Maternal undernutrition is a major public health issue in the developing world, and it is estimated that between 10 and 19% of women are undernourished, with a BMI of less than 18.5 1. In addition, dietary intake studies show that maternal micronutrient deficiencies in iron, vitamin A, zinc, vitamin B12, iodine, and folate are widespread and have a negative impact on pregnancy outcomes, increasing maternal morbidity and mortality 2–4.
Zinc deficiency has long been considered a common but overlooked problem in developing countries. It is widely believed that zinc deficiency is as widespread as iron deficiency, affecting nearly half of the world’s population 5. According to data provided by the Research Institute of Nutrition (Russian), on average, 77% of pregnant women have deficiency of vitamins, essential trace elements, and minerals, and the daily intake includes no more than 50% of the daily requirement of zinc 6.
Zinc is required for cellular division and differentiation. In addition to DNA synthesis, zinc regulates gene expression. Growth-stimulating hormones such as insulin-like growth factors need zinc for their activity. Zinc is also involved in the regulation of apoptosis-programmed cell death. Zinc is an essential nutrient for normal embryogenesis 7.
The consequences of severe human zinc deficiency have been known since the 1960s, but only more recently have the effects of milder degree of zinc deficiency been recognized. Severe maternal zinc deficiency has been associated with spontaneous abortion and congenital malformations (i.e. anencephaly), whereas milder forms of zinc deficiency have been associated with low birth weight, intrauterine growth retardation, and preterm delivery. Importantly, milder forms of zinc deficiency have also been related to complications of labor and delivery, including prolonged or inefficient first-stage labor and protracted second-stage labor, premature rupture of membranes, and the need for assisted or operative delivery 8.
This study aimed to assess the zinc status and dietary intake of zinc and other macronutrients and micronutrients among pregnant women of low and middle socioeconomic levels in Alexandria, Egypt.
This study is part of a larger double-blinded, placebo-controlled, parallel-group randomized trial conducted in Alexandria, Egypt, to test the effect of two regimens of zinc supplementation on the outcome of pregnancy. Women with a low serum zinc level were eligible for enrollment in the trial. Screening for zinc deficiency (n=1055) was carried out by measuring the level of serum zinc. Eligible participants (n=675) were assigned randomly to one of three parallel groups in a 1 : 1: 1 ratio. The control group (group 1) received placebo, the zinc group (group 2) received a daily supplement of 30 mg of zinc as zinc sulfate, and the zinc plus multivitamins group (group 3) received 30 mg zinc as zinc sulfate added to multivitamins.
Eligibility criteria for participants
Women who presented for antenatal care in two antenatal care centers that serve low-income and middle-income pregnant population were assessed for eligibility. The inclusion criteria were as follows: age range between 20 and 45 years, gestational age below 16 weeks assessed by ultrasonography, BMI between 18 and 26 kg/m2, normal course of pregnancy, and a serum zinc level below the estimated median for gestational age at the time of enrollment 9. The exclusion criteria were as follows: women identified through interviews to be on any other form of zinc supplements at any dosage, women with an established risk of having reduced or excessive birth weight of infants (e.g. diabetes, hypertension, renal and heart disease), old primigravidae, and cases that developed complications or twin pregnancy during the follow-up period.
The sample size required to enable the detection of a mean difference of 150 g in birth weight with 80% power, 0.5 SD for each group, 5% level of significance was estimated to be 534 (178 per each group). The study included up to 675 cases in the three groups in order to overcome the dropout. Therefore, after randomization of cases, there were 223 cases in the control group, 225 cases in the zinc group, and 227 cases in the combined zinc and multivitamin group. In all, 199 cases in the placebo group, 198 cases in the zinc group, and 200 cases in the zinc plus multivitamins group completed the study.
Eligible women provided free and informed consent before enrollment. Women who agreed to participate in the study signed/thumb-printed the consent form and those who consented were given copies of the signed consent form. After enrollment, each participant was assigned a unique serial number, and this was recorded on her antenatal care card. The protocol of the study was approved by the ethical committees of Ministry of Health (MOH) and the High Institute of Public Health (HIPH). The trial was registered in the WHO trial registry (PACTR20130300045309).
Methods of data collection
Determination of serum zinc
Nonfasting venous blood was obtained during morning hours using plastic syringes, stainless-steel needles, and trace mineral-free plastic tubes. Serum was separated at a maximum of 6 h after collection and stored at −20°C until analyzed. Zinc concentration was measured using flame atomic absorption spectrophotometry. Serum zinc level was measured at enrollment in the study and a second measurement was performed between 28 and 32 weeks’ gestation.
The reference median serum zinc level at the second trimester was based on the values obtained from a recent study on pregnant women attending MCH centers in Alexandria (75 μg/dl) 9. Women with serum zinc levels below the median and who fulfilled the inclusion criteria for the study were subjected to the following.
A structured interview was administered to mothers to collect the following data:
- Personal and sociodemographic data such as age, residence, educational level, working status, family size, income, and housing conditions.
- Obstetric data such as gravidity, parity, abortions, and any obstetric complications in previous pregnancies or deliveries.
- Dietary intake using the 24-h recall method and food frequency questionnaire, with a focus on intake of foods that might enhance or inhibit zinc absorption. This assessment was performed on a subsample of 100 women in the three groups studied. Enhancers of zinc absorption that were determined were low calcium intake represented by low consumption of dairy products and protein intake. Inhibitors of zinc absorption were represented by fibers, phytates, and iron.
Routine antenatal examination included the following:
- Gestational age determination using the last menstrual period and ultrasound.
- Routine laboratory investigations: urine analysis, random blood glucose level, and hemoglobin concentration using the cyanmethemoglobin method.
Anthropometry of women during pregnancy
The weights of the women were measured to the nearest 0.1 kg on an electronic bathroom weighing scale and height was measured to the nearest 0.1 cm with a height stick. BMI was calculated as follows: BMI=weight (kg)/height (m2).
Management of dietary data
Dietary intake was assessed by a 24-h dietary recall and separate questions on the use of vitamin or mineral supplements. Portion sizes were estimated using standard household measures quantified in grams. Dietary data intake of the 24-h recall method was analyzed using the Egyptian food composition tables 10 to determine the daily intake of macronutrients (protein, fat, carbohydrates, and energy) and that of specified micronutrients (zinc, calcium, iron, and vitamin A). The mean daily intake was compared with that of the recommended dietary allowance (RDA) level of the Food and Nutrition Board, Institute of Medicine (IOM) 11 to determine the percent adequacy of intake from the specified nutrient.
Data were fed to the computer using the Predictive Analytics Software (PASW Statistics 18; SPSS Inc., Illinois, Chicago, USA). The intention-to-treat strategy was used for primary analysis, and involved all participants who were assigned randomly. The association between categorical variables was tested using the χ2-test. Yate’s exact correction was applied when more than 20% of the cells had an expected count less than 5. Quantitative data were described using mean and SD. When there were at least 30 observations per group, parametric statistics were used for comparing means in this study irrespective of the state of normality of the data as the conclusions drawn by both the t and F distributions will not be seriously affected. Independent one-way analysis of variance was used to compare quantitative variables among more than two groups.
The mean age of the participants at recruitment was 27±5.4 years, with a range of 16–44 years. The mean gestational age at recruitment was 13.0±3.0 completed weeks. The study groups did not differ significantly in terms of their baseline characteristics, except for age, where the iron–zinc group included older participants [F(1,598)=4.864, P=0.028] (data were not shown).
Out of 1115 women, 675 had low serum zinc level (53.5%). The mean serum zinc values were 60.2±6.46, 58.6±6.87, and 59.2±6.46 μg/dl for the placebo group, zinc, and zinc plus multivitamins, respectively. There were statistically significant difference between the three studied groups in first sample serum zinc (P=0.025). Hemoglobin level ranged between 9 and 11.8 g/dl, with a mean and SD of 10.5±0.63, 10.5±0.64, and 10.3±0.57 g/dl for the three groups, respectively. There was no statistically significant difference in hemoglobin level (P=0.051). About one-third (29.3%) of the total sample had hemoglobin level below 10 g/dl (Table 1).
Table 2 shows the intake of macronutrients in the three groups. The mean protein intake was 48.08, 48.32, and 44.98 g/day for the placebo, zinc, and zinc plus multivitamins groups, respectively. They represent 67.7, 68.1, and 63.4 of the RDA for the three groups, respectively.
The total fat intake was highest among pregnant women of the zinc group, with a mean of 57±52.71 g/day. The mean intake of fat among the other two groups was 42.1±21.75 and 44.5±15.8 for the placebo and zinc plus multivitamins groups, respectively.
In all groups, the mean carbohydrate intake was higher than the RDA, representing 109.7, 121.1, and 112.2 of the RDA.
Fiber intake was very low and constituted only about one quarter of the recommendation (21.8, 23.6, and 22.4%, respectively).
The mean energy intakes were 1379.1, 1445, and 1343.9 kcal/day for the placebo, zinc, and zinc plus multivitamins groups, respectively. They represent 51.1, 53.5, and 49.8% of the RDA for the three groups, respectively. Except for fat (P=0.022) and energy intake (P<0.001), there was no statistically significant difference between the three groups.
Table 3 shows a comparison between the three groups studied in the mean intake and percent adequacy of micronutrients in relation to RDA. Intake of vitamin A represents 60.8% of RDA during pregnancy. Differences between the three groups studied were statistically significant (P=0.021).
The calcium mean intakes were 399.8, 417.2, and 360.1 mg/day for the placebo, zinc, and zinc plus multivitamins groups, respectively. These mean intakes represent 40, 42, and 36% of the RDA. Differences between the three groups studied were statistically significant (P=0.041).
The mean iron intake in the three groups studied was 10.1, 10.4, and 9.3 g/day, respectively. They represent 37, 38.6, and 34.4 of the RDA of iron for pregnant women. There was no statistically significant difference between the three groups studied.
Zinc mean intake in the three groups studied was 6.8, 6.5, and 6.5 mg/day, respectively. These mean intakes represent 62, 59.4, and 59.4% of the RDA. There were no statistically significant differences among the three groups studied in zinc intake.
Enhancer and inhibitors of zinc absorption
Table 4 shows the enhancers of zinc absorption in the study subsample represented by protein of meat and fish. In terms of the meat intake pattern, most of the study sample (92%) consumed meat less than three times a week, with comparable percentages of consumption. Intake more than three times a week was rare and was found in 5.0% of the total sample.
In terms of fish consumption, 82.0% of the total sample consumed fish less than three times a week. Ten percent of the study sample rarely consumed fish.
Consuming eggs less than three times per week was the prevailing pattern among the majority of women (63%). There were no statistically significant differences between the three groups studied in the consumption of fish, meat, and egg.
Table 5 shows the intake of inhibitors of zinc absorption in the subsample. In terms of vegetable consumption, most of the study subsample (43%) consumed vegetables more than three times a week.
With respect to milk consumption, about half of the study sample (49.0%) consumed milk less than three times a week. Daily consumption was nil and was found in 2.0% of the total sample. Consumption of cheese more than three times a week was reported by the majority of women (65%).
Likewise, consumption of beans more than three times per week was reported by the majority of women (67%). There was no statistically significant difference between the three groups in the consumption of inhibitors of zinc absorption.
Serum zinc concentration decrease progressively during the course of pregnancy in relation to blood volume expansion. Thus, the values must be interpreted in relation to the stage of pregnancy or serum albumin concentrations. Despite many limitations, serum zinc concentration is still the recommended biochemical indicator of zinc status during pregnancy at the population level. In the present study, 53.3% of pregnant women had serum concentration lower than the median values for the stage of pregnancy. This high prevalence of zinc deficiency is comparable with the rate reported by an Indian study (64.6%) 12. Studies carried out in developing countries documented that zinc deficiency in pregnant women is because of the low intake of dietary zinc 12–14. The present study was carried out in a community that consumed a diet composed mainly of vegetables and beans. The low intake of enhancers and the presence of higher amounts of phytates and dietary fibers in this diet, known to cause poor zinc absorption, could be a major contributing factor toward the high prevalence of zinc deficiency in this study population. Also, populations with poor access to health, water, and sanitation are at an increased risk of infectious diseases, which increases the risk of zinc deficiency.
Because inadequate dietary intake of zinc is the most likely cause of zinc deficiency, dietary assessment is an important component in evaluating the risk of zinc deficiency. Information on the adequacy of dietary zinc intakes should be interpreted together with data derived from other assessment methods, such as biochemical assessment 15. Dietary surveys from 17 developing countries have shown that zinc intake of women is on average 9.6 mg/day (1.2 SD) in contrast to the 1990 RDAs of 15 and 19 mg, respectively, during pregnancy and lactation. From these data and application of the probability method, it was calculated that 82% of pregnant women worldwide are likely to have inadequate zinc intake. The prevalence may be much lower now (∼31%), with the recent RDA for zinc being reduced to 11 mg for pregnancy and 12 mg for lactation 16,17, but still raise a concern in terms of the potential adverse effects of maternal zinc deficiency on pregnancy outcomes.
In this study, the mean maternal dietary intake of zinc was less than 7 mg/day in the three groups. These intakes represent about 59.4, 59.4, and 62% of the recommended recent RDA. Carboné et al.18, in their study, reported that the mean zinc intake among pregnant women at 20 and 36 weeks of gestation was ∼66% of the RDAs. Zinc intakes reported by Osendarp et al.19 in Bangladesh were 6.3 and 6.4 mg/day in the zinc-supplemented group and the placebo group, respectively. The findings of the current study are comparable with the figures reported by Osendarp and colleagues. This may be because the nutritional data in both studies were obtained approximately at the same time at about 4–5 months of gestation and maternal nutritional status was very poor during this period of gestation. Also, in a recent study in India 8, it was found that the mean intake of zinc was 61.1±16.6μg/dl; this mean intake is also comparable with the intake reported in this study.
In a recent study in Jordan 20 that included 700 pregnant women, it was found that the mean maternal intake of zinc was 8.86±0.14 mg/day. This figure is higher than the findings of the present study and could be attributed to the higher socioeconomic class of the Jordanian women in that study.
The bioavailability of zinc is considerably influenced by the composition of the diet in the content of inositol phosphates (phytates), the total zinc content of the meal, and the amount and source of protein. Animal protein is a rich source of zinc and, in addition, exerts a possible enhancing effect on the overall absorption of zinc from the diet. It is well known that phytic acid is a strong inhibitor of zinc absorption and a concomitant intake of protein seems to counteract the negative effects on absorption induced by high intakes of phytic acid 21. Increasing the amount of total protein enhances zinc absorption and if the protein is from cellular animal sources, the enhancing effect is even greater 22.
There is additional protein requirement for a pregnant woman to support the synthesis of maternal and fetal tissues, but the magnitude of this increase is uncertain. Protein requirement increases throughout gestation and is maximum during the third trimester. The current RDA of 0.66 g/kg/day of protein for pregnant woman is the same as that for nonpregnant women in the first half of pregnancy and increases in the second half to 71 g/day 23.
The mean dietary protein intake in this study was 48.1, 48.3, and 44.98 g/day for the three groups, respectively. This intake represents less than 70% of the RDA. The protein intake in the Jordanian study 20 was 90.46±0.95, which is obviously higher than the present results. However, Osendarp et al.19, in Bangladesh, found a mean maternal protein intake of 40 and 39 g in the zinc-supplemented and the placebo group, respectively, figures that are comparable with the findings of the present study. This could be because Osendarp and colleagues carried out their study in an urban, poor population in Bangladesh that may have characteristics similar to those of the current study population. The overall low protein intake in this study adds to the lowered bioavailability of zinc in the study population.
A marked increase in iron consumption during pregnancy considerably increases the demand for iron. A pregnant woman must consume an additional 700–800 mg of iron throughout her pregnancy: 500 mg for hematopoiesis and 250–300 mg for fetal and placental tissues. The 2001 RDA for iron during pregnancy is 27 mg/day, an increase of 9 mg/day over that for nonpregnant women 23.
The mean iron intake in this study was 10.1, 10.4, and 9.3 mg/day for the three groups, respectively. This intake comprises less than 40% of the RDA. It is lower than that reported by Osendarp et al.19, who reported 11.3 and 11.7 mg/day for the zinc-supplemented group and the placebo group, respectively. The Jordanian study 20 also found a mean intake of 13.46±0.27 mg/day. Actually, iron intake in the present study was very low and covered only about one-third of the RDA for pregnant women. This could be because of the vegetarian diet usually consumed in our country, which leads to low bioavailability of iron (animal proteins are usually the best sources of iron) and high intake of inhibitors of iron absorption (phytates and oxalates).
Additional energy is required during pregnancy to support the metabolic demands of pregnancy and fetal growth. Metabolism increases by 15% during pregnancy. It is difficult to specify precise energy requirements because they vary with pregnancy weight, amount and composition of weight gain, and stage of pregnancy and activity level 24. In the present study, the findings of the 24-h recall showed that the mean maternal energy intake was around 50% of the 2004 RDA (2743 kcal/day) for the three groups studied. The low level of intake of energy in the current study may be because of decreased appetite in the beginning of the second trimester at the time of collection of nutritional data. However, energy intake in this study was comparable with the findings reported by Osendarp et al.19 in Bangladesh slums, where the mean energy intakes were 1400 and 1488 kcal/day for the zinc-supplemented group and the placebo group, respectively. In the study carried out in Jordan 20, the mean energy intake was about 2593.8 kcal/day; this figure may show that our country may have nutritional problems in comparison with other Middle East countries. Nielsen et al.25, who carried out a prospective study on pregnant women living in the US state of North Carolina, reported a median energy intake of 2470.2 kcal/day. This difference in the daily energy intake between the present study and other studies may be attributed to the methodology of recall and its timing in the early period of the second trimester.
Conclusion and recommendations
Women in the present study had multiple nutritional deficiencies. More than half of the screened women had serum zinc values lower than the average for the trimester of pregnancy. The intake of all studied nutrients except carbohydrates was low compared with that found in some other developing countries. Zinc intake represented about 60% of the RDA. The iron intake was below 50% of the RDA. Protein intake represents less than 70% of the RDA and the mean energy intake was less than 40% of the RDA. The following are recommended:
- Zinc should be included in the prenatal supplementation programs in women at risk of zinc deficiency in Egypt as the occurrence of multiple micronutrient deficiency is more likely than the occurrence of a single deficiency.
- Nutritional health education should be used as a preventive approach to allow the large sector of the low-income population in our society to maximize the use of the limited resources in the best way.
Conflicts of interest
There are no conflicts of interest.
1. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, et al..Maternal and child undernutrition: global and regional exposures and health consequences.Lancet2008;371:243–260.
2. Bhutta ZA, Haider BA.Maternal micronutrient deficiencies in developing countries.Lancet2008;371:186–187.
3. Ramakrishnan U, Manjrekar R, Rivera J, Gonzales-Cossio T, Martorell R.Micronutrients
outcome: a review of the literature.Nutr Res1999;19:103–159.
4. Huffman SL, Baker J, Shumann J, Zehner E.The case for promoting multiple vitamin and mineral supplements for women of reproductive age in developing countries.Food Nutr Bull1999;4:379–394.
5. .Reducing risks, promoting healthy life2002.Geneva:WHO.
6. Spiritchev V.How many vitamins one needs?2000;70Moscow:Russian Medical Academy Institute, Pitanya;185–190.
7. Scheplyagina LA.Impact of the mother’s zinc
deficiency on the woman’s and newborn’s health status.J Trace Elem Med Biol2005;19:29–35.
8. Fall CHD, Yajnik CS, Rao S, Davies AA, Brown N, Farrant HJW.A review of the evidence that maternal micronutrient status influences fetal growth and survival.J Nutr2003;133:S1747–S1756.
9. El-Kassas GM.Levels of some trace elements in pregnant women [Thesis MPH]. Alexandria: University of Alexandria, High Institute of Public Health; 2004.
10. .Food composition tables for Egypt
. ARE 1996. Cairo: Egypt
11. Erick MMahan L, Arlin MT, Krause MV.Nutrition in pregnancy
and lactation, dietary reference intakes.Krause’s food and nutrition therapy2008:12th ed..Philadelphia:Saunders;160–189.
12. Pathak P, Kapil U, Dwivedi SN, Singh R.Serum zinc
levels amongst pregnant women in a rural block of Haryana state, India.Asia Pac J Clin Nutr2008;17:276–279.
13. Lehti KK.Iron, folic acid and zinc
intakes and status of low socio-economic pregnant and lactating Amazonian women.Eur J Clin Nutr1989;43:505–513.
14. Sacco LM, Caulfield LE, Zavaleta N, Retamozo L.Dietary pattern and usual nutrient intakes of Peruvian women during pregnancy
.Eur J Clin Nutr2003;57:1492–1497.
15. Gibson RS, Ferguson EL.An interactive 24-hour recall for assessing the adequacy of iron and zinc
intakes in developing countries. Harvest Plus, Technical Monograph 8
. Washington, DC and Cali: International Food Policy Research Institute (IFPRI) and International Center for Tropical Agriculture (CIAT); 2008.
16. Aminisani N, Ehdaivand F, Shamshirgaran SM, Mohajery M, Pourfarzi F, Ahari S.Zinc
supplementation during pregnancy
: a randomized controlled trial.Int J Pharm Technol2009;8:67–71.
17. Martin M.Zinc
for better health. International Zinc
Nutrition Consultative Group (IZiNCG). 2004. Available at: www.zinc-health.org
. [Accessed 7 February 2014].
18. Carboné P, Sobreviela M, Jiménez D, Martínez C, Pocoví M.Hair zinc
and dietary zinc
intake during pregnancy
and puerperium.Eur J Obstet Gynecol Reprod Biol1992;47:103–108.
19. Osendarp SJM, Baqui AH, Wahed MA, Arifeen SE, van Raaij JMA, Fuchs GJ.A randomized, placebo-controlled trial of the effect of zinc
supplementation during pregnancy
outcome in Bangladeshi urban poor.Am J Clin Nutr2000;71:114–119.
20. Bawadia HA, Al-Kuran O, Al-Bastonia LAA, Tayyemc RF, Jaradatd AN, Tuuri G.Gestational nutrition improves outcomes of vaginal deliveries in Jordan: an epidemiologic screening.Nutr Res2010;30:110–117.
21. Olivares M, Pizarro F, de Pablo S, Araya M, Uauy R.Iron, zinc
, and copper: contents in common Chilean foods and daily intakes in Santiago, Chile.Nutrition2004;20:205–212.
22. Cuco G, Arija V, Iranzo R, Vila J, Prieto MT, Femandez-Ballart J.Association of maternal protein intake before conception and throughout pregnancy
with birth weight.Acta Obstet Gynecol Scand2006;85:413–421.
23. Scholl TO.Iron status during pregnancy
: setting the stage for mother and infant.Am J Clin Nutr2005;81SupplS1218–S1222.
24. Forsum E, Lo FM.Energy metabolism during human pregnancy
.Annu Rev Nutr2007;27:277–292.
25. Nielsen SJ, Siega-Riz AM, Popkin BM.Trends in energy intake in U.S. between 1977 and 1996: similar shifts seen across age groups.Obes Res2002;10:370–378.