Effect of iron-fortified foods on hematologic and biological outcomes:
systematic review of randomized controlled trials14
Tarun Gera, Harshpal Singh Sachdev, and Erick Boy
ABSTRACT
Background: The utility of iron fortification of food to improve
iron deficiency, anemia, and biological outcomes is not proven un-
equivocally.
Objectives: The objectives were to evaluate 1) the effect of iron
fortification on hemoglobin and serum ferritin and the prevalence
of iron deficiency and anemia, 2) the possible predictors of a pos-
itive hemoglobin response, 3) the effect of iron fortification on
zinc and iron status, and 4) the effect of iron-fortified foods on
mental and motor development, anthropometric measures, and
infections.
Design: Randomized and pseudorandomized controlled trials
that included food fortification or biofortification with iron were
included.
Results: Data from 60 trials showed that iron fortification of foods
resulted in a significant increase in hemoglobin (0.42 g/dL; 95% CI:
0.28, 0.56; P , 0.001) and serum ferritin (1.36 lg/L; 95% CI: 1.23,
1.52; P , 0.001), a reduced risk of anemia (RR: 0.59; 95% CI: 0.48,
0.71; P , 0.001) and iron deficiency (RR: 0.48; 95% CI: 0.38, 0.62;
P , 0.001), improvement in other indicators of iron nutriture, and
no effect on serum zinc concentrations, infections, physical growth,
and mental and motor development. Significant heterogeneity was
observed for most of the evaluated outcomes. Sensitivity analyses
and meta-regression for hemoglobin suggested a higher response
with lower trial quality (suboptimal allocation concealment and
blinding), use of condiments, and sodium iron edetate and a lower
response when adults were included.
Conclusion: Consumption of iron-fortified foods results in an im-
provement in hemoglobin, serum ferritin, and iron nutriture and
a reduced risk of remaining anemic and iron deficient. Am J
Clin Nutr 2012;96:30924.
INTRODUCTION
Iron deficiency anemia is a widespread problem with health
and economic consequences, such as poor cognitive development
in children, lower worker productivity, and increased maternal
mortality (1, 2). Anemia affects nearly one-third of the worlds
population, primarily infants and young children from de-
veloping countries (35).
Dietary strategies to counter anemia include iron supple-
mentation, food fortification, or dietary modification. Food for-
tification is often propagated as the most realistic way to increase
iron intake on a widespread and sustainable basis and is currently
implemented in the United States, Britain, and most of Latin
America, among other locations. Currently, biofortification of
Am J Clin Nutr 2012;96:30924. Printed in USA. 2012 American Society for Nutrition
crops is also being intensively evaluated as a more sustainable
and complementary alternative to food fortification.
Hemoglobin and ferritin are currently considered the most
efficient indicators of population response to iron interventions
(6). Relevant randomized controlled trials provide conflicting
evidence regarding the utility of iron-fortified foods in improving
the iron status and reducing anemia in populations (79). A recent
systematic review of randomized controlled trials in children
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documented that iron-fortified foods resulted in a substantially
lower average hemoglobin response in comparison with oral
medicinal iron supplementation (0.25 compared with 0.74 g/dL)
(7). The success of iron-fortified food interventions depends on
several factors, including the consumption pattern of the fortified
food, effect of the fortificants on the taste and appearance of the
food vehicle, shelf life of the fortified food, bioavailability of the
iron fortificants, and the baseline iron status of the population (10,
11), which need greater evaluation for the success of this strategy.
A new dimension has been added with the emergence of zinc
as an important micronutrient for child health (12). Iron and zinc
deficiencies frequently coexist in populations that consume diets
with insufficient animal-source foods (13). Iron and zinc have
been thought to compete for absorptive pathways at the enter-
ocyte level (14). It is, therefore, important to determine how iron
fortification of foods affects zinc deficiency, particularly in
vegetarian populations subsisting on borderline zinc nutriture.
Policy makers, program implementers, and the target pop-
ulation need to carefully weigh the benefits and safety of food
fortification and biofortification with iron before recommend-
ing them for populations. The current systematic review was
therefore conducted to evaluate 1) the effect of iron-fortified
foods and biofortified crops on hemoglobin and serum ferritin
and the prevalence of iron deficiency and anemia and other
1
From the S.L. Jain Hospital, Delhi, India (TG); the Sitaram Bhartia
Institute of Science and Research, New Delhi, India (HSS); and the Inter-
national Food Policy Research Institute, Washington, DC (EB).
2
Protocol available from http://www.harvestplus.org/content/iron-fortified-
foods-protocol.
3
Supported by research agreement no. 2006X053SAC from the Interna-
tional Food Policy Research Institute, 2033 K Street, NW Washington, DC
20006. Time support was provided by the Sitaram Bhartia Institute of Sci-
ence and Research, New Delhi, India (to HSS).
4
Address correspondence and reprint requests to HS Sachdev, E-6/12
Vasant Vihar, New Delhi 110057, India. E-mail: hpssachdev@gmail.com.
Received December 12, 2011. Accepted for publication April 13, 2012.
First published online July 3, 2012; doi: 10.3945/ajcn.111.031500.
309
Supplemental Material can be found at:
http://ajcn.nutrition.org/content/suppl/2012/07/31/ajcn.111.0
31500.DC1.html
310 GERA ET AL
biochemical indicators of iron status; 2) possible predictors of
a positive response, particularly focusing on the food vehicle,
iron fortification compound, iron content, baseline hemoglobin
and ferritin concentrations, and duration of fortification; 3) the
effect of iron-fortified foods and biofortified crops on zinc sta-
tus; and 4) the effect of iron-fortified foods on other functional
outcomes, namely mental and motor development, anthropo-
metric measures, and infections.
SUBJECTS AND METHODS
Types of trials
The predefined criteria for inclusion were randomized placebo-
controlled trials with variations in design, including random
allocation of individuals or clusters; multi-arm trials; factorial
trials; and crossover trials for the first period of measurement
only. Quasirandomized controlled trials were also eligible for
inclusion.
Types of participants
The participants were apparently healthy (nondiseased) in-
dividuals, families, or communities irrespective of age and sex
considerations. Trials conducted exclusively in specifically dis-
eased participants (eg, those with AIDS or tuberculosis or in-
habitants of mental rehabilitation centers) were excluded.
Intervention
The intervention was additional dietary iron through the route
of food fortification or biofortification. Food for the purpose of
this systematic review was defined as a usually consumed dietary
item in the population, either in a raw or cooked form. Use of iron
as a separate additive to dietary items (eg, as sprinkles) was not
considered food fortification.
Comparison
Participants provided similar food without iron fortification
served as the comparison group. Trials with simultaneous for-
tification of additional micronutrients were included if the only
difference between the intervention and comparison arms was iron
fortification. Similarly, trials using simultaneous co-interventions,
such as health education and/or drugs (eg, deworming or anti-
malarials), were included if the only difference between the in-
tervention and comparison arms was iron fortification.
Outcome measures
The primary outcomes evaluated included 1) hemoglobin
(g/dL), 2) anemia (%, as defined in individual trials), 3) serum
ferritin (lg/L), 4) iron deficiency (%, as defined in individual
trials), and 5) serum or plasma zinc (lmol/L). Secondary out-
comes evaluated included the following: 1) serum transferrin
receptor, 2) transferrin saturation (%), 3) total-iron-binding ca-
pacity, 4) serum or plasma iron, 5) zinc protoporphyrin, 6) ad-
verse effects (any, as defined in individual trials), 7) malaria (as
defined in individual trials), 8) diarrhea (as defined in individual
trials), 9) pneumonia or acute lower respiratory tract infections
(as defined in individual trials), 10) upper respiratory tract in-
fections (as defined in individual trials), 11) weight-for-age in
children aged ,5 y (z scores or crude weight), 12) height-for-
age in children aged ,5 y (z scores or crude height), 13) weight-
for-height in children aged ,5 y (z scores), 14) cognitive or
mental development in children aged ,18 y (specific tests re-
ported in individual trials), and 15) motor development in children
aged ,18 y (specific tests reported in individual trials).
Method for identification of trials
We aimed to identify all relevant trials regardless of language or
publication status. Computerized bibliographic databases, including
PubMed (www.ncbi.nlm.nih.gov/pubmed), Embase (www.embase.
com), Web of Knowledge (http://thomsonreuters.com/products_
services/science/science_products/a-z/isi_web_of_knowledge/),
Cochrane Controlled Trials Register (http://onlinelibrary.wiley.
com/o/cochrane/cochrane_clcentral_articles_fs.html), and In-
ternational Bibliographic Information on Dietary Supplements
(http://ods.od.nih.gov/health_information/ibids.aspx) were searched
by using appropriate key words. Websites of the organizations
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such as the Food and Agriculture Organization (www.fao.org),
International Nutritional Anemia Consultative Group (http://
www.ilsi.org/ResearchFoundation/Pages/INACG-IVACG.aspx),
International Food Policy Research Institute (www.ifpri.org),
Micronutrient Initiative (www.micronutrient.org), and Micro-
nutrient Forum (www.micronutrientforum.org) were searched, and
key researchers working in the field were contacted to identify
ongoing and unpublished trials. The reference lists of the identified
articles were also reviewed to search for citations that were not
listed in the computerized databases, which were supplemented by
hand searches of reviews and proceedings over the past 3 y of
Micronutrient Forum international conferences or meetings.
Data collection and analyses
The title and abstract of the trials identified were scanned in
duplicate to exclude studies that were obviously irrelevant. The
full text of the remaining trials was retrieved, and the relevant
reports were identified and the data were extracted by 2 in-
vestigators independently. Differences in opinion (if any) were
resolved by mutual discussion. The data included in the review
were derived from the published manuscript or as provided by the
authors for unpublished studies. The authors were contacted for
clarifications, if required.
Assessment of quality and risk of bias
Trial quality and risk of bias were evaluated by considering 6
features (Cochrane recommendations): sequence generation,
allocation sequence concealment, blinding, incomplete outcome
data, selective outcome reporting, and other potential sources
of bias (15).
Quantitative data synthesis
In factorial trials and in multi-arm designs yielding 2 iron-
intervention groups (eg, different dose or duration or iron salts)
and a single control group, the data in the intervention groups,
including the variation in the intervention characteristic, were
pooled and compared against the single comparison arm to
prevent unit-of-analysis error (16). However, for sensitivity
 IRON FORTIFICATION AND HEMATOLOGIC OUTCOMES
and subgroup analyses [eg, multi-arm designs using iron salts
with wide variation in bioavailability, such as ferrous sulfate or
fumarate compared with sodium iron edetate (NaFeEDTA)], we
split the shared comparison group into 2 groups with smaller
sample sizes (analytic components) and included 2 (reason-
ably independent) comparisons. For dichotomous outcomes,
both the number of events and the total number of participants
were divided up. For continuous outcomes, only the total number
of participants was divided up, and the means and SDs were left
unchanged (16).
For variables usually known to have a skewed distribution
(eg, serum ferritin and serum transferrin receptor), pooling was
performed on natural logarithmtransformed values (17). To
maximize the data input for pooled outcome measures, we
primarily used the postintervention values (means and SDs) in
preference to the changes from baseline, which were not
reported in all trials (18). For the primary outcome variable
hemoglobin, we also performed the pooled analyses for
changed values without imputing variances (19) for trials not
providing such data. For cluster-randomized trials, the stated
cluster-adjusted values were used, irrespective of the method
used.
Data entry and initial analysis were performed by using SPSS
(version 17.0) software. Meta-analysis and meta-regression were
performed with user-written programs on Stata (version 9.2)
software. The presence of bias in the extracted data were eval-
uated quasistatistically by using the funnel plot (20). Formal
statistical tests for funnel plot asymmetry, namely the Beggs and
Eggers methods, were also conducted with the user-written
metabias command in Stata (21, 22). Pooled estimates of the
evaluated outcome measures were primarily calculated by using
the generic inverse variance method by using the user-written
metan command in Stata (21, 23). This program also computes
the formal tests of heterogeneity, namely the Cochran Q and I2
statistics (24). Binary outcomes were pooled as RRs and 95%
CIs. If the continuous outcome variable was reported in different
units or measurements across trials, effort was made to convert
them to one standard unit for pooled estimates; when this was
not possible, the standardized mean difference was used instead
of the weighted mean difference (WMD). Pooled estimates were
made by using both fixed-effects and random-effects model
assumptions. The random-effects model was preferred if there
was evidence of significant heterogeneity (I2 . 25% and/or P ,
0.05 for Cochran Q).
Sensitivity and subgroup analyses (specified below) were
conducted for the primary outcome hemoglobin to explore
predictors of positive response. This was done by disaggregating
results with the user-written metan command (by option) in
Stata (21, 23). The contribution of these variables to heterogeneity
was also explored by meta-regression by using the metareg
command in Stata with the restricted maximum likelihood option
(25). The specified variables for subgroup analyses and metare-
gression included the following: 1) risk of bias (low compared
with others) (26), 2) age group (only children compared with
adults included), 3) fortification vehicle, 4) fortification com-
pound, 5) iron consumed as fortificant (mg), 6) fortification du-
ration (mo), 7) compliance estimation (directly observed or
replacement compared with others), 8) baseline hemoglobin (12
compared with .12 g/dL), 9) baseline serum ferritin (geometric
mean 20 compared with .20 lg/L), 10) geographic location
311
(developed compared with developing countries and malarial en-
demic areas compared with malarial nonendemic areas), and 11)
type of trial (cluster or individual randomized or quasirandomized).
We report this systematic review as per the Preferred Reporting
Items for Systematic Reviews and Meta-Analyses guidelines out-
lined at http://www.prisma-statement.org.
RESULTS
Trial flow
A total of 185 reports (8, 9, 27209), were identified to be
potentially eligible for inclusion in the systematic review. After
thorough scrutiny, 116 of these were excluded for specific reasons
(Figure 1) (85, 95209). Thus, 60 trials reported in 69 publi-
cations (8, 9, 2784, 8694) were included.
Baseline characteristics
The baseline characteristics, fortification details, and risk of
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bias in the analyzed trials are summarized elsewhere (see Sup-
plemental Tables 13 under Supplemental data in the online
issue). These 60 trials contributed 85 analytic components for
sensitivity and subgroup analyses and provided data on 11,750
iron-fortified subjects and 9077 control subjects. The distri-
bution of analytic components according to continents was as
follows: Asia, 41; Africa, 13; South America, 14; Europe, 9;
Australia, 1; and North America, 7. Most of the studies were
from low- to middle-income countries (71 of 85 analytic com-
ponents) and nonmalarial endemic regions (77 of 85 analytic
components). Almost two-thirds of the analytic components
were conducted exclusively in children (60 of 85), whereas the
remaining also included adults (25 of 85). Of the 85 analytic
components, 48 used individual randomization, 23 were cluster
randomized, and 14 were quasirandomized. Thirty-seven of the
85 analytic components had a parallel arm study design, 42 had
a multi-arm study design, and 6 studies used factorial design.
The duration of fortification was ,7 mo in 44 (51%), 712 mo
in 30 (35%), and .12 mo in 11 (13%) studies.
Cereal-based fortification was commonly used (n = 36 studies;
42%) followed by salt (12; 14%), sauces (fish and soy) (9; 11%),
and milk (9; 11%). The most common iron fortificant used was
ferrous sulfate (24; 28%) followed by NaFeEDTA (17; 20%),
electrolytic iron (11; 13%), ferric pyrophosphate (7; 8%),
hydrogen-reduced iron (3; 3%), and heme (3; 3%) or ferric or-
thophosphate (3; 3%), ferrous fumarate (6; 7%), amino acid
chelates (2; 2%), iron gluconate (1; 1%), or ammonium citrate
(1; 1%). Only one biofortification trial, which was rice based,
was identified. Three trials did not mention the salt used. For-
tified food was consumed daily in 50 analytic components and
intermittently in the rest. The computed additional iron intake
per day from the fortified food in the 78 analytic components
providing this information was 10 mg in 49 (63%) and .10
mg in 29 (37%). The mean baseline hemoglobin concentration
was 120 g/L in 49 of 80 (57%), and the geometric mean
baseline serum ferritin was 20 lg/L in 22 of 47 (47%).
Details of sequence generation were clearly mentioned in 15
(18%) analytic components, were unclear in 65 (76%) trials, and
were not mentioned in 5 of the 85 (6%) components. Allocation
was concealed in almost one-third of the analytic components
312 GERA ET AL

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FIGURE 1. Trial flow for the systematic review. Databases used are as follows: PubMed, www.ncbi.nlm.nih.gov/pubmed; Cochrane Controlled Trials
Register, tp://onlinelibrary.wiley.com/o/cochrane/cochrane_clcentral_articles_fs.html; Embase, www.embase.com; Web of Knowledge, http://thomsonreuters.
com/products_services/science/science_products/a-z/isi_web_of_knowledge/; Popline, www.popline.org.

(28/85; 33%), not concealed in 8 (9%), and unclear in 49 of 85
(58%). Most of the included trials were double blind (57 of 85;
67%), 6 of 85 (7%) were not blinded, and details were unclear in
the remaining 22 (26%). Selective outcome data reporting was
done in 20 of 85 (24%) analytic components. Incomplete outcome
data were reported in 2 analytic components (1 trial), and other
threats to validity were apparent in 1 trial. Because of the paucity of
analytic components for contrast, the sensitivity analyses were not
feasible for incomplete outcome data and other threats to validity.
Primary outcome variables
Hemoglobin
Data on hemoglobin were available from 54 trials providing 77
analytic components on 10,895 iron-fortified subjects and 8266
control subjects. The funnel plot (Figure 2) was symmetrical,
which suggests an absence of a publication bias in the included
trials. This was confirmed by using the Egger (weighted re-
gression) method (P-bias = 0.46) or the Begg (rank correlation)
method (continuity corrected P = 0.46). The pooled WMD for
postintervention hemoglobin by random-effects model was 0.42
g/dL (95% CI: 0.28, 0.56; P , 0.001; I2 = 94.9%; Q test for
heterogeneity = 1048.57, P , 0.001) (Figure 3). Similar esti-
mates were obtained with the fixed-effects model (0.37 g/dL;
95% CI: 0.34, 0.40; P , 0.001). For hemoglobin change (data
from 18 trials), the pooled WMD by random-effects model was
similar, namely 0.40 g/dL (95% CI: 0.21, 0.59; P , 0.001; I2 =
94.6%, Q test for heterogeneity = 314.59, P , 0.001) (Table 1).
However, the pooled WMD for hemoglobin change with the
fixed-effects model was lower (0.18 g/dL; 95% CI: 0.14, 0.21;
P , 0.001). There was evidence of considerable and statistically
significant heterogeneity with all of these estimates. To perform
the sensitivity and subgroup analyses, we split the shared in-
tervention group in some included trials into 2 reasonably
independent analytic components. The pooled WMD for post-
intervention hemoglobin in these 77 analytic components by
both random- and fixed-effects model was similar to the
pooled estimate obtained with trials as unit of analysis.
The stratified (sensitivity) analyses for the prespecified vari-
ables are detailed in Table 1. The overall test for heterogeneity
 IRON FORTIFICATION AND HEMATOLOGIC OUTCOMES
FIGURE 2. Funnel plot for the WMD of hemoglobin (after intervention)
of iron-fortified foods compared with placebo. The funnel plot was
constructed by using user-written programs on Stata (version 9.2) software
(20). WMD, weighted mean difference.
between subgroups was significant for all of these prespecified
variables (generally P , 0.001). Important exploratory leads in
this context related to the possibility of higher hemoglobin re-
sponse in developing countries, in malarial nonendemic coun-
tries, in suboptimal trial quality (sequence generation, allocation
concealment, selective outcome reporting, and blinding), in di-
rectly observed intake, in quasirandomized trials, in the use of
salt or sauce as fortification vehicles, in NaFeEDTA salt, in the
duration of fortification ,1 y, and in lower baseline hemoglobin
concentrations. The response with sulfate, pyrophosphate, or
fumarate salts was also substantial. A significant improvement
in hemoglobin was shown in a post hoc analysis of the sub-
group of trials conducted on cereals (n = 33). The largest effect
size in this subset was again with NaFeEDTA, and the response
with sulfate, pyrophosphate, or fumarate salts appeared lower
but was statistically significant. The sole biofortification trial
that used rice did not document an improvement in hemoglobin
(51).
The results of univariate and multivariate meta-regression
analyses to explore heterogeneity are summarized in Table 2. In
view of the potential limit to the number of explanatory factors
used in the multivariate model, only significant predictors on
univariate analysis and factors of practical importance (iron
intake, fortification vehicle, and iron compound) were included
in the model. For analytic purposes, condiments were defined as
a grouping of salt, sugar, sauce, or spices (masala), and con-
sumption of any cereal in any form was grouped as cereals.
The significant predictors of heterogeneity on univariate analy-
ses included a higher hemoglobin response with suboptimal trial
quality (allocation concealment, blinding, and quasirandomiza-
tion), use of condiments, and NaFeEDTA salt and a lower he-
moglobin response when adults were included. On multivariate
analyses, a higher hemoglobin response with suboptimal blind-
ing retained its statistical significance.
Anemia
Data pertaining to anemia were available from 33 trials
conducted on 7606 subjects in the fortification group and 5725
control subjects at the end of the intervention period. The trial
definition of anemia, which invariably accounted for age and sex
313
differences for defining hemoglobin cutoff concentrations, was
used for pooling the RR by random-effects model. A significantly
lower RR of remaining anemic was observed at the end of
fortification, namely 0.59 (95% CI: 0.48, 0.71; P , 0.001; I2 =
89.5%, Q test for heterogeneity = 304.94, P , 0.001).
Serum ferritin
Data on serum ferritin were available from 33 trials conducted
on 6796 subjects in the intervention group and 5354 control
subjects at the end of the intervention period (Table 3). The
pooled WMD for postintervention values was 1.36 lg/L
(random-effects model; 95% CI: 1.23, 1.52; P , 0.001; I2 =
95.6%, Q test for heterogeneity = 724.43, P , 0.001).
Iron deficiency
Data pertaining to iron deficiency were available from 21 trials
conducted on 3234 subjects in the intervention group and 2531
control subjects at the end of the intervention period. A signif-
icantly lower risk of being iron deficient was found (RR: 0.48,
random-effects model; 95% CI: 0.38, 0.62; P , 0.001; I2 =
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84.6%, Q test for heterogeneity = 130.25, P , 0.001).
Serum or plasma zinc
Serum or plasma zinc concentrations were estimated in only 2
trials. The zinc concentrations were similar in the 2 arms of both
the trials at the end of the intervention (Table 3). The pooled
estimates of WMD in the intervention and control groups for the
serum zinc concentrations were 0.05 mg/dL (95% CI: 20.33,
0.42; P = 0.810; I2 = 0.0%, Q test for heterogeneity = 0.07, P =
0.793).
Secondary outcome variables
Iron status
The available data on biomarkers of iron status suggested an
improvement in iron nutriture (Table 3). However, there was
evidence of significant heterogeneity for all of these biomarkers,
except for serum iron (6 trials).
Infections
For acute respiratory tract infection (both lower and upper), 4
trials were included incorporating information from 439 iron-
fortified subjects and 359 control subjects. There was no evidence
of an effect of iron fortification on upper and lower respiratory
tract infections (RR: 0.81; 95% CI: 0.30, 2.22; P = 0.687; I2 =
0.0%, Q test for heterogeneity = 0.11, P = 0.99). Diarrhea was
evaluated in 4 trials on 341 iron-fortified subjects and 280
control subjects. There was no evidence of an effect on the risk
of developing diarrhea (RR: 0.83; 95% CI: 0.35, 1.93; P =
0.657; I2 = 0.0%, Q test for heterogeneity = 0.85, P = 0.836).
Malaria was studied in one trial only. No significant effect of
iron fortification on malaria was found (RR: 0.94; 95% CI: 0.75,
1.18; P = 0.602).
Anthropometric measures
No evidence of a significant effect on weight, height, or weight-
for-height were observed (see Supplemental Table 4 under Sup-
plemental data in the online issue).
314
FIGURE 3. Forest plot for hemoglobin (after intervention) of iron-fortified foods compared with placebo. The forest plot and pooled estimates were derived
by using the generic inverse variance method by the user-written metan command in Stata (version 9.2) software (21, 23). ID, identification; WMD,
weighted mean difference.
Mental and motor development
Three trials (263 iron-fortified subjects and 267 controls) eval-
uated theimpactonmentaldevelopment. The pooledestimates ofthe
SMD of the postintervention levels was 20.03 (95% CI: 20.23,
0.17; P = 0.799; I2 = 24.4%, Q test for heterogeneity = 2.65, P =
0.266), which indicated no evidence of an effect on mental de-
velopment. Of the 3 trials, 2 studies used the Bayley Mental De-
velopment Index score to assess the mental development. No
evidence of a significant difference in the pooled estimate of WMD
was found (0.36; 95% CI: 22.31, 3.04; P = 791; I2 = 17.7%, Q test
for heterogeneity = 1.21, P = 0.270). Psychomotor development
was studied in 2 trials with the Bayley Psychomotor Development
Index score in 210 iron-fortified subjects and 212 control subjects.
The pooled estimate of WMD was 1.09 (95% CI: 21.33, 3.51; P =
0.376; I2 = 32.9%, Q test for heterogeneity = 1.49, P = 0.22), which
indicated no significant effect of fortification.
DISCUSSION
Iron fortification of foods resulted in a significant increase in
hemoglobin, serum ferritin, and other biomarkers of iron nutri-
GERA ET AL
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ture and a reduced risk of anemia and iron deficiency, but there
was no evidence of an effect on zinc concentrations, infections,
anthropometric measures, or mental and motor development.
Significant heterogeneity was found for most of the evaluated
outcomes. Sensitivity analysis and metaregression for hemo-
globin suggested a higher response with lower trial quality
(suboptimal allocation concealment and blinding), use of con-
diments, and NaFeEDTA salts and a lower effect when adults
were included.
Strengths and limitations
The main conclusion regarding the rise in hemoglobin after
iron fortification remained stable over a large spectrum of sensi-
tivity analyses. Significant explanatory variables could be identified
to explain heterogeneity, including study quality, fortification ve-
hicle, and compound, and the age group of the subjects. No evi-
dence of publication bias was found. Another influence on the
analyses, namely the omission of one study at a time, did not show
an overwhelming effect of any single trial (data not depicted).
However, the following possible limitations merit consideration.
TABLE 1
Summary of pooled and stratified estimates for weighted mean differences in hemoglobin (g/dL)1
Heterogeneity
No. of Tests for heterogeneity between subgroups
analytic Random-effects model Fixed-effects model
Stratification variable components (95% CI) P value I2 Q P (95% CI) P value Q P

%
Pooled effect in trials
After intervention 542 0.42 (0.28, 0.56) ,0.001 94.9 1048.57 ,0.001 0.37 (0.34, 0.40) ,0.001 NA NA
Change SDs available 182 0.40 (0.21, 0.59) ,0.001 94.6 314.59 ,0.001 0.18 (0.14, 0.21) ,0.001 NA NA
Pooled effect estimated in analytic components
After intervention 77 0.42 (0.30, 0.54) ,0.001 93.3 1130.08 ,0.001 0.37 (0.34, 0.41) ,0.001 NA NA
Change SDs available 26 0.36 (0.19, 0.52) ,0.001 92.2 320.74 ,0.001 0.18 (0.15, 0.21) ,0.001
Age group
Infants 9 0.5 (0.28, 0.72) ,0.001 74.7 31.57 ,0.001 0.42 (0.32, 0.52) ,0.001 184.24 ,0.001
Children .1 y 45 0.49 (0.31, 0.67) ,0.001 94 733.28 ,0.001 0.47 (0.43, 0.51) 0.001
Adults only 15 0.24 (20.08, 0.56) 0.148 91.4 162.60 ,0.001 0.24 (0.15, 0.33) ,0.001
Pregnant women 1 0.69 (0.26, 1.12) 0.001 NA NA NA 0.69 (0.26, 1.12) 0.001
Adults and children 7 0.14 (20.25, 0.53) 0.482 96.1 152.13 ,0.001 0.25 (0.19, 0.30) ,0.001
Age group
Only children 54 0.50 (0.34, 0.65) ,0.001 93.1 765.68 ,0.001 0.46 (0.42, 0.50) ,0.001 49.67 ,0.001
Only adults 15 0.24 (20.08, 0.56) 0.148 91.4 162.60 ,0.001 0.24 (0.15, 0.33) ,0.001
Adults and children 7 0.14 (20.25, 0.53) 0.482 96.1 152.13 ,0.001 0.25 (0.19, 0.30) ,0.001
Developed country
No 64 0.45 (0.32, 0.58) ,0.001 93.4 951.21 ,0.001 0.40 (0.37, 0.43) ,0.001 18.38 ,0.001
Yes 13 0.27 (20.08, 0.63) 0.126 92.5 160.49 ,0.001 0.19 (0.10, 0.28) ,0.001
Malarial endemicity
No 71 0.44 (0.31, 0.57) ,0.001 93.7 1109.81 ,0.001 0.39 (0.36, 0.42) ,0.001 16.29 ,0.001
Yes 6 0.09 (20.05, 0.23) 0.217 0.0 3.98 0.552 0.09 (20.05, 0.23) 0.217
Allocation concealment
Yes 25 0.16 (0.08, 0.25) ,0.001 52.6 50.67 0.001 0.15 (0.09, 0.20) ,0.001 96.11 ,0.001
Others 52 0.53 (0.36, 0.71) ,0.001 94.8 983.3 ,0.001 0.48 (0.44, 0.51) 0.001
Sequence generation
Yes 14 0.19 (0.09, 0.30) 0.001 63.4 35.51 0.001 0.19 (0.13, 0.26) ,0.001 40.41 ,0.001
Others 63 0.47 (0.32, 0.62) ,0.001 94.1 1054.16 ,0.001 0.43 (0.39, 0.46) 0.001
Blinding
IRON FORTIFICATION AND HEMATOLOGIC OUTCOMES

Yes 52 0.27 (0.18, 0.37) ,0.001 83.6 310.27 ,0.001 0.26 (0.23, 0.30) ,0.001 157.52 ,0.001
Others 25 0.72 (0.39, 1.05) ,0.001 96.4 662.29 ,0.001 0.72 (0.66, 0.78) ,0.001
Selective outcome
Others 15 0.49 (0.20, 0.79) 0.001 93.1 202.46 ,0.001 0.48 (0.40, 0.55) ,0.001 7.42 0.006
Yes 62 0.40 (0.26, 0.54) ,0.001 93.4 920.21 ,0.001 0.36 (0.32, 0.39) ,0.001
Compliance
Directly observed 21 0.44 (0.11, 0.76) 0.008 95.8 474.71 ,0.001 0.44 (0.37, 0.50) ,0.001 4.22 0.04
Others 56 0.41 (0.28, 0.54) ,0.001 91.6 651.15 ,0.001 0.36 (0.32, 0.39) ,0.001
Type of trial
Individual randomized 42 0.28 (0.15, 0.40) ,0.001 83.8 253.38 ,0.001 0.23 (0.19, 0.28) ,0.001 113.69 ,0.001
Cluster randomized 22 0.38 (0.20, 0.56) ,0.001 90.6 222.39 ,0.001 0.37 (0.33, 0.42) ,0.001
Quasirandomized 13 0.89 (0.38, 1.39) 0.001 97.8 540.62 ,0.001 0.71 (0.64, 0.79) ,0.001
(Continued)
315

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 316

TABLE 1 (Continued )

Heterogeneity
No. of Tests for heterogeneity between subgroups
analytic Random-effects model Fixed-effects model
Stratification variable components (95% CI) P value I2 Q P (95% CI) P value Q P

Fortification vehicle
Cereals 33 0.31 (0.14,0.48) 0.001 92.0 398.72 ,0.001 0.24 (0.19, 0.29) ,0.001 234.23 ,0.001
Wheat and rice 19 0.41 (0.13, 0.70) 0.004 94.8 345.6 ,0.001 0.32 (0.26, 0.38) ,0.001
Salt 10 0.84 (0.55, 1.13) ,0.001 86.5 66.48 ,0.001 0.91 (0.81, 1.02) ,0.001
Sauce 8 0.86 (0.36, 1.36) 0.001 97.5 282.68 ,0.001 0.56 (0.50, 0.61) ,0.001
Milk 8 0.50 (0.22, 0.79) 0.001 79.6 34.39 ,0.001 0.39 (0.27, 0.51) ,0.001
Others 18 0.14 (20.07, 0.35) 0.194 85.0 113.58 ,0.001 0.07 (20.003, 0.15) 0.059
Fortification salt
NaFeEDTA 14 0.70 (0.31, 1.09) ,0.001 97.7 568.05 ,0.001 0.47 (0.43, 0.52) ,0.001 114.35 ,0.001
Electrolyte iron 11 0.15 (0.04, 0.27) 0.010 33.9 15.14 0.127 0.13 (0.04, 0.22) 0.005
Sulfate or fumarate 27 0.51 (0.33, 0.69) ,0.001 86.5 192.94 ,0.001 0.50 (0.44, 0.57) ,0.001
Pyrophosphate 7 0.51 (0.20, 0.82) 0.001 80.7 31.16 ,0.001 0.56 (0.42, 0.69) ,0.001
Others 15 0.11 (20.18, 0.39) 0.471 93.3 208.24 ,0.001 0.13 (0.06, 0.20) ,0.001
Various iron salts in cereals only
NaFeEDTA 3 1.13 (20.21, 2.47) 0.098 98.5 133.75 ,0.001 0.75 (0.59, 0.90) ,0.001 103.77 ,0.001
Electrolyte iron 9 0.08 (20.01, 0.18) 0.09 0.0 6.98 0.539 0.08 (20.01, 0.18) 0.090
Sulfate/fumarate 9 0.55 (0.30, 0.79) ,0.001 81.4 43.11 ,0.001 0.49 (0.39, 0.59) ,0.001
GERA ET AL

Pyrophosphate 3 0.41 (0.22, 0.61) ,0.001 0.0 1.42 0.490 0.41 (0.22, 0.61) ,0.001
Others 9 20.05 (20.37, 0.26) 0.746 92.7 109.68 ,0.001 0.03 (20.05, 0.11) 0.453
Iron dose (mg/d)
10 44 0.42 (0.28, 0.56) 0.001 93 610.74 ,0.001 0.35 (0.31, 0.38) ,0.001 15.35 ,0.001
.10 26 0.39 (0.09, 0.69) 0.01 94.1 421.59 ,0.001 0.44 (0.37, 0.51) ,0.001
Fortification duration (mo)
6 41 0.48 (0.29, 0.68) ,0.001 92.7 548.06 ,0.001 0.54 (0.49, 0.59) ,0.001 64.46 ,0.001
712 25 0.42 (0.18, 0.66) 0.001 93.5 368.57 ,0.001 0.33 (0.28, 0.39) ,0.001
.12 11 0.19 (20.04, 0.42) 0.099 93.3 149 ,0.001 0.26 (0.21, 0.30) ,0.001
Baseline hemoglobin, mean (g/dL)
12 46 0.47 (0.28, 0.66) ,0.001 94.4 799.16 ,0.001 0.47 (0.43, 0.51) ,0.001 35.83 ,0.001
.12 28 0.31 (0.15, 0.48) ,0.001 90.8 295.03 ,0.001 0.28 (0.24, 0.33) ,0.001
Baseline ferritin, geometric mean (lg/L)
20 22 0.26 (0.07, 0.45) 0.008 91.6 248.53 ,0.001 0.27 (0.22, 0.32) ,0.001 69.00 ,0.001
.20 23 0.59 (0.31, 0.86) ,0.001 95.1 447.47 ,0.001 0.59 (0.53, 0.65) ,0.001
1
The pooled estimates (fixed- and random-effects models) and their statistics were derived by using the generic inverse variance method with the user-written metan command in Stata (version 9.2)
software (21, 23). NA, not applicable; NaFeEDTA, sodium iron edetate.
2
No. of trials.

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 IRON FORTIFICATION AND HEMATOLOGIC OUTCOMES 317
TABLE 2
Meta-regression analyses for the WMDs in hemoglobin (restricted maximum likelihood method)1
Univariable analysis Control for additional variables

Study characteristic WMD (95% CI) P WMD (95% CI) P

Risk of bias
Allocation concealment (yes compared with others) 0.35 (0.08, 0.62) 0.011 0.12 (20.16, 0.41) 0.394
Sequence generation (yes compared with others) 0.28 (20.05, 0.61) 0.097 0.11 (20.22, 0.43) 0.521
Blinding (yes compared with others) 0.44 (0.18, 0.71) 0.001 0.31 (0.02, 0.60) 0.035
Incomplete outcome reported (yes compared with others) 0.17 (20.69, 1.03) 0.69 NI NI
Directly observed compared with others 20.03 (20.33, 0.27) 0.86 NI NI
Quasirandomized compared with others 0.19 (0.08, 0.31) 0.001 0.05 (20.08, 0.18) 0.468
Adults included compared with only children 20.27 (20.55, 0.01) 0.062 20.28 (20.54, 20.01) 0.040
Only adults compared with only children (n = 69) 20.26 (20.60, 0.07) 0.127 NI NI
Developed compared with developing country 20.18 (20.53, 0.18) 0.326 NI NI
Malarial endemic compared with others 20.33 (20.83, 0.18) 0.205 NI NI
Unit increase in mean iron dose (mg/d) 20.0004 (20.02, 0.02) 0.958 NI NI
Unit increase in duration of fortification (mo) 0.02 (20.04, 0.01) 0.135 NI NI
Others compared with cereals 0.19 (20.07, 0.46) 0.151 NI NI
Others compared with condiments 20.40 (20.68, 20.114) 0.006 20.24 (20.55, 0.06) 0.117
Others compared with milk 20.13 (20.58, 0.31) 0.557 NI NI
Others compared with NaFeEDTA 20.34 (20.67, 20.02) 0.040 20.24 (20.69, 0.11) 0.181

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Others compared with sulfate/fumarate 20.15 (20.42, 0.13) 0.298 NI NI
Unit increase in mean baseline hemoglobin status (g/L) 0.05 (20.07, 0.17) 0.399 NI NI
Unit increase in log mean serum ferritin (lg/L) (n = 20) 0.001 (20.08, 0.08) 0.964 NI NI
1
Meta-regression was performed by the metareg command in Stata (version 9.2) software with the restricted maximum likelihood option (25).
NaFeEDTA, sodium iron edetate; NI, not included in multivariable analyses because of a limit to the number of variables that can be introduced; WMD,
weighted mean difference.

First, several trials (23 of 85 analytic components) used
a cluster randomization design but none adjusted the study es-
timates or mentioned it in the published text. In the absence of
relevant information, a cluster designcorrected pooled estimate
could not be computed. The estimated CIs should therefore be
considered to be spuriously narrower. Although, considering the
significance levels, it is highly unlikely that the main in-
terpretation would be altered with this correction, the computed
pooled effect size is probably a slight overestimate.
Second, there is a distinct possibility of false-positive results
from multiple analyses in view of the relatively large number of
prespecified variables for exploring heterogeneity. The identified
predictors should therefore be considered exploratory in nature
only.
Third, only a few trials had adjusted for the subclinical
infection-induced rise in serum ferritin concentrations. However,
all of the included trials were randomized and controlled, which
should have minimized aberrations as a result of this factor.
Fourth, we had used the author definitions for anemia and iron
deficiency. Whereas the age-specific hemoglobin cutoffs for defining
anemia were largely consistent across the studies, there was vari-
ability in defining iron deficiency, which may have had some bearing
on the impact estimates for this variable.
Finally, anemia is a disease with a multifactorial etiology. Most
of the included trials did not attempt to identify the cause of
anemia and the relative contribution of additional micronutrient
deficiencies, worm infestation, malaria, and other coexistent in-
fections. However, the included trials were randomized and

TABLE 3
Pooled estimates (weighted mean difference) of iron fortification on biochemical markers of iron status and serum zinc concentrations1
Tests for
heterogeneity
Random-effects model
Biochemical marker No. of trials (95% CI) P value I2 Q P Fixed-effects model P value

%
Serum ferritin (lg/L)2 33 1.36 (1.23, 1.52) ,0.001 95.6 724.63 ,0.001 1.17 (1.15, 1.20) ,0.001
Serum zinc (lmol/L) 2 0.05 (20.33, 0.42) 0.810 0.0 0.07 0.793 0.05 (20.33, 0.42) 0.810
Serum transerrin receptor (mg/L)2 15 0.88 (0.80, 1.03) 0.008 98.4 870.89 ,0.001 0.81 (0.81, 0.82) ,0.001
Transferrin saturation (%) 8 2.47 (0.76, 4.19) 0.005 85.0 46.54 ,0.001 2.24 (2.03, 2.46) ,0.001
Total-iron-binding capacity (lg/dL) 5 212.92 (234.31, 8.46) 0.236 81.4 21.5 ,0.001 211.71 (219.88, 23.53) 0.005
Serum iron (lg/dL) 6 0.130 (0.04, 0.22) 0.004 41.6 8.57 0.128 0.134 (0.08, 0.19) ,0.001
Zinc protoporphyrin (lg/dL) 4 212.22 (223.71, 20.74) 0.037 94.3 52.56 ,0.001 25.02 (27.34, 22.66) ,0.001
1
The pooled estimates (fixed- and random-effects models) and their statistics were derived by using the generic inverse variance method with the user-
written metan command in Stata (version 9.2) software (21, 23).
2
Geometric estimate (antilog of natural log-transformed values).
318 GERA ET AL
controlled, which should have controlled for most of these
factors.
Implications
This systematic review provides unambiguous evidence that
iron-fortified foods can improve iron nutriture and hemoglobin
concentrations. When all of the evaluated age groups were
considered, the pooled postintervention reductions in anemia and
iron deficiency were 41% and 52%, respectively. A systematic
review in children (7) indicated that pharmacologic iron sup-
plementation results in a greater hemoglobin response (0.53 g/dL
higher; 95% CI: 0.02, 1.04), and the average (ballpark)
expected reductions in anemia (hemoglobin ,110 g/L) preva-
lence range from 38% to 62%. These ballpark expectations
appear higher but are not substantially greater than estimates
from food fortification. However, it would be prudent to caution
that these ballpark assessments from different systematic reviews
are not based on head-to-head comparisons. Furthermore, apart
from the efficacy for anemia reduction, pragmatic public health
choices require careful evidence-based comparative analyses
of additional aspects, including biological benefits (develop-
ment, growth, and physical performance), adverse effects, organ-
oleptic qualities, economic considerations, and logistics, which
are infrequently reported. Future iron-fortification trials should
record these outcomes and economic aspects and preferably
compare them with pharmacologic supplementation to guide
policy.
Exploratory analyses for heterogeneity suggested that the
hematologic response varies with the choice of fortification ve-
hicle and the iron compound used. The hemoglobin response was
significantly higher with condiments, particularly salt and sauce.
Use of NaFeEDTA predicted a greater hemoglobin response. A
promotive effect of soy sauce on iron absorption has been doc-
umented in humans, which is either a result of the lack of soy
protein content or the presence of fermentation products other
than organic acids (210). Similarly, fish sauce has highly bio-
available heme iron. Also the iron-fortified condiments may have
been infrequently consumed with a diet high in iron-absorption
inhibitors, such as cereals. The relatively high bioavailability of
NaFeEDTA in humans is well documented, and it also acts as an
enhancer of iron absorption, such as ascorbic acid (211214).
Earlier reports comment on the scarcity of controlled evidence
regarding the utility of iron fortification of major staple foods,
such as cereals or cereal flours, in improving anemia and iron
deficiency (211, 212). Phytic acid, which is widely present in
cereals, inhibits absorption of even the most bioavailable com-
pounds (211213). However, in this meta-analysis, cereal forti-
fication proved efficacious. This could be attributed to 3 factors: 1)
the use of more bioavailable iron compounds such as NaFeEDTA,
ferrous sulfate, or fumarate; 2) the use of strategies to improve the
bioavailability of iron, such as low-extraction flours (50); and 3) a
larger number of trials in developing countries with a higher
prevalence of iron deficiency and anemia, which are likely to
respond more to iron fortification.
These findings suggest that iron fortification of foods is
effective and can be a viable public health option to combat
iron deficiency. Even fortification of cereals, hitherto consid-
ered ineffective, can constitute potential vehicles by increasing
the fortified iron content, using more bioavailable compounds
(eg, NaFeEDTA), and using innovative strategies to enhance bio-
availability (eg, encapsulation of iron salts in lipid coatings or
micronization).
A higher hemoglobin response with greater compliance and
poorer methodologic quality (suboptimal allocation concealment
and blinding) is not surprising. A lower hemoglobin effect in
trials including adults (P = 0.06) may represent a dose effect
phenomenon as a result of decreased iron consumption per unit
weight. Contrary to expectations, the duration of fortification did
not emerge as a significant predictor of hematologic response in
this and an earlier review (7). Evidence from pregnant women in
Bangladesh indicates that, over a period of 12 wk, 50% of the
iron in a daily regimen (60 mg elemental Fe/d) is sufficient for
a maximum hemoglobin effect (215). The current analysis
suggests that a 6-mo intervention may be sufficient to determine
the likelihood of a hematologic response with fortification.
A useful contribution of this review is to provide better quan-
tification of the expected hematologic response for designing and
evaluating the efficacy of future iron fortification and bio-
fortification trials. In view of heterogeneity related to the for-
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tification vehicle, it would be prudent to refer to effect sizes of the
corresponding food item. On the basis of the limited data from 2
trials, no evidence of zinc depletion was founda result con-
sistent with radioisotope labeling trials (216219). Nevertheless,
future iron fortification trials should also include zinc nutriture as
an outcome measure to address this issue definitively.
The lack of benefit on infections and growth is consistent with
previous systematic reviews (220, 221). However, there is un-
equivocal evidence of a beneficial effect of iron supplementation,
albeit modest, on mental development in older children. The
absence of a similar demonstrable effect with fortification could
be attributed either to a dose effect (lower dose of iron being used
in fortification in comparison with medicinal supplementation) or
most likely to a scarcity of data (only 3 trials). Given the im-
portance of this biological consequence for human resource
development, it is imperative to urgently generate relevant high-
quality data.
Conclusions
Synthesized evidence indicates that iron-fortified foods result
in a significant improvement in hemoglobin, serum ferritin, and
iron nutriture and a reduced risk of remaining anemic and iron
deficient at the end of intervention. No evidence of zinc depletion
was observed from the extremely limited data for this outcome.
Important exploratory predictors of heterogeneity were a higher
response associated with suboptimal trial quality, the use of
condiments, and the use of NaFeEDTA salt and a lower response
when adults were included. Future work on fortification should
focus on increasing the iron content and using more bioavailable
compounds (eg, NaFeEDTA) or innovative strategies to enhance
bioavailability in the foodstuffs and demonstrating the effect of
(or lack thereof) of fortification on biological outcomes, par-
ticularly mental development in children.
The authors responsibilities were as followsHSS and TG: designed the
study, conducted the search, extracted the data, performed the statistical anal-
yses, and drafted the manuscript; and EB: contributed to the study design and
drafting of the manuscript. HSS and TG were guarantors. None of the authors
had any conflict of interest with regard to this manuscript. The funders had no
role in the design, implementation, or analysis and interpretation of the data.
 IRON FORTIFICATION AND HEMATOLOGIC OUTCOMES
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