Zinc status of Iranian preschool children
Sayyed Morteza Safavi, Robabeh Sheikholeslam, Mohsen Naghavi, Saeed Sadeghian, Elham Sadeqzadeh, Fariba Kolahdooz, and Somayyeh Mohammadian Abstract Background. Zinc deficiency is one of the most prevalent micronutrient deficiencies in developing countries, including Iran. The main direct causes of zinc deficiency are insufficient zinc intake, absorption or metabolic disorder, and increase in need during acute growth periods. Objective. To determine the prevalence of zinc deficiency in preschool boys and girls in urban and rural populations in order to assist policy makers. Children of preschool age (i.e., 6 years old in Iran) were studied because interventions in this age group are believed to result in greater improvement in learning skills once these children enter school. Methods. A national cross-sectional study was carried out on 4,374 randomly selected healthy preschool children from Iranian families in 2001. Serum zinc concentration was measured by atomic absorption spectrometry. The cutoff point for zinc deficiency was set at a serum level of 10 µmol/L (65 µg/dL). Results. The prevalence of zinc deficiency was estimated at approximately 19.3%. The highest prevalence was seen in the region that includes Sistan and Baluchistan, South Khorasan, and the southeast area of Kerman and the lowest in the region of Boushehr, Hormozgan, and South Khoozestan. The prevalence of zinc deficiency was significantly higher in rural areas than in urban areas. No significant difference in prevalence was seen between boys and girls. Conclusions. In the long run, nutritional security and increased access to and intake of foods with high levels of zinc are the most sustainable strategies to overcome zinc deficiency. Fortification of staple foods, improved quality of traditional bread, and supplementation for at-risk population groups are considered short- and mid-term The authors are affiliated with the Ministry of Health and Medical Education, Tehran, Iran. Please direct queries to the corresponding author: Dr. Sayyed Morteza Safavi, Nutrition Department, Cross of Hafez and Jomhouri Ave., Ministry of Health and Medical Education, Tehran, Iran; e-Mail: [email protected].
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interventions. Nutrition education and behavioral change may be long-term strategies.
Key words: Serum zinc levels, zinc deficiency, preschool children, Iranian preschool children
Introduction Zinc is an essential micronutrient for humans. It is known to have a role in the catalytic (synthesis of digestive enzymes and antioxidant effects), structural (bone growth and protein synthesis), and regulatory (DNA synthesis) functions of the body [1]. Zinc deficiency primarily affects tissues with high turnover (e.g., gastrointestinal mucosa, skin, and blood cells), but disorders in physical growth and sexual development are among the best-known consequences of chronic zinc deficiency [1]. Insufficient intake, increase in demand, food habits (consumption of foods inhibiting zinc absorption), and some diseases (such as chronic or recurrent diarrhea) are the major causes of zinc deficiency [2]. The production of some hormones affecting bone growth, such as somatomedin C, osteocalcin, testosterone, thyroid hormones, and insulin, requires zinc [3]. Zinc deficiency also affects smell and taste and has direct and indirect effects on growth retardation [4]. Development, growth, and differentiation of brain cells depend on the presence of zinc [5], and chronic zinc deficiency can result in learning disorders and memory problems [6, 7]. The World Health Organization (WHO) reported the number of disability-adjusted life years (DALYs) lost due to zinc deficiency to be about 29 million, with 90% of lost DALYs affecting developing countries. According to the same report, 800 thousand deaths per year are directly or indirectly due to zinc deficiency, especially in Southeast Asia and Africa, with 300 thousand and 350 thousand annual deaths, respectively [8]. Zinc is found in expensive foods such as meat and other high-protein foods. Thus, zinc deficiency is
Food and Nutrition Bulletin, vol. 28, no. 2 © 2007, The United Nations University.
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Zinc status of Iranian children
directly related to poverty [1]. Plant-source foods that are most common in the diets of developing countries are low in zinc and also contain zinc absorption inhibitors (phytates). This results in a high prevalence of zinc deficiency in these countries [9, 10]. Studies carried out in the last two decades show that zinc deficiency is a major problem globally and affects people’s health and social welfare. The studies have shown that diarrhea, pneumonia, and malaria are 1.28, 1.52, and 1.56 times more prevalent in zinc-deficient children than in nondeficient children [11]. In order to help policy makers in decision-making, a national survey was carried out in 2001 to gather baseline information about the zinc status of preschool Iranian children.
TABLE 1. Regional divisions Region number 1 2 3
4 5 6 7
Methods Iran, with a population of about 75 million and a land area of over 1,648,000 km2, is divided into 31 provinces. Sixty-two percent of the population resides in urban areas and 38% in rural areas. This cross-sectional study was carried out on 4,374 healthy preschool children (aged from 5 years, 11 months, and 30 days to 6 years, 11 months, and 29 days) selected from Iranian families in 11 regions (400 samples in each region) nationwide from May 25 to June 3, 2001. The sampling framework to access the statistical units in each urban and rural area of each region was as follows. The statistical framework of families in rural areas was based on the census of health houses and ambulant teams** carried out in March 2000. The statistical framework of families in urban areas was based on the census carried out for polio eradication in 1996 or the census carried out by urban health centers or health posts*** in March 2001. In consultation with sociology and epidemiology experts, the country was divided into 11 regions based on the results obtained from the anthropometric nutritional indicators survey in Iranian children under 6 years of age [12] and on ethnic, geographic, and socioeconomic characteristics (table 1). Samples were chosen as clusters with unequal numbers of households but equal numbers of children under 6. Eighty cluster heads were selected in each region according to urban and rural household statistical frameworks and divided proportionately between urban and rural areas. In each cluster, five statistical units were studied. Sample selection was performed by the Ministry of Health and Medical Education using population data Health houses are the smallest units providing primary health care services to rural populations. ** Ambulant teams render primary health care services to rural populations in villages that do not have health houses. *** Urban health posts deliver primary care services only and are supervised by urban health centers.
8 9 10 11
Provinces Gilan, Mazandaran East Azerbayjan, West Azarbayjan, Ardabil Golestan, North Khorasan (including Esfarayen, Bojnoord, Jajarm, Chenaran, Dargaz, and the districts of Shirvan and Ghoochan) Semnan, Central Khorasan Sistan and Baluchestan, South Khorasan (including Birjand, Nehbandan), East Kerman (including Kahnooj) Yazd, Esfahan, Chaharmahal and Bakhtiari, Kerman (including Rafsanjan, Zarand, Kerman) Boushehr, Hormozgan, South Khoozestan (including Abadan, Ahvaz, Khorramshahr, Mahshahr, Shadegan) Tehran Zanjan, Qazvin, Qom, Markazi Kordestan, Hamedan, Lorestan, Kermanshah, Ilam, North Khoozestan Fars, Central Kerman, Kohkilooyeh and Boyerahmad
from each province and district. Ethical approval was received from the ethical committee of the Ministry of Health and Medical Education, located in the office of the Undersecretary for Research, which is responsible for dealing with the ethical issues of all research carried out in the health and medical sector of the country. A week before the study started, clusters and selected households were identified through the primary health care (PHC) network in different districts. A day was fixed and mothers were invited to come to rural health houses or urban health centers. The health or nutrition expert of the district informed the mothers of the goals of the study and answered their questions. In some districts fathers were also informed. Written consent was then obtained, and the mothers were asked to bring their children to the health house or health center on the appointed day for blood sampling. A 4-mL blood sample was taken from the child in the nonfasting state between about 9 and 11 AM and poured into an acid-washed test tube. All blood samples were collected, placed in dry ice, and sent to the district laboratory within 30 minutes. In this laboratory, blood was immediately centrifuged (2,000 RPM for 15 minutes) and serum was separated from the clot. Serum was collected in acid-washed polyethylene tubes using a sampler and capped. The test tubes were labeled with an identification number and the date of sampling and kept at –20°C until they were sent to the Tehran reference laboratory with maintenance of the cold chain. The level of zinc was measured twice in each sample by atomic absorption spectrometry, and the mean value
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was obtained for each child. The data were analyzed with EPI6 (version 6.04b) and Microsoft Excel software. The cutoff point for the diagnosis of zinc deficiency was set at a zinc serum level of less than 10 µmol/L [13], with 7.7 µmol/L as the cutoff point to define severe cases [14]. The prevalence of zinc deficiency in each region was calculated in urban and rural areas separately and compared by the chi-square nonparametric test. The mean zinc serum levels for the total of all samples were compared between boys and girls and between urban and rural populations by Student’s t-test.
in the national census of 1996 [15]. There were no significant differences in mean serum zinc levels between boys and girls and between urban and rural populations. Serum zinc levels were below 10 µmol/L in 19.6% (95% confidence interval [CI], 18.3%–20.9%) of children studied. The prevalence of serum zinc levels below this limit was significantly higher in rural areas (22.1% [95% CI, 19.6%–24.5%]) than in urban areas (17.7% [95% CI, 16.4%–19.1%]). No significant difference was seen between boys (18.75 [95% CI, 16.7%–20.8%]) and girls (20.35% [95% CI, 18.6%–22.1%]). Severe zinc deficiency (serum zinc levels lower than 7.7 µmol/L) was observed in 2.9% (95% CI, 2.6%–3.2%) of all children, 3.7% (95% CI, 3.4%–4.1%) of rural children, and 2.3% (95% CI, 2.1%–2.5%) of urban children (table 3). The highest prevalence of zinc deficiency was seen in the rural population of northwest Iran (region 2) and the lowest in the urban population of southwest Iran (region 7). In five regions, the prevalence of zinc deficiency was significantly higher in rural than in urban populations. No significant differences in the prevalence of zinc deficiency were found between boys
Results Of the total of 4,400 samples taken, 26 were not analyzed because of insufficient volume or other errors during sampling, leaving 4,374 samples to be analyzed (table 2). The number of samples was equal in each region. The percentages of urban and rural residents (57.3% and 42.7%, respectively) in this study reflect the urban and rural distribution of the population obtained
TABLE 2. Number of samples per region in rural and urban areas and in boys and girls Group
Region Region Region Region Region Region Region Region Region Region Region 1 2 3 4 5 6 7 8 9 10 11
Total
Urban Rural Boys Girls
184 213 210 187
221 173 219 175
169 232 196 205
245 156 198 203
169 230 197 202
272 130 206 196
243 155 201 197
331 55 190 196
249 150 213 186
215 185 199 201
208 189 207 190
2,506 1,868 2,235 2,139
Total
397
394
401
401
399
402
398
386
399
400
397
4,374
TABLE 3. Serum zinc levels in rural and urban areas and in boys and girls % (no.) of cases with Zn ≥ 10 µmol/L
% (no.) of cases with Zn < 10 and ≥ 7.7 µmol/L
Group
N
Mean Zn level (µmol/L)
% (no.) of cases with Zn < 7.7 µmol/L
Rural Urban Boys Girls
1,868 2,506 2,235 2,139
12.26 ± 3.67 12.68 ± 3.94 12.54 ± 3.97 12.45 ± 3.84
77.9 (1,455) 82.2 (2,060) 81.1 (1,813) 79.5 (1,702)
18.4 (343) 15.4 (387) 16.1 (360) 17.3 (370)
3.7 (70) 2.3 (59) 2.8 (62) 3.1 (67)
Total
4,374
12.50 ± 2.30
80.3 (3,514)
16.7 (730)
2.9 (129)
TABLE 4. Prevalence of zinc deficiency, (serum zinc levels < 10 µmol/L) in rural and urban areas and in boys and girls Group
Region 1
Region 2
Region 3
Region 4
Region 5
Region 6
Region 7
Region 8
Region 9
Region 10
Region 11
Urban Rural Boys Girls
15.2 12.2 13.8 13.4
20.4* 28.9 23.3 25.2
16.6 18.1 16.3 18.5
20.0 17.3 17.7 20.2
28.4 27.4 27.4 28.2
20.2 23.1 19.9 22.4
9.9* 18.7 11.9 14.7
13.9* 23.7 14.2 16.3
22.9* 28.7 25.3 24.7
19.5 24.4 20.6 22.9
11.5* 23.8 16.4 18.4
Total (not weighted)
13.6
24.1
17.5
18.9
27.8
21.1
13.3
15.3
25.1
21.7
17.4
* The prevalence of zinc deficiency was significantly higher in rural compared to urban areas (p < .05)
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Zinc status of Iranian children
.ATIONAL
2EGION
FIG. 1. Weighted prevalences of zinc deficiency in each region
and girls in any of the 11 regions (table 4). The weighted prevalence of zinc deficiency in each region was calculated based on the percentages of urban and rural residents in each region. National rates were also calculated by taking into account the percentages of urban and rural residents in each region compared with the national population (figs. 1 and 2).
Discussion and conclusions The information presented in figure 2 shows that 19.3% of preschool Iranian children had serum zinc levels lower than 10 µmol/L. The prevalence of low serum zinc levels was significantly higher in rural than in urban children (22.5% and 17.2%, respectively). It should be noted that children with acute inflammatory symptoms were not excluded from the study, and laboratory tests for inflammation were not performed in this study. National data from Mexico showed that 21.4% (95% CI, 15.6%–27.1%) of all children 5 to 6 years of age were zinc deficient, with the prevalence higher in rural areas (34.3%) than in urban areas (13.9%), results very similar to those of our study
5RBAN
2URAL
.ATIONAL RATE
"OYS
'IRLS
FIG. 2. Weighted prevalences of zinc deficiency in boys and girls and in urban and rural areas
[16]. A survey conducted in Saudi Arabia found a 22% prevalence of low serum zinc levels (< 10 µmol/L) in urban preschoolers [17]. Holt et al. reported a 50% prevalence of hypozincemia in 5- to 15-year-old Australian schoolchildren [18]. Bahl et al. studied zinc plasma levels as a predictor of respiratory and diarrheal diseases in the children of poor urban areas of India [19]. Thirty-two percent of the children had serum zinc levels lower than 8.4 µmol/L, a much higher percentage than that in the current study (5.4%). Severe zinc deficiency was found in 2.9% of children (2.3% of urban and 3.7% of rural children); this prevalence is close to that found by Alshatawi [17] in preschoolers (2.3%) but is less than that reported by Al-Timimi et al. [20] in 2- to 10-year old Iraqi children (7.7%). In the present study in Iran, 46.6% of the children had serum zinc levels less than 12.2 µmol/L. This prevalence is lower than those reported by Alshatawi [17] (54.4%), Torrejon et al. [21] (79.7%), and Al-Timimi et al. [20] (54.8%). Moreover, although no comprehensive survey of zinc deficiency in Iran has yet been performed, our results show that the problem in preschool children is worrisome and needs prompt action in all regions. Compared with other micronutrient deficiencies in the same age group as described in a recent Iranian government report [22], zinc deficiency is more prevalent. The prevalence of zinc deficiency increases with age from 10.8% in 15- to 24-month-old children [22] to 19.3% in the preschool age group. This indicates that in order to reduce the prevalence of zinc deficiency in preschool children, it is necessary to perform certain preventive measures in younger children. The intake status of zinc-containing foods or zinc absorption inhibitors was not assessed in this study. Taking into consideration other studies on the intake status of these foods (as a direct cause of zinc deficiency), together with the results of studies on the prevalence of poverty (as the major cause of nutrition insecurity and thus of zinc deficiency), in addition to
234
the results obtained from this survey would be very helpful for outlining and designing sustainable strategies to alleviate zinc deficiency in this age group. The comprehensive food-consumption study of Iranian families carried out in 2000 showed that proteins contribute only about 10% of daily energy needs. Furthermore, the per capita consumption of meat and protein products, the main food sources of zinc, and also of legumes, another major source of zinc, is not sufficient [23]. Bread is the staple food in Iranian families, with a daily per capita intake of 320 g, providing up to onethird of energy needs in the population [23]. Unfortunately, the phytate content of traditional Iranian bread is high [24], resulting in low bioavailability of zinc. Phytic acid has been shown to be an inhibitor of zinc absorption in human and animal studies. This is true especially when the molar ratio of phytate to zinc is over 15. At this level an insoluble complex is formed in the gastrointestinal tract, resulting in low absorption of zinc [25, 26]. One of the important measures in Iran to overcome zinc deficiency will be improvement of the quality of bread. According to the food-consumption survey, the per capita intake of meat and protein products is lower in
S. M. Safavi et al.
rural than in urban areas [23]. This may partly explain the higher prevalence of zinc deficiency in rural areas. Other surveys show that the per capita income of rural families is lower than that of urban families [27], which might be a reason for the lower consumption of meat by rural families. The long-term sustainable strategy to decrease the prevalence of zinc deficiency will involve economic development programs. But short- and medium-term interventions, such as supplementation, fortification, nutritional behavior changes that target increases in per capita intake of high-protein foods and reductions in intakes of foods containing inhibitors of zinc absorption, and self-sufficiency programs at the local levels, may also be considered to alleviate the problem. One of the programs that the Nutrition Department of the Ministry of Health and Medical Education of Iran has designed to address the control of zinc deficiency is fortification of flour with multiple micronutrients, including zinc. This program is being carried out as a pilot project and will be scaled up to the national level if proved to be efficient. A supplementation program for preschool children, at least on a regional scale, is worth considering.
References 1. Mahan LK, Escott-Stump S. Krause’s food, nutrition and diet therapy. 11th ed. Philadelphia, PA, USA: Health Sciences Rights Department, 2000:143–7. 2. Reddy V. Importance of zinc for human health. (Part 2 of a 3-part series.). Consequences and causes of zinc deficiency. International Association of Infant Food Manufacturers, February 2005. Available at: http://www. ifm.net/industry/zinc2.htm. Accessed 15 March 2007.. 3. Ortega RM, Quintas ME, Andres P, Martinez RM, Lopez-Sobaler AM, Requejo AM. Zinc status of a group of pregnant Spanish women: Effects on anthropometric data and Apgar score of neonates. Nutr Res 1999;19:1423–8. 4. Salgueiro MJ, Zubillaga MB, Lysionek AE, Caro RA, Weill R, Boccio JR. The role of zinc in the growth and development of children. Nutrition 2002; 18:510–9. 5. Ploysangam A, Falciglia GA, Brehm BJ. Effect of marginal zinc deficiency on human growth and development. J Trop Pediatr 1997;43:192–8. 6. Sandstead HH. Zinc: Essentiality for brain development and function. Nutr Rev 1985;43:129–37. 7. Golub MS, Keen CL, Gershwin ME, Hendrickx AG. Developmental zinc deficiency and behavior. J Nutr 1995;125(8 suppl):2263S–71S. 8. World Health Organization Report (2002) IBLF dialogue with WHO London, October 28, 2002. Available at: http://www.who.int/dietphysicalactivity/media/en/ gsdoc_principles_charts.pdf. Accessed 15 March 2007. 9. Chen XC, Yin TA, He JS, Ma QY, Han ZM, Li LX. Low levels of zinc in hair and blood, pica, anorexia, and poor growth in Chinese preschool children. Am J Clin Nutr
1985;42:694–700. 10. Rosado JL. Zinc deficiency and its functional implications (in Spanish). Salud Publica Mex 1998;40:181–8. 11. Caulfield LE, Richard SA, Black RE. Undernutrition as an underlying cause of malaria morbidity and mortality in children less than five years old. Am J Trop Med Hyg 2004; 71: 55–63. 12. Iran Ministry of Health and Medical Education, Nutrition Department. Final report of the Anthropometric Nutritional Indicators Survey, Tehran: Senobar Publications, 1998 . 13. Hotz C, Peerson JM, Brown KH. Suggested lower cutoffs of serum zinc concentrations for assessing zinc status: Reanalysis of the second National Health and Nutrition Examination Survey data (1976–1980). Am J Clin Nutr 2003;78:756–64. 14. Prasad AS. Clinical manifestations of zinc deficiency. Annu Rev Nutr 1985;5:341–63. 15. Iran National Statistics Center. The 5th national population census: Population characteristics of provinces. Tehran: National Statistics Center, 1996; 3: 789–861. 16. Villalpando S, Garcia-Guerra A, Ramirez-Silva CI, Mejia-Rodriguez F, Matute G, Shamah-Levy T, Rivera JA. Iron, zinc and iodide status in Mexican children under 12 years and women 12–49 years of age. A probabilistic national survey. Salud Publica Mex 2003;45 (suppl 4):S520–9. 17. Alshatawi AA. Zinc nutritional status of preschool children in Riyadh city. Pakistan J Nutr 2006;5:429–31. 18. Holt AB, Spargo RM, Iveson JB, Faulkner GS, Cheek DB. Serum and plasma zinc, copper and iron concentrations
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19.
20. 21.
22.
23.
in Aboriginal communities of North Western Australia. Am J Clin Nutr 1980;33:119–32. Bahl R, Bhandari N, Hambidge KM, Bhan MK. Plasma zinc as a predictor of diarrheal and respiratory morbidity in children in an urban slum. Am J Clin Nutr 1998;68(2 suppl):414S–7S. Al-Timimi DJ, Al-Sharbatti SS, Al-Najjar F. Zinc deficiency among a healthy population in Baghdad, Iraq. Saudi Med J 2005;26:1777–81. Torrejon CS, Castillo-Duran C, Hertrampf ED, Ruz M. Zinc and iron nutrition in Chilean children fed fortified milk provided by the Complementary National Food Program. Nutrition 2004;20:177–80. Iran Ministry of Health and Medical Education, Nutrition Department. Final report of the National Integrated Micronutrients Survey. Tehran: Amirkabir Publications, 2001:325–78. National Nutrition and Food Technology Research
24. 25. 26.
27.
Institute. National Comprehensive Food Consumption Survey (2000–2002). 1st ed. Tehran: Research and Education Management and Planning Higher Council, 2004: 29–40. Reinhold JG. High phytate content of rural Iranian bread: A possible cause of human zinc deficiency. Am J Clin Nutr 1971;24:1204–6. Oberleas D, Harland BF. Phytate content of foods: Effect on dietary zinc bioavailability. J Am Diet Assoc 1981;79:433–6. Bindra GS, Gibson RS, Thompson LU. Phytate:Calcium/ zinc ratios in Asian immigrant lacto-ovo vegetarian diets and their relationship to zinc nutriture. Nutr Res 1986;6:475–83. Ministry of Social Welfare. Poverty and inequality in Iran: Policy making to reduce poverty and improve social welfare. Tehran: Ministry of Social Welfare, 2005:5–6.
Sayyed Morteza Safavi, Robabeh Sheikholeslam, Mohsen Naghavi, Saeed Sadeghian, Elham Sadeqzadeh, Fariba Kolahdooz, and Somayyeh Mohammadian Abstract Background. Zinc deficiency is one of the most prevalent micronutrient deficiencies in developing countries, including Iran. The main direct causes of zinc deficiency are insufficient zinc intake, absorption or metabolic disorder, and increase in need during acute growth periods. Objective. To determine the prevalence of zinc deficiency in preschool boys and girls in urban and rural populations in order to assist policy makers. Children of preschool age (i.e., 6 years old in Iran) were studied because interventions in this age group are believed to result in greater improvement in learning skills once these children enter school. Methods. A national cross-sectional study was carried out on 4,374 randomly selected healthy preschool children from Iranian families in 2001. Serum zinc concentration was measured by atomic absorption spectrometry. The cutoff point for zinc deficiency was set at a serum level of 10 µmol/L (65 µg/dL). Results. The prevalence of zinc deficiency was estimated at approximately 19.3%. The highest prevalence was seen in the region that includes Sistan and Baluchistan, South Khorasan, and the southeast area of Kerman and the lowest in the region of Boushehr, Hormozgan, and South Khoozestan. The prevalence of zinc deficiency was significantly higher in rural areas than in urban areas. No significant difference in prevalence was seen between boys and girls. Conclusions. In the long run, nutritional security and increased access to and intake of foods with high levels of zinc are the most sustainable strategies to overcome zinc deficiency. Fortification of staple foods, improved quality of traditional bread, and supplementation for at-risk population groups are considered short- and mid-term The authors are affiliated with the Ministry of Health and Medical Education, Tehran, Iran. Please direct queries to the corresponding author: Dr. Sayyed Morteza Safavi, Nutrition Department, Cross of Hafez and Jomhouri Ave., Ministry of Health and Medical Education, Tehran, Iran; e-Mail: [email protected].
230
interventions. Nutrition education and behavioral change may be long-term strategies.
Key words: Serum zinc levels, zinc deficiency, preschool children, Iranian preschool children
Introduction Zinc is an essential micronutrient for humans. It is known to have a role in the catalytic (synthesis of digestive enzymes and antioxidant effects), structural (bone growth and protein synthesis), and regulatory (DNA synthesis) functions of the body [1]. Zinc deficiency primarily affects tissues with high turnover (e.g., gastrointestinal mucosa, skin, and blood cells), but disorders in physical growth and sexual development are among the best-known consequences of chronic zinc deficiency [1]. Insufficient intake, increase in demand, food habits (consumption of foods inhibiting zinc absorption), and some diseases (such as chronic or recurrent diarrhea) are the major causes of zinc deficiency [2]. The production of some hormones affecting bone growth, such as somatomedin C, osteocalcin, testosterone, thyroid hormones, and insulin, requires zinc [3]. Zinc deficiency also affects smell and taste and has direct and indirect effects on growth retardation [4]. Development, growth, and differentiation of brain cells depend on the presence of zinc [5], and chronic zinc deficiency can result in learning disorders and memory problems [6, 7]. The World Health Organization (WHO) reported the number of disability-adjusted life years (DALYs) lost due to zinc deficiency to be about 29 million, with 90% of lost DALYs affecting developing countries. According to the same report, 800 thousand deaths per year are directly or indirectly due to zinc deficiency, especially in Southeast Asia and Africa, with 300 thousand and 350 thousand annual deaths, respectively [8]. Zinc is found in expensive foods such as meat and other high-protein foods. Thus, zinc deficiency is
Food and Nutrition Bulletin, vol. 28, no. 2 © 2007, The United Nations University.
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Zinc status of Iranian children
directly related to poverty [1]. Plant-source foods that are most common in the diets of developing countries are low in zinc and also contain zinc absorption inhibitors (phytates). This results in a high prevalence of zinc deficiency in these countries [9, 10]. Studies carried out in the last two decades show that zinc deficiency is a major problem globally and affects people’s health and social welfare. The studies have shown that diarrhea, pneumonia, and malaria are 1.28, 1.52, and 1.56 times more prevalent in zinc-deficient children than in nondeficient children [11]. In order to help policy makers in decision-making, a national survey was carried out in 2001 to gather baseline information about the zinc status of preschool Iranian children.
TABLE 1. Regional divisions Region number 1 2 3
4 5 6 7
Methods Iran, with a population of about 75 million and a land area of over 1,648,000 km2, is divided into 31 provinces. Sixty-two percent of the population resides in urban areas and 38% in rural areas. This cross-sectional study was carried out on 4,374 healthy preschool children (aged from 5 years, 11 months, and 30 days to 6 years, 11 months, and 29 days) selected from Iranian families in 11 regions (400 samples in each region) nationwide from May 25 to June 3, 2001. The sampling framework to access the statistical units in each urban and rural area of each region was as follows. The statistical framework of families in rural areas was based on the census of health houses and ambulant teams** carried out in March 2000. The statistical framework of families in urban areas was based on the census carried out for polio eradication in 1996 or the census carried out by urban health centers or health posts*** in March 2001. In consultation with sociology and epidemiology experts, the country was divided into 11 regions based on the results obtained from the anthropometric nutritional indicators survey in Iranian children under 6 years of age [12] and on ethnic, geographic, and socioeconomic characteristics (table 1). Samples were chosen as clusters with unequal numbers of households but equal numbers of children under 6. Eighty cluster heads were selected in each region according to urban and rural household statistical frameworks and divided proportionately between urban and rural areas. In each cluster, five statistical units were studied. Sample selection was performed by the Ministry of Health and Medical Education using population data Health houses are the smallest units providing primary health care services to rural populations. ** Ambulant teams render primary health care services to rural populations in villages that do not have health houses. *** Urban health posts deliver primary care services only and are supervised by urban health centers.
8 9 10 11
Provinces Gilan, Mazandaran East Azerbayjan, West Azarbayjan, Ardabil Golestan, North Khorasan (including Esfarayen, Bojnoord, Jajarm, Chenaran, Dargaz, and the districts of Shirvan and Ghoochan) Semnan, Central Khorasan Sistan and Baluchestan, South Khorasan (including Birjand, Nehbandan), East Kerman (including Kahnooj) Yazd, Esfahan, Chaharmahal and Bakhtiari, Kerman (including Rafsanjan, Zarand, Kerman) Boushehr, Hormozgan, South Khoozestan (including Abadan, Ahvaz, Khorramshahr, Mahshahr, Shadegan) Tehran Zanjan, Qazvin, Qom, Markazi Kordestan, Hamedan, Lorestan, Kermanshah, Ilam, North Khoozestan Fars, Central Kerman, Kohkilooyeh and Boyerahmad
from each province and district. Ethical approval was received from the ethical committee of the Ministry of Health and Medical Education, located in the office of the Undersecretary for Research, which is responsible for dealing with the ethical issues of all research carried out in the health and medical sector of the country. A week before the study started, clusters and selected households were identified through the primary health care (PHC) network in different districts. A day was fixed and mothers were invited to come to rural health houses or urban health centers. The health or nutrition expert of the district informed the mothers of the goals of the study and answered their questions. In some districts fathers were also informed. Written consent was then obtained, and the mothers were asked to bring their children to the health house or health center on the appointed day for blood sampling. A 4-mL blood sample was taken from the child in the nonfasting state between about 9 and 11 AM and poured into an acid-washed test tube. All blood samples were collected, placed in dry ice, and sent to the district laboratory within 30 minutes. In this laboratory, blood was immediately centrifuged (2,000 RPM for 15 minutes) and serum was separated from the clot. Serum was collected in acid-washed polyethylene tubes using a sampler and capped. The test tubes were labeled with an identification number and the date of sampling and kept at –20°C until they were sent to the Tehran reference laboratory with maintenance of the cold chain. The level of zinc was measured twice in each sample by atomic absorption spectrometry, and the mean value
232
S. M. Safavi et al.
was obtained for each child. The data were analyzed with EPI6 (version 6.04b) and Microsoft Excel software. The cutoff point for the diagnosis of zinc deficiency was set at a zinc serum level of less than 10 µmol/L [13], with 7.7 µmol/L as the cutoff point to define severe cases [14]. The prevalence of zinc deficiency in each region was calculated in urban and rural areas separately and compared by the chi-square nonparametric test. The mean zinc serum levels for the total of all samples were compared between boys and girls and between urban and rural populations by Student’s t-test.
in the national census of 1996 [15]. There were no significant differences in mean serum zinc levels between boys and girls and between urban and rural populations. Serum zinc levels were below 10 µmol/L in 19.6% (95% confidence interval [CI], 18.3%–20.9%) of children studied. The prevalence of serum zinc levels below this limit was significantly higher in rural areas (22.1% [95% CI, 19.6%–24.5%]) than in urban areas (17.7% [95% CI, 16.4%–19.1%]). No significant difference was seen between boys (18.75 [95% CI, 16.7%–20.8%]) and girls (20.35% [95% CI, 18.6%–22.1%]). Severe zinc deficiency (serum zinc levels lower than 7.7 µmol/L) was observed in 2.9% (95% CI, 2.6%–3.2%) of all children, 3.7% (95% CI, 3.4%–4.1%) of rural children, and 2.3% (95% CI, 2.1%–2.5%) of urban children (table 3). The highest prevalence of zinc deficiency was seen in the rural population of northwest Iran (region 2) and the lowest in the urban population of southwest Iran (region 7). In five regions, the prevalence of zinc deficiency was significantly higher in rural than in urban populations. No significant differences in the prevalence of zinc deficiency were found between boys
Results Of the total of 4,400 samples taken, 26 were not analyzed because of insufficient volume or other errors during sampling, leaving 4,374 samples to be analyzed (table 2). The number of samples was equal in each region. The percentages of urban and rural residents (57.3% and 42.7%, respectively) in this study reflect the urban and rural distribution of the population obtained
TABLE 2. Number of samples per region in rural and urban areas and in boys and girls Group
Region Region Region Region Region Region Region Region Region Region Region 1 2 3 4 5 6 7 8 9 10 11
Total
Urban Rural Boys Girls
184 213 210 187
221 173 219 175
169 232 196 205
245 156 198 203
169 230 197 202
272 130 206 196
243 155 201 197
331 55 190 196
249 150 213 186
215 185 199 201
208 189 207 190
2,506 1,868 2,235 2,139
Total
397
394
401
401
399
402
398
386
399
400
397
4,374
TABLE 3. Serum zinc levels in rural and urban areas and in boys and girls % (no.) of cases with Zn ≥ 10 µmol/L
% (no.) of cases with Zn < 10 and ≥ 7.7 µmol/L
Group
N
Mean Zn level (µmol/L)
% (no.) of cases with Zn < 7.7 µmol/L
Rural Urban Boys Girls
1,868 2,506 2,235 2,139
12.26 ± 3.67 12.68 ± 3.94 12.54 ± 3.97 12.45 ± 3.84
77.9 (1,455) 82.2 (2,060) 81.1 (1,813) 79.5 (1,702)
18.4 (343) 15.4 (387) 16.1 (360) 17.3 (370)
3.7 (70) 2.3 (59) 2.8 (62) 3.1 (67)
Total
4,374
12.50 ± 2.30
80.3 (3,514)
16.7 (730)
2.9 (129)
TABLE 4. Prevalence of zinc deficiency, (serum zinc levels < 10 µmol/L) in rural and urban areas and in boys and girls Group
Region 1
Region 2
Region 3
Region 4
Region 5
Region 6
Region 7
Region 8
Region 9
Region 10
Region 11
Urban Rural Boys Girls
15.2 12.2 13.8 13.4
20.4* 28.9 23.3 25.2
16.6 18.1 16.3 18.5
20.0 17.3 17.7 20.2
28.4 27.4 27.4 28.2
20.2 23.1 19.9 22.4
9.9* 18.7 11.9 14.7
13.9* 23.7 14.2 16.3
22.9* 28.7 25.3 24.7
19.5 24.4 20.6 22.9
11.5* 23.8 16.4 18.4
Total (not weighted)
13.6
24.1
17.5
18.9
27.8
21.1
13.3
15.3
25.1
21.7
17.4
* The prevalence of zinc deficiency was significantly higher in rural compared to urban areas (p < .05)
233
Zinc status of Iranian children
.ATIONAL
2EGION
FIG. 1. Weighted prevalences of zinc deficiency in each region
and girls in any of the 11 regions (table 4). The weighted prevalence of zinc deficiency in each region was calculated based on the percentages of urban and rural residents in each region. National rates were also calculated by taking into account the percentages of urban and rural residents in each region compared with the national population (figs. 1 and 2).
Discussion and conclusions The information presented in figure 2 shows that 19.3% of preschool Iranian children had serum zinc levels lower than 10 µmol/L. The prevalence of low serum zinc levels was significantly higher in rural than in urban children (22.5% and 17.2%, respectively). It should be noted that children with acute inflammatory symptoms were not excluded from the study, and laboratory tests for inflammation were not performed in this study. National data from Mexico showed that 21.4% (95% CI, 15.6%–27.1%) of all children 5 to 6 years of age were zinc deficient, with the prevalence higher in rural areas (34.3%) than in urban areas (13.9%), results very similar to those of our study
5RBAN
2URAL
.ATIONAL RATE
"OYS
'IRLS
FIG. 2. Weighted prevalences of zinc deficiency in boys and girls and in urban and rural areas
[16]. A survey conducted in Saudi Arabia found a 22% prevalence of low serum zinc levels (< 10 µmol/L) in urban preschoolers [17]. Holt et al. reported a 50% prevalence of hypozincemia in 5- to 15-year-old Australian schoolchildren [18]. Bahl et al. studied zinc plasma levels as a predictor of respiratory and diarrheal diseases in the children of poor urban areas of India [19]. Thirty-two percent of the children had serum zinc levels lower than 8.4 µmol/L, a much higher percentage than that in the current study (5.4%). Severe zinc deficiency was found in 2.9% of children (2.3% of urban and 3.7% of rural children); this prevalence is close to that found by Alshatawi [17] in preschoolers (2.3%) but is less than that reported by Al-Timimi et al. [20] in 2- to 10-year old Iraqi children (7.7%). In the present study in Iran, 46.6% of the children had serum zinc levels less than 12.2 µmol/L. This prevalence is lower than those reported by Alshatawi [17] (54.4%), Torrejon et al. [21] (79.7%), and Al-Timimi et al. [20] (54.8%). Moreover, although no comprehensive survey of zinc deficiency in Iran has yet been performed, our results show that the problem in preschool children is worrisome and needs prompt action in all regions. Compared with other micronutrient deficiencies in the same age group as described in a recent Iranian government report [22], zinc deficiency is more prevalent. The prevalence of zinc deficiency increases with age from 10.8% in 15- to 24-month-old children [22] to 19.3% in the preschool age group. This indicates that in order to reduce the prevalence of zinc deficiency in preschool children, it is necessary to perform certain preventive measures in younger children. The intake status of zinc-containing foods or zinc absorption inhibitors was not assessed in this study. Taking into consideration other studies on the intake status of these foods (as a direct cause of zinc deficiency), together with the results of studies on the prevalence of poverty (as the major cause of nutrition insecurity and thus of zinc deficiency), in addition to
234
the results obtained from this survey would be very helpful for outlining and designing sustainable strategies to alleviate zinc deficiency in this age group. The comprehensive food-consumption study of Iranian families carried out in 2000 showed that proteins contribute only about 10% of daily energy needs. Furthermore, the per capita consumption of meat and protein products, the main food sources of zinc, and also of legumes, another major source of zinc, is not sufficient [23]. Bread is the staple food in Iranian families, with a daily per capita intake of 320 g, providing up to onethird of energy needs in the population [23]. Unfortunately, the phytate content of traditional Iranian bread is high [24], resulting in low bioavailability of zinc. Phytic acid has been shown to be an inhibitor of zinc absorption in human and animal studies. This is true especially when the molar ratio of phytate to zinc is over 15. At this level an insoluble complex is formed in the gastrointestinal tract, resulting in low absorption of zinc [25, 26]. One of the important measures in Iran to overcome zinc deficiency will be improvement of the quality of bread. According to the food-consumption survey, the per capita intake of meat and protein products is lower in
S. M. Safavi et al.
rural than in urban areas [23]. This may partly explain the higher prevalence of zinc deficiency in rural areas. Other surveys show that the per capita income of rural families is lower than that of urban families [27], which might be a reason for the lower consumption of meat by rural families. The long-term sustainable strategy to decrease the prevalence of zinc deficiency will involve economic development programs. But short- and medium-term interventions, such as supplementation, fortification, nutritional behavior changes that target increases in per capita intake of high-protein foods and reductions in intakes of foods containing inhibitors of zinc absorption, and self-sufficiency programs at the local levels, may also be considered to alleviate the problem. One of the programs that the Nutrition Department of the Ministry of Health and Medical Education of Iran has designed to address the control of zinc deficiency is fortification of flour with multiple micronutrients, including zinc. This program is being carried out as a pilot project and will be scaled up to the national level if proved to be efficient. A supplementation program for preschool children, at least on a regional scale, is worth considering.
References 1. Mahan LK, Escott-Stump S. Krause’s food, nutrition and diet therapy. 11th ed. Philadelphia, PA, USA: Health Sciences Rights Department, 2000:143–7. 2. Reddy V. Importance of zinc for human health. (Part 2 of a 3-part series.). Consequences and causes of zinc deficiency. International Association of Infant Food Manufacturers, February 2005. Available at: http://www. ifm.net/industry/zinc2.htm. Accessed 15 March 2007.. 3. Ortega RM, Quintas ME, Andres P, Martinez RM, Lopez-Sobaler AM, Requejo AM. Zinc status of a group of pregnant Spanish women: Effects on anthropometric data and Apgar score of neonates. Nutr Res 1999;19:1423–8. 4. Salgueiro MJ, Zubillaga MB, Lysionek AE, Caro RA, Weill R, Boccio JR. The role of zinc in the growth and development of children. Nutrition 2002; 18:510–9. 5. Ploysangam A, Falciglia GA, Brehm BJ. Effect of marginal zinc deficiency on human growth and development. J Trop Pediatr 1997;43:192–8. 6. Sandstead HH. Zinc: Essentiality for brain development and function. Nutr Rev 1985;43:129–37. 7. Golub MS, Keen CL, Gershwin ME, Hendrickx AG. Developmental zinc deficiency and behavior. J Nutr 1995;125(8 suppl):2263S–71S. 8. World Health Organization Report (2002) IBLF dialogue with WHO London, October 28, 2002. Available at: http://www.who.int/dietphysicalactivity/media/en/ gsdoc_principles_charts.pdf. Accessed 15 March 2007. 9. Chen XC, Yin TA, He JS, Ma QY, Han ZM, Li LX. Low levels of zinc in hair and blood, pica, anorexia, and poor growth in Chinese preschool children. Am J Clin Nutr
1985;42:694–700. 10. Rosado JL. Zinc deficiency and its functional implications (in Spanish). Salud Publica Mex 1998;40:181–8. 11. Caulfield LE, Richard SA, Black RE. Undernutrition as an underlying cause of malaria morbidity and mortality in children less than five years old. Am J Trop Med Hyg 2004; 71: 55–63. 12. Iran Ministry of Health and Medical Education, Nutrition Department. Final report of the Anthropometric Nutritional Indicators Survey, Tehran: Senobar Publications, 1998 . 13. Hotz C, Peerson JM, Brown KH. Suggested lower cutoffs of serum zinc concentrations for assessing zinc status: Reanalysis of the second National Health and Nutrition Examination Survey data (1976–1980). Am J Clin Nutr 2003;78:756–64. 14. Prasad AS. Clinical manifestations of zinc deficiency. Annu Rev Nutr 1985;5:341–63. 15. Iran National Statistics Center. The 5th national population census: Population characteristics of provinces. Tehran: National Statistics Center, 1996; 3: 789–861. 16. Villalpando S, Garcia-Guerra A, Ramirez-Silva CI, Mejia-Rodriguez F, Matute G, Shamah-Levy T, Rivera JA. Iron, zinc and iodide status in Mexican children under 12 years and women 12–49 years of age. A probabilistic national survey. Salud Publica Mex 2003;45 (suppl 4):S520–9. 17. Alshatawi AA. Zinc nutritional status of preschool children in Riyadh city. Pakistan J Nutr 2006;5:429–31. 18. Holt AB, Spargo RM, Iveson JB, Faulkner GS, Cheek DB. Serum and plasma zinc, copper and iron concentrations
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Zinc status of Iranian children
19.
20. 21.
22.
23.
in Aboriginal communities of North Western Australia. Am J Clin Nutr 1980;33:119–32. Bahl R, Bhandari N, Hambidge KM, Bhan MK. Plasma zinc as a predictor of diarrheal and respiratory morbidity in children in an urban slum. Am J Clin Nutr 1998;68(2 suppl):414S–7S. Al-Timimi DJ, Al-Sharbatti SS, Al-Najjar F. Zinc deficiency among a healthy population in Baghdad, Iraq. Saudi Med J 2005;26:1777–81. Torrejon CS, Castillo-Duran C, Hertrampf ED, Ruz M. Zinc and iron nutrition in Chilean children fed fortified milk provided by the Complementary National Food Program. Nutrition 2004;20:177–80. Iran Ministry of Health and Medical Education, Nutrition Department. Final report of the National Integrated Micronutrients Survey. Tehran: Amirkabir Publications, 2001:325–78. National Nutrition and Food Technology Research
24. 25. 26.
27.
Institute. National Comprehensive Food Consumption Survey (2000–2002). 1st ed. Tehran: Research and Education Management and Planning Higher Council, 2004: 29–40. Reinhold JG. High phytate content of rural Iranian bread: A possible cause of human zinc deficiency. Am J Clin Nutr 1971;24:1204–6. Oberleas D, Harland BF. Phytate content of foods: Effect on dietary zinc bioavailability. J Am Diet Assoc 1981;79:433–6. Bindra GS, Gibson RS, Thompson LU. Phytate:Calcium/ zinc ratios in Asian immigrant lacto-ovo vegetarian diets and their relationship to zinc nutriture. Nutr Res 1986;6:475–83. Ministry of Social Welfare. Poverty and inequality in Iran: Policy making to reduce poverty and improve social welfare. Tehran: Ministry of Social Welfare, 2005:5–6.
