Determinants of Anemia Among Young Children in Rural India

Sant-Rayn Pasricha, James Black, Sumithra Muthayya, Anita Shet, Vijay Bhat,
Savitha Nagaraj, N. S. Prashanth, H. Sudarshan, Beverley-Ann Biggs and Arun S.
Shet
Pediatrics 2010;126;e140-e149; originally published online Jun 14, 2010;
DOI: 10.1542/peds.2009-3108

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/126/1/e140

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Determinants of Anemia Among Young Children in
Rural India
WHAT’S KNOWN ON THIS SUBJECT: The immense burden of
anemia among toddlers in developing countries, particularly
India, has been documented and attributed to iron deficiency.
Limited data are available, however, regarding the biological,
nutritional, and socioeconomic etiologies of anemia, especially in
rural settings in which the prevalence is maximal.
WHAT THIS STUDY ADDS: We present a comprehensive
evaluation in rural Indian children of biological (micronutrient,
infectious disease, and genetic), maternal, and socioeconomic
factors possibly associated with hemoglobin. In addition to iron
status, folate level, maternal hemoglobin level, family wealth/food
insecurity, and hemoglobinopathy were also independently
associated with hemoglobin.
abstract
OBJECTIVE: More than 75% of Indian toddlers are anemic. Data on
factors associated with anemia in India are limited. The objective of
this study was to determine biological, nutritional, and socioeconomic
risk factors for anemia in this vulnerable age group.
METHODS: We conducted a cross-sectional study of children aged 12
to 23 months in 2 rural districts of Karnataka, India. Children were
excluded if they were unwell or had received a blood transfusion. He-
moglobin, ferritin, folate, vitamin B12, retinol-binding protein, and
C-reactive protein (CRP) levels were determined. Children were also
tested for hemoglobinopathy, malaria infection, and hookworm infes-
tation. Anthropometric measurements, nutritional intake, family
wealth, and food security were recorded. In addition, maternal hemo-
globin level was measured.
RESULTS: Anemia (hemoglobin level ⬍ 11.0 g/dL) was detected in
75.3% of the 401 children sampled. Anemia was associated with iron
deficiency (low ferritin level), maternal anemia, and food insecurity.
Children’s ferritin levels were directly associated with their iron intake
and CRP levels and with maternal hemoglobin level and inversely as-
sociated with continued breastfeeding and the child’s energy intake. A
multivariate model for the child’s hemoglobin level revealed associa-
tions with log(ferritin level) (coefficient: 1.20; P ⬍ .001), folate level
(0.05; P ⬍ .01), maternal hemoglobin level (0.16; P ⬍ .001), family
wealth index (0.02; P ⬍ .05), child’s age (0.05 per month; P ⬍ .005),
hemoglobinopathy (⫺1.51; P ⬍ .001), CRP level (⫺0.18; P ⬍ .001), and
male gender (⫺0.38; P ⬍ .05). Wealth index and food insecurity could
be interchanged in this model.
CONCLUSIONS: Hemoglobin level was primarily associated with iron
status in these Indian toddlers; however, maternal hemoglobin level,
family wealth, and food insecurity were also important factors. Strat-
egies for minimizing childhood anemia must include optimized iron
intake but should simultaneously address maternal anemia, poverty,
and food insecurity. Pediatrics 2010;126:e140–e149
e140 PASRICHA et al
Downloaded from www.pediatrics.org by on July 20, 2010
AUTHORS: Sant-Rayn Pasricha, MBBS, MPH,a,b James
Black, MBBS, PhD, FAFPHM,a Sumithra Muthayya, BSc,
PhD,b Anita Shet, MBBS, MD, FAAP,c,d Vijay Bhat, MSc,e
Savitha Nagaraj, MBBS, MD,f N. S. Prashanth, MBBS,
MPH,g H. Sudarshan, MBBS,g Beverley-Ann Biggs, MBBS,
PhD, FRACP,h and Arun S. Shet, MBBS, MDd,i
aNossal Institute for Global Health, University of Melbourne,
Parkville, Victoria, Australia; bHematology and Nutrition Units
and Departments of cPediatrics, fMicrobiology, and iMedical
Oncology, St Johns National Academy of Health Sciences,
Bangalore, India; eBiochemistry Laboratory, Manipal Hospital,
Bangalore, India; gKaruna Trust, Bangalore, India; hDepartment
of Medicine and Victorian Infectious Diseases Service, University
of Melbourne, Royal Melbourne Hospital, Parkville, Victoria,
Australia; and dDivision of Global Health, Department of Public
Health Sciences, Karolinska Institutet, Stockholm, Sweden
KEY WORDS
anemia, India, child preschool, iron-deficiency anemia, public
health, poverty, food security
ABBREVIATIONS
WHO—World Health Organization
NFHS—National Family Health Survey
PHC—primary health center
INR—Indian rupees
RBP—retinol-binding protein
CRP—C-reactive protein
CI— confidence interval
www.pediatrics.org/cgi/doi/10.1542/peds.2009-3108
doi:10.1542/peds.2009-3108
Accepted for publication Mar 26, 2010
Address correspondence to Arun S. Shet, MBBS, MD, Department
of Medical Oncology, St Johns National Academy of Health
Sciences, Sarjapur Road, Bangalore 560034, India. E-mail:
arunshet@sjri.res.in
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2010 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have
no financial relationships relevant to this article to disclose.

The World Health Organization (WHO)
has estimated that, globally, 1.62 bil-
lion people are anemic, with the high-
est prevalence of anemia (47.4%)
among preschool-aged children; of
these 293 million children, 89 million
live in India.1 The third National Family
Health Survey (NFHS) 2005–2006 re-
vealed that at least 80% of Indian chil-
dren aged 12 to 23 months were ane-
mic.2 Anemia was especially prevalent
among rural children,2 and the major-
ity of India’s population (72.2%) is ru-
ral.3 However, despite recent eco-
nomic development4 and the existence
of a national anemia-control program,5
the prevalence of anemia in India be-
tween 2000 and 2005 increased from
75.3% to 80.9% in children aged 6 to 36
months.2,6 Alleviating childhood iron-
deficiency anemia is a public-health
priority, because anemia is associated
with impaired cognitive and psy-
chomotor development.7,8
Iron deficiency is believed to be the
most important cause of anemia
among children in India9 and is attrib-
utable to poor nutritional iron intake
and low iron bioavailability.10 Other
factors, including folate and vitamin
B12 and A deficiencies, malaria infec-
tion, hookworm infestation, and hemo-
globinopathies, are also associated
with childhood anemia.11–13 To our
knowledge, no previous report in the
published literature has described the
relative contribution of these factors
to anemia in rural Indian children. To
effectively control this problem, health
care providers must have a compre-
hensive understanding of the etiologic
factors associated with anemia.
We hypothesized that low hemoglobin
concentrations in rural Indian children
primarily result from micronutrient
(especially iron) deficiencies attribut-
able to poor nutritional intake com-
pounded by adverse socioeconomic
conditions and food insecurity. To test
this hypothesis we conducted labora-
PEDIATRICS Volume 126, Number 1, July 2010
Downloaded from www.pediatrics.org by on July 20, 2010
tory, nutritional, anthropometric, and
socioeconomic evaluations in a cross-
section of rural Indian children aged
12 to 23 months.
PATIENTS AND METHODS
Study Site and Participants
Study participants were members of eli-
gible sample populations in villages
served by 2 primary health centers
(PHCs), the basic units of health care de-
livery in rural India. The Gumballi PHC in
the Chamarajnagar district, 112 miles
south of Bangalore, serves 21 700 people
in 13 villages. The Sugganahalli PHC in
the Ramnagara district, 56 miles north-
west of Bangalore, serves 14 400 people
in ⬃80 villages.14 Both districts have
agrarian economies and per-capita an-
nual incomes (Chamarajnagar, Indian
rupees [INR] 22 006 [US $478]; Ramna-
gara, INR 26 009 [US $565]) that reflect
the state and national averages (Karna-
taka overall, INR 26 123 [US $567]; India
overall, INR 25 825 [US $561]).15
We randomly selected 3 of 4 subcenters
of each PHC.16 Lists of children living in
the villages were compiled from lists ob-
tained from both PHCs and from Angan-
wadi (child care centers for preschool-
aged children), and the information was
confirmed by investigators who con-
ducted house-to-house visits. All children
aged 12 to 23 months in selected villages
were eligible, unless the child was
acutely unwell or had received a blood
transfusion. The detailed study methods
have been published.17
Study Procedures
The food-security questionnaire module
was adapted from the Household Food
Insecurity Access Scale, which has been
validated for use in settings in develop-
ing countries.18 The scale covers percep-
tions about food insecurity and enables
calculation of a score from 0 (no food
insecurity) to 27 (maximum food insecu-
rity).19 The Wealth Index, an estimation of
household wealth in which assets are as-
ARTICLES
signed a weighted score (maximum of
63), 20 was adapted from the third NFHS.2
Study participants used containers of
standardized sizes for a 24-hour dietary
recall to estimate nutrient intake,21
which was expressed as a percentage of
the Indian recommended daily intake.22
Information on continued and previous
breastfeeding practices was obtained
with specific questions about whether
the child was currently breastfeeding,
the duration of exclusive breastfeeding,
and the child’s age at introduction of
complementary foods and age at breast-
feeding cessation.
Each child’s length (from the crown of
the head to the heel) (Seca 210 [Seca,
Hamburg, Germany) and weight (Seca
872) were measured. Height for age,
weight for age, and weight for length
were calculated. For these variables,
results with z scores less than ⫺2
were defined as stunting, under-
weight, and wasting, respectively, in
accordance with the 2008 WHO child
growth standards.23
Mothers underwent field estimation of
capillary hemoglobin level (HemoCue
201⫹ [HemoCue, Angelholm, Swe-
den]). Venous blood (3 mL) was drawn
from each child, processed appropri-
ately in the PHC laboratory within 6
hours of collection, and then packed
with ice and transported to the refer-
ence laboratory. Samples were ana-
lyzed within 48 hours of collection.
Laboratory Assays
Laboratory assays were performed as
follows: automated complete blood ex-
amination (Sysmex XT-2000i [Sysmex Inc,
Kobe, Japan]) (used only for hemoglobin
estimation); serum ferritin, folate, and vi-
tamin B12 (electrochemiluminescent im-
munoassay, ELECSYS 2010 [ELECSYS, Hi-
tachi High Technologies Corporation,
Tokyo, Japan]; reagents from Roche Di-
agnostics [Penzberg, Germany]), retinol-
binding protein (RBP), high-sensitivity C-
reactive protein (CRP) (nephelometry,
e141
Siemens BN-Prospec Nephelometer [Sie-
mens, Marburg, Germany]), and hemo-
globin variant (high-performance liquid
chromatography, Biorad D10 [Biorad
Laboratories Inc, Hercules, CA]). Thick
and thin blood films were prepared by
use of the Jaswant-Singh-Bhattacherji
method and evaluated for malaria para-
sites by technicians for the National Ma-
laria Control Program. For study partici-
pants for whom stool samples were
returned (n ⫽ 142), stool was evaluated
microscopically for hookworm ova by
use of wet mounts.24
Definitions
Anemia was defined as a hemoglobin
level of ⬍11 g/dL in children, ⬍12 g/dL in
nonpregnant women, and ⬍11 g/dL in
pregnant women, on the basis of WHO
definitions.9 Iron deficiency was defined
as a ferritin level of ⬍12 ng/mL, or ⬍30
ng/mL if the CRP level was ⬎5 mg/L.9 Us-
ing the manufacturer’s reference
ranges, we defined vitamin B12 defi-
ciency as serum vitamin B12 level of
⬍210 pg/mL and folate deficiency as a
serum folate level of ⬍3.3 ng/mL. Bio-
chemical evidence of inflammation was
defined as a CRP level of ⬎5 mg/L25 and
␤-thalassemia trait as a hemoglobin A2
level of ⬎3.5%.26 Although RBP level is
highly correlated with serum retinol lev-
els, reference ranges in the pediatric
population are unclear and cutoffs were
not applied.27,28 Malaria was diagnosed if
plasmodium parasites (trophozoites,
schizonts, or gametocytes) were identi-
fied in serum. Results for hookworm ova
in stool samples were expressed as
present or absent.
Ethics Considerations
Information obtained through commu-
nity consultation was used to formu-
late the study design and procedures.
Plain-language statements explaining
the study were provided to and written
informed consent was obtained from
the guardians of all child participants.
The study was approved by the ethics
e142 PASRICHA et al
Downloaded from www.pediatrics.org by on July 20, 2010
Total number of children
potentially eligible in
target villages
470a Away from
village/
declined
55
Total number of children
presenting for study;
examined for eligibility
415 Exclusions 10
Febrile 7
Previous blood
transfusion 3
Total number of children
included, questionnaires
administered
405
Presented with
mother
374
Blood samples collected
and analyzedb
401 (EDTA)
Mother’s 396 (serum)
hemoglobin
tested
364
FIGURE 1
Subject enrollment.17 a Compiled from Anganwadi Centre lists, health worker’s lists, and house-to-
house surveys (when lists were inadequate). b Blood could not be collected from 4 children, and
serum was not collected from another 5 subjects.
committees of St John’s National Acad- threshold for defining anemia has age
emy of Health Sciences, Bangalore, In- and ethnic ambiguities.30 CRP level was
dia, and the Faculty of Medicine, Den- analyzed as an ordered categorical vari-
tistry and Health Sciences, University able. Associations between risk factors
of Melbourne, Australia. and outcomes were first evaluated by us-
ing univariate linear regression. A
Statistical Methods
multiple-regression model was then iter-
Data were entered into Epi Info 3.4.3 (US atively developed. Variables were re-
Centers for Disease Control and Preven- tained if the P value for their coefficient
tion, Atlanta, GA) and exported to Stata 9 remained ⬍.05. Standardized (␤) coeffi-
(Stata Corp, College Station, TX) for anal-
cients (coefficient standardized with a
ysis. A sample size of 390 ensured a ⫾5%
mean of 0 and SD of 1) were calculated.
range for the 95% confidence intervals
An R2 value was used to determine the
(CIs) of estimates of prevalence. The
variation in hemoglobin level revealed by
study had 80% power to detect regres-
the model. The Shapiro-Wilk test was
sion coefficients between continuous
used to determine if residual values for
variables for which the coefficient was at
least 0.1 and the correlation between the model had a normal distribution.
variables was at least 0.2. Linear regres-
RESULTS
sion performed by using continuous
variables retained maximum informa- Between August and October 2008,
tion29; in particular, hemoglobin level 88.3% of 470 eligible children living in
was analyzed (rather than “anemia”) as the selected villages were recruited
the outcome variable, because the (Fig 1).17 Mean values with 95% CIs in
 ARTICLES

parenthesis are shown unless other- TABLE 1 Mean Nutrient Intake From Non–Breast Milk Sources During the Previous 24 Hours
wise indicated. Mean (95% CI) RDI Mean Intake, % Consuming
% RDI ⬍75% RDI

Demographics and Food Insecurity Iron, mg/24 h 1.4 (1.3–1.5)a 12 11.7 100.0
Folate, mg/24 h 33.8 (31.4–36.3)a 30 112.7 27.2 (22.7–31.7)
The mean age of children was 17.2 Vitamin B12, mg/24 h 0.31 (0.30–0.36)a 0.2 147.6 46.6 (41.6–51.6)
Vitamin A, mg/24 h 131.0 (113.1–151.8)b 350 37.4 65.5 (60.8–70.3)
months, and 204 of 405 (50.3%) were
Energy, kcal/24 h 415.0 (393.9–436.1)c 1240 33.5 98.5 (97.2–99.7)
boys. Mean maternal age was 23.2 CI indicates confidence interval; RDI, recommended daily intake.
years, and 45 of 376 mothers (12%) a Geometric mean.

b Geometric mean; transformation after addition of 1; 1 subtracted after exponentiation.

were pregnant. Overall socioeconomic c Arithmetic mean.

status was low, with a mean wealth in-

dex of 18 (17.0 –19.0). The median food
TABLE 2 Mean Indices of Hemoglobin Level and Associated Factors
insecurity score was 3 (0 –27), and
Mean (95% CI)
more than half of the mothers (212 of
Hemoglobin (n ⫽ 401), g/dLa 9.75 (9.59 to 9.91)
402 [52.7%]) reported some degree of Ferritin (n ⫽ 396), ng/mLb 10.97 (10.09 to 11.92)
household food insecurity during the Vitamin B12 (n ⫽ 396), pg/mLb 420.1 (403.0 to 437.9)
previous month. Food insecurity and Folate (n ⫽ 396), ng/mLa 9.88 (9.54 to 10.22)
RBP (n ⫽ 382), g/Lb 0.028 (0.026 to 0.030)
wealth indices were inversely associ- CRP (n ⫽ 396), mg/mLc 0.91 (0.77 to 1.06)
ated (Spearman rank correlation: Length for age (n ⫽ 401), z scorea ⫺1.45 (⫺1.57 to ⫺1.34)
⫺0.65; P ⬍ .001). Weight for age (n ⫽ 400), z scorea ⫺1.55 (⫺1.65 to ⫺1.45)
Weight for length (n ⫽ 400), z scorea ⫺1.14 (⫺1.24 to ⫺1.04)
CI indicates confidence interval.
Nutritional Intake a Arithmetic mean.

b Geometric mean.
The mean nutritional intake for chil- c Geometric mean; transformation following addition of 1; 1 subtracted after reverse transformation.

dren is shown in Table 1. Mean iron

intake from non– breast milk sources
consumed during the previous 24
hours was 1.4 (1.3–1.5) mg, which was
11.2% of the recommended daily in-
take for Indian children. Children who
were still breastfed had lower iron in-
take from complementary food (1.10
[1.00 –1.20] mg) than children who
were no longer breastfed (1.99 [1.85–
2.13] mg; P ⬍ .001). Iron intake was
positively associated with wealth index
(coefficient: 0.01 [0.00 – 0.02]; P ⬍
.005) but not with food insecurity.
Anthropometry
Mean growth indices are shown in Ta-
ble 2. Almost one-third of the children
were underweight (129 of 400 [32.3%]
[range: 27.7%–36.9%]). Stunting was
seen in 115 of 401 children (28.7%
[24.2%–33.1%]), and wasting was seen
in 83 of 400 (20.8% [16.8%–24.7%]) (Ta-
ble 3). Length-for-age z scores between
boys and girls were similar, but abso-
lute length was greater in boys (77.8 vs
75.6 cm; P ⬍ .001).
Anemia and Associated Conditions
Mean hemoglobin levels and biological
factors possibly associated with he-
moglobin levels are shown in Table 2.
Anemia was detected in 75.3% of the
children (hemoglobin level: 9.75 g/dL
[9.59 –9.91]). Anemia was prevalent to
a similar extent in nonpregnant
women (63.3%; hemoglobin level: 11.2
g/dL [11.0 –11.4]) and pregnant moth-
ers (61.0%; hemoglobin level: 10.6 g/dL
[10.1–11.1]). Childhood iron deficiency
(ferritin level: ⬍12 or ⬍30 ng/mL if
CRP level was ⬎5 mg/L) was seen in
61.9% (57.1%– 66.7%). Children with
anemia were more likely to have iron
deficiency (odds ratio [OR]: 6.1; P ⬍
.001), maternal anemia (OR: 1.9; P ⬍
.01); continued breastfeeding (OR: 1.6;
P ⬍ .05), and food insecurity (OR: 2.2;
P ⬍ .005) compared with children
without anemia (Table 3).
Associations With Hemoglobin
Hemoglobin was positively associated
with child’s age (coefficient: 0.05
[0.00 – 0.10]; P ⬍ .05) and was lower in
boys compared with girls (t test, mean
difference in hemoglobin: ⫺0.51 g/dL
[⫺0.19 to ⫺0.82]; P ⬍ .01). Univariate
regression analysis, controlled for age
and gender, revealed that hemoglobin
level was positively associated with
ferritin, folate, and vitamin A intake;
wealth; and maternal hemoglobin level
and negatively associated with food in-
security (Table 4). Multiple regression
analysis results indicated that chil-
dren’s hemoglobin levels were primar-
ily associated with ferritin intake but
also positively associated with mater-
nal hemoglobin level, child folate in-
take and age, and family wealth and
were inversely associated with male
gender, CRP level, and presence of the
␤-thalassemia trait (Table 5). The food-
insecurity score could be substituted
for wealth index without affecting
other factors. The residuals for this
model were normally distributed
(Shapiro-Wilk test, P ⬎ .05), and the R2
value was 0.51.

PEDIATRICS Volume 126, Number 1, July 2010 e143

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TABLE 3 Proportion of Children With Anemia (Hemoglobin ⬍ 11 g/dL) and Associated Conditions
Factor Overall, % (95% CI) Anemic, % Not Anemic, % Odds Ratio P
n/N (95% CI) (95% CI)
Laboratory indices
Iron deficiencya 245/396 61.9 (57.1 to 66.7) 72.2 (67.1 to 77.3) 29.9 (20.6 to 39.2) 6.1 (3.6 to 10.5) ⬍.001
Folate deficiencyb 5/396 1.3 (0.2 to 2.4) 1.0 (⫺0.1 to 2.1) 2.1 (⫺0.8 to 4.9) 0.5 (0.1 to 5.9) .42
Vitamin B12 deficiencyc 11/396 2.8 (1.2 to 4.4) 2.7 (0.1 to 4.5) 3.1 (⫺0.0 to 6.5) 0.9 (0.2 to 5.1) .828
Inflammationd 39/396 9.9 (6.9 to 12.8) 10.7 (7.2 to 14.2) 7.2 (2.1 to 12.4) 1.5 (0.6 to 4.3) .317
Hemoglobinopathye 5/401 1.3 (0.2 to 2.3) 1.7 (0.2 to 3.1) 0.0 — —
Hookworm infestationf 19/142 13.4 (7.7 to 19.0) 16.2 (8.9 to 23.4) 7.5 (⫺0.7 to 15.7) 2.4 (0.6 to 13.4) .178
Malaria infectionf 0/0 — 0.0 0.0 — —
Nutritional intake
Low iron intakeg 386/386 100.0 100.0 100.0 —
Continued breastfeedingh 234/404 57.9 (53.1 to 62.8) 60.9 (55.4 to 66.4) 49.0 (39.1 to 58.9) 1.6 (1.0 to 2.6) ⬍.05
Food insecurityi 212/402 52.7 (47.8 to 57.6) 57.1 (51.5 to 62.8) 38.1 (28.3 to 48.0) 2.2 (1.3 to 3.6) ⬍.005
Maternal hemoglobin level: maternal anemiaj 227/360 63.1 (58.1 to 68.1) 66.8 (61.2 to 72.4) 51.1 (40.8 to 61.6) 1.9 (1.1 to 3.2) ⬍.01
Child growth
Stuntingk 115/401 28.7 (24.2 to 33.1) 29.2 (24.1 to 34.4) 26.5 (17.6 to 35.4) 1.1 (0.7 to 2.0) .61
Underweightl 129/400 32.3 (27.7 to 36.9) 32.6 (27.2 to 37.9) 30.9 (21.6 to 40.3) 1.1 (0.6 to 1.8) .76
Wastingm 83/400 20.8 (16.8 to 24.7) 19.9 (15.3 to 24.4) 22.9 (14.4 to 31.5) 0.8 (0.5 to 1.5) .52
CI indicates confidence interval.
a Ferritin level ⬍ 12 ng/mL, or ⬍ 30 ng/mL if CRP ⬎ 5 mg/L.

b Serum folate level ⬍ 3.3 ng/mL.

c Serum vitamin B level ⬍ 210 pg/mL.

12
d CRP level ⬎ 5 mg/L.

e Hemoglobin A ⬎ 3.5%.
2
f Parasites identified on microscopy.

g Iron intake ⬎75% of Indian recommended daily intake.

h The child was continuing to receive breast milk at the time of the study.

i Household Food Insecurity Access Scale score ⱖ1.

j Hemoglobin level ⬍ 12 g/dL, or hemoglobin level ⬍ 11 g/dL if pregnant.

k Length-for-age z score less than ⫺2.

l Weight-for-age z score less than ⫺2.

m Weight-for-length z score less than ⫺2.

Associations With Ferritin
By using univariate regression we
found that child’s (log)ferritin level
was associated with maternal hemo-
globin level (coefficient: 0.09 [0.03–
0.13]; P ⬍ .01) and CRP level (coeffi-
cient: 0.18 [0.12– 0.25]; P ⬍ .001) but
not with child’s age, family wealth,
food insecurity, or child’s nutrient in-
take. According to multiple regression
analysis results, child’s log(ferritin)
was independently, positively associ-
ated with maternal hemoglobin level
(coefficient: 0.07 [0.02– 0.12]; P ⬍ .01),
CRP level (coefficient: 0.20 [0.13– 0.27];
P ⬍ .01), and log(iron intake) (coeffi-
cient: 0.25 [0.01– 0.49]; P ⬍ .05). On the
other hand, child’s (log)ferritin was
negatively associated with a history of
breastfeeding beyond 12 months (co-
efficient: ⫺0.24 [⫺0.42 to ⫺0.06]; P ⬍
.01) and increased calorie intake from
complementary foods (coefficient:
⫺0.001 [⫺0.002 to ⫺0.000]; P ⬍ .02).
DISCUSSION
We made the following observations
among 12- to 23-month-old rural In-
dian children. (1) Hemoglobin levels
in children were primarily related to
iron stores. (2) Levels of hemoglobin
were also associated with levels of
folate, CRP, and the ␤-thalassemia
trait. (3) Hemoglobin levels were in-
dependently associated with mater-
nal hemoglobin level, family wealth,
and food insecurity. (4) Ferritin level
was positively associated with
dietary-iron intake and inversely
associated with continued breast-
feeding beyond 1 year of age and in-
creased energy intake from comple-
mentary foods. Taken together, these
data identify major determinants of
childhood anemia in rural Indian tod-
dlers and raise questions regarding
anemia-control policies.
The association between child’s hemo-
globin level and child’s iron status and
maternal hemoglobin level may have
multiple pathways (Fig 2). For in-
stance, antenatal anemia contributes
to low birth weight and prematurity,
both of which increase the risk of
childhood anemia.31 Severe maternal
anemia may also reduce breast milk
iron content.32 Children’s iron intake in
this population is universally low, par-
ticularly in children continuing to
breastfeed. Calories are predomi-
nantly available in cereals, which con-
tain inhibitors of iron absorption.33
Thus, increased caloric intake may be
associated with reduced dietary-iron
bioavailability.34 Finally, the mother
and child share a socioeconomic envi-

e144 PASRICHA et al
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 ARTICLES

TABLE 4 Regression Coefficients (Univariate) Between Hemoglobin Level and Conditions tors,35 did not identify an association
in the Child
between growth and anemia. Mea-
Factor Coefficient (95% CI)b P
surement of children’s growth trajec-
Proximate factor
Ferritina 1.17 (1.02 to 1.32) ⬍.001
tories may have helped us identify
Folate 0.08 (0.03 to 0.12) ⬍.001 such an association, but unfortunately,
Vitamin B12a 0.07 (⫺0.31 to 0.45) .706 birth records were generally unavail-
RBPa 0.17 (⫺0.12 to 0.45) .250
able or unreliable. Our data did con-
␤ -Thalassemia traitc ⫺0.76 (⫺2.20 to 0.68) .301
CRPd 0.01 (⫺0.12 to 0.13) .897 firm previously reported associations
Hookworm ova in stool ⫺0.69 (⫺1.49 to 0.11) .088 between lower hemoglobin levels and
Growth male gender,36 findings that were pos-
Length for age, z score 0.05 (⫺0.09 to 0.19) .493
Weight for age, z score 0.04 (⫺0.11 to 0.20) .588 sibly related to greater absolute longi-
Weight for length, z score 0.02 (⫺0.13 to 0.17) .826 tudinal growth among boys.
Distal factor
Wealth 0.02 (0.01 to 0.04) ⬍.01
The risk of iron-deficiency anemia may
Food insecuritye thus depend on complex interactions
Score 0 Reference between dietary-iron content (type of
Score 1–5 ⫺0.08 (⫺0.70 to 0.53) .789
Score 6–10 ⫺0.66 (⫺1.02 to ⫺0.30) ⬍.000
diet), iron bioavailability (duration of
Score 11–15 ⫺0.94 (⫺1.68 to ⫺0.19) ⬍.05 breastfeeding and appropriate com-
Score ⱖ16 ⫺0.24 (⫺0.80 to 0.33) .411 plementary feeding practices), in-
Maternal education 0.10 (⫺0.01 to 0.22) .083
creased iron use (growth velocity and
Maternal literacy 0.18 (⫺0.17 to 0.54) .311
Maternal hemoglobin level 0.28 (0.18 to 0.37) ⬍.001 erythroid mass expansion), and inap-
Child’s birth order ⫺0.11 (⫺0.32 to 0.09) .280 propriate iron losses (infection and in-
Iron intake 0.16 (⫺0.07 to 0.43) .158 festation).
Folate intake 0.00 (⫺0.00 to 0.01) .193
Vitamin B12 intake 0.37 (⫺0.14 to 0.87) .157 Other biological factors associated
Vitamin A intake 0.17 (0.05 to 0.27) ⬍.01 with childhood hemoglobin levels in-
Child still breastfeedingf ⫺0.28 (⫺0.62 to 0.06) .108
cluded serum folate level, presence of
The regression coefficients were controlled for age and gender.
a Logarithmically transformed. inflammation, and hemoglobinopathy
b The child’s age (in months) and gender were included in each regression equation but not reported separately; age and
status. We identified associations be-
gender were associated with hemoglobin in all equations.
c A positive result for ␤ -thalassaemia minor was coded as 1; all other results were coded as 0. tween hemoglobin and CRP levels only
d The results for CRP level were categorized as 0, 0.1–1, 1–3, 3–5, 5–10, and ⬎10 mg/L.
when we included ferritin levels in the
e The n values for the food insecurity scores were 190 (score 0), 30 (score 1–5), 123 (score 6 –10), 21 (score 11–15), and 49

(score ⱖ 16).
regression equation; higher CRP levels
f The results were coded as 1 if the child was still breastfeeding or 0 if the child was fully weaned. decreased the coefficient of the rela-
tionship between hemoglobin and fer-
TABLE 5 Multiple Regression Model of Associations With Hemoglobin ritin levels, a result related to ferritin
Association With Coefficient (95% CI) Standardized P
being an acute-phase protein. Al-
Hemoglobin Coefficienta though vitamin A intake was often low
Log(ferritin), ng/mLb 1.20 (1.06 to 1.35) 0.64 ⬍.001 and was associated with hemoglobin
Serum folate, ng/mL 0.05 (0.01 to 0.09) 0.11 ⬍.01 levels, serum RBP level was not associ-
CRP, mg/Lc ⫺0.18 (1.06 to 1.35) ⫺0.14 ⬍.001
␤ -Thalassaemia traitd ⫺1.51 (⫺2.53 to ⫺0.48) ⫺0.11 ⬍.001
ated with hemoglobin level, a finding
Maternal hemoglobin, g/dL 0.16 (0.08 to 0.23) 0.17 ⬍.001 that may be related to a successful
Wealth 0.02 (0.00 to 0.03) 0.10 ⬍.05 government program to supplement
Gendere ⫺0.38 (⫺0.62 to ⫺0.13) ⫺0.12 ⬍.01
vitamin A.
Age of child, mo 0.05 (0.02 to 0.09) 0.11 ⬍.005
a The regression coefficient was standardized with a mean of 0 and an SD of 1. The results of our study highlight impor-
b Logarithmically transformed.
c The results for CRP level were categorized as 0, 0.1–1, 1–3, 3–5, 5–10, and ⬎10 mg/L.
tant associations of wealth and food in-
d A positive result for ␤ -thalassaemia minor was coded as 1; all other results were coded as 0. security with anemia that, although pre-
e Gender was coded as 1 (male) or 0 (female).
viously reported,37 are independent of
other measured environmental and bio-
logical factors. This observation sug-
ronment, and by the time the child is 12 Although growth may contribute to the gests that broader socioeconomic con-
months old, his or her dietary quality development of anemia in this age ditions directly influence hemoglobin
may be similar. group, we, similar to other investiga- levels in children. Potential explanations

PEDIATRICS Volume 126, Number 1, July 2010 e145

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Socioeconomic
status
FIGURE 2
Pathway of factors associated with hemoglobin. Determinants of anemia, such as deficiencies in iron and folate, should be considered in the broader
context of family wealth, food insecurity, and associated nutritional intake and maternal nutritional status. Gender and hemoglobinopathies also contribute
to anemia.
include generalized bone marrow failure
because of malnutrition,38 deficiencies in
other micronutrients,39 exposure to bio-
fuel smoke,40 and possibly other unex-
plained mechanisms associated with
lower socioeconomic status. We were
surprised that we found no association
between the highest level of food insecu-
rity and hemoglobin level (Table 4), a re-
sult that may have been related to the
nonlinear performance of the Household
Food Insecurity Access Scale.19
Major consequences of climate change
are impairments of crop yield and agri-
cultural productivity,41 conditions that
could increase food insecurity and
worsen childhood anemia. Furthermore,
the continuing global financial crisis
may threaten the health status of low-
and middle-income countries42 and may
play a role in childhood anemia through
its effect on food insecurity. Thus, child-
hood anemia may worsen if the stres-
sors listed above undermine socioeco-
nomic advancement or worsen food
insecurity in India. Incorporation of strat-
egies to support nutrition and address
socioeconomic conditions may help mit-
igate these phenomena.
Few studies conducted worldwide
have comprehensively examined the
etiology of anemia in children in the
e146 PASRICHA et al
Maternal
hemoglobin
Child’s nutrition
Food • Complementary
food iron and
insecurity
energy
• Breastfeeding
infant-to-toddler age group. Although
to our knowledge there have been no
studies of anemia etiology in rural In-
dia, a study in urban slums of New
Delhi investigated 90 anemic children
and identified important contributions
from iron and vitamin B12 deficiency.43
A study of young Mexican children re-
vealed that anemia attributable to
iron-deficiency anemia was less com-
mon than anemia from other causes.11
In Malawi, infectious diseases and vita-
min B12 and folate deficiencies, but not
iron deficiency, were important fac-
tors associated with severe childhood
anemia.12 Results of studies in Thai-
land and the United States also indi-
cated that iron deficiency was a
nondominant cause of pediatric ane-
mia.44,45 In addition to confirming the
findings of the NFHS (which was a
large prevalence study), our data pro-
vide major insights into biological,
sociodemographic, and economic fac-
tors associated with anemia in rural
toddlers. The contrast between our
findings of predominant iron-
deficiency anemia and the findings re-
ported in the published literature may
reflect differences in diet and socio-
economic patterns in this area and
also in study methods.
Downloaded from www.pediatrics.org by on July 20, 2010
Childhood
nutritional
de
iciencies: Child’s
Iron hemoglobin
Folate
Genetic:
Gender
Thalassemia
trait
The findings of our study should be
considered with awareness of the fol-
lowing limitations. First, this is a cross-
sectional study, for which we report
association rather than causation.
Second, measurement of additional
laboratory variables, particularly lev-
els of soluble transferrin receptor,
methylmalonic acid, and homocys-
teine, could have increased the detec-
tion of iron deficiency and functional
folate and vitamin B12 deficiencies.
Furthermore, we did not evaluate lev-
els of lead46 or selenium,47, which have
been previously demonstrated to be
associated with anemia. These assays
were prohibited because the amount
of blood they require exceeded the
maximum phlebotomy volume accept-
able to the community. Third, incom-
plete stool sampling in the field may
have resulted in failure to detect an
association between hookworm infes-
tation and hemoglobin or ferritin lev-
els. Finally, the 24-hour dietary-recall
method we used has limitations,21 and
may have led to overestimation of nu-
tritional intake in young children com-
pared with methods that use weight
measurement.48,49 However, this
method was the tool that could be
most feasibly administered within the

available time frame to assess nutri-
tional intake in our field setting.
Despite these limitations, we have
identified a comprehensive set of fac-
tors associated with hemoglobin lev-
els in rural Indian toddlers. The high
level of community participation, iden-
tification of anemia prevalence that re-
flects nationwide prevalence,2 and
socioeconomic similarities of the
selected districts of Karnataka with
other states in India suggest that the
results of this study may be generaliz-
able to much of India and perhaps to
other resource-limited settings in Asia.
Iron-deficiency anemia, a leading risk
factor for burden of disease in devel-
oping countries,50 is associated with
impaired cognitive development7 and
potentially restricts economic devel-
opment.51 Globally, policy makers have
deployed strategies against anemia
that include iron supplementation,
food fortification, and dietary diversifi-
cation.52 Although the Indian anemia-
control program recommends that
children younger than 5 years receive
iron and folic acid supplements,5,53 our
study results show that this approach
has not successfully controlled ane-
mia prevalence. This apparent lack of
success may be related to suboptimal
program implementation,54 lack of
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ACKNOWLEDGMENTS
This study was supported by grant
funding from the Allen Foundation,
Michigan (to Dr Shet) and funds from
the Fred P. Archer Charitable Trust,
Victoria, Australia, and the Melbourne
Research Scholarship, University of
Melbourne, Victoria, Australia (to Dr
Pasricha).
We acknowledge the field team, led by
Mrs Varalaxmi Vijaykumar, which was
involved in data collection. We thank
Ms Shubha K. for assistance with data
entry. We are indebted to the commu-
nity health workers and village Angan-
wadi workers who assisted with our
field work. We are grateful to Dr Julie
Simpson for guidance with the statisti-
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Moodie for guidance in developing the
study.
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e149
 Determinants of Anemia Among Young Children in Rural India
Sant-Rayn Pasricha, James Black, Sumithra Muthayya, Anita Shet, Vijay Bhat,
Savitha Nagaraj, N. S. Prashanth, H. Sudarshan, Beverley-Ann Biggs and Arun S.
Shet
Pediatrics 2010;126;e140-e149; originally published online Jun 14, 2010;
DOI: 10.1542/peds.2009-3108
Updated Information including high-resolution figures, can be found at:
& Services http://www.pediatrics.org/cgi/content/full/126/1/e140
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