RESEARCH

Research and Professional Briefs

Iron Deciency Is Associated with Food Insecurity
in Pregnant Females in the United States: National
Health and Nutrition Examination Survey 1999-2010
Clara Y. Park, PhD; Heather A. Eicher-Miller, PhD
ARTICLE INFORMATION
Article history:
Accepted 24 April 2014
Keywords:
Iron deciency
Pregnancy
Food security
Iron intake
National Health and Nutrition Examination Survey
(NHANES)
Copyright 2014 by the Academy of Nutrition
and Dietetics.
2212-2672/$36.00
http://dx.doi.org/10.1016/j.jand.2014.04.025
ABSTRACT
Food-insecure pregnant females may be at greater risk of iron deciency (ID) because
nutrition needs increase and more resources are needed to secure food during preg-
nancy. This may result in a higher risk of infant low birth weight and possibly cognitive
impairment in the neonate. The relationships of food insecurity and poverty income
ratio (PIR) with iron intake and ID among pregnant females in the United States were
investigated using National Health and Nutrition Examination Survey 1999-2010 data
(n1,045). Food security status was classied using the US Food Security Survey
Module. One 24-hour dietary recall and a 30-day supplement recall were used to assess
iron intake. Ferritin, soluble transferrin receptor, or total body iron classied ID. Dif-
ference of supplement intake prevalence, difference in mean iron intake, and associa-
tion of ID and food security status or PIR were assessed using c
2
analysis, Student t test,
and logistic regression analysis (adjusted for age, race, survey year, PIR/food security
status, education, parity, trimester, smoking, C-reactive protein level, and health in-
surance coverage), respectively. Mean dietary iron intake was similar among groups.
Mean supplemental and total iron intake were lower, whereas odds of ID, classied by
ferritin status, were 2.90 times higher for food-insecure pregnant females compared
with food-secure pregnant females. Other indicators of ID were not associated with food
security status. PIR was not associated with iron intake or ID. Food insecurity status may
be a better indicator compared with income status to identify populations at whom to
direct interventions aimed at improving access and education regarding iron-rich foods
and supplements.
J Acad Nutr Diet. 2014;-:---.
I
RON DEFICIENCY (ID) IS ONE OF THE MOST COMMON
nutritional deciencies. Among pregnant females in the
United States, 16.1% were ID during 2003-2006.
1
Low
maternal iron status is correlated with low and very-
low infant birth weight,
2,3
preterm birth,
4
and low infant iron
stores.
5,6
Low iron status during infancy has been linked with
learning and memory decits and mental retardation.
7-9
Accordingly, the World Health Organization recommends
iron supplementation
10
and the Healthy People 2020 objec-
tives include the reduction of ID status
11
among pregnant fe-
males. Despite the greater iron needs during pregnancy,
12
females in this life stage may have less energy and ability
to prepare foods due to physical constraints. Pregnancy
may also increase nancial burden because greater energy
and nutrients are necessary to support the pregnancy and
decreased or refrained employment may occur. This may
exacerbate the difculties food-insecure pregnant females
face to meet their nutrition needs and may incur food insecu-
rity among females who were food secure preceding preg-
nancy. Alternatively, pregnant females might be protected
from nutritional decits related to food insecurity by the
prioritized receipt of nutritious food and supplements within
the household.
Few studies investigating the relationship of food insecu-
rity, iron intake, and ID have been documented among
pregnant females. Previous research completed among chil-
dren,
13,14
women with children,
15
and elderly persons
15,16
have shown greater likelihood for ID anemia and lower iron
intakes among food-insecure compared with food-secure
groups. Among pregnant women living in North Carolina,
food insecurity was not associated with anemia,
17
but the
relationships of food security to iron intake and status have
not been described for all US pregnant females.
Although the lack of access to food might facilitate the
relationship of food insecurity to low iron intake and status
among food-insecure groups, the low purchasing ability of
those with a reduced household poverty income ratio (PIR)
may facilitate a relationship to low iron intake and status
among groups with low PIR. Food-insecure and reduced-PIR
groups are similar but may comprise slightly different
populations, resulting in the mixed ndings describing the
relationship of PIR to iron intake and status in previous
2014 by the Academy of Nutrition and Dietetics. JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 1
studies.
18-22
Therefore, both food insecurity and PIR were
examined in our study using a hypothesis that food-insecure
pregnant females in the United States have lower iron intake
from food, beverages, and supplements and higher odds of ID
compared with food-secure pregnant females. In addition,
the hypothesis that pregnant females in the United States
with low PIR status have lower iron intake from diet and
supplements and higher odds of ID compared to those with
higher PIR status was also tested.
SUBJECTS AND METHODS
Study Population
National Health and Nutrition Examination Survey (NHANES)
data collected during 1999-2010 were used. NHANES pro-
vides a cross-sectional representation of the health status
and nutrition-related behaviors of noninstitutionalized
civilian residents of the United States. Oversampling was
performed for pregnant females during 1999-2006.
23-26
The study population was limited to participants with a
positive urine pregnancy test that was performed at the
mobile examination center (MEC) (n1,383). Pregnant fe-
males missing food security status (n53), Day 1 24-hour
dietary recall (n42), iron status (n85), or family PIR sta-
tus (n69), and those whose race was not categorized as
non-Hispanic white, non-Hispanic black, or Hispanic (n69)
were excluded. A total of 1,045 females were included (aged
13 to 54 years). The National Center for Health Statistics
Research Ethics Review Board approved the protocol for all
NHANES content.
27
Dietary Assessment
Dietary iron and energy intake information was obtained
from the 24-hour dietary recall.
28,29
Mean daily supple-
mental iron intake was calculated from the 30-day dietary
supplement questionnaire.
30,31
Total iron intake was deter-
mined as the sum of 24-hour dietary iron intake and
mean daily supplemental iron intake. Only participants
with complete information of iron supplement use or self-
reported nonusers were included to calculate the mean
daily iron supplement intake and total iron intake. Categor-
ical variables for dietary iron intake were created as less
than or greater than or equal to the Estimated Average
Requirement (EAR) for pregnant females (aged 14 to 18
years: 23 mg/day; aged 19 to 50 years: 22 mg/day
32
). Energy
intake was categorized (ie, <1,500, 1,500 to 2,800, and
>2,800 kcal/day).
Iron Status Assessment and Other Laboratory
Examinations
Serum ferritin was assessed by immunoturbidimetric
(NHANES 1999-2002 and 2004-2008), immunoradiometric
(NHANES 2003), or sandwich immunoassay (NHANES 2009-
2010) and adjusted for comparability.
33,34
Details of analyses
of soluble transferrin receptor (sTfR), hemoglobin, and he-
matocrit are provided elsewhere.
23-26,35
Total body iron (TBI) calculations were computed using the
equation developed by Cook and colleagues.
36,37
An equation
was used to adjust sTfR obtained through the Roche method
(used by NHANES) to values equivalent to the Flowers
method (used by Cook and colleagues).
19,38,39
Afterward, TBI
was calculated as:
TBImg=kglog10sTfR1;000=ferritin2:8229=0:1207
Iron deciency was recognized if TBI <0 mg/kg, sTfR
>4.4 mg/L,
19,40
or ferritin <12 mg/L for all races.
C-reactive protein (CRP) was categorized as 5 mg/L or
>5 mg/L.
19
Comparison between food-secure females and
food-insecure females among those without inammation
present, indicated by CRP 5 mg/L, was not possible due to
the inadequate sample size of food-insecure females (n66).
Food Security Assessment and Classication of
Other Characteristics
Food security was assessed using the US Food Security Survey
Module. During NHANES 1999-2002, the questionnaire was
administered as part of the household interview to one adult
to classify food security among household adults or children.
Individual-level food security status was determined at the
MEC since 2001 for adults (aged 16 years) and children
(aged <12 years), and for adolescents (aged 12 to 15 years)
from 2005 onward.
41
Food security status was dened as
either food secure or food insecure. For adults (aged 16
years) food secure classication included full food secu-
rity and marginal food security, whereas food insecure
encompassed low food security and very low food secu-
rity. Child (aged <16 years) food security classication fol-
lowed a similar classication scheme.
Age was categorized as <20 years, 20 to 29 years, and 30
years at the time of the in-house survey. Race/ethnicity was
self-reported and categorized as non-Hispanic white, non-
Hispanic black, or Mexican American/other Hispanic. Other
race/ethnic classications were not sampled to be represen-
tative and, thus, were not included in the analyses. Survey
year was categorized as 1999-2000, 2001-2002, 2003-2004,
and 2005-2010. Years 2005-2010 comprise a greater span of
time due to the small sample size representing years 2007-
2010 when the oversampling of pregnant females was dis-
continued. Income was determined by family PIR and was
categorized as 75% PIR, 76% to 130% PIR, or >130% PIR to
ensure adequate sample size for the analyses and because the
130% cutoff is frequently used to determine eligibility for
government programs. Education was categorized as less
than high school or high school graduate/General Educational
Development diploma. Smoking was determined by self-
reported use (yes or no) of any tobacco product within the
past 5 days. Parity was determined by the reported number of
live births from a previous pregnancy and was categorized as
zero to one, 2, or missing to maintain adequate sample size
for the analysis. Trimester (3 months, 4 to 6 months, or 7
months pregnant) was classied by the reported number of
months of pregnancy at the time of the in-house visit.
Missing trimester data of 161 females (13.7% of the sample)
were categorized as missing. Special Nutrition Assistance
Program (previously known as Food Stamps) receipt was not
included as a variable because 50% of participants were
missing data. Current household receipt of Special Supple-
mental Nutrition Program for Women, Infants, and Children
benets was considered as a covariate in the analysis
but ultimately not included because it did not affect the as-
sociations reported nor was it a signicant variable in the
RESEARCH
2 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume - Number -
regression models. Coverage by any type of health insurance
(yes or no) was also assessed by questionnaire. Mean age,
distribution of education, smoking status, parity, trimester,
and health insurance coverage rate among the pregnant fe-
males excluded from the analyses did not differ from those
included in the analyses.
Statistical Analysis
Differences in characteristics and prevalence of supplement
intake and ID among food security groups were investigated
using Rao-Scott c
2
analysis. Geometric means of diet (food
and beverage), supplement, and total iron intake were
calculated and compared by t test. To account for those
consuming no iron from diet and the nonnormal distribution
of iron intake, a ln(x1) transformation was applied. Logistic
regression analysis determined the odds of low dietary iron
intake and ID by food security status and PIR levels. All lo-
gistic regression models were adjusted for age, race, survey
year, education, parity, trimester, health insurance coverage,
and either food security or PIR. ID models were additionally
controlled for smoking and CRP, whereas the dietary iron
intake model was additionally controlled for energy intake.
Day 1 dietary weights (WTD4YR/3 [1999-2002], WTDRD/6
[2003-2010]) and MEC weights (WTMEC4YR/3 [1999-2002],
WTMEC2YR/6 [2003-2010]) were applied to iron intake and
ID models, respectively. Analysis was performed using SAS
9.2 (2002, SAS Institute Inc). Null hypotheses were rejected
when P<0.05.
RESULTS AND DISCUSSION
Among the total 1,045 pregnant females, 881 were food
secure and 164 were food insecure. The distributions of race,
PIR, education, smoking status, and health insurance
coverage differed among the food-secure and food-insecure
pregnant females (Table 1).
Meanstandard error of the mean iron intake from diet
(food and beverage) of the population was 151 mg/day,
which is 7 to 8 mg/day lower than the EAR, and did not differ
between the food-secure and food-insecure respondents
(Table 2). Dietary iron intake was not associated with food
security status (data not shown).
Mean daily iron intake from supplements among supple-
ment users was 10 mg/day higher among food-secure preg-
nant females compared with food insecure pregnant females
(P0.02) (Table 2). As a result, mean total (diet plus supple-
ment) iron intake was higher in food-secure pregnant fe-
males compared with those who were food insecure (38 and
26 mg/day, respectively; P0.002). Both groups mean total
iron intake surpassed the EAR. However, the prevalence of
iron-containing supplement consumption was not signi-
cantly different between food-secure or food-insecure preg-
nant females with complete supplement consumption data.
The higher iron intake from supplements despite the similar
prevalence of supplement intake in food-secure compared
with food-insecure pregnant females suggests more frequent
prescription, adherence to prescribed intake schedule, and
intake monitoring in the former population. Also, food-secure
females may have more access to and awareness of the need
for iron supplements compared with food-insecure females,
as evidenced by the higher rate for health insurance coverage
and education.
When using ferritin to classify ID, food-insecure pregnant
females had a higher prevalence of ID (31% vs 22% in food-
secure females; P0.0025) (Table 2) and were 2.90-fold more
likely to have ID than food-secure pregnant females after
adjusting for covariates (P<0.05) (Table 3). The lower prev-
alence and risk of ID in food-secure pregnant females may be
due to differences in the amount and source of iron intake.
First, supplemental iron intake may strongly inuence iron
status. Iron supplement use, but not dietary iron intake, is
associated with lower odds of ID and higher iron status in
nonpregnant US women
18
and has been reported to be an
effective method to increase iron status in controlled trials.
42-44
Interestingly, the higher risk of ID in food-insecure females
despite adjustment for health insurance coverage indicates
that these females may have less physical access to and/or
awareness of health care services and healthy behaviors, or
have other priorities in use of time and nances compared
with food-secure females. Second, bioavailability of dietary
iron may differ among food-secure and food-insecure fe-
males despite similar intake. Heme iron is used more ef-
ciently than nonheme iron, whereas nonheme iron
absorption is negatively associated with maternal iron status
and the iron dose consumed.
45
Sources of heme iron (ie, red
meat, sh, and poultry) may be more expensive compared
with foods high in nonheme iron, such as lentils, beans, and
iron-enriched and iron-fortied cereals and foods.
46,47
This
may decrease the availability of heme ironecontaining foods
for persons with food insecurity. Hence, increased and
consistent intake of supplemental iron and heme iron may be
an effective strategy to prevent further ID especially among
food-insecure pregnant females.
Neither prevalence nor odds for ID classied by TBI and
sTfR were different among food security groups. The low
number of food-insecure pregnant females with ID by TBI
(n32) and sTfR (n39) may be a cause of these results.
However, another explanation of the different association
with food security status among ID markers (ferritin vs TBI
and sTfR) may be provided by the stages of iron depletion
that each marker indicates. Previous reports suggest that low
ferritin precedes the depletion of functional or tissue iron
stores, which is indicated by high sTfR concentrations and
low TBI.
48,49
In light of these ndings, food-insecure females
may be more likely to experience functional ID and anemia
postpartum due to blood loss during delivery. Thus, our re-
sults suggest a need for additional screening among pregnant
and postpartum food-insecure females to prevent ID and
anemia.
PIR was also not associated with iron intake or ID (data not
shown). PIR and food security may be closely related, but
their associations with iron intake and status are clearly
different. Those at 130% PIR are eligible for many federal
assistance programs, but pregnant females with lower in-
come are reported to be less likely to take iron-containing
supplements.
50
Others have also found no association of PIR
with ID or anemia in non-Hispanic white women and preg-
nant US women.
19
Perhaps food-insecure, rather than low-
PIR, females should be the population specically targeted
to receive supplemental iron and heme sources of dietary
iron during pregnancy.
A limitation of our investigation was the differential
timeframe for assessment of food security and PIR
(12 months), iron intake (24 hours), iron supplementation
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-- 2014 Volume - Number - JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 3
Table 1. Characteristics of 1,045 pregnant female participants in the National Health and Nutrition Examination Survey
1999-2010 by food security status (aged 13 to 54 y)
a
Characteristic
Food Secure (n[881) Food Insecure (n[164)
Weighted c
2
P value
b
n
Percentage
n
Percentage
Unweighted Weighted Unweighted Weighted
Age (y) 0.24
<20 106 12 71 26 16 103
20-29 492 56 553 100 61 585
30 283 32 392 38 23 326
Race <0.0001
Non-Hispanic white 461 52 643 30 18 308
Non-Hispanic black 143 16 152 27 16 216
Mexican Americans /other Hispanics 277 31 202 107 65 507
Survey year 0.94
1999-2000 161 18 192 29 19 166
2001-2002 219 25 192 35 21 205
2003-2004 181 21 172 28 18 156
2005-2010 320 36 453 72 42 497
Poverty income ratio (%) <0.0001
75 143 16 111 72 44 466
76-130 128 15 101 52 32 264
>130 610 69 792 40 24 287
Education <0.0001
<High school/GED
c
237 27 192 96 59 486
Parity 0.75
0-1 353 40 433 53 32 377
2 256 29 293 66 40 316
Missing 272 31 283 45 27 316
Trimester 0.19
1 145 16 222 33 20 184
2 317 36 303 53 32 286
3 302 34 313 43 26 266
Missing 117 13 172 35 21 286
Smoking
d
<0.0001
Yes 84 10 102 29 19 285
C-reactive protein 0.33
>5 mg/L 452 51 483 98 60 546
Health insurance coverage
e
Yes 763 88 901 97 59 655 <0.0001
a
Total of percentages may exceed 100 due to rounding.
b
Weights from the mobile examination center visit (WTMEC4YR/3 [1999-2002], WTMEC2YR/6 [2003-2010]) were applied according to the directions of the Centers for Disease Control and
Prevention.
c
GEDgeneral education development diploma.
d
Forty-nine subjects are missing data.
e
One subject is missing data.
RESEARCH
4 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume - Number -
(30 days), pregnancy (<10 months), and iron markers
(<4 months). A 24-hour dietary recall may provide a partic-
ularly crude estimate of mean dietary iron intake for the
small sample of food-insecure pregnant females. However,
because NHANES has discontinued the oversampling of
pregnant females and 2-day diet recalls were only available
for 51% of our study population, our analysis was an optimal
opportunity for a nationally representative analysis. In addi-
tion, self-reported diet and supplement intake may be biased.
Erroneous reporting of energy intake is common among fe-
males
51-53
and may indicate erroneous iron intake because
energy and iron intake are positively associated. Actual iron
intake is most likely higher than indicated in these results.
NHANES data do not include participants who are homeless
or those temporarily residing in shelters, which may make up
a signicant portion of the food-insecure population. Finally,
the cross-sectional data used in this analysis did not provide
information on the cause of ID, nor whether this status was
due to prepregnancy nutritional status.
CONCLUSIONS
Our study is the rst to compare iron intake and ID among
food-secure and food-insecure pregnant females in the
United States using a nationally representative dataset. Food-
insecure pregnant females have similar mean dietary intakes
of iron but consume less iron from supplements and, thus,
have lower total iron intake compared with food-secure
pregnant females. Food-insecure pregnant females are more
likely to deplete circulating iron stores, but not functional
iron, compared with food-secure females. However, iron
intake and risk of ID was not different among different PIR
statuses. Public health policy should continue to focus on
improving access to iron-rich foods and iron supplements for
food-insecure pregnant females.
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a
Food secure Food insecure P value
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b
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c
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a
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a
Logistic regression analysis was used to estimate the odds ratio of iron deciency for
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AUTHOR INFORMATION
C. Y. Park is a postdoctoral fellow, Department of Nutrition Science, Purdue University, West Lafayette, IN, and a postdoctoral fellow, Department
of Biochemistry and Cell Biology, BK21 Plus KNU Biomedical Convergence Program, Kyungpook National University School of Medicine, Daegu,
Korea. H. A. Eicher-Miller is an assistant professor, Department of Nutrition Science, Purdue University, West Lafayette, IN.
Address correspondence to: Heather A. Eicher-Miller, PhD, Department of Nutrition Science, Purdue University, 700 W State St, West Lafayette,
IN 47907-2059. E-mail: heicherm@purdue.edu
STATEMENT OF POTENTIAL CONFLICT OF INTEREST
No potential conict of interest was reported by the authors.
FUNDING/SUPPORT
This research was funded by the Department of Nutrition Science, Purdue University, West Lafayette, IN.
ACKNOWLEDGEMENTS
The authors thank Amy Branum, PhD, MSPH, branch chief of the Reproductive Statistics Branch at the National Center for Health Statistics, for her
thoughtful review and helpful comments.
RESEARCH
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