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3 Department of Nutrition, University of California, Davis, CA 95616; 4 Institute of Nutrition of Central America and Panama, Guatemala City, Guatemala; and 5 USDA, ARS-Western Human Nutrition Research Center, 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 IntroductionMaterial and MethodsResultsDiscussionLITERATURE CITED |
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Introduction |
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TOPABSTRACTIntroductionMaterial and MethodsResultsDiscussionLITERATURE CITED |
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40% of individuals across all age groups (12), and in Guatemala specifically, in at least one-third of periurban infants, school-aged children, and women (6,7). In Guatemalan school-aged children, plasma vitamin B-12 concentration was associated with their estimated dietary intake of the vitamin (7), suggesting that low intake of ASF and/or vitamin B-12 fortified foods contributes to deficiency in this population.
When the vitamin B-12 status of women is poor during pregnancy and lactation, their infants may have smaller stores of the vitamin at birth (13), and the concentration of the vitamin in breast milk is likely to be low (14). Severe deficiency can occur after 4 mo of age in exclusively breast-fed infants of mothers not consuming ASF. Symptoms of deficiency in such infants include developmental delays (15–19), which may not be completely reversible with vitamin B-12 therapy (16,20,21). In low-income communities in Guatemala, access to ASF is limited and partial breast-feeding commonly continues through the 2nd y of life. The objective of the present study was to identify predictors of plasma vitamin B-12 concentrations in infants 12 mo of age living in periurban Guatemala, where we previously identified a high prevalence of the vitamin deficiency (6,7).
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Material and Methods |
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TOPABSTRACTIntroductionMaterial and MethodsResultsDiscussionLITERATURE CITED |
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Infants were excluded from the study if they were a twin, had a major health problem, showed severe developmental delay at baseline, or their mother was <17 y of age or >3 mo pregnant. Severe developmental delay was defined as a baseline Bayley Scale II (22) Mental Scale score outside the normal range for a 10-mo–old at age 12 mo; infants achieving a raw score of <72 points (standard score, <64) were referred for further diagnosis. Those who were severely stunted [length-for-age Z-score (LAZ) <–3.0] or moderately to severely wasted [weight-for-length Z-score (WLZ) <–2.0] (23) were also excluded from the study but were offered vitamin-mineral supplements, baby foods, and nutritional counseling and referred to their primary health care center. In addition, infants with hemoglobin (Hb) <95 g/L [including a 5.0 g/L altitude correction factor (24)] were excluded from the study but were offered iron supplements. Those with baseline plasma vitamin B-12 concentrations <74 pmol/L (100 pg/mL) were treated with multiple intramuscular vitamin B-12 injections (500 µg methylcobalamin per injection) and kept in the study. All plasma samples used in these analyses were collected prior to treatment for deficiency.
Protocol.
A door-to-door census was conducted in San Jose La Comunidad to identify eligible infants. Recruitment began in October 2003 and ended in December 2004, with 20 subjects entering the study each month. Initially, a home visit was made by a specially trained local motivator, during which informed consent was obtained from the infant's legal guardian. The project manager, a physician, then made a 2nd home visit to examine the infant for signs of serious illness and to obtain a verbal history of the child's health since birth. During an office visit scheduled as close to the infant's 1st birthday as possible, 7 mL of blood was drawn by venipuncture from both the infant and the mother. Infant anthropometric data and socio-demographic information were collected at subsequent home visits.
Socioeconomic status. Demographic data, including size of the family and size of the household, maternal data, including history of pregnancies and pregnancy outcomes, age, education, occupation, and ethnicity, were elicited through a questionnaire administered to the mother by an interviewer at a home visit. Paternal data, such as age and education, are missing in cases where the mother was unable, or did not wish, to respond to questions about the infant's father. Data were collected on the characteristics of the home, access to water and sanitation, and income and expenditures.
Anthropometry. Recumbent length was measured to the nearest 0.1 cm using a portable wooden length-measuring board, and body weight to the nearest 0.01 kg using an electronic weighing scale (Tanita). Z-scores for length-for-age and weight-for-length were calculated using WHO/CDC reference data (23). Triceps, subscapular, and suprailiac skinfolds were measured to the nearest 0.1 mm with skinfold calipers (Holtain) and the sum of skinfolds was calculated. A nonelastic flexible tape measure was used to determine the mid-upper arm circumference (MUAC) to the nearest 0.1 cm, using the midpoint marked for measurement of the triceps skinfold. Tibia length was measured using a sliding caliper (GPM, Seritex). All measurements were made on the left side of the infant and performed in duplicate, using standard methods (25). A 3rd measurement was made if the difference between the first 2 values was greater than a predetermined acceptable range, which was based on mean intra-examiner errors (25,26). Maternal weight and height were measured at the field office. Examiners were tested for exactitude and precision (26) against an experienced project field coordinator.
Dietary intake of vitamin B-12.
A semiquantitative FFQ, administered by trained, standardized interviewers, was used to estimate the usual daily intake of vitamin B-12 by the mother and the infant intake of the vitamin from complementary foods. Mothers or primary caregivers reported infant intake and maternal consumption based on an abbreviated list of foods containing vitamin B-12, including fortified foods and supplements, over the previous 4 wk. The FFQ was developed by INCAP for use in Guatemala and included ASF commonly available in the region. Vitamin B-12 intake estimated with this FFQ was significantly correlated with Guatemalan school children's plasma vitamin B-12 concentrations in a prior study (27). The questionnaire was modified to include vitamin B-12 rich foods widely consumed by infants, such as powdered milks and fortified cereals and atoles. The vitamin B-12 content was estimated using food tables specific to Central America (28) and the USDA food composition database. Intake of vitamin B-12 from organ meats (beef liver, kidney, brain, and chicken liver and intestines) was calculated as 20% that of other foods; absorption of high doses, such as found in liver, is 11% compared with 50% from other foods (29) due to saturation of the ileal receptors when >1.5–2.5 µg of B-12 is consumed in a meal. Mean portions of chicken and beef liver consumed by infants in this study contained 8.7 µg and 26.5 µg vitamin B-12, respectively, so failure to correct for the lower absorption from these sources would overestimate the contribution of these foods to vitamin B-12 status.
Breast-feeding frequency over the previous 24 h was reported by mothers. Motivators visited mothers in the home to provide them with a sheet of paper that had a series of boxes to be checked, one after each time their child fed from the breast. The day and time at which to begin and end recording were printed on the form, and motivators returned to collect the sheet as close to the end of the recording period as possible.
Blood collection.
Infant blood samples were collected by venipuncture from the back of the hand, early in the morning at the field office, as close to the infant's 1st birthday as possible. Fasting samples were not required because newly absorbed vitamin B-12 does not appear in the blood until 5 h after consumption of a physiological dose (0.5–1.0 µg), concentrations peak between 8–12 h after consumption, and only a fraction of newly absorbed vitamin B-12 (1.5–4.5 pmol/L) is present in the blood at any given time (30). Nonetheless, in the present study, caregivers were asked to arrive at the office after fasting and to minimize infant intake as much as possible on the morning of the visit. If a sufficient volume of blood could not be drawn easily at the field office, infants were transported to a professional laboratory for venipuncture (
25% of cases). One mL of blood was drawn into an EDTA vacutainer and 6 mL into a trace-mineral free heparinized vacutainer (Becton Dickinson). Aliquots of whole blood (500 µL) were prepared in amber microcentrifuge tubes and delivered, on ice, to a commercial laboratory in Guatemala City, where a complete blood count (CBC) was performed by Coulter counter. The remaining sample was transported to INCAP on ice, where plasma and red blood cells were separated by centrifuge at 1500 x g for 15 min. Aliquots of plasma were placed in 1-mL vials and frozen at –55° for subsequent analysis.
Assessment of micronutrient status. Plasma vitamin B-12 and folate were measured simultaneously by radioassay (MP Biomedicals). Hb concentrations were measured as part of the CBC, and plasma ferritin by immunoradiometric assay (DPC). Hb and ferritin were used to compare the prevalence of anemia and iron deficiency with the prevalence of vitamin B-12 deficiency. C-reactive protein (CRP) was measured by radial immunodiffusion (The Binding Site). Lot-specific controls were used to monitor the precision and accuracy of the vitamin B-12/folate (Immunoassay Plus 1, 2, 3 Controls, MP Biomedicals) and ferritin (CON6 Multivalent Control Module, DPC) assays. The interassay CV for the low, normal, and high controls was 12.0, 5.6, and 8.4% for vitamin B-12, and 10.3, 8.9, and 8.3% for ferritin, respectively. Samples were run in duplicate and an intrasample difference <15% was accepted. When vitamin B-12 values were in the deficient range (<74 pmol/L) a difference of <25% was accepted.
Micronutrient status cutoffs.
Plasma vitamin B-12 concentration was used as an indicator of vitamin B-12 status. The cutoff for vitamin B-12 deficiency, based on plasma vitamin B-12 concentration, has traditionally been set at 148 pmol/L, but individuals in this range may show clinical symptoms of deficiency (31,32). A cutoff of 220 pmol/L has been suggested to identify depleted individuals prior to the development of more severe deficiency (33), and, in a study of infants, plasma MMA was markedly elevated when plasma vitamin B-12 concentrations were 
220 pmol/L (34). Therefore, plasma vitamin B-12 concentrations of <148 pmol/L, 148–220 pmol/L, and >220 pmol/L were used to classify individuals as deficient, marginally deficient, or adequate, respectively. The reference values for plasma folate were <6.8 nmol/L for deficient, and 6.8–13.4 nmol/L for marginal status. A plasma ferritin concentration <12 µg/L plasma indicated iron deficiency. Because Guatemala City is 1200 m above sea level, a +5 g/L correction factor was added to Hb reference values (24), making the Hb cutoff for anemia <125 g/L in mothers and <105 g/L in infants (35). Iron-deficiency anemia was defined as the presence of anemia plus low ferritin. The presence of infection was detected as a CRP concentration >19.9 mg/L, the concentration found in mild inflammation by the kit manufacturer.
Satistical Methods. Data were entered in duplicate into Epi Info 6 (version 6.04 for DOS, CDC) for cross-validation, and exported to SAS (version 8.2, SAS Institute). Data were missing for a few subjects when caregivers were unable to attend appointments at the field office, or were repeatedly unavailable in the home, and 17 of 304 mothers were unavailable for, or refused, a blood draw. The vitamin B-12/folate assay could not be performed in duplicate for 2 infants due to insufficient sample volume, so these 2 values were not included in analyses. Highly elevated plasma vitamin B-12 concentrations (>850 pmol/L) were also not included in analyses (n = 5 mothers and n = 4 infants) because they may indicate chronic disease (36). Logarithmic transformations were performed on variables that were not normally distributed (specifically, plasma ferritin and vitamin B-12 concentrations) and estimated dietary intake of B-12. Factor analysis was used to generate 4 SES variables (economic status, household size, maternal education, and acculturation) from the substantial amount of socio-demographic data. The economic status variable incorporated data on household income, expenditure, ownership of valued items, and characteristics of the home, including access to water and sanitation; the household size variable included data on maternal parity and pregnancies, as well as total persons living within the household; the maternal education variable contained data on maternal schooling and literacy; and the acculturation variable (which represented acculturation to urban life in Guatemala City) incorporated data on maternal ethnicity, birthplace, and time living in the community.
Pearson coefficients were determined to assess correlations between variables, and t tests were used to check for sex differences. Differences among infant vitamin B-12 status groups were assessed by ANOVA; means were adjusted to test for significance of multiple comparisons using the Tukey-Kramer method. Chi-square tests were used to assess whether the presence of low plasma B-12 (220 pmol/L) in infants was related to maternal B-12 status and infant intake of B-12 from complementary foods. Multiple linear regression tested the relation between maternal vitamin B-12 status and infant diet, and infant plasma vitamin B-12 concentration, controlling for maternal pregnancy status and the 4 SES variables. Infant sex and anthropometric variables were not included as covariates because they were not significantly associated with vitamin B-12 status. Values in the text are means ± SD, and significance was defined as P 0.05 for all analyses.
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Results |
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TOPABSTRACTIntroductionMaterial and MethodsResultsDiscussionLITERATURE CITED |
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3 mo). Mean reported monthly household income was Q1815 ($230). The study population was predominantly Ladino, with 9% of mothers classified as indigenous based on ability to speak an indigenous language (Table 1).
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Nutritional status of infants and mothers. Micronutrient status did not differ between male and female infants, and only 4% of infants and 2.1% of mothers had an elevated CRP concentration. Plasma concentrations of vitamin B-12, folate, hemoglobin, and ferritin in infants were 262.2 ± 163.5 pmol/L, 210.1 ± 128.0 pmol/L, 36.9 ± 11.0 nmol/L, and 27.1 ± 9.2 nmol/L; and in mothers they were 114.4 ± 9.2 g/L, 136.7 ± 10.5 g/L, 21.6 ± 23.3 µg/L, and 40.4 ± 38.5 µg/L. More mothers were vitamin B-12 deficient than infants (Fig. 1); deficient (<148 pmol/L) plus marginally deficient (148–220 pmol/L) plasma vitamin B-12 concentrations were found in 49.3% of infants and in 68.1% of mothers. Iron deficiency (ferritin <12 µg/L) was common in infants (39.4%). Prevalence of anemia (Hb 95–104 g/L) was 14.5% in infants and 9.8% in mothers, and 9.3 and 4.6% were classified as having iron deficiency anemia (low Hb and low ferritin), respectively. No infants or mothers were folate deficient and few had a marginal plasma folate concentration. Infant plasma vitamin B-12 and folate concentrations were correlated with maternal concentrations (r = 0.26, P < 0.001 and r = 0.17, P < 0.001, respectively). Within infants, plasma vitamin B-12 was correlated with plasma folate (r = 0.35, P < 0.001), ferritin (r = 0.12, P < 0.05) and Hb (r = 0.20, P < 0.0005), and within mothers, plasma vitamin B-12 was correlated with plasma folate (r = 0.22, P < 0.001).
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220 pmol/L was 1.4 (95% CI, 1.2–1.7) when their mothers had a marginal or deficient vs. adequate plasma vitamin B-12 concentration (P < 0.0001) and 2.0 (1.6, 2.6) when the infant consumed <1.34 µg/d (50th percentile of intake) vs. >1.34 µg/d of vitamin B-12 from complementary foods (P < 0.0001).
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Predictors of plasma vitamin B-12 in infants. Multiple linear regression was performed to determine whether infant plasma vitamin B-12 concentration was predicted by maternal vitamin B-12 status (maternal plasma vitamin B-12 concentration) and infant diet (infant vitamin B-12 intake from complementary foods, and frequency of breast-feeding). Covariates included in the model were the mother being currently pregnant (a lower pregnancy plasma vitamin B-12 concentration may be caused by plasma volume expansion (37)), and the SES variables (economic status, household size, maternal education, acculturation). Thirty-four children were excluded because of missing data, half of these were due to lack of a maternal plasma sample, so regression was performed with 270 infants. Maternal plasma vitamin B-12 concentration, infant B-12 intake from complementary foods, and larger household size were positively associated with infant plasma vitamin B-12, whereas the frequency of breast-feeding was a negative predictor (R2 = 0.34, P < 0.0001) (Table 3).
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Discussion |
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TOPABSTRACTIntroductionMaterial and MethodsResultsDiscussionLITERATURE CITED |
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At the age of 12 mo, when micronutrient requirements are high due to rapid growth and development, vitamin B-12 status of these infants was associated with both their iron and folate status, suggesting a common cause for these micronutrient deficiencies. Infants with deficient plasma vitamin B-12 concentrations had lower economic status, plasma folate and ferritin, and Hb than those with adequate status, and their mothers had lower plasma vitamin B-12 concentrations. They also consumed less vitamin B-12 from fortified foods and breast-fed more frequently. Because economic status was a covariate in the linear regression model, the higher income of larger households does not explain why household size was positively associated with infant plasma vitamin B-12.
In this population, lactating women are likely to have a low concentration of vitamin B-12 in their milk due to their poor vitamin B-12 status (14), especially as lactation progresses (38,39). In previous studies, two-thirds of women at 8 mo of lactation in Mexico (4), and one-third at 3 mo of lactation in Guatemala (6), had low vitamin B-12 concentrations (<362 pmol/L) in their breast milk. In the current study, breast-feeding frequency was negatively associated with infant plasma vitamin B-12 concentration even after controlling for infant vitamin B-12 intake from complementary foods. This suggests that maternal and infant depletion during pregnancy, and/or low breast milk concentrations, may contribute to the high prevalence of vitamin B-12 deficiency in these infants.
The ASF intake of the 12-mo–old Guatemalan infants is mostly limited to powdered milk and eggs. Several commercially available powdered milks (not infant formulas) some of which are fortified with iron and zinc, are commonly fed to these infants. Because there was a highly significant inverse relation between breast milk and powdered milk intake, and powdered milk has 10 times the amount of vitamin B-12 per unit energy compared with the breast milk of well-nourished women (40), powdered milk was by far the largest source of B-12 in the diet of these infants and explains its positive relation to infant plasma B-12 concentrations. The plasma vitamin B-12 concentration of the mothers was not associated with their dietary intake of the vitamin, even in those (n = 61) who were not currently breast-feeding. A possible explanation is that maternal stores of the vitamin were depleted as a result of pregnancy and lactation.
The lack of folate deficiency in this population has been reported in prior studies in Guatemala (6,7) and might be explained by the inclusion of folate-rich foods, such as beans, in the local diet. In addition, folic acid fortification of wheat flour (1.8 mg/kg) was adopted by Guatemala in 2002. Fortification can contribute directly to the folate status of the women and to the infants to the extent that they consume foods containing fortified flour. The prevalence of anemia and iron deficiency reported here underestimates the community prevalence because infants were excluded from the study if their initial Hb concentration was <95 g/L (n = 23), or a baseline blood sample could not be collected.
In conclusion, vitamin B-12 deficiency is highly prevalent in women and infants in low-income periurban Guatemala City, and infant status is strongly, positively associated with maternal status and intake of complementary foods (particularly powdered milk), and inversely related to the frequency of breast-feeding and household size. Supplementation of lactating (as well as pregnant) women with vitamin B-12 (41–43), and greater use of vitamin B-12 rich complementary foods for infants after age 6 mo, are strategies by which the prevalence of deficiency might be reduced. We observed in a pilot study that mothers believed that meat was an inappropriate complementary food, and there was a perceived and actual inability of infants to consume meats because they were not prepared appropriately for children who lack the ability to chew larger pieces. However, the investigators prepared a ground beef recipe that was well-accepted daily for 9 mo in the subsequent intervention study, so meat consumption from or before this age is certainly feasible and would improve intakes of vitamin B-12 and iron for these infants. Maternal, and subsequently infant, vitamin B-12 status may also be improved by fortification of wheat flour with vitamin B-12.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Author disclosure: K. M. Jones, no conflicts of interest; M. Ramirez-Zea, no conflicts of interest; C. Zuleta, no conflicts of interest; and L. H. Allen, no conflicts of interest.
6 Abbreviations used: ASF, animal source foods; Hb, hemoglobin; CRP, C-reactive protein; INCAP, Institute of Nutrition of Central American and Panama; SES, socioeconomic status.
Manuscript received 28 July 2006. Initial review completed 26 August 2006. Revision accepted 15 February 2007.
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