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© 2005 The American Society for Nutritional Sciences J. Nutr. 135:465-468, March 2005

Community and International Nutrition

The Addition of Milk or Yogurt to a Plant-Based Diet Increases Zinc Bioavailability but Does Not Affect Iron Bioavailability in Women1

Jorge L. Rosado2, Margarita Díaz*, Karla González, Ian Griffin{dagger}, Steven A. Abrams{dagger} and Roxana Preciado

Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Querétaro, México; * Instituto Nacional de Ciencias Médicas y Nutricion Salvador Zubirán, México, D.F.; and {dagger} USDA/ARS Children Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX

2To whom correspondence should be addressed. E-mail: jlrosado{at}avantel.net.


   ABSTRACT
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 ABSTRACT
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The addition of milk and milk-based products to the diets of individuals subsisting on plant-based diets was reported to have positive effects on nutritional status and functional outcomes such as growth, morbidity, and cognition. We examined the effect of the addition of milk or yogurt on the bioavailability of zinc and iron from a plant-based rural diet. The subjects were 48 Mexican women (30.9 ± 5.7 y) who habitually consumed a plant-based diet. The women were assigned to 1 of 3 groups: 1) the typical rural Mexican diet, 2) that diet with milk added, or 3) that diet with yogurt for 13 d. Zinc absorption was measured after extrinsically labeling meals with 67Zn and an i.v. dose of 70Zn; iron absorption was measured by extrinsically labeling meals with 58Fe and a reference oral dose of 57Fe. Including milk and yogurt in the diet increased zinc absorption by 50 and 68%, respectively (P < 0.05). The 3 groups did not differ in the percentage iron absorption. The total amount of zinc absorbed was increased (P < 0.05) by 70% when milk was added to the meal and 78% when yogurt was added. The total amount of iron absorbed did not differ among the groups. The addition of milk and yogurt to a plant-based diet high in phytate increases zinc bioavailability without affecting iron bioavailability.

KEY WORDS: • nutrient bioavailability • zinc absorption • iron absorption • Mexican diets • stable isotopes

Iron deficiency anemia is the most common nutritional deficiency with ~1 billion individuals worldwide having the condition (1). A high prevalence of zinc deficiency was also suggested to occur in different countries (2,3). In Mexico, ~24% of children < 12 y old and 20% of women have anemia. Zinc deficiency occurs in 25% of children and 30% of women (4). Individuals with marginal deficiencies of zinc and iron develop important health and functional consequences including growth stunting (5), increased morbidity (6,7), and reduced neurocognitive development and learning capacity (8). Thus, several strategies are being implemented around the world to improve the zinc and iron nutritional status of populations.

A decrease in iron and zinc bioavailability has been identified as a major mechanism by which marginal deficiencies of these nutrients affect populations. Iron and zinc absorption from a meal depends on the mineral’s absorption from each food and the inhibitors present in the meal. Plant foods and diets usually contain a considerable amount of inhibitors of mineral absorption such as phytic acid, other polyphenols, and dietary fiber. Phytic acid is the main form in which phosphorus is stored in cereals, oilseeds, and legumes. It is also the most potent inhibitor of zinc and iron absorption (9). Intake of these inhibitors is more common in diets that contain little or no animal products, especially in low-income populations. One study compared iron and zinc absorption from a rural plant-based diet with an urban diet in Mexican women. Both of these diets are habitually consumed in Mexico (10). The rural diet contained ~20 times more phytic acid and 4 times more dietary fiber than the urban diet and significantly reduced iron and zinc absorption by 160 and 300%, respectively.

Many attempts are being made in different regions of the world to increase the intake of iron and zinc through mineral supplements (11,12), the addition of nutrients to traditional foods (13,14), or in the design of supplemental foods (15). In several of these products, milk was chosen as the vehicle for mineral fortification or as an ingredient in a supplemented food. Supplementation with milk or milk-based products had positive effects on zinc and iron nutritional status and on functional outcomes such as growth, morbidity, and neurocognitive development (16–18). Furthermore, milk supplementation without added nutrients had beneficial effects on nutritional status, growth, and cognition (16,19,20). Among other potential explanations for the beneficial effects of milk is the possibility that foods of animal origin improve the absorption of micronutrients already present in the diet. Yogurt has such properties, making it a food source with the potential to reduce the negative effect of inhibitors of micronutrient bioavailability. Some of its characteristics include the quality and content of protein, the beneficial effect of microorganisms on the gastrointestinal tract, and the buffer effect of yogurt in the processes of digestion and absorption (21). The purpose of the study described in this report was to evaluate the effect of the addition of milk or yogurt on the bioavailability of zinc and iron from a plant-based rural diet.


   SUBJECTS AND METHODS
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 LITERATURE CITED
 
    Preparation of isotopes. The stable isotopes 58Fe and 57Fe were obtained as the metal (Horizon Tech) with 95.48 and 93.13% isotopic enrichment, respectively. Both forms of metal iron were converted to ferrous sulfate with 0.5 mol/L H2SO4. The 58Fe isotope was dissolved at room temperature in 9 mL of 7 mol/L HNO3 and 37.5 mL of 0.5 mol/L H2SO4 and dried uncovered at 120°C in a muffle furnace for 2–3 h followed by drying at 230°C for 30 min and 500°C for 30 min. The whitish powder was then reconstituted in 50 mL of 0.2 mol/L H2SO4. The ferrous sulfate solution obtained was filtered through a 0.5-µm FH-13 Millex filter (Millipore) and brought to a final volume of 372 mL and a 0.75 mg/L concentration, which was verified by atomic absorption spectrometry (AAS; Perkin-Elmer). The 57Fe oxide as metal was converted to a ferrous sulfate solution by adding 38 mL of concentrated H2SO4 in a sealed vial with a nonreactive lid (Teflon cap) at 110°C until the solution was clear (~2 h). This solution was transferred to a beaker, and the vial was rinsed with 41 mL of 0.5 mol/L H2SO4. The solution was dried in a muffle furnace at 120°C for 2–3 h, 230°C for 30 min, then 500°C for 30 min. The powder obtained was reconstituted with 50 mL of 0.2 mol/L H2SO4, filtered through a 0.5-µm FH-14 Millex filter (Millipore), and brought to a final volume of 308 mL. The final iron concentration was verified using AAS. Stable zinc isotopes, 67Zn and 70Zn, were acquired as oxide salt from Trace Science International and prepared by weighing in a beaker to which concentrated HCl was added until a complete and homogenous solution was obtained; the amount of HCl was determined. The solution was transferred to a 0.5 mol/L saline solution to a final concentration of 3 mg/L and a pH of 5.5. The final solution was stored at 5°C. 67Zn was enriched to 89.5% and 70Zn to 88%. The final samples were stored until analysis of sterility and pyroxenes.

    Subjects and location. The research was conducted in a rural area of the state of Queretaro Mexico where a metabolic unit and community clinic were used for the study. Nonpregnant nonlactating women (n = 48) were recruited for the study. The characteristics of the subjects are described in Table 1. All women were healthy and had not received any medical treatment or nutritional supplements for at least 3 mo before the study. The subjects were originally from La Fuente, a rural community located ~35 km south of Queretaro City. An initial evaluation of the habitual diets of subjects was made to ensure that they consumed primary a plant-based diet. A 24-h dietary recall was administered to each women for 3 consecutive days in addition to a FFQ. Both of these dietary tools were validated and utilized in previous studies (22). Subjects consumed 63% of their energy as carbohydrates, with 46.6% of this from tortillas alone; intakes of iron, zinc, and calcium were 13.3 ± 6.4, 7.2 ± 2.9, and 805 ± 371 mg, respectively. The study was explained to each subject and informed written consent was obtained. The project was evaluated and approved by the Committee of Biological and Clinical Research of the University of Queretaro and the Institutional Review Board of Baylor College of Medicine and Affiliated Hospitals. Results for 4 subjects in the iron absorption trial were not included in the statistical analyses due to laboratory error in handling samples.


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  		TABLE 1 Characteristics of the women at baseline1

 
    Study design and test meal. The test meal consisted of 120 g of corn tortillas (4 tortillas of 30 g each) and 200 mg of cooked black beans based on the model rural diet described by Rosado et al. (10). Women were stratified into 3 groups according to age and initial plasma zinc and iron concentrations (10). One group consumed the test meal plus 250 mL of water (control group), the second group consumed the same meal plus 250 mL of low-fat ultra-high-temperature–treated milk (Alpura 2000) (milk group), and the third group consumed the test meal plus 150 g of flavored yogurt (Danvive, Danone de Mexico) (yogurt group). A description of the nutrient content of the test meal for each treatment group is given in Table 2. Iron and zinc absorptions from the meals were measured with 58Fe and 57Fe isotopes, and with 67Zn and 70Zn isotopes, respectively as described by Abrams (23). Experimental meals were administered to each group at breakfast and lunch for 13 consecutive days. On d 1 of the study, the women were transported to the community clinic after an overnight fast, their weights and heights were measured, and a venous blood sample was obtained before intake of the test meal at breakfast. On d 13, meals were extrinsically labeled with 3 mg of 58Fe and 1 mg of 67Zn distributed among the components of the meal (tortilla, beans, yogurt and milk) in proportion to their intrinsic iron or zinc content. In addition, on d 13, an i.v. dose of 1.0 mg of 70Zn was administered to all subjects. On d 14 and 15, a reference dose of 5.0 mg of 57Fe with 25 mg of ascorbic acid as limeade was given to subjects in all groups (10 mg of total isotope). A urine sample was collected on d 15 for zinc isotope analysis. On d 28, a final blood sample was taken, and the final weight of the women was measured. After the 1st meal of each day, the subjects were monitored in the clinic for at least 4 h to ensure that they did not consume other foods during this time. They had the second meal at the community clinic and returned to their homes for the remainder of the day, having been instructed not to eat anything for the next 4 h.


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  		TABLE 2 Food and nutrient composition of the experimental meals

 
    Biochemical determinations. Total iron and zinc plasma concentrations were measured in duplicate samples by AAS using a Perkin-Elmer spectrophotometer. Iron and zinc certified standards were used on each run of samples and were obtained from Perkin- Elmer. A CV < 5% was reached before analysis of actual samples. Sterility and pyroxene analysis of zinc isotopes used i.v. was conducted using the standard method of the Mexican Pharmacopea (24).

    Estimation of iron and zinc absorption. The stable isotopes of iron and zinc were measured in blood by magnetic sector thermal ionization MS (TIMS-MS) following the procedures previously documented (25,26). All samples were analyzed for isotopic enrichment using a Finnigan MAT 261 TIMS-MS. RBC iron incorporation was determined by evaluating the recovery of the orally administered isotopes in blood obtained 14 d after isotope administration, as previously described (25). Circulating hemoglobin-iron was calculated using a mean blood volume of 65 mL/kg, the measured hemoglobin concentration, and the concentration of iron in hemoglobin (3.47 mg/g). Fractional Fe absorption was calculated assuming that 80% of absorbed iron was incorporated into RBC. Fractional zinc absorption was calculated from the relative fractional excretion of the oral and i.v. isotope in the urine samples. Absolute Fe and Zn absorption were calculated by multiplying the fractional absorption by the iron and zinc content of the meal.

    Statistical analysis. Statistical analyses were performed using SPSS Version 11.0. Differences among treatments in the percentage of absorption were compared by analysis of covariance. To conform to a normal distribution, the percentage of absorption results for iron and zinc were transformed to their logarithms or square root for statistical analysis and results were reconverted to antilogarithms or squares to recover the original units. Because the dose of the minerals was not adjusted to the weight of the women, weight was used as a control variable (covariant). For a comparison of iron absorption, the percentage 57Fe used as reference dose was also included as a covariable. Means were compared by the method of least significant difference using a level of significance of 5%.


   RESULTS
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 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
At the beginning of the study, the nutritional characteristics measured did not differ among the groups. Plasma concentrations of iron and zinc did not differ among the 3 groups. Zinc fractional absorption was increased in the milk and yogurt groups by ~50 and 68% respectively (P < 0.05; Table 3) compared with the control group. The percentage of iron absorption did not differ among the 3 treatments. Total amount of zinc absorbed was increased by 70 and 78%, respectively, in the milk and yogurt group compared with the control group (P < 0.05). The total amount of iron absorbed did not differ among the 3 groups.


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  		TABLE 3 Zinc and iron absorption in women after intake at breakfast and lunch of a plant-based test meal or that meal supplemented with milk or yogurt1

 

   DISCUSSION
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 RESULTS
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LITERATURE CITED
 
The experimental diet chosen for the present study represents a typical diet that is consumed by a high proportion of the population in rural areas of Mexico. Zinc and iron deficiencies are common in populations consuming this type of diet. It was reported previously that this diet is rich in inhibitors of mineral absorption such as phytic acid (10); as a result, lower absorption was suggested to be the major mechanism for the extended deficiency in the population. Thus, the study of strategies to overcome the negative effect of phytate-rich foods on the absorption of minerals is clearly warranted. Milk and milk products either fortified or unfortified have beneficial effects in correcting the functional consequences of zinc and iron deficiencies such as anemia, growth stunting, or delayed cognitive development. We hypothesized, therefore, that milk and yogurt when ingested with a high-phytate plant-based meal could increase the absorption of these minerals. Milk was chosen because it is the animal food that is most commonly used in nutritional support of low-income populations. We found that the inclusion of 250 mL of milk in a typical rural Mexican plant-based meal increased zinc absorption by ~50% and that 150 mL of yogurt increased it by ~68%. However, we did not find any positive or negative effect of milk or yogurt on the absorption of iron.

Animal tissue enhances nonheme iron absorption, especially consumption of pork, veal, beef, lamb, chicken, and fish (27,28). In a recent study, the addition of 50 and 75 g of meat to a phytate-rich meal increased nonheme iron absorption 44 and 57%, respectively (29). More controversial, however, are the studies evaluating the effect of milk as the source of animal tissue on the absorption of iron. Some studies suggested that calcium, which is a major constituent of dairy products, reduced iron absorption (30–32); the hypothesis is that calcium salts, and calcium phosphate in particular, form an aggregate macromolecule with nonheme iron that does not release iron. That effect, however, was demonstrated primarily with calcium supplements. Little information is available concerning the effect of milk products on dietary iron absorption in humans and that information is also controversial. Deehr et al. (33) measured the effect of milk products on whole-body retention of 59Fe in postmenopausal women and found significantly lowered iron retention when milk was added to a meal. On the other hand, Galan et al. (34) measured the effect of the addition of 1 glass of milk or yogurt on iron absorption from a typical French diet by an extrinsic tag method using 55Fe and 59Fe in adult men and found no effect. The results of our study with a typical rural Mexican diet were similar to those of the French study (34).

The fact that we did not find an effect of milk or yogurt on iron absorption from the experimental diet does not completely rule out the possibility that a high calcium concentration from dairy products reduces iron absorption from other diets. It is possible that an inhibitory effect of calcium on Fe was already present in the experimental diet. In support of this possibility are the reports of Cook et al. (30) and Hallberg et al. (32) who demonstrated that that the maximal inhibitory effect of calcium on iron absorption was reached at a level of ~300 mg of calcium. The calcium content of the experimental meal was 218 mg and it came mainly from lime treatment of corn masa flour during the preparation of the tortillas (35).

Similar to the effect on iron absorption, animal proteins counteract the inhibitory effect of phytate on zinc absorption from single meals (36); however, the specific effect of milk on zinc absorption is somewhat controversial. Initial studies suggesting that calcium in milk could reduce zinc absorption (37,38) were made using high amounts of calcium as mineral supplements. More recent studies (31,39–41) found no effect of calcium addition to foods on the absorption of 65Zn. One study (42) compared zinc absorption between cow’s milk and infant formulas and suggested that casein in milk had a negative effect on zinc absorption compared with whey protein, which is adjusted in infant formula. Although calcium and casein were suggested to be potential inhibitors of zinc absorption, no studies have addressed the effect of milk addition on zinc absorption from a meal based on plant foods in which zinc absorption is already inhibited. We found that zinc absorption increased significantly in subjects consuming milk and yogurt added to such meals by 50 and 68% respectively. The total amount of zinc absorbed was also increased by 70 and 78% with milk and yogurt, respectively, compared with the control meal alone. We found that milk and yogurt counteracted the inhibitory effect of phytate on zinc absorption from single meals as was found for other animal proteins (36). This effect was attributed to the amino acids released from the protein that keep the zinc in solution (38). The exact mechanism for a positive effect of milk and yogurt on zinc absorption, as with other animal proteins, remains to be elucidated.

Milk is used as a supplementary food in many countries to feed undernourished populations and it is a food that is used for emergency situations in many regions of the world. In addition, some developing countries obtain milk at subsidized prices under special programs. The use of milk in such situations has also gained support from several studies in which milk supplementation of traditional diets has resulted in nutritional and functional benefits in different populations (19,43–45). An increase in intestinal absorption of some nutrients such as zinc might be contributing to these observations. The present study suggests that milk and yogurt when added to a plant-based meal significantly increase zinc absorption and did not affect iron absorption. The exact mechanism producing these effects requires further study.


   FOOTNOTES
 
1 Supported in part by Instituto de Nutrición Danone A.C. Mexico. Back

Manuscript received 13 October 2004. Initial review completed 19 November 2004. Revision accepted 28 December 2004.


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