Int. J. Vitam. Nutr. Res., 83 (6), 2013, 335 – 345
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Original Communication
Zinc Status as Compared to Zinc Intake and Iron Status: a Case Study of Iranian Populations from Isfahan Province Nazanin Abbaspour1, Rita Wegmueller2, Roya Kelishadi3, Rainer Schulin1, and Richard F. Hurrell2 1
ETH Zurich, Institute of Terrestrial Ecosystem, Zurich, Switzerland ETH Zurich, Institute of Food, Nutrition and Health, Zurich, Switzerland 3 Faculty of Medicine and Child Health Promotion Research Center, Isfahan University of Medical Sciences, Isfahan, Iran 2
Received: January 10, 2012; Accepted: July 9, 2014
Abstract: The aim of this study was to estimate the zinc (Zn) and iron (Fe) status of different age groups in rural (Rooran) and suburban (Khomeini Shahr) populations in central Iran, to relate the Zn status to Zn intake from animal and plant foods, and to examine the relationship between Zn and Fe status. Blood samples from 341 subjects including preschool children (27), schoolchildren (157), women (91), and men (66) were analyzed for serum zinc (SZn), serum ferritin (SF), total C-reactive protein, and hemoglobin. Daily Zn and phytic acid (PA) intakes from major food groups were estimated using a 3-day weighed food record. The overall prevalence of Zn deficiency based on low SZn was 5.9 % in Rooran and 7.2 % in Khomeini Shahr. Anemia was higher in the village than in the suburb (33.5 % vs. 22.7 %; p = 0.04) and almost half of the anemia in Khomeini Shahr and 36 % in Rooran was associated with iron deficiency (ID) based on low SF. The PA:Zn molar ratio in the diet was 10 – 13, indicating a diet of moderate Zn bioavailability. About 18 % of the population consumed less Zn than their WHO Estimated Average Requirements. There was no association between Zn status and Fe status. The modest prevalence of Zn deficiency in the study populations can be explained by a relatively high Zn intake from animal source foods. Anemia however is a serious public health problem affecting some 30 % of the subjects, with almost half due to ID. The lower Fe status than Zn status could be due to the frequent consumption of tea and dairy products. Key words: Zinc deficiency, iron deficiency, Iramian diet, serum zinc, dietary zinc, anemia
Introduction Zinc (Zn) deficiency can have negative health consequences in relation to growth, immune competence, DOI 10.1024/0300-9831/a000175
reproductive function, and neural development [1]. It is still considered a potential problem in Iran [2], where it was first observed in adolescent boys in 1963 [3]. Subsequent Zn supplementation studies [2, 4, 5],
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one as recent as 2006 [4], have reported that Zn supplements increase the height and weight of Iranian children. However, diet and lifestyle have changed considerably in some Iranian populations over the last 50 years and more recent estimates of Zn deficiency in Iran have varied widely depending on the province and the population studied. Based on low serum Zn (SZn), estimates of Zn deficiency have varied from 8 – 30 % [6 – 11]. The most recent study by Dehghani et al. [11] reported only 8 % Zn deficiency in 3- to 18-year-old children. They suggested that changes in the diet, use of Zn supplements, and differences in soil Zn and thus the Zn content of local foods could explain the variation in Zn deficiency reported in different Iranian provinces. The traditional Iranian diet is based on bread and rice [12, 13] that is low in Zn and high in phytic acid (PA), which is a potent inhibitor of Zn absorption [1]. With improved income, the consumption of animal source foods, such as milk and meat, which are higher in Zn, are expected to increase the Zn status. Iron (Fe) and Zn status are often linked [1] as they share PA as the common inhibitor and because animal foods increase their absorption [14]. Iron deficiency anemia (IDA) is also prevalent in Iran, with recent studies reporting 29 % IDA in children (< 5 years) in southwest Iran [15] and 10 % IDA in adult women in Northwest Iran [16]. Urban populations usually enjoy a higher quality of life and consume a more diverse diet than rural populations [17, 18], and therefore might be expected to have a lower prevalence of Zn and Fe deficiencies [19, 20]. There is little evidence, however, as these assumptions lack age- and gender-specific data on the Zn and Fe status of the Iranian population. In the present study, we estimated Zn and Fe status in children and adults from a rural (Rooran) and a suburban (Khomaini Shahr) population in Isfahan Province. We compared Zn status to Zn intake that was based on a 3-day weighed food record and measured Zn and PA contents [21] in relation to the Estimated Average Requirements (EAR) for Zn [22].
Subjects and Methods
sume mostly the same products as consumed in the city of Isfahan. The survey was conducted from November to December 2009 in Khomeini Shahr, a suburb of Isfahan with a population over 200,000 inhabitants, and in Rooran, a rural community with around 2000 inhabitants. Khomeini Shahr is a small city in the northwestern part of Isfahan and is now a part of the Isfahan Metropolitan area. Rooran is located 40 km to the southeast of Isfahan city. It still maintains typical characteristics of a village, including dependence on agriculture as the main occupation and self-production of rice and wheat.
Subjects The study subjects were from the same 24 households in Khomeini Shahr and 28 households in Rooran that took part in a previous dietary survey [21]. The households were selected randomly from these communities. In each site, the target enrollment was at least 40 per age group (preschool children aged < 5 years, school-age children aged 5 – 14 years, females aged ≥ 15 years, and males aged ≥ 15 years). The sample size of 320 participants was selected based on an expected moderately high prevalence of Zn deficiency [1]. Due to the small number of children in the households, additional children of preschool age (< 5 years) and school age (5 – 18 years) were recruited through schools, local mosques, and health centers. However, despite these efforts, we did not reach the target number of preschool children in either community (Table I). A representative of each household that had participated in the previous study and a parent of the newly participating children were invited to attend a meeting in which the survey was presented orally and questions were answered. Volunteers were enrolled after written consent was obtained from all full-aged participants (over 18) and oral consent from the children. In addition, permission to conduct the survey was obtained from the respective health centers for both communities. The protocol was reviewed and approved by the Ethics Committees of ETH Zurich and the Research Affairs office of Isfahan University of Technology.
Location Subject characteristics Our criteria for selecting study sites were: i) they should be accessible; ii) the rural community should represent a typical life style of a village; and iii) the suburb should have a more urban life style and con-
Socioeconomic data were collected using a specially prepared questionnaire. We specifically designed the questionnaire to rank the subject families as de-
Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
23.3 (20.1, 27.0) 24.7 (19.9, 30.6) 70.3 ± 10.0 171.23 ± 9.7
173.1 ± 6.4
74.6 ± 18.3
Blood analyses
2
Arithmetic mean ± SD. Geometric mean (-1 SD, +1 SD). F: female, M: male.
34.5 (22.2, 53.6) 32.8 (21.1, 51.0) 38 28 M ≥ 15 yrs
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prived, low middle class, middle class, semi-wealthy, or wealthy. The ranking was based on reported monthly expenditure, profession, ownership of house, cars, etc., residential area, household size, and education. Each family characteristic was given a score and the total score defined the socioeconomic class. Anthropometric measurements of height and weight were made with the participants barefoot and dressed in light clothes. All measurements were taken in the morning, according to a standardized procedure given by the World Health Organization (WHO) [23]. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2).
1
22.3 (18.4, 27.0)
16.2 (13.4, 19.6)
24.4 (20.3, 29.3) 55.6 ± 9.5 47 F ≥ 15 yrs
44
25.0 (17.3, 36.1)
30.8 (19.9, 47.6)
160.4 ± 6.2
157.2 ± 8.0
64.0 ± 12.3
16.5 (13.9, 19.6)
14.7 (13.4, 16.1) 15.5 (14.6, 16.5)
29.5 ± 13.2
30.1 ± 12.0
100.1 ± 6.7
133.0 ± 17.6 129.51 ± 18.9
103.8 ± 3.3 4.1 (2.6, 6.4)
9.2 (6.9, 12.1) 8.0 (5.6, 11.2)
4.3 (3.8, 4.8)
68 5-14 yrs
14 13 < 5 yrs
89
16.8 ± 1.7
14.9 ± 3.0
R Kh R Kh R Kh
R
Kh
R
Kh
BMI (kg/m2)1 Weight (kg)2 Height (cm)2 Age (yrs)1 N Age group
Table I: Anthropometric measurements including height, weight, and body mass index (BMI) together with age and number of the participants (N) in Khomeini Shahr (Kh) and Rooran (R).
N. Abbaspour et al.: Zinc and Iron Status in Iran
Approximately 6 mL venous blood was taken in the morning so as to avoid diurnal and physiological variations in SZn [24]. The subjects were classified as fasting or non-fasting. About 2 mL of each blood sample was transferred into EDTA-treated tubes and the rest (≈ 4 mL) into trace-element free tubes without added anticoagulants. The 4-mL blood samples were allowed to clot for at least 40 minutes in a cooling chest before the serum was separated by centrifugation (High-Speed Refrigerated Centrifuge, SIGMA 3K30, Germany) at room temperature for 10 minutes at 3000 g and divided into aliquots. The serum aliquots and the whole-blood samples in the EDTA-tubes were kept on ice and transported to the Isfahan University of Medical Sciences (IUMS) for analysis. The wholeblood samples in the EDTA-tubes were used for hemoglobin (Hb) analysis within 12 hours of arrival at the laboratory. The serum samples were frozen and stored at – 20 °C until further analysis. For some of the preschool children, less than 5 mL blood was drawn and not all the analyses could be performed. C-reactive protein (CRP) as a measure of acute infection or inflammation was determined in serum samples using an immunoturbidometric assay (Atomatic analyzer 902, Hitachi, Japan). Values of ≥10 mg/L were taken to indicate the presence of inflammation or infection as recommended by the manufacturer (Darman Kave 2000) and according to the International Zinc Consultative Group (IZiNCG) recommendation [1]. Serum Zn (SZn) was analyzed by flame atomic absorption spectrophotometry (Atomic Absorption Spectrophotometer, Perkin-Elmer 2380, Norwalk, Connecticut, USA) using deproteinized samples. All analyses were performed in duplicate and a certified reference material, Seronorm™, (Sero AS, Billinstad, Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
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Norway) was analyzed in parallel for quality control [1]. Analyses were repeated when the difference between duplicates was > 10 % if sufficient serum sample was available. Zn deficiency was defined as SZn levels in non-fasting blood samples of < 65 μg/dL, < 66 μg/dL, and < 70 μg/dL for children < 10 years, non-pregnant females >10 years, and males >10 years, respectively; and < 70 μg/dL and < 74 μg/dL, respectively, for fasting blood samples from non-pregnant females > 10 years and males > 10 years [1]. As no cut-off value has been recommended for fasting blood samples of children < 10 years, the same cut-off (65 μg/dL) was used as for non-fasting blood samples. Samples were carefully examined for hemolysis by judging the color of the serum samples. Hemolysis confers a pink to red hue coloration to the plasma or serum [25]. Hemolyzed samples or samples with a CRP value ≥ 10 were excluded from the statistical analysis of SZn. Hemoglobin (Hb) was measured using an electronic Coulter Counter (Automated Hematology Analyzer, Sysmex K-1000, Kobe Japan). Anemia was defined as recommended by WHO [26]: Hb < 130 g/L for males ≥ 15 years, Hb < 120 g/L for children of 12 – 14 years of age and non-pregnant women ≥15 years, Hb < 115 g/L for children aged 5 – 11 years, and Hb < 110 g/L for children < 5 years. Serum ferritin (SF) was analyzed using an enzymelinked immunoassay (Monobind Inc. California, USA) at a commercial laboratory (Ferdowsi, Isfahan). The serum samples were frozen before transportation to the laboratory. ID was classified with SF < 12 μg/L (< 5 years) and < 15 μg/L (≥ 5 years) [27]. Samples with CRP ≥ 10 mg/L were also excluded from the statistical analysis of SF.
Zn intake and bioavailability Dietary Zn intake was measured using a 3-day weighed food record. Data were collected on 3 consecutive days, including 2 weekdays and one weekend day, during which the households were asked to maintain their usual food habits. The total food prepared for consumption, the individual portions consumed by each household member, as well as the uneaten remains were weighed. Zn and PA intakes were estimated separately for men, women, preschool-, and school aged-children. They were based on the analyzed Zn and PA contents reported previously for the foods and dishes consumed within our test communities [21], with additional data from food composition tables [28]. The PA:Zn molar ratios were calculated for the
whole diet and Zn bioavailability (low, moderate, or high) was estimated as recommended by the WHO [22]. Zn intake was estimated and compared to the EAR for different age and gender groups based on the level of Zn bioavailability of the diet [22].
Statistical evaluation The Kolmogorov-Smirnov test showed that SZn, Hb, height, and weight were normally distributed in both communities. These data are presented as means ± SDs. The data for age, BMI, and SF were normal for each age group after transformation into natural logarithms. They are presented as geometric means ± 1 SD. Since the CRP data were skewed, even after logarithmic transformation, the median range is reported. Oneway analysis of variance (ANOVA) was used to test for differences in the means of SZn, SF, and Hb concentrations among age groups and genders. The independent sample t-test was applied to compare sample means between the two communities. The chi-square test was performed for prevalence analysis and to test whether there were significant differences in categorical variables between rural and suburban populations. For those age groups with small sample size, the Fisher exact test was used instead of the chi-square test. To evaluate correlations between biochemical parameters, the data of all participants in the two communities were pooled in order to have a statistically meaningful sample size. The Pearson’s correlation coefficient was used to examine the relationship between SZn, logSF, and Hb. Logistic regression analysis was used to investigate relationships between Zn deficiency prevalence and potential predictors. Adjusted odd ratios (OR) were calculated for age, gender, and community with 95 % confidence interval (CI). To assess the relationships between SZn concentration and potential predictors, multiple linear regression was employed. Differences were considered statistically significant in case of p < 0.05. Statistical analyses were performed using SPSS version 16 (SPSS Inc., Chicago, IL, USA).
Results Subject characteristics The results of the anthropometric measurements are shown in Table I. The adult female participants tended to be taller (p = 0.03) and heavier (p = 0.001) in suburban Khomeini Shahr than in rural Rooran and had
Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
12 [41] The EARs are for moderate bioavailability diet as recommended by WHO [22] based on the average PA:Zn molar ratios of 5-15. N: Total number of participants in each age group. F: female, M: male. 2
1
11 13
35 [23] 9.5 [42]
10 11
15 [48] 33 [12]
9.5 10
12 [17] 33 [3] % 0.05). The average daily PA:Zn molar ratio was similar in both populations (10.7 in Rooran and 12.4 in Khomeini Shahr). According to WHO, moderate Zn bioavailability has an average PA:Zn molar ratio of 5 – 15 [22]. Based on this definition, both populations had moderate Zn bioavailability diets (PA:Zn molar ratio 10 – 13). According to EAR values given by WHO [22], 18.3 % of the entire study population consumed less Zn than they required. This was similar between rural and suburban areas but varied considerably depending on the population age group (Table II). Almost equal amounts of daily Zn intake were consumed with bread and red meat, although on a weight basis, these foods provided 12 % (182 g) and 4 % (49 g) of daily food intake (Figure 1). Dairy products (milk, yoghurt, and cheese) and rice provided 13 % and 12 % of the daily Zn intake, respectively. Animal source foods (red meat, chicken, milk, yoghurt, cheese, and eggs) provided 46 % of the daily Zn intake. The main Zn-containing foods, providing 80 % of daily intake, were red meat, chicken, dairy, bread, and rice. Eggs, fruits, vegetables, and pulses provided most of the remaining Zn intake. The diet records showed that neither Zn nor Fe supplements were consumed to any great extent by the study population, and that daily tea consumption averaged 276 mL extracted from about 4 g tea leaves per individual. Tea was frequently consumed directly after food.
R
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Table III: The hemoglobin (Hb) and serum ferritin (SF) concentration, and prevalence of anemia, iron deficiency (ID), and iron deficiency anemia (IDA) for different age groups of the study participants with C-Reactive Protein (CRP) 0.05) between SZn and SF, but SZn and Hb had a positive correlation (0.31, p < 0.01). Hb was also positively correlated (0.34, p < 0.01) with SF. Only 25 % (4/16) of Zn-deficient subjects were ID, and the mean SZn concentration in the 42 subjects with ID was 90.6 μg/dL, compared to 91.3 μg/dL in those with normal SF. Of the participants with Zn deficiency, 37.5 % (6/16) were also anemic and the SZn concentration was significantly lower in subjects with anemia than in those without anemia (mean SZn of 85.7 ± 13.1 μg/dL vs. 93.0 ± 16.0 μg/
dL, p = 0.001). Iron-deficient anemic participants had the lowest SZn concentrations, with an average of 84.5 ± 11.9 μg/dL as compared to the mean value for non-anemic subjects (91.8 ± 15.8 μg/dL, p = 0.02).
Discussion The mean prevalence of Zn deficiency based on SZn was 6 – 7 % and similar in both the suburban and the rural study populations. The tested communities were mainly middle-class and their relatively high prevalence of overweight and obesity indicated an ample supply of energy from their diet, which is in line with the 43 % overweight and obesity reported for the whole of Iran [29]. Although the diet was high in bread and rice, which provided a high PA intake, the regular consumption of animal source foods in the form of dairy products, red meat, chicken, and eggs provided almost half of the dietary Zn intake. This also helped decrease the PA:Zn molar ratio to 10 – 13, which is indicative of a diet of moderate Zn bioavailability. Although the mean intake of red meat was only about 50 g/day, it provided 24 % of the Zn intake, with dairy products providing a further 13 %. The modest intake of animal source foods presumably results from a reasonably good socioeconomic status of both the rural and suburban populations, as only 5 % of our study subjects were classified as deprived. Red meat is expensive and failure to consume red meat by our study subjects would put many more at risk of Zn deficiency. Previous reports of Zn deficiency in Iran have varied widely. In Tehran, Zn deficiency was reported to be 28 % [6], 30.1 % [7], and 85.5 % [9] in three different studies. Fesharakinia et al. [8] reported Zn deficiency in Khorasan to be 28.1 %. A recent study by Dehghani et al. [11] reported an 8 % prevalence of Zn deficiency in children in Shiraz. They suggested that increased animal source food consumption, increased use of Zn supplements, and variations in the
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Zn levels in soil could explain the national variations. Our results confi rm that regular animal-source food consumption greatly improves Zn intake and leads to low levels of Zn deficiency. Zn supplements were not routinely taken by our study subjects; however, the level of soil Zn might have contributed to the modest levels of Zn deficiency observed. Karami et al. [30] reported a normal range of soil Zn in the province of Isfahan. Their field surveys showed acceptable levels of extractable Zn, indicating good Zn bioavailability for crops. Additionally, only 20 % of the wheat grain samples grown in the province of Isfahan were found to have critically low Zn concentration (< 24 mg/kg dry matter) [30]. Another explanation for the variable estimates of Zn deficiency in Iran could be the use of different cutoff values for Zn deficiency. In the present study, we used 65 – 74 μg/dL SZn as recommended by IZiNCG [1], although in the Zn status surveys reported above [6 – 9,11], SZn cut-off values ranged from 70 – 100 μg/ dL. The mean SZn concentrations measured in our study subjects, however, were of the same order as reported in other Iranian studies. In our study, the mean SZn ranged from 87 – 102 μg/dL, with a mean of 91.1 ± 15.5 μg/dL. Several studies have reported similar mean SZn values for healthy Iranian adults [10,31,32] and for healthy children and adolescents [33]. In addition to the wide provincial variations, socioeconomic conditions cause basic differences in the food consumption pattern of the populations living in different parts of Iran [34]. The low socioeconomic classes found mostly in the southern, southeastern, and some northern provinces may not be able to consume dairy foods and red meat products because they are expensive [34]. In these provinces, bread is the main food for rural dwellers and poor urban residents. Therefore, these groups of people may be in danger of higher incidence of Zn deficiency. Such differences in socioeconomic status could also explain the wide variation of the reported prevalence of Zn deficiency in Iran. Estimates of Zn deficiency in the different population groups in the present study varied from 0 – 17.2 % based on SZn. The higher prevalence of Zn deficiency in men than in women could be due to the higher Zn requirements in men compared to women, a reportedly lower Zn absorption, and higher endogenous losses [1]. However, SZn is regarded as a useful measure of Zn status in populations but not for individuals [1]. Therefore, due to the low subject number of SZn measurements for children < 5 years and adult males, Zn deficiency estimates for these populations should be treated with caution.
Overall, 18.3 % of the study subjects consumed less Zn than their respective EAR for Zn as recommended by WHO [22]. This is somewhat higher than the 6 – 7 % Zn deficiency as predicted by SZn. Those with low dietary Zn intake may develop Zn deficiency over time. Biochemical indicators, however, are a more quantitative means of assessing the Zn status of a population [1]. The ability to maintain adequate Zn status depends on the amount and bioavailability of Zn in the diet [35]. IZiNCG [1] and the Food and Nutrition Board/ Institute of Medicine (FNB/IOM) [36] have also recommended EAR values for Zn. These EAR values are higher than those recommended by WHO [22]. Using the FNB/IOM values, 41.4 % of our study population had Zn intakes below their respective EARs compared to 33.5 % when the IZiNCG values were used. Thus the WHO EAR values agreed more closely with the Zn deficiency estimated based on SZn. Our results show that the FNB/IOM and IZiNCG EAR values overestimated the prevalence of low Zn intakes for our study populations. Anemia appeared to be a greater public health problem than Zn deficiency. ID had an important role in the prevalence of anemia in most of our study populations. In the whole population, ID accounted for about 50 % of the anemia in older children and women but was not a major cause in younger children and adult men. This is because women of childbearing age have higher Fe requirements due to menstruation, and older children need more Fe for increased blood volume during the adolescent growth spurt. Other recent studies have reported similar anemia prevalence in women (25.8 %) in Northern Iran [37] and in 14- to 20-year-old girls (21.4 %) in Western Iran [38]. As in the present study, ID explained about half of the anemia in those studies. Similar results were found in other parts of the world [22]. Reasons for anemia in the Roorani men could be inflammation, hemoglobinopathies such as sickle cell or thalassemia, or other infections [39]. The role of Zn in the production of red blood cells [48 – 50] might explain the positive correlation between Zn and Hb. As there was no correlation between SF and SZn, it is possible that Zn deficiency be an independent cause of anemia [51]. Inflammation can increase SF [40] as an acute phase protein, decrease Fe absorption [41], and increase SZn [1]. That is why serum from subjects with CRP > 10 mg/L were excluded from analysis. The rather high prevalence of overweight and obesity in our adult study population, especially in the suburban area, could also contribute to the prevalence of anemia. Recent studies have indicated that overweight and obesity, as inflammatory conditions, are linked to a higher level of anemia [42].
Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
N. Abbaspour et al.: Zinc and Iron Status in Iran
It is sometimes argued that Zn and Fe deficiencies occur together because Fe and Zn absorption is low from high-phytate plant foods; and meat provides a good source of bioavailable Fe and Zn. One exception to this pattern might be populations such as ours that consume a high proportion of dairy foods that provide a useful source of Zn, but are low in Fe. This could be one of the main reasons why we found much higher prevalence of ID than Zn deficiency. Dairy products are also high in calcium, which is an inhibitor of both heme and non-heme Fe [43], and proteins in cow’s milk also inhibit the absorption of Fe [44]. It should also be noted that PA is a stronger inhibitor of Fe than Zn absorption [45]. High tea consumption would also be expected to decrease Fe [46] but not Zn absorption. Tea is the most potent inhibitor of Fe, decreasing its absorption from a meal by up to 90 % [47]. One limitation of the present study was not including the dietary intake of Fe, which was due to the lack of a local food composition table for Iran and the time limitation to measure all foods and ingredients for their Fe levels. Estimating the Fe intake would throw more light on the interrelationship between Fe and Zn and the status of Fe. The small sample size in the group of young children also limited our study to assess their risk of Zn and Fe deficiency with higher confidence. Therefore, a larger sample size, especially for young children, addition of the Fe intake, as well as inclusion of data on the inhibitors of Fe absorption in the local foods, would benefit future studies.
Conclusion In conclusion, our study demonstrated a modest level of Zn deficiency (6 – 7 %) in the mostly middle-class rural and suburban communities, but an almost 30 % incidence of anemia, of which about half was due to ID. There was no evidence of a less diverse diet in the rural community than in the suburban community. There was not a higher prevalence of Zn and Fe deficiencies in the rural community. The relatively good Zn status in both populations was due to an adequate supply of dietary Zn from animal source foods, which provided almost half of the Zn intake and supplemented the bread and rice staples. The higher level of ID than Zn deficiency may be due to the frequent consumption of tea, which inhibits iron absorption, the stronger inhibitory effect of PA on iron absorption than on Zn absorption, and the relatively high consumption of dairy products, which increase zinc intake but not iron intake.
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Acknowlegements We greatly appreciate the cooperation of the people of Khomeini Shahr and Rooran and the grant provided by the Swiss Development Cooperation, SDC. We also appreciate the cooperation by the Isfahan University of Medical Sciences, and the Isfahan Cardiovascular Research Center. We thank Dr. Ghasem Yadegarfar for his help with statistical analysis. The author’s responsibilities were as follows – NA collected the data, designed the study, performed the analysis, and prepared the manuscript; RH formulated the research question, checked data quality, helped with data interpretation and preparation of the manuscript; RW helped with manuscript preparation; RS formulated the research question, helped with preparation of the manuscript. None of the authors declared a conflict of interest. This work was funded by the Swiss Development and Cooperation
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12. Kalantari, N., Abdollahi, M., Mohmmadpour, B., Sheikholeslam, R. and Naghavi, M. (2006) Characterization and diagnosis of major micronutrient deficiencies at national and provincial level and relation to socio-demographic, geographic level and other relevant factors using relevant consumption data, biochemical indicator and available technical reports. Food/Flour Fortification Plan. Final Report. 13. Pirzadeh, M., Afyuni, M., Khoshgoftarmanesh, A. and Schulin, R. (2010) Micronutrient status of calcareous paddy soils and rice products: implication for human health. Biol. Fert. Soils 46, 317 – 22. 14. Hurrell, R.F. and Egli, I. (2010) Iron bioavailability and dietary reference values. Am. J. Clin. Nutr. 91 (suppl), 1461S – 7S. 15. Keikhaei, B., Zandian, K., Ghasemi, A. and Tabibi, R. (2007) Iron-deficiency anemia among children in southwest Iran. Food Nutr. Bull.28 (4), 406 – 11. 16. Kolahi, S., Farzin, H. and Khoshbaten, M. (2008) Hypochromic microcytic anemia in northwestern of Tabriz, Iran. Eur. J. Gen. Med. 5 (3), 178 – 80. 17. Sastry, N. (1997) What explains rural-urban differentials in child mortality in Brazil? Soc. Sci. Med. 44 (7), 989 – 1002.
24. Cole, C.C., Grant, F.K., Swaby-Ellis, E.D., Smith, J.L., Jacques, A., Northrop-Clewes, C.A., Caldwell, K.L., Pfeiffer, C.M. and Ziegler, T.R. (2010) Zinc and iron deficiency and their interrelations in low-income African American and Hispanic children in Atlanta. Am. J. Clin. Nutr. 91, 1027 – 34. 25. Lippi, G., Salvagno, G.L., Montagnana, M., Brocco, G. and Guidi, G.C. (2006) Influence of hemolysis on routine clinical chemistry testing. Clin. Chem. Lab. Med. 44 (3), 311 – 6. 26. World Health Organization. (2008) Worldwide prevalence of anemia 1993 – 2005: WHO global database on anemia. (de Benoist, B., McLean, E., Egli, I. and Cogswell, M., eds.) Geneva, Switzerland. 27. World Health Organization. Iron deficiency anemia: assessment, prevention, and control: A guide for programme managers. Geneva; (WHO/NHD/01.3), 2001. 28. Nutrisurvey, 2009. http://www.nutrisurvey.de/ (accessed December 2011). 29. Kelishadi, R., Alikhani, S., Delavari, A., Alaedini, F., Safaie, A. and Hojatzadeh, E. (2007) Obesity and associated lifestyle behaviours in Iran: findings from the First National Non-communicable Disease Risk Factor Surveillance Survey. Public Health Nutr. 11 (3), 246 – 251.
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30. Karami, M., Afyuni, M., Khoshgoftarmanesh, A., Papritz, A. and Schulin, R. (2009) Grain zinc, iron, and copper concentrations of wheat grown in central Iran and their relationships with soil and climate variables. J. Agr. Food Chem. 57, 10876 – 82. 31. Farzin, L., Moassesi, M.E., Sajadi, F., Amiri, M. and Shams, H. (2009) Serum levels of antioxidants (Zn, Cu, Se) in healthy volunteers living in Tehran. Biol. Trace Elem. Res. 129, 36 – 45. 32. Mir, E., Hossein-Nezhad, A., Bahrami, A., Bekheirnia, M.R., Javadi, E., Afshar Naderi, A. and Larijani, B. (2007) Serum zinc concentration could predict bone mineral density and protect osteoporosis in healthy men. Iran J. Public Health, A supplementary issue on osteoporosis 30 – 36. 33. Kelishadi, R., Alikhassy, H. and Amiri, M. (2002) Zinc and copper status in children with high family risk of premature cardiovascular disease. Ann. Saudi Med. 22, 5 – 6. 34. Lahsaeizadeh, A. (2001) Sociological analysis of food and nutrition in Iran. Nutr. Food Sci. 31 (3), 129 – 35. 35. Gibson, R.S. Preventing zinc deficiency through diet diversification and modification. IZiNCG Technical Brief No. 5. 2007. 36. FNB/IOM Food and Nutrition Board, Institute of Medicine. (2002) Dietary reference intakes of vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. National Academy Press, Washington, D.C. 37. Vagheri, G. (2007) Anemia in north of Iran (Southeast of Caspian Sea). Pak. J. Biol. Sci. 10 (10), 1703 – 7. 38. Akramipour, R., Rezaei, M. and Rahimi, Z. (2008) Prevalence of iron deficiency anemia among adolescent schoolgirls from Kermanshah, Western Iran. Hematology 13 (6), 352 – 5. 39. Kassebaum, N.J., Jasrasaria, R., Naghavi, M. et al. (2014) A systematic analysis of global anemia burden from 1990 to 2010. Blood 123 (5), 615 – 24. 40. World Health Organization. (2011) Serum ferritin concentrations for the assessment of iron status and iron deficiency in populations. VMNIS Vitamin and Mineral Nutrition Information System. Geneva; World Health Organization, (WHO/NMH/NHD/MNM/11.2). 41. Cercamondi, C.I., Egli, I.M., Ahouandjinou, E., Dossa, R., Zeder, C., Salami, L., Tjalsma, H., Wiegerinck, E., Tanno, T., Hurrell, R.F., Hounhoutgan, J. and Zimmermann, M.B. (2010) Afebrile plasmodium falciparum parasitemia decreases absorption of fortification iron but does not affect systemic iron
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utilization a double stable isotope study in young Beninese women. Am. J. Clin. Nutr. 92, 1385 – 92. 42. Cepeda-Lopez, A.C., Aeberli, I. and Zimmermann, M.B. (2010) Does obesity increase risk for iron deficiency? A review of the literature and the potential mechanisms. Int. J. Vitam. Nutr. Res. 80 (4 – 5), 263 – 70. 43. Hallberg, L., Brune, M., Erlandsson, M., Sandberg, A.S. and Rossander-Hulten, L. (1991) Calcium: effect of different amounts on nonheme- and heme-iron absorption in humans. Am. J. Clin. Nutr. 53, 112 – 9. 44. Hurrell, R.F., Lynch, S.R., Trinidad, T.P., Dassenko, S.A. and Cook, J.D. (1989) Iron absorption in humans as influenced by bovine milk proteins. Am. J. Clin. Nutr. 9 (3), 546 – 52. 45. Hurrell, R.F. (2003) Influence of Vegetable Protein Sources on Trace Element and Mineral Bioavailability. J. Nutr.133, 2973S– 7S. 46. Hurrell, R.F., Reddy, M. and Cook, J.D. (1999) Inhibition of non-haem iron absorption in man by polyphenolic-containing beverages. Brit. J. Nutr. 81, 289 – 95. 47. Disler, P.B., Lynch, S.R., Charlton, R.W., Torrance, J.D., Bothwell, T.H., Walker, R.B. and Mayet, F. (1975) The effect of tea on iron absorption. Gut 16, 193 – 200. 48. Rifkind, J.M. and Heim, J.M. (1977) Interaction of zinc with hemoglobin: Binding of zinc and the oxygen affinity. Biochemistry 16 (20), 4438 – 43. 49. Prasad, A.S., Abbasi, A.A., Rabbani, P. and DuMouchelle, E. (1981) Effect of zinc supplementation on serum testosterone level in adult male sickle cell anemia subjects. Am. J. Hematol. 10, 119 – 27. 50. Folin, M., Contiero, E. and Vaselli, G.M. (1994) Zinc content of normal human serum and its correlation with some hematic parameters. Biometals 7, 75 – 79. 51. Idei, M., Miyake, K., Horiuchi, Y., Tabe, Y., Miyake, N., Ikeda, N. and Miida, T. (2010) Serum zinc concentration decreases with age and is associated with anemia in middle-aged and elderly people. Jpn. J. Clin. Pathol. 58 (3), 205 – 210. Nazanin Abbaspour ETH Zurich Institute of Terrestrial Ecosystems (ITES) CHN F 27 Universitätstrasse 16 8092 Zurich Switzerland Tel.: +41 44 632 84 45 Fax: +41 44 632 11 23 [email protected]
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Original Communication
Zinc Status as Compared to Zinc Intake and Iron Status: a Case Study of Iranian Populations from Isfahan Province Nazanin Abbaspour1, Rita Wegmueller2, Roya Kelishadi3, Rainer Schulin1, and Richard F. Hurrell2 1
ETH Zurich, Institute of Terrestrial Ecosystem, Zurich, Switzerland ETH Zurich, Institute of Food, Nutrition and Health, Zurich, Switzerland 3 Faculty of Medicine and Child Health Promotion Research Center, Isfahan University of Medical Sciences, Isfahan, Iran 2
Received: January 10, 2012; Accepted: July 9, 2014
Abstract: The aim of this study was to estimate the zinc (Zn) and iron (Fe) status of different age groups in rural (Rooran) and suburban (Khomeini Shahr) populations in central Iran, to relate the Zn status to Zn intake from animal and plant foods, and to examine the relationship between Zn and Fe status. Blood samples from 341 subjects including preschool children (27), schoolchildren (157), women (91), and men (66) were analyzed for serum zinc (SZn), serum ferritin (SF), total C-reactive protein, and hemoglobin. Daily Zn and phytic acid (PA) intakes from major food groups were estimated using a 3-day weighed food record. The overall prevalence of Zn deficiency based on low SZn was 5.9 % in Rooran and 7.2 % in Khomeini Shahr. Anemia was higher in the village than in the suburb (33.5 % vs. 22.7 %; p = 0.04) and almost half of the anemia in Khomeini Shahr and 36 % in Rooran was associated with iron deficiency (ID) based on low SF. The PA:Zn molar ratio in the diet was 10 – 13, indicating a diet of moderate Zn bioavailability. About 18 % of the population consumed less Zn than their WHO Estimated Average Requirements. There was no association between Zn status and Fe status. The modest prevalence of Zn deficiency in the study populations can be explained by a relatively high Zn intake from animal source foods. Anemia however is a serious public health problem affecting some 30 % of the subjects, with almost half due to ID. The lower Fe status than Zn status could be due to the frequent consumption of tea and dairy products. Key words: Zinc deficiency, iron deficiency, Iramian diet, serum zinc, dietary zinc, anemia
Introduction Zinc (Zn) deficiency can have negative health consequences in relation to growth, immune competence, DOI 10.1024/0300-9831/a000175
reproductive function, and neural development [1]. It is still considered a potential problem in Iran [2], where it was first observed in adolescent boys in 1963 [3]. Subsequent Zn supplementation studies [2, 4, 5],
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one as recent as 2006 [4], have reported that Zn supplements increase the height and weight of Iranian children. However, diet and lifestyle have changed considerably in some Iranian populations over the last 50 years and more recent estimates of Zn deficiency in Iran have varied widely depending on the province and the population studied. Based on low serum Zn (SZn), estimates of Zn deficiency have varied from 8 – 30 % [6 – 11]. The most recent study by Dehghani et al. [11] reported only 8 % Zn deficiency in 3- to 18-year-old children. They suggested that changes in the diet, use of Zn supplements, and differences in soil Zn and thus the Zn content of local foods could explain the variation in Zn deficiency reported in different Iranian provinces. The traditional Iranian diet is based on bread and rice [12, 13] that is low in Zn and high in phytic acid (PA), which is a potent inhibitor of Zn absorption [1]. With improved income, the consumption of animal source foods, such as milk and meat, which are higher in Zn, are expected to increase the Zn status. Iron (Fe) and Zn status are often linked [1] as they share PA as the common inhibitor and because animal foods increase their absorption [14]. Iron deficiency anemia (IDA) is also prevalent in Iran, with recent studies reporting 29 % IDA in children (< 5 years) in southwest Iran [15] and 10 % IDA in adult women in Northwest Iran [16]. Urban populations usually enjoy a higher quality of life and consume a more diverse diet than rural populations [17, 18], and therefore might be expected to have a lower prevalence of Zn and Fe deficiencies [19, 20]. There is little evidence, however, as these assumptions lack age- and gender-specific data on the Zn and Fe status of the Iranian population. In the present study, we estimated Zn and Fe status in children and adults from a rural (Rooran) and a suburban (Khomaini Shahr) population in Isfahan Province. We compared Zn status to Zn intake that was based on a 3-day weighed food record and measured Zn and PA contents [21] in relation to the Estimated Average Requirements (EAR) for Zn [22].
Subjects and Methods
sume mostly the same products as consumed in the city of Isfahan. The survey was conducted from November to December 2009 in Khomeini Shahr, a suburb of Isfahan with a population over 200,000 inhabitants, and in Rooran, a rural community with around 2000 inhabitants. Khomeini Shahr is a small city in the northwestern part of Isfahan and is now a part of the Isfahan Metropolitan area. Rooran is located 40 km to the southeast of Isfahan city. It still maintains typical characteristics of a village, including dependence on agriculture as the main occupation and self-production of rice and wheat.
Subjects The study subjects were from the same 24 households in Khomeini Shahr and 28 households in Rooran that took part in a previous dietary survey [21]. The households were selected randomly from these communities. In each site, the target enrollment was at least 40 per age group (preschool children aged < 5 years, school-age children aged 5 – 14 years, females aged ≥ 15 years, and males aged ≥ 15 years). The sample size of 320 participants was selected based on an expected moderately high prevalence of Zn deficiency [1]. Due to the small number of children in the households, additional children of preschool age (< 5 years) and school age (5 – 18 years) were recruited through schools, local mosques, and health centers. However, despite these efforts, we did not reach the target number of preschool children in either community (Table I). A representative of each household that had participated in the previous study and a parent of the newly participating children were invited to attend a meeting in which the survey was presented orally and questions were answered. Volunteers were enrolled after written consent was obtained from all full-aged participants (over 18) and oral consent from the children. In addition, permission to conduct the survey was obtained from the respective health centers for both communities. The protocol was reviewed and approved by the Ethics Committees of ETH Zurich and the Research Affairs office of Isfahan University of Technology.
Location Subject characteristics Our criteria for selecting study sites were: i) they should be accessible; ii) the rural community should represent a typical life style of a village; and iii) the suburb should have a more urban life style and con-
Socioeconomic data were collected using a specially prepared questionnaire. We specifically designed the questionnaire to rank the subject families as de-
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23.3 (20.1, 27.0) 24.7 (19.9, 30.6) 70.3 ± 10.0 171.23 ± 9.7
173.1 ± 6.4
74.6 ± 18.3
Blood analyses
2
Arithmetic mean ± SD. Geometric mean (-1 SD, +1 SD). F: female, M: male.
34.5 (22.2, 53.6) 32.8 (21.1, 51.0) 38 28 M ≥ 15 yrs
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prived, low middle class, middle class, semi-wealthy, or wealthy. The ranking was based on reported monthly expenditure, profession, ownership of house, cars, etc., residential area, household size, and education. Each family characteristic was given a score and the total score defined the socioeconomic class. Anthropometric measurements of height and weight were made with the participants barefoot and dressed in light clothes. All measurements were taken in the morning, according to a standardized procedure given by the World Health Organization (WHO) [23]. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2).
1
22.3 (18.4, 27.0)
16.2 (13.4, 19.6)
24.4 (20.3, 29.3) 55.6 ± 9.5 47 F ≥ 15 yrs
44
25.0 (17.3, 36.1)
30.8 (19.9, 47.6)
160.4 ± 6.2
157.2 ± 8.0
64.0 ± 12.3
16.5 (13.9, 19.6)
14.7 (13.4, 16.1) 15.5 (14.6, 16.5)
29.5 ± 13.2
30.1 ± 12.0
100.1 ± 6.7
133.0 ± 17.6 129.51 ± 18.9
103.8 ± 3.3 4.1 (2.6, 6.4)
9.2 (6.9, 12.1) 8.0 (5.6, 11.2)
4.3 (3.8, 4.8)
68 5-14 yrs
14 13 < 5 yrs
89
16.8 ± 1.7
14.9 ± 3.0
R Kh R Kh R Kh
R
Kh
R
Kh
BMI (kg/m2)1 Weight (kg)2 Height (cm)2 Age (yrs)1 N Age group
Table I: Anthropometric measurements including height, weight, and body mass index (BMI) together with age and number of the participants (N) in Khomeini Shahr (Kh) and Rooran (R).
N. Abbaspour et al.: Zinc and Iron Status in Iran
Approximately 6 mL venous blood was taken in the morning so as to avoid diurnal and physiological variations in SZn [24]. The subjects were classified as fasting or non-fasting. About 2 mL of each blood sample was transferred into EDTA-treated tubes and the rest (≈ 4 mL) into trace-element free tubes without added anticoagulants. The 4-mL blood samples were allowed to clot for at least 40 minutes in a cooling chest before the serum was separated by centrifugation (High-Speed Refrigerated Centrifuge, SIGMA 3K30, Germany) at room temperature for 10 minutes at 3000 g and divided into aliquots. The serum aliquots and the whole-blood samples in the EDTA-tubes were kept on ice and transported to the Isfahan University of Medical Sciences (IUMS) for analysis. The wholeblood samples in the EDTA-tubes were used for hemoglobin (Hb) analysis within 12 hours of arrival at the laboratory. The serum samples were frozen and stored at – 20 °C until further analysis. For some of the preschool children, less than 5 mL blood was drawn and not all the analyses could be performed. C-reactive protein (CRP) as a measure of acute infection or inflammation was determined in serum samples using an immunoturbidometric assay (Atomatic analyzer 902, Hitachi, Japan). Values of ≥10 mg/L were taken to indicate the presence of inflammation or infection as recommended by the manufacturer (Darman Kave 2000) and according to the International Zinc Consultative Group (IZiNCG) recommendation [1]. Serum Zn (SZn) was analyzed by flame atomic absorption spectrophotometry (Atomic Absorption Spectrophotometer, Perkin-Elmer 2380, Norwalk, Connecticut, USA) using deproteinized samples. All analyses were performed in duplicate and a certified reference material, Seronorm™, (Sero AS, Billinstad, Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
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Norway) was analyzed in parallel for quality control [1]. Analyses were repeated when the difference between duplicates was > 10 % if sufficient serum sample was available. Zn deficiency was defined as SZn levels in non-fasting blood samples of < 65 μg/dL, < 66 μg/dL, and < 70 μg/dL for children < 10 years, non-pregnant females >10 years, and males >10 years, respectively; and < 70 μg/dL and < 74 μg/dL, respectively, for fasting blood samples from non-pregnant females > 10 years and males > 10 years [1]. As no cut-off value has been recommended for fasting blood samples of children < 10 years, the same cut-off (65 μg/dL) was used as for non-fasting blood samples. Samples were carefully examined for hemolysis by judging the color of the serum samples. Hemolysis confers a pink to red hue coloration to the plasma or serum [25]. Hemolyzed samples or samples with a CRP value ≥ 10 were excluded from the statistical analysis of SZn. Hemoglobin (Hb) was measured using an electronic Coulter Counter (Automated Hematology Analyzer, Sysmex K-1000, Kobe Japan). Anemia was defined as recommended by WHO [26]: Hb < 130 g/L for males ≥ 15 years, Hb < 120 g/L for children of 12 – 14 years of age and non-pregnant women ≥15 years, Hb < 115 g/L for children aged 5 – 11 years, and Hb < 110 g/L for children < 5 years. Serum ferritin (SF) was analyzed using an enzymelinked immunoassay (Monobind Inc. California, USA) at a commercial laboratory (Ferdowsi, Isfahan). The serum samples were frozen before transportation to the laboratory. ID was classified with SF < 12 μg/L (< 5 years) and < 15 μg/L (≥ 5 years) [27]. Samples with CRP ≥ 10 mg/L were also excluded from the statistical analysis of SF.
Zn intake and bioavailability Dietary Zn intake was measured using a 3-day weighed food record. Data were collected on 3 consecutive days, including 2 weekdays and one weekend day, during which the households were asked to maintain their usual food habits. The total food prepared for consumption, the individual portions consumed by each household member, as well as the uneaten remains were weighed. Zn and PA intakes were estimated separately for men, women, preschool-, and school aged-children. They were based on the analyzed Zn and PA contents reported previously for the foods and dishes consumed within our test communities [21], with additional data from food composition tables [28]. The PA:Zn molar ratios were calculated for the
whole diet and Zn bioavailability (low, moderate, or high) was estimated as recommended by the WHO [22]. Zn intake was estimated and compared to the EAR for different age and gender groups based on the level of Zn bioavailability of the diet [22].
Statistical evaluation The Kolmogorov-Smirnov test showed that SZn, Hb, height, and weight were normally distributed in both communities. These data are presented as means ± SDs. The data for age, BMI, and SF were normal for each age group after transformation into natural logarithms. They are presented as geometric means ± 1 SD. Since the CRP data were skewed, even after logarithmic transformation, the median range is reported. Oneway analysis of variance (ANOVA) was used to test for differences in the means of SZn, SF, and Hb concentrations among age groups and genders. The independent sample t-test was applied to compare sample means between the two communities. The chi-square test was performed for prevalence analysis and to test whether there were significant differences in categorical variables between rural and suburban populations. For those age groups with small sample size, the Fisher exact test was used instead of the chi-square test. To evaluate correlations between biochemical parameters, the data of all participants in the two communities were pooled in order to have a statistically meaningful sample size. The Pearson’s correlation coefficient was used to examine the relationship between SZn, logSF, and Hb. Logistic regression analysis was used to investigate relationships between Zn deficiency prevalence and potential predictors. Adjusted odd ratios (OR) were calculated for age, gender, and community with 95 % confidence interval (CI). To assess the relationships between SZn concentration and potential predictors, multiple linear regression was employed. Differences were considered statistically significant in case of p < 0.05. Statistical analyses were performed using SPSS version 16 (SPSS Inc., Chicago, IL, USA).
Results Subject characteristics The results of the anthropometric measurements are shown in Table I. The adult female participants tended to be taller (p = 0.03) and heavier (p = 0.001) in suburban Khomeini Shahr than in rural Rooran and had
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12 [41] The EARs are for moderate bioavailability diet as recommended by WHO [22] based on the average PA:Zn molar ratios of 5-15. N: Total number of participants in each age group. F: female, M: male. 2
1
11 13
35 [23] 9.5 [42]
10 11
15 [48] 33 [12]
9.5 10
12 [17] 33 [3] % 0.05). The average daily PA:Zn molar ratio was similar in both populations (10.7 in Rooran and 12.4 in Khomeini Shahr). According to WHO, moderate Zn bioavailability has an average PA:Zn molar ratio of 5 – 15 [22]. Based on this definition, both populations had moderate Zn bioavailability diets (PA:Zn molar ratio 10 – 13). According to EAR values given by WHO [22], 18.3 % of the entire study population consumed less Zn than they required. This was similar between rural and suburban areas but varied considerably depending on the population age group (Table II). Almost equal amounts of daily Zn intake were consumed with bread and red meat, although on a weight basis, these foods provided 12 % (182 g) and 4 % (49 g) of daily food intake (Figure 1). Dairy products (milk, yoghurt, and cheese) and rice provided 13 % and 12 % of the daily Zn intake, respectively. Animal source foods (red meat, chicken, milk, yoghurt, cheese, and eggs) provided 46 % of the daily Zn intake. The main Zn-containing foods, providing 80 % of daily intake, were red meat, chicken, dairy, bread, and rice. Eggs, fruits, vegetables, and pulses provided most of the remaining Zn intake. The diet records showed that neither Zn nor Fe supplements were consumed to any great extent by the study population, and that daily tea consumption averaged 276 mL extracted from about 4 g tea leaves per individual. Tea was frequently consumed directly after food.
R
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Table III: The hemoglobin (Hb) and serum ferritin (SF) concentration, and prevalence of anemia, iron deficiency (ID), and iron deficiency anemia (IDA) for different age groups of the study participants with C-Reactive Protein (CRP) 0.05) between SZn and SF, but SZn and Hb had a positive correlation (0.31, p < 0.01). Hb was also positively correlated (0.34, p < 0.01) with SF. Only 25 % (4/16) of Zn-deficient subjects were ID, and the mean SZn concentration in the 42 subjects with ID was 90.6 μg/dL, compared to 91.3 μg/dL in those with normal SF. Of the participants with Zn deficiency, 37.5 % (6/16) were also anemic and the SZn concentration was significantly lower in subjects with anemia than in those without anemia (mean SZn of 85.7 ± 13.1 μg/dL vs. 93.0 ± 16.0 μg/
dL, p = 0.001). Iron-deficient anemic participants had the lowest SZn concentrations, with an average of 84.5 ± 11.9 μg/dL as compared to the mean value for non-anemic subjects (91.8 ± 15.8 μg/dL, p = 0.02).
Discussion The mean prevalence of Zn deficiency based on SZn was 6 – 7 % and similar in both the suburban and the rural study populations. The tested communities were mainly middle-class and their relatively high prevalence of overweight and obesity indicated an ample supply of energy from their diet, which is in line with the 43 % overweight and obesity reported for the whole of Iran [29]. Although the diet was high in bread and rice, which provided a high PA intake, the regular consumption of animal source foods in the form of dairy products, red meat, chicken, and eggs provided almost half of the dietary Zn intake. This also helped decrease the PA:Zn molar ratio to 10 – 13, which is indicative of a diet of moderate Zn bioavailability. Although the mean intake of red meat was only about 50 g/day, it provided 24 % of the Zn intake, with dairy products providing a further 13 %. The modest intake of animal source foods presumably results from a reasonably good socioeconomic status of both the rural and suburban populations, as only 5 % of our study subjects were classified as deprived. Red meat is expensive and failure to consume red meat by our study subjects would put many more at risk of Zn deficiency. Previous reports of Zn deficiency in Iran have varied widely. In Tehran, Zn deficiency was reported to be 28 % [6], 30.1 % [7], and 85.5 % [9] in three different studies. Fesharakinia et al. [8] reported Zn deficiency in Khorasan to be 28.1 %. A recent study by Dehghani et al. [11] reported an 8 % prevalence of Zn deficiency in children in Shiraz. They suggested that increased animal source food consumption, increased use of Zn supplements, and variations in the
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Zn levels in soil could explain the national variations. Our results confi rm that regular animal-source food consumption greatly improves Zn intake and leads to low levels of Zn deficiency. Zn supplements were not routinely taken by our study subjects; however, the level of soil Zn might have contributed to the modest levels of Zn deficiency observed. Karami et al. [30] reported a normal range of soil Zn in the province of Isfahan. Their field surveys showed acceptable levels of extractable Zn, indicating good Zn bioavailability for crops. Additionally, only 20 % of the wheat grain samples grown in the province of Isfahan were found to have critically low Zn concentration (< 24 mg/kg dry matter) [30]. Another explanation for the variable estimates of Zn deficiency in Iran could be the use of different cutoff values for Zn deficiency. In the present study, we used 65 – 74 μg/dL SZn as recommended by IZiNCG [1], although in the Zn status surveys reported above [6 – 9,11], SZn cut-off values ranged from 70 – 100 μg/ dL. The mean SZn concentrations measured in our study subjects, however, were of the same order as reported in other Iranian studies. In our study, the mean SZn ranged from 87 – 102 μg/dL, with a mean of 91.1 ± 15.5 μg/dL. Several studies have reported similar mean SZn values for healthy Iranian adults [10,31,32] and for healthy children and adolescents [33]. In addition to the wide provincial variations, socioeconomic conditions cause basic differences in the food consumption pattern of the populations living in different parts of Iran [34]. The low socioeconomic classes found mostly in the southern, southeastern, and some northern provinces may not be able to consume dairy foods and red meat products because they are expensive [34]. In these provinces, bread is the main food for rural dwellers and poor urban residents. Therefore, these groups of people may be in danger of higher incidence of Zn deficiency. Such differences in socioeconomic status could also explain the wide variation of the reported prevalence of Zn deficiency in Iran. Estimates of Zn deficiency in the different population groups in the present study varied from 0 – 17.2 % based on SZn. The higher prevalence of Zn deficiency in men than in women could be due to the higher Zn requirements in men compared to women, a reportedly lower Zn absorption, and higher endogenous losses [1]. However, SZn is regarded as a useful measure of Zn status in populations but not for individuals [1]. Therefore, due to the low subject number of SZn measurements for children < 5 years and adult males, Zn deficiency estimates for these populations should be treated with caution.
Overall, 18.3 % of the study subjects consumed less Zn than their respective EAR for Zn as recommended by WHO [22]. This is somewhat higher than the 6 – 7 % Zn deficiency as predicted by SZn. Those with low dietary Zn intake may develop Zn deficiency over time. Biochemical indicators, however, are a more quantitative means of assessing the Zn status of a population [1]. The ability to maintain adequate Zn status depends on the amount and bioavailability of Zn in the diet [35]. IZiNCG [1] and the Food and Nutrition Board/ Institute of Medicine (FNB/IOM) [36] have also recommended EAR values for Zn. These EAR values are higher than those recommended by WHO [22]. Using the FNB/IOM values, 41.4 % of our study population had Zn intakes below their respective EARs compared to 33.5 % when the IZiNCG values were used. Thus the WHO EAR values agreed more closely with the Zn deficiency estimated based on SZn. Our results show that the FNB/IOM and IZiNCG EAR values overestimated the prevalence of low Zn intakes for our study populations. Anemia appeared to be a greater public health problem than Zn deficiency. ID had an important role in the prevalence of anemia in most of our study populations. In the whole population, ID accounted for about 50 % of the anemia in older children and women but was not a major cause in younger children and adult men. This is because women of childbearing age have higher Fe requirements due to menstruation, and older children need more Fe for increased blood volume during the adolescent growth spurt. Other recent studies have reported similar anemia prevalence in women (25.8 %) in Northern Iran [37] and in 14- to 20-year-old girls (21.4 %) in Western Iran [38]. As in the present study, ID explained about half of the anemia in those studies. Similar results were found in other parts of the world [22]. Reasons for anemia in the Roorani men could be inflammation, hemoglobinopathies such as sickle cell or thalassemia, or other infections [39]. The role of Zn in the production of red blood cells [48 – 50] might explain the positive correlation between Zn and Hb. As there was no correlation between SF and SZn, it is possible that Zn deficiency be an independent cause of anemia [51]. Inflammation can increase SF [40] as an acute phase protein, decrease Fe absorption [41], and increase SZn [1]. That is why serum from subjects with CRP > 10 mg/L were excluded from analysis. The rather high prevalence of overweight and obesity in our adult study population, especially in the suburban area, could also contribute to the prevalence of anemia. Recent studies have indicated that overweight and obesity, as inflammatory conditions, are linked to a higher level of anemia [42].
Int. J. Vitam. Nutr. Res. 83 (6) © 2013 Hans Huber Publishers, Hogrefe AG, Bern
N. Abbaspour et al.: Zinc and Iron Status in Iran
It is sometimes argued that Zn and Fe deficiencies occur together because Fe and Zn absorption is low from high-phytate plant foods; and meat provides a good source of bioavailable Fe and Zn. One exception to this pattern might be populations such as ours that consume a high proportion of dairy foods that provide a useful source of Zn, but are low in Fe. This could be one of the main reasons why we found much higher prevalence of ID than Zn deficiency. Dairy products are also high in calcium, which is an inhibitor of both heme and non-heme Fe [43], and proteins in cow’s milk also inhibit the absorption of Fe [44]. It should also be noted that PA is a stronger inhibitor of Fe than Zn absorption [45]. High tea consumption would also be expected to decrease Fe [46] but not Zn absorption. Tea is the most potent inhibitor of Fe, decreasing its absorption from a meal by up to 90 % [47]. One limitation of the present study was not including the dietary intake of Fe, which was due to the lack of a local food composition table for Iran and the time limitation to measure all foods and ingredients for their Fe levels. Estimating the Fe intake would throw more light on the interrelationship between Fe and Zn and the status of Fe. The small sample size in the group of young children also limited our study to assess their risk of Zn and Fe deficiency with higher confidence. Therefore, a larger sample size, especially for young children, addition of the Fe intake, as well as inclusion of data on the inhibitors of Fe absorption in the local foods, would benefit future studies.
Conclusion In conclusion, our study demonstrated a modest level of Zn deficiency (6 – 7 %) in the mostly middle-class rural and suburban communities, but an almost 30 % incidence of anemia, of which about half was due to ID. There was no evidence of a less diverse diet in the rural community than in the suburban community. There was not a higher prevalence of Zn and Fe deficiencies in the rural community. The relatively good Zn status in both populations was due to an adequate supply of dietary Zn from animal source foods, which provided almost half of the Zn intake and supplemented the bread and rice staples. The higher level of ID than Zn deficiency may be due to the frequent consumption of tea, which inhibits iron absorption, the stronger inhibitory effect of PA on iron absorption than on Zn absorption, and the relatively high consumption of dairy products, which increase zinc intake but not iron intake.
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Acknowlegements We greatly appreciate the cooperation of the people of Khomeini Shahr and Rooran and the grant provided by the Swiss Development Cooperation, SDC. We also appreciate the cooperation by the Isfahan University of Medical Sciences, and the Isfahan Cardiovascular Research Center. We thank Dr. Ghasem Yadegarfar for his help with statistical analysis. The author’s responsibilities were as follows – NA collected the data, designed the study, performed the analysis, and prepared the manuscript; RH formulated the research question, checked data quality, helped with data interpretation and preparation of the manuscript; RW helped with manuscript preparation; RS formulated the research question, helped with preparation of the manuscript. None of the authors declared a conflict of interest. This work was funded by the Swiss Development and Cooperation
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