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Article

Prenatal Iron Supplements Impair Zinc Absorption in Pregnant Peruvian Women^{1 ,2}

Kimberly O. O’Brien^*3, Nelly Zavaleta^**, Laura E. Caulfield^*, Jianping Wen and Steven A. Abrams

^* The Johns Hopkins School of Hygiene and Public Health, Division of Human Nutrition Baltimore, MD 21205, ^** The Instituto de Investigacion Nutricional, Lima, Peru, and The U.S. Department of Agriculture/Agricultural Research Service Children’s Nutrition Research Center, Baylor College of Medicine, 1100 Bates St., Houston, TX 77030

³To whom correspondence should be addressed.

	ABSTRACT

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Prenatal iron supplements may adversely influence zinc absorption during pregnancy. To examine the impact of prenatal iron supplements on supplemental zinc absorption, fractional zinc absorption was measured in 47 pregnant Peruvian women during the third trimester of pregnancy (33 ± 1 wk gestation). Of these 47 women, 30 received daily prenatal supplements from wk 10–24 of pregnancy until delivery. Supplements contained 60 mg of Fe and 250 µg of folate without [iron group (Fe), n = 16] or with [iron and zinc supplemented group (Fe + Zn), n = 14] 15 mg of Zn. The remaining 17 women [unsupplemented control group (C)] received no prenatal supplementation. Zinc concentrations were measured in plasma, urine and cord blood and percentage zinc absorption was determined following dosing with oral (⁶⁷Zn) and intravenous (⁷⁰Zn) stable zinc isotopes. Percentage zinc absorption was significantly lower than controls in fasting women receiving iron- containing prenatal supplements (20.5 ± 6.4 vs. 20.2 ± 4.6 vs. 47.0 ± 12.6%, Fe, Fe + Zn and C groups, respectively, P < 0.0001, n = 40). Plasma zinc concentrations were also significantly lower in the Fe group compared to the C group (8.2 ± 2.2 vs. 9.2 ± 2.2 vs. 10.9 ± 1.8 µmol/L, Fe, Fe + Zn and C groups, respectively, P = 0.002), and cord zinc concentrations were significantly related to maternal plasma Zn levels (y = 6.383 + 0.555x, r = 0.486, P = 0.002). The inclusion of zinc in prenatal supplements may reduce the potential for iron supplements to adversely influence zinc status in populations at risk for deficiency of both these nutrients.

KEY WORDS: • stable isotopes • zinc • pregnancy • iron • Peru • absorption • women

	INTRODUCTION

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Suboptimal zinc intakes may be relatively common throughout the world (Tamura and Goldenberg 1996 ). Low zinc intakes may be especially detrimental during pregnancy due to the role that zinc plays in growth and development. Potential adverse consequences of zinc deficiency during pregnancy include increased maternal mortality, low birth weight, prolonged labor, spontaneous abortion and prematurity (Caulfield et al. 1998 , Tamura and Goldenberg 1996 ). Impaired zinc status during pregnancy was also recently found to adversely influence late fetal development (Merialdi et al. 1999 ).

Despite the fact that multiple micronutrient deficiencies often coexist, most supplementation programs in developing countries focus only on iron supplementation. This practice may further exacerbate deficiencies of other nutrients such as zinc. Studies in iron-replete nonpregnant women have found that iron (Fe) to zinc (Zn)⁴ ratios above 2:1 can impair zinc absorption (Solomons 1986 ), and several studies have reported that acute periods of iron supplementation from 38 to 65 mg/d may lower plasma zinc concentrations (Bloxam et al. 1989 , Dawson et al. 1989 , Hambidge et al. 1987 ).

During pregnancy, the potential adverse influence of iron supplementation on zinc status may be more detrimental due to the increased requirements for both iron and zinc. Previous studies in a nutritionally replete population found that the level of prenatal iron supplementation was negatively correlated with maternal plasma zinc concentrations during the third trimester of pregnancy (Hambidge et al. 1983 ).

Although most studies have demonstrated Fe and Zn interactions with amounts of supplemental iron over 30 mg/d, multivitamins containing as little iron as 18 mg/d have also been found to lower plasma zinc concentrations in pregnant teens (Dawson et al. 1989 ). Furthermore, alterations in plasma zinc concentrations during pregnancy may be evident following only 1 wk of iron supplementation (201 mg/d) (Hambidge et al. 1987 ).

At this time, few data exist on the ability of prenatal iron supplements to influence zinc absorption in populations with marginal intakes of both iron and zinc. Recently, we demonstrated that plasma zinc concentrations were significantly lower in pregnant Peruvian women who were receiving iron supplements during pregnancy (O’Brien et al. 1999 ). The goal of the proposed study was to directly examine the influence of prenatal iron supplementation on percentage zinc absorption during the third trimester of pregnancy. To examine this issue, dual stable isotope studies of zinc absorption were undertaken in iron-supplemented and unsupplemented pregnant women, living in a low-income Peruvian community with a high prevalence of both zinc and iron deficiency.

	MATERIALS AND METHODS

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Subject selection.

Pregnant women, between the ages of 18 and 35 y were recruited during their third trimester of pregnancy (30–36 wk gestation), from Villa El Salvador, a peri-urban low-income community on the outskirts of Lima, Peru. Women recruited into this study had a parity between 0 and 3 and had no known underlying metabolic or other disease processes that might influence mineral metabolism.

Three groups of women were recruited. Supplemented women were recruited from an on-going USAID-funded prenatal supplementation study in this community that was designed to address the impact of zinc supplementation on birth outcomes (Caulfield et al. 1999b ). This study was comprised of 1,295 women who were randomly assigned to receive daily prenatal tablets containing either 60 mg of Fe (as ferrous sulfate) and 250 µg of folate (Fe, iron group) or the same prenatal tablet containing 15 mg of zinc as zinc sulfate (Fe + Zn group). These women consumed prenatal supplements and scheduled prenatal check-ups from 10 to 24 wk of pregnancy until delivery. Longitudinal compliance data were monitored by biweekly pill counts. The third group of women [Control (C) group] was recruited from the same community but did not receive prenatal supplements because they did not seek medical attention until late in gestation. Information was also obtained from women in this group regarding their prenatal ingestion of other mineral-containing tonics that are available within this community, and women were only recruited into this group if they did not consume any mineral supplements during pregnancy.

Informed written consent was obtained from each woman, and the study was approved by the Committee for Human Research at The Johns Hopkins School of Hygiene and Public Health and by the ethical committee at the Instituto de Investigacion Nutricional, Lima, Peru. Data on iron absorption and iron status of these subjects have been previously published (O’Brien et al. 1999 ).

Isotope preparation.

Zinc isotopes were purchased from Trace Sciences International (Ontario, Canada) as the metal (⁶⁷Zn at 94.67% enrichment and ⁷⁰Zn at 93.13% enrichment). The oral ⁶⁷Zn tracer was converted into zinc sulfate, and the intravenous ⁷⁰Zn isotope converted into a sterile and pyrogen-free solution of zinc chloride by the Merck Frost Company (Quebec, Canada). Total zinc concentrations of the final tracer solutions were determined using atomic absorption spectrophotometry (Perkin Elmer 3300, Norwalk, CT). Isotopic composition of the final tracer solutions was validated using magnetic sector thermal ionization mass spectrometry (MAT 261; Finnigan, Bremen, Germany).

Study design and isotope dosing.

On the morning of each study, fasted women reported to the Maternal Infant Hospital "Cesar Lopez Silva" (CLS) in Villa El Salvador, and a baseline height and weight were obtained. Blood samples were then obtained from fasting subjects for analysis of plasma zinc and iron status indicators. Each woman received an intravenous tracer infusion of ⁷⁰Zn (0.3 mg) and an oral dose of ⁶⁷Zn tracer (0.25 mg/kg) in 60–90 mL of a flavored drink made from a powdered mix using deionized water. Women in the Fe and Fe + Zn group also consumed their prenatal supplement at this time. Women fasted for 1.5 h after dosing. We chose to measure zinc absorption in fasting subjects because women from this community are advised to consume their prenatal supplements between meals. On the day of the study, all subjects were fed a standard breakfast and lunch meal as previously described (O’Brien et al. 1999 ).

Three days postdosing, women returned to the CLS clinic and a 5-mL blood sample was obtained for analysis of zinc isotopes. Blood samples for zinc analyses were collected into Sarstedt lithium-heparin tubes (Sarstedt, Newton, NC). Blood was immediately centrifuged and the plasma was collected and frozen at -70^°C until analysis. Two weeks postdosing, an additional 5-mL of blood was obtained for analysis of zinc and iron status indicators. A field worker also visited each woman at her home to collect spot urine samples 60, 68 and 72-h postdosing. At birth, a 5-mL sample of cord blood was obtained.

Isolation of zinc from samples.

Plasma (1 mL) was digested with 15 mL of nitric acid in a 25-mL Erlenmeyer flask by heating overnight on a hot plate. After the solution was clear, it was transferred to a beaker and evaporated completely.

Zinc was isolated from urine samples by first heating 60–100 mL of urine until all liquid had evaporated. Dried residues were reconstituted in 10 mL of concentrated nitric acid, and were maintained at sub-boiling temperatures overnight before evaporating to dryness. Digested urine and plasma residues were redissolved in 4 mL of 6 mol/L HCl and were redried and reconstituted in 1 mL of 6 mol/L HCl prior to anion exchange chromatography. Briefly, small disposable columns were filled with 1 mL of anion exchange resin (Biorad AG 1 x 8 resin, Hercules, CA). Columns were washed with 10 mL of deionized water and conditioned with 4 mL of 6 mol/L HCl. Digested plasma and urine samples were loaded onto conditioned columns which were then washed with 10 mL of 6 mol/L HCl and 5 mL of 0.5 mol/L HCl. Zinc was eluted from the column using 10 mL of deionized water. The final eluate was dried on a hotplate and reconstituted in 10 µL of 0.7 mol/L phosphoric acid before loading onto filaments for mass spectrometric analyses. All acids used in the digestions and chromatography were ultrapure (Ultrex; JT Baker, Phillipsburg, NJ).

Mass spectrometry.

Zinc isotope ratios were measured using a Finnigan MAT 261 magnetic sector thermal ionization mass spectrometer. A ratio was made between each administered zinc tracer to ⁶⁶Zn, and the data were corrected for isotope fractionation by normalizing the ratios based on a correction factor for the ^64/66Zn ratio.

The degree to which the zinc isotope ratios differed from baseline ratios was determined as:

The same equation was used for the ^70/66 Zn excess, substituting the ^70/66 Zn baseline and observed ratios into the equation. The natural abundance ratios used for the ^67/66 Zn and ^70/66 Zn isotopes were 0.146063 and 0.02235, respectively. Precision and accuracy achieved for the ^70/66Zn and ^67/66Zn ratios were within 0.5%.

Calculation of zinc absorption.

Percentage zinc absorption was determined by measuring the ratio of the oral to the intravenous zinc tracer in urine or plasma samples as previously reported (Friel et al. 1992 ). Briefly:

A total of four samples were collected 58 h postdosing for determination of percentage zinc absorption. These samples were collected 58 h postdosing after which time the rates of disappearance of the oral and the intravenous tracer parallel one another (Friel et al. 1992 ).

In women receiving prenatal supplements containing both Fe and Zn, true zinc absorption from the prenatal supplement was calculated as the product of supplemental zinc intake and the fractional zinc absorption.

Zinc measurements.

Atomic absorption spectrophotometry was used to measure zinc concentrations in urine and in maternal plasma and cord plasma samples (model 3100; Perkin Elmer). Iron status indicators were measured as previously reported (O’Brien et al. 1999 ).

Statistical analyses.

Analysis of variance was used to detect potential differences in measured variables among supplementation groups. Scheffé’s test was used for post-hoc comparisons. Linear regression analysis was used to determine relationships between maternal plasma and cord concentrations. Statistical analyses were completed using the Statview 5.0 software program (SAS Institute, Cary, NC). Differences were considered significant if P < 0.05.

	RESULTS

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The characteristics of the study population are presented in Table 1 . No significant differences were found in any of the measured physical characteristics among groups. Women in the Fe and Fe + Zn group began prenatal supplementation at the same stage of pregnancy (16.1 ± 5.0 and 15.6 ± 5.0 wk gestation, respectively). Hemoglobin concentrations did not differ significantly between women in the Fe and Fe + Zn group at the start of supplementation (111.8 ± 13.4 vs. 114.6 ± 10.8 g/L, respectively). Compliance (based on biweekly pill counts) did not differ significantly between these groups. Women in the Fe and Fe + Zn groups consumed 139 ± 42 and 159 ± 38 pills, respectively, over the supplementation period.

View larger version (14K): [in this window] [in a new window]   Figure 1. Relationship between maternal cord zinc concentrations and maternal plasma zinc concentrations in Peruvian women (y = 6.383 + 0.555x, r = 0.486, n = 37, P = 0.002). Women in the intervention groups had received prenatal supplements containing 60 mg of iron and 250 µg of folate with (Fe + Zn group) or without (Fe group) the addition of 15 mg of zinc from wk 10 to 24 of gestation until delivery. Women in the nonsupplemented group did not consume prenatal supplements during pregnancy.

	DISCUSSION

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Few studies have addressed the degree to which women with habitually low zinc intakes can increase zinc absorption during pregnancy. Our data indicate substantially higher percentage zinc absorption in unsupplemented pregnant women from this community (47.0 ± 12.6%) compared to iron-supplemented pregnant U.S. women at the same stage of gestation (19.4 ± 2.6%) (Fung et al. 1997 ). However, because we administered the zinc tracers to fasting women, we were unable to determine if the higher percentage absorption measured in this group was related to the lower zinc intakes of this population or if this difference was primarily due to differences in isotope dosing. We chose to administer the tracers during fasting to specifically examine the impact of iron supplements on zinc absorption given that women from this community are advised to take their prenatal supplements between meals. Further, it should be added that percentage zinc absorption in iron-supplemented women in this community is similar to those observed in U.S. women. Further, studies carried out in lactating women have also demonstrated that iron supplementation prevented the increase in percentage zinc absorption that would normally be expected during lactation (Fung et al. 1997 ).

The inclusion of 15 mg of Zn to prenatal supplements did not significantly increase plasma zinc concentrations compared to women consuming only iron supplements. Due to the variability in plasma zinc concentrations, however, larger sample sizes would be required to adequately address this issue. In a larger supplementation study of 500 pregnant women from this community, maternal plasma zinc concentrations were significantly improved in women consuming prenatal Fe + Zn supplements compared to women consuming only Fe supplements (Caulfield et al. 1999a ). The impact of iron supplementation on zinc status could not be addressed directly in this larger study because, due to ethical concerns, it did not include unsupplemented pregnant women. Regardless, evidence from the larger study indicates that the combination of a usual intake of zinc of 7 mg/d and daily supplement of 15 mg/d are likely insufficient to maintain optimal zinc status given that plasma and urinary zinc concentrations in women from this community are typically lower than those reported in women living in other areas of the world (Caulfield et al. 1999a ).

The mechanism by which iron may inhibit zinc absorption has not been fully identified. Specific mammalian zinc transporters in the intestine have been identified (McMahon and Cousins 1998 ). Furthermore, a divalent metal ion transporter (DMTI) in the apical membrane of the intestinal cell intestine has been characterized (Gunshin et al. 1997 ). The affinity of this transporter is greatest for iron, followed by zinc (Gunshin et al. 1997 ). Iron may inhibit both zinc uptake into the cell and transfer through the intestinal cell. Prior studies in pregnant women reported that zinc absorption, as measured by increases in plasma concentration, was reduced after the termination of a 2-wk prenatal vitamin containing 350 µg of folate and 100 mg of ferrous iron (Simmer et al. 1987 ). Because zinc was not given simultaneously with the prenatal supplements of iron and folic acid, these authors postulated that the reduction in zinc absorption occurred at the level of the intestinal mucosal cells rather than within the lumen (Simmer et al. 1987 ).

Zinc homeostasis is maintained not only through alterations in intestinal absorption but also by regulation of endogenous fecal zinc excretion. Studies in nonpregnant Chinese women with marginal or adequate zinc intakes reported a significant conservation of endogenous fecal zinc in women with marginal zinc intakes (Sian et al. 1996 ). Despite the observed conservation of endogenous fecal zinc, fractional zinc absorption in these women did not differ significantly from that measured in Chinese woman with adequate zinc intakes (Sian et al. 1996 ). We did not obtain complete fecal collections in this study population and are therefore unable to address the potential differences between groups in endogenous fecal zinc excretion. Although endogenous fecal zinc losses may have differed, this did not appear to be sufficient to conserve enough zinc to meet both maternal and fetal needs, given the differences in plasma and cord zinc concentrations.

Maternal plasma zinc concentrations are generally lower than those found in cord plasma, indicating an active transfer of zinc to the fetus. The average ratio of cord to maternal plasma zinc concentrations observed in our study was 1.266 ± 0.298, a ratio that did not differ significantly among groups. Furthermore, the ratio of cord/maternal plasma zinc concentration in this population was lower, but comparable to, the mean ratio reported in 32 published studies (1.51 ± 0.3) (Tamura and Goldenberg 1996 ). In our study population, prenatal iron supplementation may have adversely influenced zinc transfer to the fetus as indicated by the slightly lower cord zinc concentrations observed in iron-supplemented women compared to nonsupplemented women (P = 0.056). Other studies have also indicated that higher maternal serum zinc concentrations favor the maternal-fetal transfer of zinc (Zapata et al. 1997 ). Cord zinc concentrations were also obtained from 252 neonates born to supplemented women enrolled in the larger Fe and Zn supplementation study in this community. In this larger group of subjects, significantly higher cord zinc concentrations were found in neonates born to mothers who consumed prenatal Fe + Zn supplements compared to women consuming only Fe supplements (Caulfield et al. 1999a ).

In summary, daily supplementation with 60 mg/d of iron and 250 µg/d of folate significantly decreased zinc absorption in fasting pregnant women in comparison to women from the same community who did not receive prenatal iron supplements. Inhibition of zinc absorption due to iron supplementation may have adversely influenced maternal zinc status and altered net zinc transfer to the fetus, given the strong relationship between maternal and cord zinc concentrations. The inclusion of 15 mg of zinc to iron-containing prenatal supplements has improved zinc status in pregnant women from this community (Caulfield et al. 1999a ). It is not known whether the differences observed in zinc status would lead to any improvements in functional outcomes, and additional studies are needed to determine the optimal composition of prenatal supplements in populations with known deficiencies in both of these nutrients.

	ACKNOWLEDGMENTS

 
The authors would like to sincerely thank the women who volunteered to participate in this study. We would also like to acknowledge Alberto Figueroa and Juanita Callallai for their excellent medical care of these women, Dong-Xiao Yang, Cindy Clarke and Lily Liang for technical assistance, and the Cesar Lopez Silva (CLS) Hospital in Villa El Salvador and the Instituto Materno Perinatal for allowing us the use of their medical facilities.

	FOOTNOTES

 
¹ Supported by a grant from the Nestle Foundation.

² Portions of this manuscript were presented in abstract form at Experimental Biology, April 6–9, 1997, New Orleans, LA. O’Brien, K. O., Zavaleta, N., Caulfield, L. E., Lembcke, J. & Abrams, S. A. Fractional Zinc Absorption in Pregnant Peruvian Women. Experimental Biology 1997; 11(3): A194.

⁴ Abbreviations used: C, unsupplemented control group; CLS, Cesar Lopez Silva; Fe, iron group; Fe + Zn, iron and zinc supplemented group.

Manuscript received October 14, 1999. Initial review completed February 14, 2000. Revision accepted April 20, 2000.

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