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2 Department of Nutritional Biology, University of California, Davis, CA 95616; 3 USDA, ARS Western Human Nutrition Research Center, University of California, Davis, CA 95616; 4 School of Public Health, University of California, Los Angeles, CA 90095; 5 Cancer Research Center of Hawaii, University of Hawaii, Honolulu, HI 96813; 6 University of Nairobi, Nairobi, Kenya; and 7 Global Livestock-CRSP, University of California, Davis, CA 95616
* To whom correspondence should be addressed. E-mail: lhallen{at}ucdavis.edu.
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ABSTRACT |
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 TOP ABSTRACT IntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Introduction |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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The high prevalence of vitamin B-12 deficiency in developing countries may be caused by a low intake of ASF, which is the only dietary source of the vitamin except in the unusual situation where foods are fortified with vitamin B-12. Thus, increasing ASF intake should reduce the prevalence of vitamin B-12 deficiency. A possible alternative explanation is malabsorption of the food-bound vitamin due to infection with Helicobacter pylori (11) or bacterial overgrowth (12). In this case, ASF-based interventions might be less effective for improving vitamin B-12 status.
In this study, vitamin B-12 status was investigated as a sub-study within the framework of the Global Livestock Collaborative Research Support Program project titled "Role of Animal Source Foods to Improve Diet Quality and Growth and Cognitive Development in East African Children" (13). The first question addressed was whether plasma vitamin B-12 concentrations were related to dietary intake of the vitamin at baseline. The second question was whether increasing the intake of milk or meat would improve the children's vitamin B-12 status after 1 or 2 y of feeding. Data on plasma vitamin B-12 changes after 1 y of supplementation has been presented elsewhere (14), as have additional details of the goals, methods, and results of the larger Global Livestock Collaborative Research Support Program project (13).
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Subjects and Methods |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Subjects were 503 school children aged 5 to 14 y. They were recruited through Embu District schools after permission was granted by the Director of the District Ministry of Education on the Central, District, and Zonal levels and the head teachers of the schools. The staple foods consumed by this population are maize and beans. During this study, rainfall was low and poor yields of the staple crops were reported.
Informed consent procedures. Meetings were held in the communities to inform parents about the study. Verbal consent was obtained from parents in parent-teacher meetings at school or at home on an individual basis. Field staff informed children throughout the study that they could choose not to participate at all or to participate in only part of the study. The University of California, Los Angeles Human Subject Protection Committee, the Office of the President of the University of Nairobi, the Kenya Ministries of Education and Health, and the University of California, Davis Human Subjects Review Committee approved the research protocols.
Experimental design. The effect of increasing ASF intake on vitamin B-12 status was assessed by randomly assigning 12 primary schools, at the school level, to 1 of 4 experimental groups: 1) control: no food provided (n = 120); 2) githeri snack: a vegetarian stew of maize, beans, and vegetables (n = 133); 3) githeri + milk snack (n = 131); and 4) githeri + meat snack (n = 119) (16). Feeding took place 5 d/wk when the children were in school, which was 9 mo/y (3 feeding terms of 4 mo, consisting of 3 mo in school with 1 mo out of school) for 2 y. Children were observed during the meal to check that they ate the snack provided to them and any leftovers (which were few) were weighed and recorded.
During the first feeding term, children in the githeri + milk group received 200 mL of milk and those in the githeri + meat group received 60 g of minced beef in addition to the githeri. After the first term, the food given to all 3 groups was increased, with those in the githeri + milk group receiving 250 mL of milk and children in the githeri + meat group receiving 85 g beef (weight before cooking) in addition to the githeri (Table 1). Snacks were relatively isocaloric starting at 239–241 kcal (
1000–1010 kJ) and increasing to 291–311 kcal (1218–1302 kJ) across the intervention groups. After accounting for absences and leftovers, children consumed 76% of the possible amount of energy in the githeri group, 89% in the githeri + milk group, and 93% in the githeri + meat group. The amount of vitamin B-12 provided was similar in the 2 ASF groups, starting at 0.90 µg and increasing to 1.27 µg in the githeri + meat group and increasing from 0.80 µg to 1.00 µg in the githeri + milk group.
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Clinical and biochemical data. Children received a general medical examination at baseline and after 1 and 2 y of feeding. At these times, 2 tubes of blood (10–12 mL total) were collected from each child and transported on ice to the district hospital in Embu (a 40-min drive). All samples were processed within 6 h of collection. Both tubes of blood were centrifuged and aliquots of serum and EDTA plasma frozen at –20°C. Samples were transported on dry ice to Nairobi and flown to the University of California, Davis for analyses. Persons who performed laboratory analyses were unaware of group assignments. Blood could not be drawn from some children at all time points due to parental refusal and absenteeism.
Plasma vitamin B-12 was determined in duplicate by radioassay (ICN Diagnostics). Children were categorized as having low vitamin B-12 status if their plasma concentration was <148 pmol/L and marginal status if the concentration was 148–221 pmol/L. Plasma vitamin B-12 concentration >221 pmol/L was considered normal (3).
C-reactive protein (CRP) was measured in plasma by radial immunodiffusion (The Binding Site) and elevated CRP defined as >10 mg/L.
Malaria infection was detected by the antigen strip test (Vision Biotech). This test detects the presence of antigens produced by Plasmodium falciparum, which accounts for 80–90% of all malaria cases in Kenya (17).
The physicians at the clinical exam diagnosed enlarged spleen, a sign of endemic malaria. Height and weight were measured throughout the intervention and results have been reported elsewhere (18). Only baseline anthropometry is presented here to describe the population. Z scores were calculated based on the CDC growth charts (19).
Statistical analysis. SAS (V. 8.2, SAS Institute) was used for statistical analyses. To meet normality assumptions, plasma vitamin B-12 was transformed by taking its natural log. Baseline characteristics of the population were compared among groups using the SAS GLM procedure.
The intake of ASF and their contribution to total energy intake were calculated to determine whether ASF consumption predicted baseline plasma vitamin B-12 concentration. The association between plasma vitamin B-12 and vitamin B-12 intake was assessed using Spearman correlations. To determine whether children who had lower intakes of ASF were at a greater risk of having lower plasma vitamin B-12, they were categorized into ASF consumption tertiles, or when consumption was low, into 2 consumption categories (none or some). The odds of having low (<148 pmol/L) or low or marginal (<221 pmol/L) plasma vitamin B-12 concentrations were calculated using logistic regression and controlling for age and sex.
A mixed ANOVA model was implemented with the SAS GLM procedure to assess the impact of the intervention on plasma vitamin B-12 concentrations. Explanatory variables included group (nested within the random effect of school), time, group by time interaction, and malaria, enlarged spleen, and elevated CRP as time-dependent covariates. School and subject were included as random effects. When a significant group by time interaction was detected, analysis of covariance (ANCOVA) was performed separately on plasma vitamin B-12 concentration at the end of years 1 and 2 to examine the nature of the interaction and to control for the initial differences in plasma vitamin B-12 between groups. Other covariates included age, gender, malaria infection, elevated CRP, enlarged spleen, and interactions between illness/inflammation indicators. Additionally, if higher-level significant interactions involving both group and time were found, analyses were performed by assigning data from children to 2 separate groups, to examine how the outcome was different in those affected by the variables contributing to the interaction. Presence of intestinal parasites was not used as a covariate in any analyses, because it was shown previously not to be associated with plasma vitamin B-12 in these children (14). For data from a child to be included in these analyses, it was necessary to have biochemical data for at least 2 of the 3 time points (n = 481).
Differences in the prevalence of low, and low + marginal, plasma vitamin B-12 concentrations between groups were assessed at each time point by Generalized Estimating Equations utilizing the GENMOD procedure. If children switched schools, they were assigned to the new treatment group as long as they had consumed the snack assigned to that school for at least 6 mo. Unless noted otherwise, values in the text are means ± SD.
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Results |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Plasma vitamin B-12 concentrations were predicted by the % of energy from ASF (r = 0.308, P < 0.001), milk (r = 0.266, P < 0.001), meat (r = 0.172, P < 0.001), and eggs (r = 0.145, P = 0.001) in the diet. The total amount of vitamin B-12 provided by these foods gave similar predictions for plasma vitamin B-12 concentration to those obtained by expressing intake as % energy from these sources, except that the correlation with total vitamin B-12 from meat was not significant. Milk was consumed in much higher quantities than meat and was the strongest dietary predictor of plasma vitamin B-12 concentration.
The odds ratio (OR) of having a low plasma vitamin B-12 concentration was 6.28 (P < 0.001) for children in the lowest vs. highest consumption tertile for "All ASF", 2.15 (P = 0.002) for those in the "none" vs. "some" meat group, and 4.99 (P < 0.001) for those in the lowest vs. highest tertile of egg consumption (Table 3). Using marginal plasma vitamin B-12 as the outcome yielded similar but nonsignificant trends.
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Mixed model ANOVA, controlling for the effect of school on group, indicated that there was a group by time interaction (P < 0.001), which allowed exploration of the changes by intervention group. Significant 4-way (group x year x CRP x malaria) and 3-way (group x year x malaria) interactions were found. We assumed that these interactions were due to measuring status at the time of illness (elevated CRP or malaria infection) and not to the treatment itself; mixed model ANOVA was performed controlling for elevated CRP, malaria, enlarged spleen, and school x group interactions. This analysis revealed that the githeri + meat and githeri + milk groups had lower adjusted plasma vitamin B-12 concentrations at baseline than the githeri or control groups (P < 0.002 for all comparisons). After 2 y of feeding, the plasma vitamin B-12 in both the meat- and milk-supplemented groups improved further. Concentrations in the meat group were now higher than in the githeri group (P < 0.001) or control group (P = 0.003), whereas in the githeri + milk group, they were higher than in the githeri group (P = 0.004) and marginally higher than in the control group (P = 0.072) (Table 4).
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Mixed model ANOVA using data only from children who were "healthy" (no elevated CRP, malaria infection, or enlarged spleen at time of blood draw) on at least 2 time points resulted in a large loss of sample size (from n = 481 to n = 266). Because children with malaria or elevated CRP were excluded, only the effect of school on group was controlled for in the analysis. This analysis revealed the same trend as the previous analysis, in that githeri + milk and githeri + meat groups tended to fare better than the non-ASF groups (P = 0.063); the lack of significant differences likely was due to the smaller sample size and consequent loss of statistical power. A follow-up ANCOVA, which yielded more power by controlling for initial plasma vitamin B-12 concentration, age, gender, enlarged spleen, and school x group interaction, demonstrated the same trend and revealed that plasma vitamin B-12 concentrations were higher in the githeri + milk group than in the 2 non-ASF groups (P < 0.011) after 1 y, and were higher in the githeri + meat group than the githeri + milk group (P = 0.037) and the 2 non-ASF groups (P < 0.006) after 2 y. Children who were excluded from the above analysis as a result of 1 or more positive indicators of infection showed the same trend: both ASF groups had significantly higher plasma vitamin B-12 than either non-ASF group after 1 and 2 y of ASF supplementation.
Change in prevalence of low plasma vitamin B-12 concentrations. The percentage of children with low (<148 pmol/L) plasma vitamin B-12 concentrations in each group changed over time (Fig. 1). These changes were analyzed controlling for initial status, age, and gender. Despite the between-group differences in plasma vitamin B-12 concentration at baseline (P = 0.001) when the githeri + meat group had the highest percentage of children with plasma vitamin B-12 concentrations <148 pmol/L (Table 2), fewer children had low plasma vitamin B-12 concentration after 1 and 2 y, respectively, in the githeri + milk group (19.4 and 10.4%) and githeri + meat group (20.9 and 29.2%), leaving only 8.9 and 4.5% of children with plasma vitamin B-12 concentration <148 pmol/L. This marked reduction in the prevalence of low plasma vitamin B-12 concentration after 1 y was greater in the githeri + milk and githeri + meat groups than in the githeri and control groups (P < 0.002). Additionally, compared with the remaining 28.0% and 23.3% in the githeri and control groups, respectively, at the end of 2 y, there were fewer low values in the milk- and meat-supplemented groups than in either of the non-ASF groups (P < 0.001). The prevalence before and after 2 y of intervention changed from 55.6 to 4.5% in the githeri + meat group and 41.0 to 8.9% in the githeri + milk group. This analysis was also run for the percentage of children with low and marginal plasma vitamin B-12 concentrations (<221 pmol/L) with very similar and significantly different changes among the groups.
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Discussion |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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There was a negative correlation between plasma vitamin B-12 concentration and age at baseline. This may indicate that there is an age-associated decline in vitamin B-12 status. However, because there were some costs associated with attending school in Kenya at the time of the study, it may simply indicate that poorer families send their children to school at a later age and these families have poorer nutritional status than those who can send their children to school at a younger age.
There was a 4-way interaction between group, time, malaria, and elevated CRP, suggesting that the children who have elevated CRP, malaria, or both were responding differently to the interventions from those who were "healthy." However, repeating the analysis with only healthy children showed similar results to those of the whole group, as did analysis of data from children who were affected by elevated CRP or malaria (data not shown).
Although not a perfect measure of vitamin B-12 status, plasma vitamin B-12 concentrations did improve in the expected way with ASF supplementation. Typically in adults, a plasma vitamin B-12 concentration <258 pmol/L is associated with an increase in methylmalonic acid (MMA), reflecting that vitamin B-12 status is inadequate to support its coenzyme function and with an increase in plasma homocysteine (Hcy) concentration (21). Although this plasma cut-off has not been confirmed in children, it is possible that the increase in plasma vitamin B-12 concentrations achieved by feeding ASF in this study increased the availability of vitamin B-12 for physiological functions. Although it may have been valuable to measure MMA or Hcy concentrations in this study, MMA may be a less valid indicator of vitamin B-12 status in the developing world; gut bacteria produce propionic acid, a precursor of MMA, which may explain why serum MMA was higher than normal even in Guatemalan children with normal plasma cobalamin concentrations (22). Elevated plasma Hcy also occurs in folate, vitamin B-6, and riboflavin deficiencies (23,24).
A low plasma vitamin B-12 concentration has been associated with anemia, neuropsychiatric abnormalities (25), and altered neurological function (26). As reported elsewhere, supplementation with meat in this study had a positive impact on cognitive performance (27). However, it cannot be determined which meat constituent(s) were responsible for this impact. Randomized, controlled vitamin B-12 supplementation trials are ongoing to evaluate the functional consequences of improving vitamin B-12 status in children with low plasma vitamin B-12 concentrations.
It is generally thought that vitamin B-12 deficiency occurs only in strict vegetarians (vegans), but more recent data show a substantial prevalence of low plasma concentrations in lacto-ovo vegetarians and low meat consumers (28–31). In Australia, there was a stepwise reduction in plasma vitamin B-12 concentration from high meat consumers to moderate meat consumers to lacto-ovo vegetarians to vegans, which was significantly different between all groups (32). In the Australian study, the lacto-ovo vegetarians had an average plasma vitamin B-12 concentration of 210 ± 97 pmol/L, very similar to the average value at baseline in this study (193.6 ± 105.3 pmol/L) for children who consumed very little meat but some milk.
In rural African households of livestock owners, the animal slaughters for familial consumption are rare and much fewer than the number of animals sold (33). However, in this same study of camel, cattle, small ruminant, and pastoral herders in Eastern Ethiopia, 73% of the milk produced by the animals was consumed while only 27% was sold, indicating that consumption of milk was more likely than consumption of meat. In this study, we found also that milk consumption was much more prevalent than the consumption of meat and that it improved plasma vitamin B-12 concentrations in those who consumed it. Ownership of small milk-producing animals might benefit the rural poor even when they do not eat the meat, because milk is also a nutritionally dense food. A dairy goat development project in Ethiopia demonstrated that goat productivity and milk intake by children could be increased by empowering women with technical knowledge and providing micro-credit programs (34).
ASF provide vitamin B-12 and are a good source of other micronutrients, including vitamin A, iron, and zinc. In this ASF intervention, a significant and sizeable effect on plasma vitamin B-12 concentrations was seen. This, coupled with the substantial prevalence of low plasma vitamin B-12 concentrations throughout the developing world, suggests that sustainable ASF production projects such as the one in Ethiopia should be encouraged to increase ASF consumption in nutritionally at-risk groups, where it is culturally acceptable.
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FOOTNOTES |
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8 Abbreviations used: ANCOVA, analysis of covariance; ASF, animal source foods; CRP, C-reactive protein; HAZ, height-for-age Z; Hcy, homocysteine; MMA, methylmalonic acid; OR, odds ratio; RAE, retinol activity equivalents.
Manuscript received 22 September 2006. Initial review completed 6 January 2006. Revision accepted 30 November 2006.
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LITERATURE CITED |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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