American Journal of Clinical Nutrition, Vol. 78, No. 5, 1011-1017,
November 2003
© 2003 American Society for Clinical Nutrition
ORIGINAL RESEARCH COMMUNICATION |
Zinc intake of US preschool children exceeds new dietary reference intakes1,2,3
Joanne E Arsenault and
Kenneth H Brown
1 From the Program in International Nutrition, Department of Nutrition,
University of California, Davis.
2 Supported by a Jastro-Shields Research Scholarship Award, University
of California, Davis (to JEA).
3 Reprints not available. Address correspondence to KH Brown, Program in International Nutrition, Department of Nutrition, University of
California, Davis, One Shields Avenue, Davis, CA 95616. E-mail:
khbrown{at}ucdavis.edu.
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ABSTRACT
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Background: The recent dietary reference intakes publication
provides updated information on the physiologic and dietary requirements for zinc and proposes new tolerable upper intake
levels.
Objective: We analyzed dietary intake data of US preschool
children to determine the prevalence of inadequate and excessive
intakes of zinc.
Design: Diets of 7474 nonbreastfeeding preschool children in the
Continuing Survey of Food Intakes by Individuals (1994-1996 and
1998) were analyzed for the intakes of zinc and other dietary
components, and factors associated with zinc intake were examined.
Results: The mean intakes of zinc by children aged < 1 y, 1-3 y,
and 4-5 y were 6.6, 7.6, and 9.1 mg/d, respectively. Less than 1%
of children had usual zinc intakes below the adequate intake or
estimated average requirement. The percentages of children with
intakes exceeding the tolerable upper intake level were 92% (0-6
mo), 86% (7-12 mo), 51% (1-3 y), and 3% (4-5 y). Controlling
for age and energy intake, zinc intake was greater in 1998 than in
1994 (P < 0.0001) and was positively associated with participation in the Women, Infants, and Children Program (P < 0.001) and
with the lowest income category (P < 0.001).
Conclusions: Preschool children in the United States have dietary
zinc intakes that exceed the new dietary reference intakes. Zinc
intakes increased during the 4 y of the study. The present level of
intake does not seem to pose a health problem, but if zinc intake
continues to increase because of the greater availability of zinc-fortified foods in the US food supply, the amount of zinc consumed by children may become excessive.
Key Words: Zinc • copper • phytate • dietary intake • preschool children • Continuing Survey of Food Intakes by Individuals • CSFII • dietary reference intakes • DRIs
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INTRODUCTION
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In 2001, the Food and Nutrition Board of the Institute of
Medicine released new dietary reference intakes (DRIs) for
zinc (1). The DRIs contain a set of 4 nutrient reference values
for various applications: the estimated average requirement
(EAR), the recommended dietary allowance (RDA), adequate
intake (AI), and the tolerable upper intake level (UL). The new
RDA is calculated as 2 SDs greater than the EAR, which is the
nutrient intake level that meets the requirements of 50% of
healthy individuals in an age and sex group. The EAR is used
to assess the adequacy of intake by populations. The RDA
specifies the intake level that meets the requirements of nearly
all (97-98%) persons in the population group, and it is used as
a dietary intake goal for individual persons. The new zinc
RDAs for preschool children are substantially lower than the
previous ones (Table 1
; 2). For infants aged 0-6 mo, an AI for
zinc, rather than an EAR, has been established. The AI is based
on the maternal zinc supply to the infant who is fed human milk
exclusively. For older infants and young children, an EAR is
based on factorial analysis, and endogenous zinc losses are
estimated by extrapolation from measured values for adults or
younger infants.
The UL is the highest average level of daily intake that is
likely to pose no risk of adverse health effects to almost all
persons in the general population. Possible adverse effects of
high zinc intake include lower copper status (3), impaired
immune responses (4), and alterations in lipoprotein metabolism (5). The UL of 4 mg for infants was based on a study in
which infants consumed 4.5 mg Zn/d from a zinc-fortified
formula, and no adverse effects on serum copper or cholesterol
were found (6). The UL values for children were derived from
the UL for infants with adjustment for body weight.
In the assessment of the dietary intake of zinc, other dietary
factors that may interact with zinc should be examined.
Phytate, a component of plant-based foods, interferes with the
absorption of dietary zinc (7). Foods that are high in phytate,
such as whole-grain breakfast cereals, peanut butter, and soy-based infant formula, are consumed by many children in the
United States. A diet with a phytate-to-zinc ratio < 5 provides
zinc with a high degree of availability, whereas a phytate:zinc
> 15 results in relatively poor absorption of zinc (8). Children
consuming a diet that provides marginal zinc intake may not
absorb an adequate amount of zinc if they are also consuming
foods high in phytate. Dietary intake of copper is also important because of the effect of excess dietary zinc on copper
status.
The current study was undertaken to reassess the adequacy
of zinc intakes of US preschool children in light of the new
DRIs. The specific goals were 1) to assess the prevalence of
both inadequate and potentially excessive zinc intakes, 2) to
describe zinc intakes in relation to the phytate and copper
contents of the diet, 3) to describe food sources of zinc for
these children, and 4) to examine demographic and socioeconomic variables associated with zinc intake.
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SUBJECTS AND METHODS
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The analyses in this report are based on dietary intake data
obtained during the 1994-1996 and 1998 Continuing Survey of
Food Intakes by Individuals (CSFII), a nationwide survey
conducted periodically by the US Department of Agriculture
(9). The CSFII sampling scheme is a stratified, clustered,
multistage probability design with oversampling of low-income households. For our analyses, we selected children < 6
y old who were not breastfeeding and for whom there were
complete dietary intake data from 2 d, which resulted in a
sample of 7474 children (Figure 1). Sampling weights from
the CSFII data set were used to account for the sampling design
of the survey. The CSFII data set without individual indentifying information is available publicly.
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FIGURE 1.. Flow chart of subjects from the Continuing Survey of Food
Intakes by Individuals from 1994-1996 and 1998 included in the current
study.
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The CSFII collected dietary intake data via in-home interviews of the caretakers of the children. Two 24-h recalls were
obtained on nonconsecutive days 3-10 d apart. For the dietary
recalls, a multiple-pass approach was used. On the first pass,
the respondent was asked to recall, without interruption by the
interviewer, all foods consumed during the previous day. On
the second pass, the interviewer asked for details and amounts
of each food consumed throughout the day. Measuring guides,
such as cups, spoons, and food pictures, were used to help the
respondents specify accurate portion sizes.
Intakes of energy, zinc, and copper were calculated with the
use of nutrient values provided in the data set. Although
information was available on whether the children took a
micronutrient supplement and, if so, on the frequency of use,
the nutrient values presented here are from food only, because
the data files did not contain quantitative information on the
nutrient contents of the supplements. Values for the phytate
content of all foods were obtained by using the NUTRIENT
DATA SYSTEM FOR RESEARCH software (10).
To determine the percentage of children with inadequate
zinc intake, the "usual" zinc intakes were obtained and the
EAR cutoffs were used, as described by the Institute of Medicine (11). The distribution of zinc intakes was skewed, and
thus the zinc intake values were transformed, by using the
natural logarithm (ln). To calculate the distribution of usual
intakes, the within-person and between-person variations in
intake were obtained by using the two 24-h intakes for each
child. The adjusted (usual) zinc intake for each child was
calculated by using the equation
 | (1) |
The proportions of children with intakes below the EAR for
each of the age groups for which an EAR for zinc exists were
calculated by counting the number of children with zinc intake
below the EAR and dividing by the total number of children in
that age group. Likewise, the proportions of children with
intakes above the UL were calculated by counting the number
of children with zinc intakes above the UL and dividing by the
total number of children in that age group.
The contributions of individual foods to zinc and copper
intakes were calculated by summing the amount of zinc or
copper consumed from each food by all subjects in each age
group and dividing by the total intake from all foods for all
subjects in the respective age group. Sampling weights were
used in the calculation.
Zinc-fortified foods were identified from the database by
examining the ingredient list on the product label for added
zinc. Zinc-fortified foods consumed by these children included
breakfast cereals, infant formula, fortified beverages (eg, meal
replacement or instant breakfast beverages), and fortified cereal bars. The amount of added zinc in food could not be
separated from the amount of zinc occurring naturally in the
product, and thus the total zinc content of zinc-fortified foods
is used to represent zinc from fortified foods. Mean daily zinc
intakes from fortified foods were obtained for each subject.
Factors associated with zinc intake were assessed with the use
of a multivariate modeling procedure (PROC SURVEYREG,
release 8; SAS Institute Inc, Cary, NC) that takes into account
the complex sampling design of CSFII. The sampling weights
were used to adjust for variations in the probability of selection
and for differential nonresponse rates. Adjustment was also
made to account for the clustering design, by using the appropriate variables provided in the data set. The ln of zinc intake
was the dependent variable, and the independent variables were
age, sex, region of the country, degree of urbanization (according to the US Census Bureau Metropolitan Statistical Area
standards), ethnic origin, income, participation in food assistance programs, use of vitamin or mineral supplements or both,
the year of the survey, and the education level and employment
status of male and female heads of households. All independent
variables were entered into the model, and nonsignificant variables were removed one variable at a time with the use of a
backwards, stepwise method. If removal of a nonsignificant
variable did not change the coefficient of the variables remaining in the model, the nonsignificant variable was eliminated.
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RESULTS
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Characteristics of the 7474 children in the study are presented in Table 2. CSFII intentionally oversampled low-income households. By applying appropriate weighting factors
supplied in the data set, the frequencies provided in the table
are representative of the US population of nonbreastfeeding
children of these ages.
The ratios of within-person to between-person SDs of zinc
intake were 0.75, 1.03, 1.47, and 1.70 for children aged 0-6
mo, 7-12 mo, 1-3 y, and 4-5 y, respectively. After adjustment
of zinc intakes to remove within-person variation and thereby
to obtain estimates of usual intakes, < 1% of the children had
inadequate zinc intakes in relation to the EAR and < 1% of
infants aged 0-6 mo had intakes below the AI (Figure 2). Notably, 92% of 0-6 mo-old infants, 86% of 7-12 mo-old
infants, 51% of 1-3 y-old children, and 3% of 4-5 y-old
children had usual intakes greater than the UL. The UL for zinc
includes intake from both food and supplements. Because
CSFII data do not include nutrient intake from supplements,
these figures may underestimate the percentages of children
with intakes greater than the UL.
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FIGURE 2.. Distribution of usual zinc intakes by age group. Intakes are adjusted to obtain an estimate of usual intake according methods described by
the dietary reference intakes committee (11). The adequate intake (AI) or estimated average requirement (EAR) and tolerable upper intake level (UL) are
depicted for each age group.
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Energy and zinc intakes increased with age, but the zinc
density (mg zinc/1000 kcal) of the children's diets decreased
(Table 3). Phytate intakes increased with age, as did the molar
ratios of phytate to zinc. Children with diets in the lowest
quartile of zinc density had higher phytate intakes and higher
phytate:zinc than did children in the highest quartile of zinc
density (Table 4). Most of the children in the highest quartile
of zinc density had phytate:zinc < 5. Less than 1% of children
had inadequate copper intakes in relation to the EAR. Only one
infant had a copper intake below the AI. Four percent of 1-3
y-old children and none of the 4-5-y-old children had copper
intakes above the UL. The children's median ratios of zinc to
copper were close to the < 10:1 ratio of the requirements
(EAR) for zinc and copper (Table 3). There was a positive
correlation between dietary zinc and copper intake (r = 0.61,
P < 0.0001). However, copper intakes did not differ significantly across quartiles of zinc density, and zinc:copper increased with increasing zinc density (Table 4). One-half of the
children in the highest quartile of zinc density were also in the
highest quartile of zinc:copper intakes.
The high zinc intakes by infants are due primarily to the
consumption of zinc-fortified infant formula, which accounted
for 77% of the zinc intake (Table 5). Milk and ready-to-eat
(RTE) breakfast cereals were the highest contributors of zinc
for children aged 1-3 y and 4-5 y, respectively. Milk contains
less zinc per serving than do some of the other foods lower on
the list, but milk was a major contributor of zinc to the
children's diets because of the high volumes that they consumed. RTE breakfast cereals were consumed by 64% of all
children in the study, and 78% of these cereals were fortified
with zinc. Infant formula was also the main contributor of
copper to the diets of infants. Fruit juice was the highest
contributor of copper to the diets of 1-3-y-old children, and
potatoes provided the largest amount of copper to 4-5-y-old
children.
Overall, 24% of the mean daily zinc intake of all children
was obtained from zinc-fortified foods, primarily infant formula and RTE breakfast cereal. Sixty-eight percent of children
consumed at least one zinc-fortified food, and among these
children, zinc-fortified foods provided 35% of their mean daily
zinc intake. Fortified foods provided a much greater proportion
of zinc to infants than they provided to children in the other age
groups (Table 6). The percentage of zinc consumed from
zinc-fortified foods doubled from 14% for children surveyed in
1994 to 28% for children surveyed in 1998 (P < 0.0001)
(Figure 3). There were no differences between any of the
survey years in the amount of zinc consumed from foods not
fortified with zinc.
The results of multiple regression analysis showed that, after
control for age and energy intake, participation in the Supplemental Food Program for Women, Infants, and Children (WIC)
was positively associated with zinc (ln) intake (P < 0.001)
(Table 7). The lowest income category was positively associated with zinc intake, even after we controlled for WIC participation (P < 0.0003). Children surveyed in 1998 consumed
more zinc than did children surveyed in 1994 (P < 0.0001).
Age was negatively associated with zinc intake in the model
because of control for energy intake—ie, the younger children's diets had greater zinc density that did the diets of the
children in the other age groups. Participation in school breakfast and lunch programs was also positively associated with
zinc intake, but these variables only applied to children who
were 5 y of age and in school, so they were not included in the
model. To determine whether the consumption of certain foods
contributed to higher zinc intake among WIC participants,
separate models were obtained by using zinc intake from
individual foods as the dependent variables. After control for
age and energy intake, WIC participation was positively associated with zinc intake from infant formula (P < 0.001), beef
(P < 0.01), and poultry (P < 0.05). RTE cereal was a major
source of zinc for both WIC participants and nonparticipants,
and thus there was no association with program participation.
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DISCUSSION
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The present study assessed the adequacy of zinc intakes in US
children according to newly released DRIs. Less than 1% of the
children had inadequate intakes based on the EAR (or based on AI
for infants aged 0-6 mo), and a substantial percentage of children
consumed higher amounts of zinc than the recently proposed UL.
The new DRIs are lower than the previous (1989) version of the
RDA. Before the publication of the new DRIs, there was concern
that children in the United States were not consuming enough
zinc. By using dietary intake data from the third National Health
and Nutrition Examination Survey (NHANES III, 1988-1994),
Briefel et al (12) found that 81% of 1-3-y-old and 48% of
4-6-y-old children had inadequate zinc intakes, which they defined as < 77% of the 1989 RDA. The mean zinc intakes in
children in NHANES III were 6.4 mg/d for 1-3-y-olds and 7.7
mg/d for 4-6-y-olds. These intakes are adequate if compared with
the current EAR or RDA, but they are lower than the zinc intakes
measured by the CSFII (1994-1996 and 1998), which was used
for the current study.
Children surveyed in 1998 had higher zinc intake than did
those in the 1994 survey, and this was true for all age groups
(data not shown). For children aged 1-5 y, the percentage of
zinc intake from zinc-fortified foods increased over the time of
this study, whereas the percentage of zinc intake from nonzinc-fortified foods remained the same. For infants, the percentage
of zinc from fortified foods remained the same over time
because zinc content of infant formula has not changed during
this period. Berner et al (13) reported the contribution of
fortified foods to total nutrient intakes among users of fortified
foods from the previous CSFII (1989-1991). Among children
who consumed at least one zinc-fortified food product, Berner
et al found that fortified foods contributed 13% of total zinc
intake for 1-3-y-old children and 17% of total zinc intake for
4-5-y-old children, compared with 24% and 25% of total zinc
for 1-3-y-old and 4-5-y-old children, respectively, who consumed a zinc-fortified food in the present study. In the previous
CSFII study (1989-1991), 18% of children aged 1-6 y consumed a food fortified with zinc; in the present study (CSFII
1994-1996 and 1998), 64% of children aged 1-5 y old did so.
The contribution of RTE cereal to the zinc intake of children
has increased over time. In the previous CSFII study (1989-1991), the primary food sources of zinc for children 2-5 y old
were milk (21%), beef (17%), and RTE cereal (11%; 14). In the
present study, the primary food sources of zinc for children 2-5
y old were RTE cereal (18%), milk (16%), and beef (13%). In
the present study, children in 1998 consumed the same amount,
by weight, of RTE cereal as did children in 1994, but the mean
amount of zinc consumed from RTE cereals increased from 0.8
mg/d in 1994 to 1.3 mg/d in 1998.
The finding of higher zinc intakes in children participating in
food assistance programs agrees with previous reports. Rose et
al (15) examined the effects of participation in the Food Stamp
(FS) and WIC programs on nutrient intake of preschoolers in
the 1989-1991 CSFII. Children in either or both of these
programs had higher zinc intakes than did nonparticipants.
Perez-Escamilla et al (16) found that inner-city preschoolers
who were enrolled in both the WIC and FS programs had
higher zinc intakes than did children enrolled only in WIC. The
WIC food packages for infants and children include infant
formula, milk, breakfast cereal, cheese, juice, peanut butter,
beans, and eggs, which together provide 3.9-4.4 mg zinc/d
(17). In the present study, zinc intake from infant formula was
predicted by participation in WIC.
In this study, children in the lowest income category had
higher zinc intakes, even after control for WIC participation,
which suggests that some additional factor associated with low
income contributed to higher zinc intake. When FS participation, but not income status, was in the model with WIC
participation, FS participation and WIC participation were significant. When income was added to the model with WIC and
FS, FS participation was no longer significant. This suggests
that income status was probably responsible for the association
of FS participation with zinc intake, but not for the association of
WIC participation with zinc intake. In separate chi-square analyses, participation in the FS Program was more strongly associated
with income status than was participation in WIC. Other variables
that are often associated with income, such as parental education
and single head of household, did not change the relation of
income to zinc intake when added to the model.
Overall, 36% of children had diets containing zinc in excess
of the UL. The UL published by the DRI committee includes
both dietary zinc and zinc consumed as a micronutrient supplement, whereas the CSFII data describe zinc intake from
foods only. If intakes in the present study had included nutrient
intakes from supplements, the intakes of even more children
would have exceeded the UL. In this population, 20% of the
children were taking a multimineral supplement that may have
contained zinc. Most children's multimineral supplements
available in the market provide 15 mg Zn—or 7.5 mg if a
half-tablet is consumed, as is advised for children < 4 y old.
Therefore, children who consume a zinc-containing multimineral supplement receive more than the UL of zinc from the
supplement alone. The UL of zinc is based on the adverse
effects of zinc on copper metabolism. Despite the high zinc
intakes of children in the present study, the children's diets
contained adequate amounts of copper, and the mean zinc:copper of the diets was in the range of the molar ratios of the
DRI values for zinc and copper. Thus, it may be less likely that
high zinc intake produces adverse effects on copper metabolism under these circumstances. However, there were some
children who had diets with high zinc density but whose
zinc:copper was also high. More research is needed on possible
adverse effects of these levels of zinc intake.
In setting the dietary requirement for zinc in children, a
single percentage of fractional zinc absorption was assumed. If
high zinc intakes are associated with consumption of inhibitors
of zinc absorption, it may be less likely that zinc would induce
adverse effects. Phytate is the major inhibitor of zinc absorption (7). In the present study, the children with diets in the
highest quartile of zinc density had a mean phytate:zinc of only
3, and thus it is unlikely that phytate exerted an important
effect on zinc absorption.
As a result of new dietary recommendations for zinc, the
assessment of the adequacy of zinc intake now finds a high
percentage of intakes above the recommended UL, rather than the
previous finding of a high proportion of inadequacy. This may
raise some concern, especially among those who misinterpret the
purpose of the UL as indicating the level at which adverse effects
may be seen. In fact, the UL is defined as the highest average daily
intake likely to pose no risk of adverse health effects to almost all
persons in the general population. There have been no recent
reports of zinc toxicity in US children. It is unlikely that zinc
intake from food is high enough to have a negative effect on health
status. However, if zinc intake continues to increase because of the
greater availability of zinc-fortified foods in the US food supply,
the amount of zinc that children consume from foods may become
excessive. Research is needed on the effect of current zinc intakes
from both food and supplements on the copper status and immune
function of US children. If no adverse effects are found, then the
currently recommended UL should be increased.
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ACKNOWLEDGMENTS
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We thank Janet Peerson for statistical consultation on the SAS procedures for handling the complex sampling design of CSFII and on the
procedures for assessing adequacy of dietary intakes.
JEA contributed to the analysis of data and writing of the manuscript. KHB
contributed to the design of the data analysis, the interpretation of results, and
the writing of the manuscript. The authors had no conflicts of interest.
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TOP
ABSTRACT
INTRODUCTION
) and zinc-fortified (
)
foods to mean daily zinc intakes. n = 1199 in 1994, 1191 in 1995, 1193 in
1996, and 3891 in 1998. There was a significant difference in zinc intake
from fortified foods between all years (ANOVA; P < 0.0001), except
between 1995 and 1996. There were no significant differences in zinc
intake from nonfortified foods between years.