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