| | The Prevalence of Low Serum Zinc and Copper Levels and Dietary Habits Associated with Serum Zinc and Copper in 12- to 36-Month-Old Children from Low-Income Families at Risk for Iron DeficiencyAbstract ObjectiveIron and zinc share common food sources, and children at risk of iron deficiency may also develop zinc deficiency. We determined the prevalence of zinc and copper deficiency and examined factors associated with serum zinc and copper in young children from low-income families at risk of iron deficiency. DesignA cross-sectional study design was used to assess serum zinc and copper, along with an interview-assisted survey to assess factors associated with serum zinc and copper in a convenience sample. Subjects/settingParticipants were 435 children aged 12 to 36 months recruited from select clinics of the Special Supplemental Nutrition Program for Women, Infants, and Children in Contra Costa and Tulare Counties, California. Statistical analyses performedFrequencies were used to report prevalence. Multiple linear regressions were conducted to examine factors associated with serum zinc and copper, controlling for age, sex, and ethnicity. ResultsThe prevalence of low serum zinc level (<70 μg/dL [<10.7 μmol/L]) was 42.8%, and low serum copper level (<90 μg/dL [<14.2 μmol/L]) was <1%. Mean±standard deviation of serum copper was 150±22 μg/dL (23.6±3.5 μmol/L) and 140±24 μg/dL (22.1±3.8 μmol/L) for anemic and non-anemic children, respectively (t test, P=0.026). In multiple linear regression consumption of sweetened beverages was negatively associated with serum zinc level, and consumption of >15 g/day meat was positively associated with serum zinc level, whereas current consumption of breast milk and >15 g/day beans were positively associated with serum copper level. ConclusionsThe prevalence of low serum zinc concentration in the sample was high, and warrants further investigation amongst vulnerable populations. Iron deficiency is recognized and monitored in the United States, and remains relatively high among low-income, preschool-aged children. The objective of Healthy People 2010, a health promotion and disease prevention agenda by the US Department of Health and Human Services, is to reduce iron deficiency in 1- to 2-year-old children to 5% (the 1988-1994 baseline prevalence is 9%) and in 3- to 4-year-old children to 1% (the 1988-1994 baseline prevalence is 4%) in all children by 2010 (1). However, the prevalence of iron deficiency was 17% for 1- to 2-year-olds and 6% for 3- to 4-year-olds among Mexican-American toddlers, and 12% for 1- to 2-year-olds and 5% for 3- to 4-year-olds in low-income (≤130% of poverty threshold) households (1). Although not always recognized as a common nutritional concern, crude estimates rank zinc deficiency second to vitamin A deficiency, and above iron deficiency amongst causes of undernutrition (2, 3). An estimated one third to one half of the world’s population is at risk of low dietary intake of absorbable zinc that can lead to a primary deficiency, because many plant-based diets may have little zinc content and poor bioavailability (4). Diets of young children may or may not provide adequate intakes of zinc or iron (5, 6), and low-income children may be at greater risk of dietary inadequacy (7). In a recent study conducted in Oklahoma, 21% of 3- to 5-year-old children from low-income families had low plasma zinc levels (≤72.0 μg/dL [≤11 μmol/L]) (8). Toddlers may be at greater risk of zinc deficiency than older children due to greater growth velocities. Nearly 34% of children aged 6 to 35 months had low serum zinc levels (<65 μg/dL [<9.9 μmol/L]) in the Mexican National Nutrition Survey of 1999 (9). This is of concern because consequences of zinc deficiency include growth faltering (10), increased risk of infection (11), decreased activity, and delayed motor development (12). Whereas intervention programs are in effect to control iron deficiency, both zinc and iron share common food sources, and inadequate intakes of zinc or iron in young children can lead to deficiency. Copper plays a role in iron metabolism through ceruloplasmin, a copper-dependent enzyme that oxidizes ferrous iron to ferric iron before binding with transferrin for plasma transport (13). The function of copper in oxidizing iron before binding with transferrin is critical in allowing iron to be transported to body tissues; thus, iron uptake by bone marrow tissue allows for its incorporation into hemoglobin synthesis during erythropoiesis. Children with iron deficiency anemia have been characterized with higher serum copper levels (and lower serum zinc concentrations) (14). Early copper deficiency coinciding with iron deficiency is characterized by hypochromia (15, 16). Although copper deficiency is rare, it has been reported in preterm infants (17, 18), infants fed cow’s milk (19, 20), and in infants recovering from malnutrition accompanied by diarrhea (21). Anemia due to copper deficiency (without iron deficiency) is responsive to copper supplementation alone (16). However, lower copper concentrations may coincide with higher dietary intakes of iron in infants and children (22, 23). Federal and state authorities have targeted low-income populations to reduce the prevalence of anemia and iron deficiency in at-risk children through programs such as the Special Supplemental Nutrition Program for Women, Infants, and Children (WIC). Approximately 45% of low-income children participate in WIC (24), which provides supplemental foods during critical times of growth and development. Based on the rationale that concurrent zinc and iron deficiency may occur in at-risk children we hypothesized that zinc deficiency would be prevalent among children aged 12 to 36 months. Furthermore we hypothesized that anemia, low iron stores, or iron deficiency would be associated with serum zinc and copper levels. Methods  Study Population Participants, 12- to 36-month-old toddlers, were recruited from California WIC waiting rooms between August 2000 and June 2002. The WIC clinics were located in Richmond (Contra Costa County), and Earlimart and Dinuba (Tulare County). Richmond is an urban community with a population of approximately 99,216, whereas Earlimart and Dinuba have populations of 5,881 and 16,849, respectively (25). Hispanics and Latinos compose approximately 27%, 75%, and 88% of the populations in Richmond, Dinuba, and Earlimart, respectively (26). Median household income is approximately $44,000, $33,000, and $21,000, with 13%, 21%, and 38% of families falling below the poverty level in Richmond, Dinuba, and Earlimart, respectively (26). The Richmond clinic has approximately 6,800 WIC participants, Earlimart 1,600 WIC participants, and Dinuba 3,800 WIC participants. Trained bilingual (English/Spanish), bicultural interviewers (one per county) approached all women in the WIC waiting rooms to recruit subjects for the study. Interviewers were instructed to introduce themselves, briefly describe the study, and ask women if they had a child between the ages of 12 and 36 months. Men were excluded because the interview included questions pertaining to pregnancy. The interviewers asked if the mothers would like to participate in the study. Approximately 673 women with children aged 12 to 36 months were approached, 498 gave consent to participate in the study (approximately 74% of those who were eligible). To be eligible for the study, a mother could not have received information about iron deficiency anemia from a doctor or nurse because this may have influenced feeding behaviors. Written informed consent was obtained from mothers before participation in the study. The University of California at Davis Institutional Review Board approved this study protocol. Laboratory Analysis Venous blood samples were collected from the toddlers by phlebotomists in laboratories adjoining the respective WIC sites from 9 am to 7 pm. Subjects were not required to fast. Serum samples were analyzed for ferritin (immunoradiometric assay, Coat-A-Count Ferritin, Diagnostic Products, Inc, Los Angeles, CA), transferrin receptor (human transferrin receptor immunoassay kit, Ramco, Houston, TX), transferrin (nephelometric assay, Beckman Coulter reagents, Brea, CA), iron, zinc, copper (27) (atomic absorption spectrophotometry, PerkinElmer 300 instrument, Boston, MA), and C-reactive protein (radial immunodiffusion, Nanorid, The Binding Site, Birmingham, UK). Transferrin saturation was computed using serum transferrin and serum iron. Total iron binding capacity was computed as serum transferrin/0.68 (28). Transferrin saturation percent was subsequently computed by the formula serum iron/total iron binding capacity)×100 (29). Hemoglobin was determined using automated analyzers (Richmond: Coulter Max M, Fullerton, CA; Earlimart: Abbott Cell-Dyn 4000, Abbott Park, IL; and Dinuba: Abbott Cell-Dyn 3200, Abbott Park, IL). Anemia was defined as hemoglobin <11.0 g/dL (<110 g/L) for 12- to <24-month-olds, or hemoglobin <11.1 g/dL (<111 g/L) for 24- to 36-month-olds (30, 31). Low iron stores was defined as ferritin ≤8.7 ng/mL (≤19.5 pmol/L). Iron deficiency was defined using a multiple indicator model, two or more out of three abnormal values for ferritin ≤8.7 μg/L, transferrin receptors ≥8.4 μg/mL, and transferrin saturation ≤13.2% (32). Low serum zinc was defined as <70 μg/dL (<10.7 μmol/L) (33, 34). Low serum copper was defined as <90 μg/dL (<14.2 μmol/L) (35). Further details on assessment of iron status can be obtained from a previously published study (32). Questionnaire A risk factor questionnaire was developed in English and Spanish to collect demographic information; data on acute illness (eg, ear infection, fever, respiratory tract infection, vomiting, and diarrhea) at the time of study or in the previous month; maternal iron status; pregnancy history; and dietary information, including infant feeding history and timing of introduction of solid foods. Select dietary variables were included in the risk factor questionnaire based on a detailed dietary analysis in a group of children similar to the current sample (36). Previously, this questionnaire was validated in a low-income sample of children aged 1 to 4 years; energy and nutrient intakes were determined by comparing a food frequency questionnaire with multiple 24-hour recalls. Pearson’s correlations between estimates of nutrient intake obtained from 24-hour recalls and the food frequency questionnaire ranged from 0.40 to 0.47 for dietary iron, copper, and zinc in low-income children with nearly 80% of the sample being Hispanic (36). Intakes of ready-to-eat cereals, beverages, commercially prepared infant foods, meat, poultry, fish, and legumes were determined using typical portion sizes and frequency of intake within the past 30 days. Measuring cups, toddler-cups, bottles, commercially prepared infant foods in jars, and food models were used to assist in estimating portion sizes. In addition to current beverage intake, breastfeeding initiation and duration, and consumption of commercial infant formulas were also determined. The questionnaire also addressed the frequency and amount of intake from nonfood substances such as clay, dirt, ice, paper, wax, and laundry starch by the mother during her pregnancy or by the child. Four additional questions addressed maternal and child participation in WIC, including current maternal WIC participation, maternal WIC participation during pregnancy, child ever participating in WIC, and child currently participating in WIC. Nutrition scientists, health educators, and University of California Cooperative Extension advisors reviewed the risk factor instrument for content validity. The instrument was then pilot tested for clarity in a sample from the intended population before use in the study. Revisions were made accordingly. Recruitment for testing the instrument took place at the County of Sacramento, Department of Health and Human Services, WIC Clinic. Statistical Analysis Frequencies were used for prevalence data. To compare proportions, χ2 test was used and t tests were used to compare means to examine risk factors associated with serum zinc or serum copper. Multiple linear regression models (stepwise) were developed to evaluate risk factors associated with serum zinc or serum copper. Only subjects with values for all variables were included in the analyses. The demographic variables age, sex, and ethnicity were forced into these stepwise models. Only serum that showed no evidence of hemolysis or elevated C-reactive protein values (≤10 mg/L) were retained for all statistical analyses because zinc and copper status may be altered during infection (37). Statistical significance was defined as P≤0.05. All statistical analyses were performed using SPSS software (version 10.0, 2000, SPSS Inc, Chicago, IL). Results In total, 498 subjects were recruited for the study (only one child excluded because the mother received information about iron deficiency anemia from a doctor or nurse). There were 432 children with successful blood draws. Thirty-three children had elevated serum C-reactive protein levels, 32 children had serum samples with evidence of hemolysis, and three children had both. The number of children with serum zinc and serum copper values were 348 and 347, respectively. The majority of children were Latino or Hispanic (93.3%), followed by African Americans (3.5%), non-Hispanic whites (1.2%), multiethnic (0.7%), Asians or Pacific Islanders (0.5%), Native Americans (0.5%), and unknown (0.5%). The average age was 23.2±6.7 months (range 12.0 to 35.8 months). The sample was composed of 52.3% boys. Forty-two percent of children lived in urban locations (32). Serum zinc levels ranged from 46 to 171 μg/dL (7.1 to 26.2 μmol/L), with a mean of 74±14 μg/dL (11.3±2.2 μmol/L). Mean serum zinc level was significantly higher in morning draws (9:00 am to 11:59 am) than afternoon/evening draws (12:00 pm to 7:00 pm), 78±15 μg/dL (11.8±2.3 μmol/L) and 70±13 μg/dL (10.7±1.9 μmol/L), respectively (t test, P<0.001). Mean serum zinc concentration was not significantly different between anemic and nonanemic children, between children with low iron stores and adequate iron stores, or between iron-deficient and iron-sufficient children (Table 1). Likewise, serum zinc concentration was not significantly different between boys and girls; between children with or without an ear infection, a fever, a respiratory tract infection, vomiting, or diarrhea; nor significantly related to the number of hours the child last ate before sample collection. All analyses excluded children with elevated C-reactive protein levels; however, it should be noted that mean serum zinc was 66±12 μg/dL (10.1±1.8 μmol/L) for children with elevated C-reactive protein levels, and 73±14 μg/dL (11.2±2.2 μmol/L) for children with normal levels of C-reactive protein (t test, P=0.005). When low serum zinc level was defined as <70 μg/dL (<10.7 μmol/L), 42.8% of children had low values. Alternative cut-offs for low serum zinc levels include <65 μg/dL (<9.9 μmol/L) (9) or <81 μg/dL (<12.3 μmol/L) (38), with 27.3% and 74.0% of the sample having low values, respectively. The prevalence of low serum copper concentration was 0.8% (<90 μg/dL [<14.2 μmol/L]). Serum copper level ranged from 85 to 228 μg/dL (13.3 to 35.8 μmol/L), with a mean of 141±24 μg/dL (22.2±3.8 μmol/L). Mean serum copper level was significantly higher in anemic children. Mean serum copper concentration was not significantly different between children with low iron stores and adequate iron stores, nor between iron-deficient and iron-sufficient children (Table 1). Table 2, Table 3 present factors associated with serum zinc and copper levels in multivariate analysis controlling for age, sex, and ethnicity. The predictive value for the regression models were 0.051 and 0.049 for serum zinc and copper, respectively. Discussion The prevalence of low serum zinc level (<70 μg/dL [<10.7 μmol/L]) was high in this population, 42.8% for children aged 12 to 36 months. Although this cut-off value is typically used in the literature, it is derived from data from the Second National Health and Nutrition Examination Survey and may not be appropriate for the age of children used in our study (34). Based on the work of Villalpando and colleagues (9), we found a 27.3% prevalence of low zinc concentration, using a lower cut-off of <65 μg/dL (<9.9 μmol/L). When using a cut-off of <81 μg/dL (<12.3 μmol/L) for serum zinc as suggested by Torrejon and colleagues (38), we observed a 74% prevalence of low serum zinc concentration. Regardless of the cut-off used the prevalence of low serum zinc concentration in our convenience sample remains high. Approximately 16% of children in this sample were iron-deficient (32) and <1% of these children had low copper concentrations (<90 μg/dL [<14.2 μmol/L]). Given that anemic children had significantly higher mean serum copper concentrations than non-anemic children, the relationship between anemia and serum copper level is likely due to poor iron status rather than poor copper status. Between 60% and 95% of serum copper is found in ceruloplasmin (39), and changes in serum copper concentration may reflect the ceruloplasmin concentration (39). It is reasonable to suggest that the higher mean copper concentration in anemic children is due to increased circulating ceruloplasmin, which may be a stress response occurring as a result of inadequate hemoglobin synthesis. It should be appreciated that increased iron intake has been shown to interfere with zinc absorption, and poor zinc nutriture may be exacerbated with supplemental iron (40). Currently, WIC offers food vouchers designed to increase nutrient intakes of iron through ready-to-eat cereals and beans (41), both of which are sources of nonheme iron. A study conducted in the Jeddah area of Saudi Arabia found that low serum zinc levels in children aged 12 to 36 months were associated with inadequate dietary intakes of zinc, and diarrhea (42). Although our study did not include a detailed analysis of dietary zinc intake, data from the Third National Health and Nutrition Examination Survey showed a mean intake of 6.4±0.07 mg/day in Mexican-American children aged 1 to 3 years, excluding infants who were breastfed (6). Given this level of dietary intake, we did not anticipate such a high prevalence of low serum zinc. It is interesting to note that 43.4% (n=355) of the mothers said that meat and hamburgers are considered junk food in an open-ended question in the survey. Meat is a good source of zinc (43), so such attitudes may result in providing less zinc-rich foods to children. This possibility requires further investigation. In our study, 39.3% and 54.9% of children aged 12 to 24 and 24 to 36 months consumed sweetened beverages (eg, fruit drinks and sodas), respectively. Similarly, the Feeding Infants and Toddlers Study reported that 29.1% to 42.6% of children (aged 12 to 24 months) consumed fruit drinks (includes beverages with <100% juice and often with added sweeteners) and 4.5% to 11.9% of children (aged 12 to 24 months) consumed carbonated beverages (eg, mineral water and soda) (44). This is of concern because these types of beverages may displace more nutrient-dense foods, possibly decreasing the zinc and iron content of their diet. However, sweetened beverage intake was not associated with anemia or iron deficiency (32). Current breastfeeding and bean intake >15 g/day were positively associated with serum copper concentration. This is not surprising because children not currently breastfed in our study were largely consuming cow’s milk, which is low in copper. Copper in breast milk appears to be well absorbed (45) and copper concentration in breast milk is independent of maternal mineral status (46). The main dietary sources of copper in US diets are meat, nuts, beans/peas, and main dishes (47). We have not found other studies reporting a positive association of bean intake with serum copper levels. However, not all dietary factors affecting zinc and copper nutriture were assessed in the modified food frequency questionnaire used in the study (eg, all sources of phytates and ascorbic acid were not documented) (45, 48). There were several limitations in this study. Serum copper is a good indicator of copper deficiency; however, neither serum zinc nor copper reflect marginal status and may not reflect dietary intakes (39, 49). The low R2 values (approximately 5%) only explain a small portion of the variation in serum zinc and copper. Random measurement errors may also have contributed to the low R2 values. Temporal relationships between exposures and the outcome variables of interest cannot be established in cross-sectional studies; thus, causality cannot be determined. Our results are not generalizable to larger population because this study is based on a convenience sample of children. Despite these limitations, this study demonstrates the importance of identifying zinc status in young children at risk of iron deficiency. Conclusions Results from our study demonstrate that the prevalence of low serum zinc level (<70 μg/dL [<10.7 μmol/L]) was high, and the prevalence of low serum copper level (<90 μg/dL [<14.2 μmol/L]) was low in a sample of low-income families. Although mean serum copper concentration was higher in anemic children, the difference was relatively small. Dietary factors explained little of the variation in serum zinc and copper, approximately 5%. Due to the unexpected high prevalence of low serum zinc in the convenience sample of children aged 12 to 36 months, efforts should focus on determining serum zinc levels in a representative sample of young children regardless of iron status. This abstract was originally presented at the Experimental Biology Annual Meeting 2006 and published in FASEB J. 2006;20:A140.7. This research was supported in part by the Food Stamp Nutrition Education Program, University of California, Davis, CA, and by a small grant from the US Department of Agriculture-Economic Research Service (grant no. 43-3AEM-8-800TZ) and by the University of California-ANR Workgroup, Anemia Prevention. The authors thank the following members of the University of California, Davis: Clinical Nutrition Research Unit and Shannon Kelleher (Department of Nutrition), for laboratory analysis; and Andrea Bersamin and Nadine Kirkpatrick (Department of Nutrition) for data entry. The authors also thank Myriam Grajales-Hall of UC-ANR Spanish Broadcast and Media Services, for translating the questionnaire to Spanish; Marianna Castro and Francisca Ramos of Cooperative Extension, University of California, for data collection; staff from Tom Powers, Richmond Health Center Clinical Laboratory, Richmond, CA; United Health Centers of the San Joaquin Valley, Inc, Clinical Laboratory, Earlimart, CA; and County of Tulare, Health and Human Services Agency, Dinuba Health Care Center Clinical Laboratory, Dinuba, CA, for sample collection. References 1. 1US Department of Health and Human Services. Tracking Healthy People 2010. Washington, DC: US Government Printing Office; 2000;. 2. 2Black RE. Micronutrient deficiencies. Global forum for health research 1999. Available at: http://www.globalforumhealth.org/pages/index.asp. Accessed April 15, 2005. 3. 3Prasad AS. Zinc deficiency. BMJ. 2003;326:409–410. 4. 4Brown KH, Wuehler SE, Peerson JM. The importance of zinc in human nutrition and estimation of the global prevalence of zinc deficiency. Food Nutr Bull. 2001;22:113–125. 5. 5Devaney B, Ziegler P, Pac S, Karwe V, Barr SI. Nutrient intakes of infants and toddlers. J Am Diet Assoc. 2004;104(suppl 1):S14–S21. 6. 6Briefel RR, Bialostosky K, Kennedy-Stephenson J, McDowell MA, Ervin RB, Wright JD. Zinc intake of the US population: Findings from the third National Health and Nutrition Examination Survey, 1988-1994. J Nutr. 2000;130(suppl 5):1367S–1373S. MEDLINE 7. 7Rose D, Habicht JP, Devaney B. Household participation in the Food Stamp and WIC programs increases the nutrient intakes of preschool children. J Nutr. 1998;128:548–555. MEDLINE 8. 8Droke EA, Kennedy TS, Hubbs-Tait L. Potential for misclassification of micronutrient status in children participating in a Head Start program. J Am Diet Assoc. 2006;106:376–382. Abstract | Full Text |
Full-Text PDF (109 KB)
|
CrossRef
9. 9Villalpando S, Garcia-Guerra A, Ramirez-Silva CI, Mejia-Rodriguez F, Matute G, Shamah-Levy T, et al. 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–S529. 10. 10Brown KH, Peerson JM, Rivera J, Allen LH. Effect of supplemental zinc on the growth and serum zinc concentrations of prepubertal children: A meta-analysis of randomized controlled trials. Am J Clin Nutr. 2002;75:1062–1071. MEDLINE 11. 11Shankar AH, Prasad AS. Zinc and immune function: The biological basis of altered resistance to infection. Am J Clin Nutr. 1998;68(suppl 2):447S–463S. MEDLINE 12. 12Black MM. Micronutrient deficiencies and cognitive functioning. J Nutr. 2003;133(suppl 2):3927S–3931S. MEDLINE 13. 13Linder MC, Hazegh-Azam M. Copper biochemistry and molecular biology. Am J Clin Nutr. 1996;63(suppl):797S–811S. MEDLINE 14. 14Ece A, Uyanik BS, Iscan A, Ertan P, Yigitoglu MR. Increased serum copper and decreased serum zinc levels in children with iron deficiency anemia. Biol Trace Elem Res. 1997;59:31–39. MEDLINE |
CrossRef
15. 15Fujita M, Itakura T, Takagi Y, Okada A. Copper deficiency during total parenteral nutrition: Clinical analysis of three cases. J Parenter Enteral Nutr. 1989;13:421–425. 16. 16Graham GG, Cordano A. Copper deficiency in human subjects. In: Prasad AS, Oberleas D editor. Trace Elements in Human Health and Disease. New York, NY: Academic Press; 1976;p. 363–372. 17. 17L’Abbe MR, Friel JK. Copper status of very-low-birth-weight infants during the first 12 months of infancy. Pediatr Res. 1992;32:183–188. MEDLINE 18. 18McMaster D, Lappin TR, Halliday HL, Patterson CC. Serum copper and zinc levels in the preterm infant (A longitudinal study of the first year of life). Biol Neonate. 1983;44:108–113. MEDLINE 19. 19Cordano A, Baertl JM, Graham GG. Copper deficiency in infancy. Pediatrics. 1964;34:324–336. 20. 20Levy Y, Zeharia A, Grunebaum M, Nitzan M, Steinherz R. Copper deficiency in infants fed cow milk. J Pediatr. 1985;106:786–788.
Full-Text PDF (602 KB)
|
CrossRef
21. 21Shaw JC. Copper deficiency in term and preterm infants. In: Fomon SJ, Zlotkin S editor. Nutritional Anemias. New York, NY: Vevey/Raven Press; 1992;p. 105–117. 22. 22Lönnerdal B, Hernell O. Iron, zinc, copper, and selenium status of breast-fed infants and infants fed trace element fortified milk-based infant formula. Acta Paediatr. 1994;83:367–373. MEDLINE |
CrossRef
23. 23Morais MB, Fisberg M, Suzuki HU, Amancio OM, Machado NL. Effects of oral iron therapy on serum copper and serum ceruloplasmin in children. J Trop Pediatr. 1994;40:51–52. MEDLINE 24. 24US Department of Agriculture, Food and Nutrition Service. WIC program coverage: How many eligible individuals participated in the Special Supplemental Nutrition Program for Women, Infants, and Children (WIC): 1994 to 2003? Available at: http://www.fns.usda.gov/oane/MENU/Published/WIC/FILES/WICEligibles.pdf. Accessed August 16, 2007. 25. 25US Census Bureau. Table 7. California incorporated place population estimates, sorted alphabetically: April 1, 2000 to July 1, 2002. Available at: http://www.census.gov/popest/archives/2000s/vintage_2002/SUB-EST2002/SUB-EST2002-07-06.pdf. Accessed August 16, 2007. 26. 26US Census Bureau. American FactFinder. Available at: http://factfinder.census.gov. Accessed August 16, 2007. 27. 27Clegg MS, Keen CL, Lonnerdal B, Hurley LS. Influence of ashing techniques on the analysis of trace elements in animal tissue (I. Wet ashing). Biol Trace Elem Res. 1981;3:107–115.
CrossRef
28. 28Tietz NW. Fundamentals of clinical chemistry. 3rd ed.. Philadelphia, PA: WB Saunders; 1987;. 29. 29Tietz NW. Clinical Guide to Laboratory Tests. 3rd ed.. Philadelphia, PA: WB Saunders; 1995;. 30. 30Centers for Disease Control and Prevention (Recommendations to prevent and control iron deficiency in the United States). MMWR Recomm Rep. 1998;47:1–29. MEDLINE 31. 31Iron Deficiency Anaemia (Assessment, Prevention, and Control). A Guide for Programme Managers. Geneva, Switzerland: World Health Organization; 2001;. 32. 32Schneider JM, Fujii ML, Lamp CL, Lönnerdal B, Dewey KG, Zidenberg-Cherr S. Anemia, iron deficiency, and iron deficiency anemia in 12-36-mo-old children from low-income families. Am J Clin Nutr. 2005;82:1269–1275. MEDLINE 33. 33In: Hotz C, Brown KH editor. Assessment of the Risk of Zinc Deficiency in Populations and Options for its Control. 1st ed.. Boston, MA: International Nutrition Foundation for the United Nations University; 2004;. 34. 34Hotz 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;78:756–764. MEDLINE 35. 35Cordano A. Clinical manifestations of nutritional copper deficiency in infants and children. Am J Clin Nutr. 1998;67(suppl 5):1012S–1016S. MEDLINE 36. 36Fechner KD. Evaluation of Nutrient Intake, Food Group Consumption, Dietary Patterns, and Trace Mineral Status of Young Children from Differing Socioeconomic Backgrounds [doctoral thesis Ph D]. Davis, CA: University of California Davis; 1998;. 37. 37Brown KH, Lanata CF, Yuen ML, Peerson JM, Butron B, Lonnerdal B. Potential magnitude of the misclassification of a population’s trace element status due to infection: Example from a survey of young Peruvian children. Am J Clin Nutr. 1993;58:549–554. MEDLINE 38. 38Torrejon 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;20:177–180. Abstract | Full Text |
Full-Text PDF (79 KB)
|
CrossRef
39. 39Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. Washington, DC: National Academies Press; 2001;. 40. 40Abrams SA. New approaches to iron fortification: Role of bioavailability studies. Am J Clin Nutr. 2004;80:1104–1105. MEDLINE 41. 41Institute of Medicine. Committee to Review the WIC Food Packages (WIC Food Packages, Time for a Change). Washington, DC: National Academies Press; 2005;. 42. 42Bahijri S. Serum zinc in infants and preschool children in the Jeddah area: Effect of diet and diarrhea in relation to growth. Ann Saudi Med. 2001;21:324–329. MEDLINE 43. 43King JC, Keen CL. Zinc. In: Shils ME, Olson JA, Shike M, Ross AC editor. Modern Nutrition in Health and Disease. 9th ed.. Baltimore, MD: Williams & Wilkins; 1999;p. 223–239. 44. 44Skinner JD, Ziegler P, Ponza M. Transitions in infants’ and toddlers’ beverage patterns. J Am Diet Assoc. 2004;104(suppl 1):S45–S50. 45. 45Lönnerdal B. Copper nutrition during infancy and childhood. Am J Clin Nutr. 1998;67(suppl 5):1046S–1053S. MEDLINE 46. 46Domellöf M, Lönnerdal B, Dewey KG, Cohen RJ, Hernell O. Iron, zinc, and copper concentrations in breast milk are independent of maternal mineral status. Am J Clin Nutr. 2004;79:111–115. MEDLINE 47. 47Pennington JAT, Schoen SA, Salmon GD. J Food Comp Anal. 1995;8:171–217. 48. 48Lönnerdal B. Dietary factors influencing zinc absorption. J Nutr. 2000;130(suppl 5):1378S–1383S. MEDLINE 49. 49Wood RJ. Assessment of marginal zinc status in humans. J Nutr. 2000;130(suppl 5):1350S–1354S. MEDLINE J. M. Schneider is a postdoctoral scholar, B. Lönnerdal is a professor, and S. Zidenberg-Cherr is a cooperative extension specialist, Department of Nutrition, University of California, Davis. M. L. Fujii is an adjunct nutrition, family, and consumer sciences advisor, University of California Cooperative Extension, Pleasant Hill. C. L. Lamp is a nutrition, family, and consumer sciences advisor, University of California Cooperative Extension, Tulare.  Address correspondence to: Sheri Zidenberg-Cherr, PhD, Department of Nutrition, One Shields Ave, Davis, CA 95616.
PII: S0002-8223(07)01621-5 doi:10.1016/j.jada.2007.08.011 © 2007 American Dietetic Association. Published by Elsevier Inc. All rights reserved. | |
|
FULL TEXT