern, suggesting that the latter is in the causal pathway between SES and vitamin B-12 status.

When we considered together the individual sources of vitamin B-12 in this population, only meat (red meat and poultry) or dairy remained associated with vitamin B-12 status, whereas multivitamin supplements or cheaper animal foods including cow liver or egg were not. One possible explanation is that vitamin B-12 from eggs or liver has lower bioavailability than vitamin B-12 from red meat or chicken (28,29). In addition, the frequency of intake of liver or multivitamin supplements was relatively low in this population. Our results are consistent with the study of school children in rural Kenya, where increased plasma vitamin B-12 was the only micronutrient response to supplementation with meat or dairy (30). These results suggest that meat- or dairy-based programs may represent an effective way of improving the vitamin B-12 status of school children.

The associations between individual food sources and vitamin B-12 status are consistent with the linear relation we found between adherence to an animal protein pattern and plasma vitamin B-12 concentrations. The difference in plasma vitamin B-12 between the highest and lowest quartiles of adherence to the animal protein pattern (26 pmol/L) was close to that between the highest and lowest categories of frequency of meat intake (24 pmol/L) or dairy intake (32 pmol/L). An explanation for the similarity is that the highest factor loadings in the animal protein pattern were for dairy and red meat intake (Supplemental Table 2). Both the dietary patterns and individual foods analytic approaches offer advantages and are complementary. The dietary patterns analysis accounts for interactive effects of nutrients in different foods (31) that may affect the bioavailability of vitamin B-12. In addition, analyses of dietary patterns overcome the possibility of finding significant associations by chance alone when several foods or food groups are examined individually in relation to nutrient status. On the other hand, analyzing the relations between individual food sources and vitamin B-12 concentrations in multivariate models allows the identification of specific foodstuffs that strongly and independently contribute to vitamin B-12 status and which may be specifically considered for supplementation programs.

We did not find folate deficiency in this population. Folate fortification of wheat flour (1.54 mg/kg) was mandated in Colombia in 1996. Although accessible published data on folate status in Colombia prior to fortification are unavailable, it is possible to speculate that the lack of folate deficiency in Bogotá school children might be linked to the fortification policy. It may also be due to high intake of folate-rich foods, including beans, but we did not find specific associations between dietary intake of these foodstuffs and folate concentrations, perhaps because of limited variability in the frequency of intake. Interestingly, despite the lack of deficiency, we did observe a gradient in folate status by household SES. This association could be indicative of unequal distribution of fortified products within the city and suggests that folate deficiency could be a problem in other areas of the country with limited access to quality-controlled, fortified wheat flour.

Our study has some limitations. First, its cross-sectional nature prevents us from establishing the temporal sequence of the associations found and limits the possibility of drawing causal inferences. Second, we lacked functional indicators of vitamin B-12 deficiency such as elevated serum methyl-malonic acid; however, low plasma vitamin B-12 concentrations have been related to adverse hematological and neurocognitive outcomes in children (15) and have been shown to increase in response to supplementation (30). Thus, plasma concentrations of vitamin B-12 are commonly used as an indicator of vitamin B-12 status in population studies. Third, although dietary intake appears to play a major role in the vitamin B-12 status of this population, we did not have indicators to determine whether and to what extent malabsorption could be a risk factor for marginal or deficient status.

In conclusion, whereas folate deficiency is rare, marginal or deficient vitamin B-12 status is moderately prevalent in low- and middle-income school children from Bogotá, Colombia. Dietary intake of animal foods, especially meat and dairy, appear to have a major influence on the vitamin B-12 status of this population. Inclusion of animal food sources in ongoing food assistance programs at schools could improve the vitamin B-12 situation of children in Colombia. The policy of wheat flour micronutrient fortification in Colombia currently includes iron, thiamin, riboflavin, niacin, and folate, but excudes vitamin B-12. Inclusion of vitamin B-12 into the micronutrient mix for wheat flour fortification needs to be considered. Future studies are warranted on the effects that suboptimal vitamin B-12 status may have on functional outcomes among school children, including neurocognitive and school performance, anemia, and morbidity.

	FOOTNOTES

 
¹ Supported by the David Rockefeller Center for Latin American Studies at Harvard University, the City of Bogotá's Secretary of Education, the National University of Colombia, and the National Institute of Health of Colombia.

² Author disclosures: E. Villamor, M. Mora-Plazas, Y. Forero, S. Lopez-Arana, and A. Baylin, no conflicts of interest.

³ Supplemental Tables 1 and 2 are available with the online posting of this paper at jn.nutrition.org.

Manuscript received 21 January 2008. Initial review completed 9 March 2008. Revision accepted 21 April 2008.

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This Article Abstract Full Text (PDF) Online Supporting Material Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Villamor, E. Articles by Baylin, A. Search for Related Content PubMed PubMed Citation Articles by Villamor, E. Articles by Baylin, A.