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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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rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Determinants of Anemia Among Young Children in
Rural India
WHAT’S KNOWN ON THIS SUBJECT: The immense burden of AUTHORS: Sant-Rayn Pasricha, MBBS, MPH,a,b James
anemia among toddlers in developing countries, particularly Black, MBBS, PhD, FAFPHM,a Sumithra Muthayya, BSc,
India, has been documented and attributed to iron deficiency. PhD,b Anita Shet, MBBS, MD, FAAP,c,d Vijay Bhat, MSc,e
Limited data are available, however, regarding the biological, Savitha Nagaraj, MBBS, MD,f N. S. Prashanth, MBBS,
MPH,g H. Sudarshan, MBBS,g Beverley-Ann Biggs, MBBS,
nutritional, and socioeconomic etiologies of anemia, especially in
PhD, FRACP,h and Arun S. Shet, MBBS, MDd,i
rural settings in which the prevalence is maximal.
aNossal Institute for Global Health, University of Melbourne,

Parkville, Victoria, Australia; bHematology and Nutrition Units


WHAT THIS STUDY ADDS: We present a comprehensive and Departments of cPediatrics, fMicrobiology, and iMedical
evaluation in rural Indian children of biological (micronutrient, Oncology, St Johns National Academy of Health Sciences,
infectious disease, and genetic), maternal, and socioeconomic Bangalore, India; eBiochemistry Laboratory, Manipal Hospital,
factors possibly associated with hemoglobin. In addition to iron Bangalore, India; gKaruna Trust, Bangalore, India; hDepartment
status, folate level, maternal hemoglobin level, family wealth/food of Medicine and Victorian Infectious Diseases Service, University
of Melbourne, Royal Melbourne Hospital, Parkville, Victoria,
insecurity, and hemoglobinopathy were also independently Australia; and dDivision of Global Health, Department of Public
associated with hemoglobin. Health Sciences, Karolinska Institutet, Stockholm, Sweden
KEY WORDS
anemia, India, child preschool, iron-deficiency anemia, public
health, poverty, food security

abstract ABBREVIATIONS
WHO—World Health Organization
NFHS—National Family Health Survey
OBJECTIVE: More than 75% of Indian toddlers are anemic. Data on PHC—primary health center
factors associated with anemia in India are limited. The objective of INR—Indian rupees
this study was to determine biological, nutritional, and socioeconomic RBP—retinol-binding protein
risk factors for anemia in this vulnerable age group. CRP—C-reactive protein
METHODS: We conducted a cross-sectional study of children aged 12 CI— confidence interval
to 23 months in 2 rural districts of Karnataka, India. Children were www.pediatrics.org/cgi/doi/10.1542/peds.2009-3108
excluded if they were unwell or had received a blood transfusion. He- doi:10.1542/peds.2009-3108
moglobin, ferritin, folate, vitamin B12, retinol-binding protein, and
C-reactive protein (CRP) levels were determined. Children were also Accepted for publication Mar 26, 2010
tested for hemoglobinopathy, malaria infection, and hookworm infes- Address correspondence to Arun S. Shet, MBBS, MD, Department
tation. Anthropometric measurements, nutritional intake, family of Medical Oncology, St Johns National Academy of Health
wealth, and food security were recorded. In addition, maternal hemo- Sciences, Sarjapur Road, Bangalore 560034, India. E-mail:
globin level was measured. arunshet@sjri.res.in
RESULTS: Anemia (hemoglobin level ⬍ 11.0 g/dL) was detected in PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
75.3% of the 401 children sampled. Anemia was associated with iron Copyright © 2010 by the American Academy of Pediatrics
deficiency (low ferritin level), maternal anemia, and food insecurity.
Children’s ferritin levels were directly associated with their iron intake FINANCIAL DISCLOSURE: The authors have indicated they have
no financial relationships relevant to this article to disclose.
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

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The World Health Organization (WHO) tory, nutritional, anthropometric, and signed a weighted score (maximum of
has estimated that, globally, 1.62 bil- socioeconomic evaluations in a cross- 63), 20 was adapted from the third NFHS.2
lion people are anemic, with the high- section of rural Indian children aged Study participants used containers of
est prevalence of anemia (47.4%) 12 to 23 months. standardized sizes for a 24-hour dietary
among preschool-aged children; of recall to estimate nutrient intake,21
these 293 million children, 89 million PATIENTS AND METHODS which was expressed as a percentage of
live in India.1 The third National Family Study Site and Participants the Indian recommended daily intake.22
Health Survey (NFHS) 2005–2006 re- Information on continued and previous
Study participants were members of eli-
vealed that at least 80% of Indian chil- breastfeeding practices was obtained
gible sample populations in villages
dren aged 12 to 23 months were ane- with specific questions about whether
served by 2 primary health centers
mic.2 Anemia was especially prevalent the child was currently breastfeeding,
(PHCs), the basic units of health care de-
among rural children,2 and the major- the duration of exclusive breastfeeding,
livery in rural India. The Gumballi PHC in
ity of India’s population (72.2%) is ru- and the child’s age at introduction of
the Chamarajnagar district, 112 miles
ral.3 However, despite recent eco- complementary foods and age at breast-
south of Bangalore, serves 21 700 people
nomic development4 and the existence feeding cessation.
in 13 villages. The Sugganahalli PHC in
of a national anemia-control program,5 Each child’s length (from the crown of
the Ramnagara district, 56 miles north-
the prevalence of anemia in India be- the head to the heel) (Seca 210 [Seca,
west of Bangalore, serves 14 400 people
tween 2000 and 2005 increased from Hamburg, Germany) and weight (Seca
in ⬃80 villages.14 Both districts have
75.3% to 80.9% in children aged 6 to 36 872) were measured. Height for age,
agrarian economies and per-capita an-
months.2,6 Alleviating childhood iron- nual incomes (Chamarajnagar, Indian weight for age, and weight for length
deficiency anemia is a public-health rupees [INR] 22 006 [US $478]; Ramna- were calculated. For these variables,
priority, because anemia is associated gara, INR 26 009 [US $565]) that reflect results with z scores less than ⫺2
with impaired cognitive and psy- the state and national averages (Karna- were defined as stunting, under-
chomotor development.7,8 taka overall, INR 26 123 [US $567]; India weight, and wasting, respectively, in
Iron deficiency is believed to be the overall, INR 25 825 [US $561]).15 accordance with the 2008 WHO child
most important cause of anemia growth standards.23
We randomly selected 3 of 4 subcenters
among children in India9 and is attrib- of each PHC.16 Lists of children living in Mothers underwent field estimation of
utable to poor nutritional iron intake the villages were compiled from lists ob- capillary hemoglobin level (HemoCue
and low iron bioavailability.10 Other tained from both PHCs and from Angan- 201⫹ [HemoCue, Angelholm, Swe-
factors, including folate and vitamin wadi (child care centers for preschool- den]). Venous blood (3 mL) was drawn
B12 and A deficiencies, malaria infec- aged children), and the information was from each child, processed appropri-
tion, hookworm infestation, and hemo- confirmed by investigators who con- ately in the PHC laboratory within 6
globinopathies, are also associated ducted house-to-house visits. All children hours of collection, and then packed
with childhood anemia.11–13 To our aged 12 to 23 months in selected villages with ice and transported to the refer-
knowledge, no previous report in the were eligible, unless the child was ence laboratory. Samples were ana-
published literature has described the acutely unwell or had received a blood lyzed within 48 hours of collection.
relative contribution of these factors transfusion. The detailed study methods
to anemia in rural Indian children. To have been published.17 Laboratory Assays
effectively control this problem, health Laboratory assays were performed as
care providers must have a compre- Study Procedures follows: automated complete blood ex-
hensive understanding of the etiologic The food-security questionnaire module amination (Sysmex XT-2000i [Sysmex Inc,
factors associated with anemia. was adapted from the Household Food Kobe, Japan]) (used only for hemoglobin
We hypothesized that low hemoglobin Insecurity Access Scale, which has been estimation); serum ferritin, folate, and vi-
concentrations in rural Indian children validated for use in settings in develop- tamin B12 (electrochemiluminescent im-
primarily result from micronutrient ing countries.18 The scale covers percep- munoassay, ELECSYS 2010 [ELECSYS, Hi-
(especially iron) deficiencies attribut- tions about food insecurity and enables tachi High Technologies Corporation,
able to poor nutritional intake com- calculation of a score from 0 (no food Tokyo, Japan]; reagents from Roche Di-
pounded by adverse socioeconomic insecurity) to 27 (maximum food insecu- agnostics [Penzberg, Germany]), retinol-
conditions and food insecurity. To test rity).19 The Wealth Index, an estimation of binding protein (RBP), high-sensitivity C-
this hypothesis we conducted labora- household wealth in which assets are as- reactive protein (CRP) (nephelometry,

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Siemens BN-Prospec Nephelometer [Sie- Total number of children
mens, Marburg, Germany]), and hemo- potentially eligible in
target villages
globin variant (high-performance liquid 470a Away from
chromatography, Biorad D10 [Biorad village/
declined
Laboratories Inc, Hercules, CA]). Thick 55
and thin blood films were prepared by Total number of children
use of the Jaswant-Singh-Bhattacherji presenting for study;
examined for eligibility
method and evaluated for malaria para- 415 Exclusions 10
sites by technicians for the National Ma-
Febrile 7
laria Control Program. For study partici-
pants for whom stool samples were Previous blood
transfusion 3
returned (n ⫽ 142), stool was evaluated Total number of children
included, questionnaires
microscopically for hookworm ova by administered
use of wet mounts.24 405
Presented with
mother
Definitions 374
Anemia was defined as a hemoglobin Blood samples collected
level of ⬍11 g/dL in children, ⬍12 g/dL in and analyzedb
401 (EDTA)
nonpregnant women, and ⬍11 g/dL in Mother’s 396 (serum)
pregnant women, on the basis of WHO hemoglobin
tested
definitions.9 Iron deficiency was defined 364
as a ferritin level of ⬍12 ng/mL, or ⬍30
ng/mL if the CRP level was ⬎5 mg/L.9 Us- FIGURE 1
Subject enrollment.17 a Compiled from Anganwadi Centre lists, health worker’s lists, and house-to-
ing the manufacturer’s reference house surveys (when lists were inadequate). b Blood could not be collected from 4 children, and
ranges, we defined vitamin B12 defi- serum was not collected from another 5 subjects.
ciency as serum vitamin B12 level of
⬍210 pg/mL and folate deficiency as a
serum folate level of ⬍3.3 ng/mL. Bio- committees of St John’s National Acad- threshold for defining anemia has age
chemical evidence of inflammation was emy of Health Sciences, Bangalore, In- and ethnic ambiguities.30 CRP level was
defined as a CRP level of ⬎5 mg/L25 and dia, and the Faculty of Medicine, Den- analyzed as an ordered categorical vari-
␤-thalassemia trait as a hemoglobin A2 tistry and Health Sciences, University able. Associations between risk factors
level of ⬎3.5%.26 Although RBP level is of Melbourne, Australia. and outcomes were first evaluated by us-
highly correlated with serum retinol lev- ing univariate linear regression. A
els, reference ranges in the pediatric Statistical Methods
multiple-regression model was then iter-
population are unclear and cutoffs were Data were entered into Epi Info 3.4.3 (US atively developed. Variables were re-
not applied.27,28 Malaria was diagnosed if Centers for Disease Control and Preven- tained if the P value for their coefficient
plasmodium parasites (trophozoites, tion, Atlanta, GA) and exported to Stata 9 remained ⬍.05. Standardized (␤) coeffi-
schizonts, or gametocytes) were identi- (Stata Corp, College Station, TX) for anal-
cients (coefficient standardized with a
fied in serum. Results for hookworm ova ysis. A sample size of 390 ensured a ⫾5%
mean of 0 and SD of 1) were calculated.
in stool samples were expressed as range for the 95% confidence intervals
An R2 value was used to determine the
present or absent. (CIs) of estimates of prevalence. The
variation in hemoglobin level revealed by
study had 80% power to detect regres-
Ethics Considerations the model. The Shapiro-Wilk test was
sion coefficients between continuous
used to determine if residual values for
Information obtained through commu- variables for which the coefficient was at
nity consultation was used to formu- least 0.1 and the correlation between the model had a normal distribution.
late the study design and procedures. variables was at least 0.2. Linear regres-
RESULTS
Plain-language statements explaining sion performed by using continuous
the study were provided to and written variables retained maximum informa- Between August and October 2008,
informed consent was obtained from tion29; in particular, hemoglobin level 88.3% of 470 eligible children living in
the guardians of all child participants. was analyzed (rather than “anemia”) as the selected villages were recruited
The study was approved by the ethics the outcome variable, because the (Fig 1).17 Mean values with 95% CIs in

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

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

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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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Maternal
hemoglobin

Childhood
Child’s nutrition nutritional
Socioeconomic Food • Complementary deiciencies: Child’s
food iron and
status insecurity Iron hemoglobin
energy Folate
• Breastfeeding

Genetic:
Gender
Thalassemia
trait

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 infant-to-toddler age group. Although The findings of our study should be
because of malnutrition,38 deficiencies in to our knowledge there have been no considered with awareness of the fol-
other micronutrients,39 exposure to bio- studies of anemia etiology in rural In- lowing limitations. First, this is a cross-
fuel smoke,40 and possibly other unex- dia, a study in urban slums of New sectional study, for which we report
plained mechanisms associated with Delhi investigated 90 anemic children association rather than causation.
lower socioeconomic status. We were and identified important contributions Second, measurement of additional
surprised that we found no association from iron and vitamin B12 deficiency.43 laboratory variables, particularly lev-
between the highest level of food insecu- A study of young Mexican children re- els of soluble transferrin receptor,
rity and hemoglobin level (Table 4), a re- vealed that anemia attributable to methylmalonic acid, and homocys-
sult that may have been related to the iron-deficiency anemia was less com- teine, could have increased the detec-
nonlinear performance of the Household mon than anemia from other causes.11 tion of iron deficiency and functional
Food Insecurity Access Scale.19 In Malawi, infectious diseases and vita- folate and vitamin B12 deficiencies.
Major consequences of climate change min B12 and folate deficiencies, but not Furthermore, we did not evaluate lev-
are impairments of crop yield and agri- iron deficiency, were important fac- els of lead46 or selenium,47, which have
cultural productivity,41 conditions that tors associated with severe childhood been previously demonstrated to be
could increase food insecurity and anemia.12 Results of studies in Thai- associated with anemia. These assays
worsen childhood anemia. Furthermore, land and the United States also indi- were prohibited because the amount
the continuing global financial crisis cated that iron deficiency was a of blood they require exceeded the
may threaten the health status of low- nondominant cause of pediatric ane- maximum phlebotomy volume accept-
and middle-income countries42 and may mia.44,45 In addition to confirming the able to the community. Third, incom-
play a role in childhood anemia through findings of the NFHS (which was a plete stool sampling in the field may
its effect on food insecurity. Thus, child- large prevalence study), our data pro- have resulted in failure to detect an
hood anemia may worsen if the stres- vide major insights into biological, association between hookworm infes-
sors listed above undermine socioeco- sociodemographic, and economic fac- tation and hemoglobin or ferritin lev-
nomic advancement or worsen food tors associated with anemia in rural els. Finally, the 24-hour dietary-recall
insecurity in India. Incorporation of strat- toddlers. The contrast between our method we used has limitations,21 and
egies to support nutrition and address findings of predominant iron- may have led to overestimation of nu-
socioeconomic conditions may help mit- deficiency anemia and the findings re- tritional intake in young children com-
igate these phenomena. ported in the published literature may pared with methods that use weight
Few studies conducted worldwide reflect differences in diet and socio- measurement.48,49 However, this
have comprehensively examined the economic patterns in this area and method was the tool that could be
etiology of anemia in children in the also in study methods. most feasibly administered within the

e146 PASRICHA et al
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ARTICLES

available time frame to assess nutri- adherence,55 or other unidentified tention. Our findings suggest that
tional intake in our field setting. causes. Thus, additional work is re- current public-health strategies such
Despite these limitations, we have quired to identify reasons for the gap as iron supplementation are neces-
identified a comprehensive set of fac- between policy and practice for ane- sary but not sufficient to reduce child-
tors associated with hemoglobin lev- mia control in this setting. hood anemia. Instead, combining iron
els in rural Indian toddlers. The high The findings of our study support the supplementation and food-fortification
level of community participation, iden- need for a broad public-health strat- programs with efforts to reduce ma-
tification of anemia prevalence that re- egy for the control of anemia among ternal anemia, family poverty, and food
flects nationwide prevalence,2 and Indian children beyond delivering iron insecurity may yield optimal improve-
socioeconomic similarities of the supplementation alone. Measures that ment of children’s hemoglobin levels.
selected districts of Karnataka with address maternal anemia could have
other states in India suggest that the functional and reproductive benefits ACKNOWLEDGMENTS
results of this study may be generaliz- for mothers and, subsequently, chil-
This study was supported by grant
able to much of India and perhaps to dren.56 The recent WHO recommenda-
funding from the Allen Foundation,
other resource-limited settings in Asia. tion to provide weekly iron and folic
Michigan (to Dr Shet) and funds from
Iron-deficiency anemia, a leading risk acid to all women of reproductive age
the Fred P. Archer Charitable Trust,
factor for burden of disease in devel- could be expanded in rural India.57 Low
Victoria, Australia, and the Melbourne
oping countries,50 is associated with dietary-iron intake, particularly in
Research Scholarship, University of
impaired cognitive development7 and breastfeeding children, ideally should
be alleviated with a combined ap- Melbourne, Victoria, Australia (to Dr
potentially restricts economic devel- Pasricha).
opment.51 Globally, policy makers have proach of iron supplementation, forti-
deployed strategies against anemia fication of complementary foods, and We acknowledge the field team, led by
that include iron supplementation, dietary education. These efforts must Mrs Varalaxmi Vijaykumar, which was
food fortification, and dietary diversifi- be coupled with strategies to address involved in data collection. We thank
cation.52 Although the Indian anemia- family poverty and food security, be- Ms Shubha K. for assistance with data
control program recommends that cause both are independently asso- entry. We are indebted to the commu-
children younger than 5 years receive ciated with hemoglobin levels in nity health workers and village Angan-
iron and folic acid supplements,5,53 our children. wadi workers who assisted with our
study results show that this approach field work. We are grateful to Dr Julie
has not successfully controlled ane- CONCLUSIONS Simpson for guidance with the statisti-
mia prevalence. This apparent lack of Anemia, an important problem world- cal analysis. We thank Professor Rob
success may be related to suboptimal wide, is increasing among young chil- Moodie for guidance in developing the
program implementation,54 lack of dren in India and requires urgent at- study.
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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:
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