Iron Deficiency in Early Childhood in the United
States: Risk Factors and Racial/Ethnic Disparities
Jane M. Brotanek, Jacqueline Gosz, Michael Weitzman and Glenn Flores
Pediatrics 2007;120;568-575
ABSTRACT
BACKGROUND. Iron deficiency affects 2.4 million US children, and childhood irondeficiency anemia is associated with behavioral and cognitive delays. Given the detrimental long-term effects and high prevalence of iron deficiency, its prevention in early childhood is an important public health issue.
OBJECTIVES. The study objectives were to (1) identify risk factors for iron deficiency in US children 1 to 3 years old, using data from the most recent waves of the National Health and Nutrition Examination Survey IV (1999–2002) and (2) examine risk factors for iron deficiency among Hispanic toddlers, the largest minority group of US children.
PATIENTS AND METHODS. Analyses of the National Health and Nutrition Examination Survey IV were performed for a nationally representative sample of US children 1 to 3 years old. Iron-status measures were transferrin saturation, free erythrocyte protoporphyrin, and serum ferritin. Bivariate and multivariable analyses were performed to identify factors associated with iron deficiency.
RESULTS. Among 1641 toddlers, 42% were Hispanic, 28% were white, and 25%
were black. The iron deficiency prevalence was 12% among Hispanics versus 6%
in whites and 6% in blacks. Iron deficiency prevalence was 20% among those with
overweight, 8% for those at risk for overweight, and 7% for normal-weight
toddlers. Fourteen percent of toddlers with parents interviewed in a non–English
language had iron deficiency versus 7% of toddlers with parents interviewed in
English. Five percent of toddlers in day care and 10% of the toddlers not in day
care had iron deficiency. Hispanic toddlers were significantly more likely than
white and black toddlers to be overweight (16% vs 5% vs 4%) and not in day care
(70% vs 50% vs 43%). In multivariable analyses, overweight toddlers and those
not in day care had higher odds of iron deficiency.
CONCLUSIONS. Toddlers who are overweight and not in day care are at high risk for
iron deficiency. Hispanic toddlers are more likely than white and black toddlers to
be overweight and not in day care. The higher prevalence of these risk factors
among Hispanic toddlers may account for their increased prevalence of iron
deficiency.
IRON DEFICIENCY AND iron-deficiency anemia affect 2.4
million and 490 000 US children, respectively.1,2 Children
1 to 3 years old are particularly vulnerable, because
maternal iron stores are depleted during a period of
rapid growth.2,3 A recent analysis of the National Health
and Nutrition Examination Survey (NHANES) III found
the prevalence rates of iron deficiency and iron-deficiency
anemia among US toddlers to be 9% and 3%,
respectively2 (herein, “toddlers” refers to children 12–30
months old, and “infants” refers to those _12 months
old4). Other investigators have reported much higher
rates, particularly in urban settings and poor households.
The Third Report on Nutrition Monitoring in the US showed
a 15% prevalence of iron-deficiency anemia among children
1 to 3 years old,5 while another study reported an
8% prevalence of iron-deficiency anemia in toddlers.6
Iron-deficiency anemia in infancy and early childhood
is associated with behavioral and cognitive delays,
including impaired learning,7 decreased school achievement,
8,9 and lower scores on tests of mental and motor
development.10–12 Given the detrimental long-term effects
and high prevalence of iron deficiency, its prevention
in early childhood is an important public health
issue. A Healthy People 2010 objective is to reduce iron
deficiency in children 1 to 2 years old to 5% (compared
with the 1988–1994 baseline prevalence of 9%) and in
children 3 to 4 years old to 1% (compared with the
1988–1994 baseline prevalence of 4%) by 2010.13
Effective approaches to the prevention of iron deficiency
in infancy and early childhood should include
screening and counseling practices targeting children
identified to be at high risk for iron deficiency.6,14–16 Iron
deficiency affects 20% to 25% of infants worldwide,17
and most studies of risk factors for iron deficiency in
early childhood have been conducted in Latin America,
Africa, India, Europe, and Canada.18–29 Several studies
have demonstrated a high prevalence of iron deficiency
in the United States among low-income infants and
children,30–32 who may experience food insecurity and
have diets low in iron.33 Important dietary risk factors
include exclusive breastfeeding beyond 6 months not
supplemented by iron-rich foods or vitamins with
iron,34,35 early introduction of milk,3,35 prolonged bottlefeeding,
36–40 and excessive cow’s milk consumption.36,38
An association between maternal prenatal anemia and
iron deficiency has also been reported.33 A comprehensive
list of known risk factors appears in the 1998 Centers
for Disease Control and Prevention recommendations
for the prevention and control of iron deficiency in
the United States.16
The most recent published estimates of the prevalence
of iron deficiency among US toddlers use data from
the NHANES III (1988–1994).2 Analyses are needed to
more clearly delineate risk factors for iron deficiency
among US toddlers using current data. In addition, striking
racial/ethnic disparities in the prevalence of iron
deficiency among toddlers were recently reported, with
high prevalence rates among Hispanic children.36,37 The
reasons for these racial/ethnic disparities in the prevalence
of iron deficiency remain unclear. The objectives of
this study were to (1) identify risk factors for iron deficiency
in US children 1 to 3 years old, using data from
the most recent waves of the NHANES IV (1999–2002);
and (2) examine risk factors for iron deficiency among
Hispanic toddlers, the largest minority group of US children.
METHODS
Data Source
The data source for these analyses was the NHANES IV,
a large-scale national survey conducted by the National
Center for Health Statistics from 1999 through 2002.41,42
The NHANES IV is the eighth in a series of national
examination studies conducted in the United States
since 1959. From 1960 to 1994, a total of 7 national
surveys have been conducted; beginning in 1999, the
survey has been conducted continuously.41,42 The
NHANES IV is a nationally representative sample of the
civilian US population _2 months of age living in households,
including 5785 children. Subjects were asked to
complete an extensive household interview and an examination
in a mobile health center. Data were collected
through interviews and physical examinations on the
prevalence of specified chronic diseases and conditions,
physical measures such as height and weight, physiologic
measures such as blood pressure and serum cholesterol
levels, levels of cognitive function, mental
health, and dental health. Low-income persons, adolescents
12 to 19 years old, persons _60 years old, African
Americans, and Mexican Americans were oversampled.
43 Results were weighted to adjust for nonresponse
and to provide national estimates.41,42
The National Center for Health Statistics released
public use data sets from the continuous NHANES in
2-year groupings: (1) NHANES 1999–2000, conducted
on a nationwide probability sample of 9965 persons of
all ages; and (2) NHANES 2001–2002, conducted on a
nationwide probability sample of 11 039 persons of all
ages. Both survey designs are stratified, multistage probability
samples of the civilian noninstitutionalized US
population. For the NHANES 1999–2000, there were
12 160 persons selected for the sample; 9965 were interviewed
(82%), and 10 477 (80%) were examined.44
For the NHANES 2001–2002, 13 156 persons were selected
for the sample; 11 039 were interviewed (84%),
and 10 477 (80%) were examined.44
All NHANES questionnaires were translated into
Spanish and administered in computer-assisted personal
interview format, along with the English-language versions.
41,42 All interviewers completed a 2-week training
program, and many of the interviewers had previous
training experience. A large percentage of the household
interviewers was bilingual in English and Spanish.
Neighbors or household interpreters were used to assist
in completing interviews with household members
speaking a language other then English or Spanish.
Independent Variables
Independent variables included age and gender. Poverty
status was dichotomized as below the poverty threshold
versus at or above the poverty threshold, based on family
size and the federal poverty threshold at the time of
the survey.45,46 The child’s race/ethnicity was defined by
parental self-identification and included non-Hispanic
white, non-Hispanic black, and Hispanic. Because of
small sample sizes, Asian/Pacific Islander, Native American,
other, and multiple race/ethnic groups were excluded
from the analyses. Other independent variables
included weight-for-height status (using age-specific and
gender-specific weight-for-length percentiles, with at
risk for being overweight defined as a weight-for-length
status of _85th and _95th percentile, and overweight
defined as a weight-for-length status of _95th percentile
[BMI was not used because only weight-for-length measurements
were available for children 1 to 3 years of
age]); birth weight (_2500 vs _2500 g); blood lead level
(_10 vs _10 _g/dL); interview language (English versus
a non-English language); household food insecurity (defined
as “limited or uncertain availability of food, or
limited or uncertain ability to acquire acceptable foods in
socially acceptable ways” as a result of inadequate financial
resources47 [based on the 18-item Food Security
Survey Module, with data released in the categories
household fully/marginally food secure versus food insecure
with or without hunger during the past 12
months]); day care/preschool attendance (attends or
ever attended day care/preschool versus does not attend
or has never attended day care/preschool); and whether
the child received Supplemental Nutrition Program for
Women, Infants, and Children (WIC) in the past 12
months. To assess the appropriateness of the duration of
breast milk or formula-feeding in relation to the American
Academy of Pediatrics’ guidelines,48 we also examined
the age at which breastfeeding or formula-feeding
was discontinued. Exclusive breastfeeding beyond 6
months was not included, because its prevalence was
low in the study sample. It was not possible to include
caretaker educational attainment and duration of bottlefeeding
as independent variables, because neither was
included in the NHANES IV questionnaire. Laboratory
values were measured by using standard measurement
assays, the details of which are described elsewhere.49,50
Definitions
We used the definitions of iron deficiency previously
described by Looker et al2 in their evaluation of the
prevalence of iron-deficiency anemia in the United
States using the NHANES III. The diagnosis of iron deficiency
was based on 3 laboratory tests of iron status:
transferrin saturation, free erythrocyte protoporphyrin,
and serum ferritin. An individual was considered iron
deficient if any 2 of these 3 values were abnormal for age
and gender. For children between the ages of 1 to 2
years, the cutoff values for tests of iron status are _10%
transferrin saturation, _10 _g/L of serum ferritin, and
_1.42 _mol/L of red blood cells erythrocyte protoporphyrin.
For 3-year-old children, these cutoff values are
_12%, _10 _g/L, and _1.24 _mol/L of red blood cells,
respectively. It was not possible to include data from the
NHANES 2003–2004 in these analyses, because beginning
with the NHANES 2003, iron-status indicators are
no longer available for children _3 years of age. Because
of small sample sizes, it was not possible to examine
iron-deficiency anemia as an outcome measure among
US children 1 to 3 years old.
Analysis
The prevalence of iron deficiency was determined for
toddlers in the different risk categories of the independent
variables defined previously: age, gender, race/ethnicity,
poverty, weight-for-height status, birth weight,
blood lead level, interview language, household food
security, day care/preschool attendance, receipt of WIC
in the past 12 months, and the age at which breastfeeding
or formula-feeding was discontinued. Bivariate analyses
were performed to examine the association between
iron deficiency and each of these independent
variables. To maintain an event-per-variable ratio of
_10, only those independent variables significant in bivariate
analyses were entered into a series of stepwise
multivariable models, in which the outcome variable
was iron deficiency.
SAS 9.1 (SAS Institute Inc, Cary, NC) was used in all
analyses. Sample weights were applied to account for
the unequal probabilities of selection, oversampling, and
nonresponse for all analyses using SAS and to estimate
standard errors using the Taylor series linearization
method. Logistic regression was used for multivariable
analyses, and _2 tests were used to test for differences in
proportions.
RESULTS
Among 1641 1- to 3-year-old children in the sample,
42% were Hispanic, 25% were non-Hispanic black, and
28% were non-Hispanic white. Of 960 toddlers with all
3 iron-status indicators present, 8% (n _ 92) had iron
deficiency (Table 1). Fourteen percent of toddlers with
parents interviewed in a non–English language had iron
deficiency, compared with only 7% of toddlers with
parents interviewed in English (P _ .01). Forty-four
percent of parents of Hispanic toddlers were interviewed
in Spanish and 56% in English. One non-English interview
was conducted with parents of a black toddler. Iron
deficiency was most prevalent among overweight toddlers
at 20%, compared with 8% in those at risk for
overweight, and 7% in normal-weight toddlers (P _
.02). Five percent of toddlers with day care/preschool
attendance and 10% of toddlers not in day care/preschool
had iron deficiency (P _ .02). The prevalence of
iron deficiency was 12% among Hispanic children, 6%
in white children, and 6% in black children; the prevalence
of iron deficiency was significantly higher in Hispanic
children than in white children (P _ .03) and also
significantly higher in Hispanic children than in black
children (P _ .02). Twelve percent of toddlers in foodinsecure
households had iron deficiency, compared with
7% of toddlers in food secure households (P _ .06). Age,
gender, poverty, lead level, birth weight, receipt of WIC
in the past 12 months, and the age at which breastfeeding
or bottle-feeding was discontinued were not found to
be significantly associated with iron deficiency.
As shown in Table 2, Hispanic toddlers were more
likely to be overweight (16%) than white (5%) and
black (4%) toddlers (P _ .0004). Hispanic toddlers were
also more likely not to be in day care/preschool (70%),
compared with white (50%) and black (44%) children 1
to 3 years old (P _ .0001).
Hispanic children had significantly greater unadjusted
odds of iron deficiency (odds ratio [OR]: 2.08; 95%
confidence interval [CI]: 1.07–4.04), compared with
white children (Table 3). The Hispanic/white disparity in
iron deficiency prevalence rates disappeared after multivariable
adjustment for parental interview language
(model 2; Table 3). Interview language remained significant
after adjustment for weight-for-height status alone
(model 3) but was no longer significant after adjustment
for preschool/day care attendance alone (model 4). After
adjustment for both preschool/day care attendance and
weight-for-height status, interview language was no
longer significant (model 5). In the full multivariable
model (model 6) that included race/ethnicity, interview
language, weight-for-height status, and preschool/day
care attendance, overweight toddlers (OR: 3.4; 95% CI:
1.1–10.1) and those not in day care (OR: 1.9; 95% CI:
1.0 –3.3) had higher odds of iron deficiency, but neither
race/ethnicity nor interview language was significantly
associated with iron deficiency in this model.
DISCUSSION
The study findings show that racial/ethnic disparities in
the prevalence of iron deficiency exist, with Hispanic
toddlers twice as likely to be iron deficient compared
with white toddlers. Hierarchical multivariable models,
however, reveal that Hispanic ethnicity is no longer
significantly associated with iron deficiency in toddlers
after adjustment for relevant covariates. Adjustment for
survey language eliminates Hispanic/white disparities in
iron deficiency prevalence. Even after adjustment for
weight-for-height status alone, toddlers with parents interviewed
in a non–English language remained almost
twice as likely to be iron deficient compared with toddlers
with parents interviewed in English. After adjustment
for both preschool/day care attendance and
weight-for-height status, differences by survey language
were eliminated, with preschool/day care attendance
and weight-for-height status each independently associated
with iron deficiency in the final multivariable
model.
Toddlers who are overweight and those not in day
care are at high risk of iron deficiency. Hispanic toddlers
are more likely to be overweight and less likely to be in
preschool/day care, compared with white toddlers (Table
2). The higher prevalence of these nonethnic risk
factors among Hispanic toddlers may account for their
increased prevalence of iron deficiency.
A key finding of this study is the alarmingly high
prevalence of iron deficiency among overweight toddlers.
This finding is consistent with a previous analysis
of the NHANES III (1988 –1994), which demonstrated
an association of overweight with iron
deficiency among US children 2 to 16 years of age.51
Our findings document an even higher prevalence of
iron deficiency among younger children (20% irondeficiency
prevalence among overweight 1- to 3-yearolds
versus 6% among overweight 2- to 5-year-olds),
using more recent data. A few other small studies,
mainly in adolescents, also reported an association
between overweight and iron deficiency.52–54 Several
factors have been proposed to explain this association,
including genetic influences, alterations in iron metabolism,
55,56 and an inadequate diet with limited intake
of iron-rich foods.51 Our study is the first, to our
knowledge, to report an association between iron deficiency
and overweight among children as young as 1
to 3 years old. The reasons for the strong association in
this age group are unclear and need to be elucidated.
Dietary practices may play an important role, since
diets high in calories but poor in micronutrients may
lead to both iron deficiency and overweight.14 Nutritional
practices such as excessive milk or juice intake,
prolonged bottle-feeding, snacking, and junk food intake,
might contribute. Prolonged bottle-feeding was
found to be significantly associated with both overweight
and iron-deficiency anemia in a survey of caregivers
of 95 WIC-enrolled children 18 to 56 months of
age.39 Children not weaned from the bottle at an appropriate
age may become accustomed to drinking
excessive amounts of milk and juices, thus having less
appetite for a more balanced and healthy diet.36,39 The
American Academy of Pediatrics’ recommendations
emphasize the role of diet in the prevention of iron
deficiency in children, because sufficient dietary intake
of iron is essential for toddlers to maintain a
positive iron balance.57
To our knowledge, this is the first study to report an
association between preschool/day care attendance and
iron deficiency in the United States, with day care being
protective against iron deficiency. One can only speculate
as to why preschool/day care attendance might be
protective against iron deficiency. It may be that children
in preschool/day care centers have better diets,
with higher amounts of iron, than children who do not
attend preschool/day care. It is possible that children
enrolled in preschool/day care are protected from adverse
nutritional practices, such as excessive milk or
juice intake, prolonged bottle-feeding, snacks, and junk
food intake, which may lead to iron deficiency. Little is
known about the quantity and types of foods and beverages
offered in child care facilities. More research is
needed to examine the nutritional quality of foods and
beverages served in childcare settings as well as staff
training on nutrition.58
Toddlers of parents who spoke a non–English language
during the NHANES IV interview had almost
twice the unadjusted odds of iron deficiency compared
with toddlers with parents interviewed in English. Interview
language is considered a crude proxy for acculturation
and is a central component of acculturation
scales.59,60 The NHANES IV is the first wave of this large
national survey to include a measure of acculturation,
using the language use subscale of the Short Acculturation
Scale for Hispanics.60 However, these questions regarding
acculturation are asked only of adolescents and
adults; in addition, there is no maternal-child link available
to provide data on maternal acculturation. The
study findings by interview language, however, suggest
that toddlers from less acculturated families could be at
greater risk of iron deficiency than toddlers from more
acculturated families. Education on appropriate infant
feeding practices by culturally competent physicians is
essential for these families. This is consistent with previous
research pointing to the role of cultural factors in
shaping infant feeding practices among Mexican American
families.36 Hispanic children have high rates of prolonged
bottle-feeding, and Hispanic normative cultural
values may be instrumental in shaping dietary practices.
36 Additional studies are needed to clarify the relationship
between acculturation and iron deficiency.
Household food insecurity was not associated with
iron-deficiency anemia in bivariate analyses, although
there was a trend toward significance, consistent with
recent work showing an association between food insecurity
and iron-deficiency anemia.61 A recent analysis of
data from the Children’s Sentinel Nutrition Assessment
Program showed an association between food insecurity
and iron-deficiency anemia.61 The authors proposed a
model in which food insecurity leads to decreased nutrient
intake, resulting in a host of negative consequences,
including iron-deficiency anemia. They argued
that policymakers need to expand programs and services
providing food assistance to families with young children.
Certain study limitations should be noted. First, certain
dietary information relevant to iron deficiency, such
as volumes of milk and iron-rich foods consumed, is not
available in the NHANES IV. Second, analyses of iron
deficiency among toddlers from other racial/ethnic
groups, particularly Native Americans and Asians/Pacific
Islanders, were not possible because of small sample
sizes. Third, the NHANES questions regarding acculturation
were asked only of adolescents and adults, and no
maternal-child link was available to provide data on
maternal acculturation. Hispanic toddlers from less acculturated
families may be at greatest risk of prolonged
bottle-feeding and iron deficiency. We plan to collect
data on maternal acculturation in future work to examine
its association with infant feeding behaviors and
iron-deficiency prevalence in Hispanic toddlers. Finally,
changes in the NHANES data set have limited the study
sample size and precluded examination of important
variables. Since 1971, the NHANES has been instrumental
as a national surveillance mechanism in the tracking
of iron deficiency and anemia among US children. However,
in the NHANES IV and future NHANES waves,
there are changes that will affect the ability of the survey
to serve as such a powerful surveillance mechanism.
Interview data are no longer being collected on several
key variables, including bottle-feeding duration and maternal
educational attainment. In addition, iron-status
measures will no longer be available for children 1 to 3
years old, starting with the NHANES 2003–2004. To be
effective in monitoring iron deficiency among US children,
the NHANES should once again consider collecting
these key measures for all children, and particularly
toddlers, a group at high risk for iron deficiency.
Community-based interventions should take into account
the increased risk of iron deficiency among overweight
toddlers, as well as the protective effects of day
care. The day care environment provides an ideal setting
in which to implement nutritional education programs
and other interventions.62 In Brazil, a recent study
showed that daily consumption of iron-fortified drinking
water in day care facilities is an effective, simple, and
inexpensive means of reducing moderate and severe
anemia in preschool children.63 Various behavior change
interventions have been tried in US day care settings
with some success.64,65 One of these studies evaluated the
effects of a preschool nutrition education and food service
intervention on 2- to 5-year-old children in 9 Head
Start Centers in upstate New York and found that the
intervention was effective in reducing the fat content of
preschool meals.65 Similar programs designed to improve
nutrition for toddlers in day care facilities might be ef-
fective in preventing both overweight and iron deficiency
in this age group.
CONCLUSIONS
Racial/ethnic disparities in the prevalence of iron deficiency
exist, with Hispanic toddlers twice as likely to be
iron deficient compared with white toddlers. Toddlers
who are overweight are at high risk of iron deficiency,
with 20% of overweight toddlers being iron deficient.
Day care/preschool attendance, on the other hand, is
protective against iron deficiency. Hispanic toddlers are
more likely than white and black toddlers to be overweight
and not in day care. The higher prevalence of
these nonethnic risk factors among Hispanic toddlers
may account for their increased risk of iron deficiency.
REFERENCES
1. National Center for Health Statistics. Plan and Operation of the
Third National Health and Nutrition Examination Survey (NHANES
III), 1988–1994. Hyattsville, MD: National Center for Health
Statistics; 1994
2. Looker AC, Dallman PR, Carroll MD, Bunter EW, Johnson CL.
Prevalence of iron deficiency in the United States. JAMA. 1997;
277:973–976
3. Oski FA. Iron deficiency in infancy and childhood. N Engl
J Med. 1993;329:190–193
4. Eiger M. Feeding of infants and children. In: Hoekelman R,
Adam H, Nelson N, Weitzman ML, Wilson M, eds. Primary
Pediatric Care. 4th ed. St Louis, MO: Mosby; 2001:1581–1586
5. Third Report on Nutrition Monitoring in the US. Bethesda, MD:
Federation of American Societies for Experimental Biology,
Life Sciences Research Office; 1995:2
6. Bogen DL, Duggan AK, Dover GH, Wilson MH. Screening for
iron deficiency by dietary history in a high-risk population.
Pediatrics. 2000;105:1254–1259
7. Politt E. Iron deficiency and cognitive function. Annu Rev Nutr.
1993;13:521–537
8. Lozoff B, Jiminez E, Wolf AW. Long-term developmental outcomes
of infants with iron deficiency. N Engl J Med. 1991;325:
687–694
9. Halterman JS, Kaczorowski JM, Aligne CA, Auinger P, Szilagyi
PG. Iron deficiency and cognitive achievement among schoolaged
children and adolescents in the United States. Pediatrics.
2001;107:1381–1386
10. Walter T, Kovalsky J, Sekel A. Effect of mild iron deficiency
anemia on infant mental development scores. J Pediatr. 1983;
102:519–522
11. Lozoff B, Brittenham GM, Wolf AW, et al. Iron deficiency
anemia and iron therapy: effects on infant development test
performance [published correction appears in Pediatrics. 1988;
81:683]. Pediatrics. 1987;79:981–985
12. Lozoff B, Smith J, Liberzon T, Argul-Barroso R, Jiminez E.
Longitudinal analysis of cognitive and motor effects of iron
deficiency in infancy [abstract]. Pediatr Res. 2004;55:23A
13. US Department of Health and Human Services. Tracking
Healthy People 2010. Washington, DC: US Government Printing
Office; 2000
14. Boutry M, Needleman R. Use of diet history in the screening of
iron deficiency. Pediatrics. 1996;98:1138–1142
15. Earl R, Woteki C. Iron Deficiency Anemia: Recommended Guidelines
for the Prevention, Detection, and Management Among US Children
and Women of Childbearing Age. Washington, DC: Institute of
Medicine, National Academy Press; 1993
16. US Department of Health and Human Services. Recommendations
to prevent and control iron deficiency in the United
States. MMWR Recomm Rep. 1998;47(RR-3):1–29
17. World Health Organization. Focusing on anaemia: towards an
integrated approach for effective anaemia control. Available at:
www.paho.org/English/AD/FCH/NU/WHO04_Anemia.pdf. Accessed
December 12, 2006
18. Florentino RF, Guirriec RM. Prevalence of nutritional anemia
in infancy and childhood with emphasis on developing countries.
In: Stekel A, ed. Iron Nutrition in Infancy and Childhood.
New York, NY: Raven Press; 1984:61–74
19. deMayer E, Adiels-Tegman M. The prevalence of anemia in the
world. World Health Stat Q. 1985;28:302–316
20. Coleman BL. Early introduction of non-formula cow’s milk to
southern Ontario infants. Can J Public Health. 2006;97:187–190
21. Christofides A, Schauer C, Zlotkin SH. Iron deficiency and
anemia prevalence and associated etiologic factors in First Nations
and Inuit communities in Northern Ontario and Nunavut.
Can J Public Health. 2005;96:304–307
22. Siegel EH, Stoltzfus RJ, Khatry SK, Leclerg SC, Tielsch JM.
Epidemiology of anemia among 4- to 17-month-old children
living in south central Nepal. Eur J Clin Nutr. 2006;60:228–235
23. Mamiro PS, Kolsteren P, Roberfroid D, Tatala S, Opsomer AS,
Van Camp JH. Feeding practices and factors contributing to
wasting, stunting, and iron-deficiency anemia among 3–23-
month old children in Kilosa district, rural Tanzania. J Health
Popul Nutr. 2005;23:222–230
24. Brabin BJ, Kalanda BF, Verhoeff FH, Chimsuku LH, Broadhead
RL. Risk factors for fetal anaemia in a malarious area of
Malawi. Ann Trop Paediatr. 2004;24:311–321
25. Meinzen-Derr JK, Guerrero ML, Altaye M, Ruiz-Palacios GM,
Morrow AL. Duration of exclusive breastfeeding and risk of
anemia in a cohort of Mexican infants. Adv Exper Med Biol.
2004;554:395–398
26. Miller CJ, Dunn EV, Abdouni SF, Shaheen HM, Ullah MS.
Factors associated with iron depletion and iron-deficiency anemia
among Arabic preschool children of the United Arab Emirates.
Saudi Med J. 2004;25:843–847
27. Soh P, Ferguson EL, McKenzie JE, Homs MY, Gibson RS. Iron
deficiency and risk factors for lower iron stores in 6–24-
month-old New Zealanders. Eur J Clin Nutr. 2004;58:71–79
28. Colomer J, Colomer C, Gutierrez D, et al. Anaemia during
pregnancy as a risk factor for infant iron deficiency: report
from the Valencia Infant Anaemia Cohort (VIAC) study. Paediatr
Perinat Epidemiol. 1990;4:196–204
29. Lozoff B, Jiminez E, Smith JB. Double burden of iron deficiency
in infancy and low socioeconomic status: a longitudinal
analysis of cognitive test scores to age 19 years. Arch Pediatr
Adolesc Med. 2006;160:1108–1113
30. Sargeant JD, Stukel TA, Dalton MA, Freeman JL, Brown MJ.
Iron deficiency in Massachusetts Communities: socioeconomic
and demographic risk factors among children. Am J Public
Health. 1996;86:544–550
31. Polhamus B, Dalenius K, Thompson D, et al. Pediatric Nutrition
Surveillance 2001 Report. Atlanta, GA: US Department of Health
and Human Services, Centers for Disease Control and
Prevention; 2003
32. Eden AN, Mir MA. Iron deficiency in 1- to 3-year-old children:
a pediatric failure? Arch Pediatr Adolesc Med. 1997;151:986–988
33. Geltman PL, Meyers AF, Mehta SD, Brugnara C, Villon I, Wu
YA, Bauchner H. Daily multivitamins with iron to prevent
anemia in high-risk infants: a randomized clinical trial. Pediatrics.
2004;114:86–93
34. Dallman PR, Siimes MA, Stekel A. Iron deficiency in infancy
and childhood. Am J Clin Nutr. 1980;33:86–118
35. Pizarro F, Yip R, Dallman PR, Olivares M, Hertrampf E, Walter
T. Iron status with different infant feeding regimens: relevance
to screening and prevention of iron deficiency. J Pediatr. 1991;
118:687–692
36. Brotanek JM, Halterman J, Auinger P, Flores G, Weitzman M.
Iron deficiency, prolonged bottle-feeding, and racial/ethnic
disparities in young children. Arch Pediatr Adolesc Med. 2005;
159:1038–1042
37. Graham EA, Carlson TH, Sodergren KK, Detter JC, Labbe RF.
Delayed bottle-weaning and iron deficiency in Southeast Asian
toddlers. West J Med. 1997;167:10–14
38. Lampe JB, Velez N. The effect of prolonged bottle-feeding on
cow’s milk intake and iron stores at 18 months of age. Clin
Pediatr (Phila). 1997;36:569–572
39. Bonuck KA, Kahn R. Prolonged bottle use and its association
with iron deficiency anemia and overweight: a preliminary
study [published correction appears in Clin Pediatr (Phila). 2003;
42:280]. Clin Pediatr (Phila). 2002;41:603–607
40. Sutcliffe TL, Khambalia A, Westergard S, Jacobson S, Peer M,
Parkin PC. Iron depletion is associated with daytime bottlefeeding
in the second and third years of life. Arch Pediatr Adolesc
Med. 2006;160:114–120
41. Centers for Disease Control and Prevention. NHANES
1999–2000 public release file documentation. Available at:
www.cdc.gov/nchs/about/major/nhanes/currentnhanes.htm.
Accessed January 4, 2007
42. Centers for Disease Control and Prevention. NHANES
2000–2001 Public release file documentation. Available at:
www.cdc.gov/nchs/about/major/nhanes/currentnhanes.htm.
Accessed January 4, 2007
43. Centers for Disease Control and Prevention. NHANES
1999–2000 public data release file documentation. Available
at: www.cdc.gov/nchs/data/nhanes/gendoc.pdf. Accessed January
4, 2007
44. National Center for Health Statistics. Analytic and Reporting
Guidelines: The National Health and Nutrition Examination Survey
(NHANES). Hyattsville, MD: National Center for Health
Statistics; 2006
45. Centers for Disease Control and Prevention. NHANES 1999–2000
sample person demographics file. Available at: www.cdc.gov/
nchs/data/nhanes/frequency/demo_doc.pdf. Accessed January
15, 2007
46. Centers for Disease Control and Prevention. NHANES 2001–2002
sample person demographics file. Available at: www.cdc.gov/
nchs/data/nhanes/nhanes_01_02/demo_b_doc_.pdf. Accessed
January 15, 2007
47. Bickel G, Nord M, Price C, Hamilton W, Cook J. Guide to
Measuring Household Food Security. Alexandria, VA: US Department
of Agriculture, Food, and Nutrition Service; 2000
48. American Academy of Pediatrics, Committee on Nutrition. The
use of whole cow’s milk in infancy. Pediatrics. 1992;89:
1105–1109
49. Gunter EW, Lewis BG, Koncikowski SM. Laboratory Procedures
Used for the Third National Health and Nutrition Examination
Survey (NHANES III), 1988–1994. Hyattsville, MD: Centers for
Disease Control and Prevention; 1996
50. Looker AC, Gunter EW, Johnson CL. Methods to assess iron
status in various NHANES surveys. Nutr Rev. 1995;53:246–254
51. Nead KG, Halterman JS, Kaczorowski JM, Auinger P, Weitzman
M. Overweight children and adolescents: a risk group for
iron deficiency. Pediatrics. 2004;114:104–108
52. Wenzel BJ, Stults HB, Mayer J. Hypoferraemia in obese adolescents.
Lancet. 1962;13:354–361
53. Seltzer CC, Mayer J. Serum iron and iron-binding capacity in
adolescents: part II—comparison of obese and nonobese subjects.
Am J Clin Nutr. 1963;13:354–328
54. Pinhas-Hamiel O, Newfield RS, Koren I, Agmon A, Lilos P,
Phillip M. Greater prevalence of iron deficiency in overweight
and obese children and adolescents. Int J Obes Relat Metab
Disord. 2003;27:416–418
55. Kennedy ML, Failla ML, Smith JC. Influence of genetic obesity
on tissue concentrations of zinc, copper, manganese, and iron
in mice. J Nutr. 1986;116:1432–1441
56. Failla ML, Kennedy ML, Chen ML. Iron metabolism in genetically
obese (ob/ob) mice. J Nutr. 1988;118:46–51
57. Kleinman RE, ed. Pediatric Nutrition Handbook. 5th ed. Elk
Grove Village, IL: American Academy of Pediatrics; 2004
58. Story M, Kaphingst KM, French S. The role of child care
settings in obesity prevention. Future Child. 2006;16:143–168
59. Flores G, Brotanek J. The healthy immigrant effect: a greater
understanding might help us improve the health of all children.
Arch Pediatr Adolesc Med. 2005;159:295–297
60. Marin G, Sabogal F, Marı´n BV, Otero-Sabogal R, Pe´ rez-Stable
E. Development of a short acculturation scale for Hispanics.
Hisp J Behav Sci. 1987;9:183–205
61. Skalicky A, Meyers AF, Adams WG, Yang A, Cook JT, Frank
DA. Child food insecurity and iron deficiency anemia in lowincome
infants and toddlers in the United States. Matern Child
Health J. 2006;10:177–185
62. Taveras EM, LaPelle N, Gupta RS, Finkelstein JA. Planning for
health promotion in low-income preschool child care settings:
focus groups of parents and child care providers. Ambul Pediatr.
2006;6:342–346
63. Beinner MA, Lamounier JA, Tomaz C. Effect of iron-fortified
drinking water of daycare facilities on the hemoglobin status of
young children. J Am Coll Nutr. 2005;24:107–114
64. Dennison BA, Erb TA, Jenkins PL. Television viewing and
television in bedroom associated with overweight risk among
low-income preschool children. Pediatrics. 2002;109:
1028–1035
65. Williams CL, Bollella MC, Strobino BA, et al. “Healthy-Start”:
outcome of an intervention to promote a heart healthy diet in
preschool children. J Am Coll Nutr. 2002;21:62–71
