European Journal of Clinical Nutrition (2013) 67, 467474

& 2013 Macmillan Publishers Limited All rights reserved 0954-3007/13

www.nature.com/ejcn

REVIEW

Micronutrient deciency and cognitive and physical performance

in Indian children
S Swaminathan, BS Edward and AV Kurpad
Several micronutrient deciencies affect functional, particularly cognition and physical performance of children. Identifying and
preventing sub-clinical deciencies may be important so that adverse effects on functional performance by these deciencies,
particularly of iron and the B vitamins, are prevented. There is also the potential for childhood micronutrient deciencies to have
long-term effects that affect health and productivity in adulthood. This is especially relevant in a developing country such as India,
which faces the dual burden of malnutrition and where the prevalence of these deciencies is high. This review highlights the
extent of micronutrient deciencies in Indian children and focuses on the effect of deciencies of the B vitamins and iron on
cognitive and physical performance in children. Most studies on multiple micronutrient supplementation or fortication in Indian
school children show modest effects on cognitive and physical performance, and it is relevant to point out that these studies have
largely been conducted on urban children with mild deciency at most; children with moderate or severe deciency have not been
studied. However, diets of rural children indicate large decits in micronutrient intake, particularly of folic acid, riboavin and iron,
and their consequences have not been studied. With the limited evidence available, a short term but economical solution to ensure
adequate micronutrient intakes could be through the fortication of staple cereals taken throughout the day. As increasing
household incomes translate into an increase in food expenditure and diet diversication, it may become necessary to dene upper
limits of intake for nutrients in India, particularly as many commercial foods are fortied.
European Journal of Clinical Nutrition (2013) 67, 467474; doi:10.1038/ejcn.2013.14; published online 13 February 2013
Keywords: childhood; micronutrients; cognitive performance; physical performance

INTRODUCTION
Several micronutrients affect the functional performance of
children. These effects could begin as early as the period of fetal
development. The clinical identication of these deciencies
occurs at a much later stage of nutritional adversity; sub-clinical
deciencies, on the other hand, are likely to be more common.
Furthermore, sub-clinical deciencies could also potentially lead to
functional impairment; the functional domains that are important
and have been studied in some detail include cognitive and
physical performance.
With India undergoing a nutrition transition,1 both undernutrition
and overweight coexist in the population. However, whether underor overweight, the risk of micronutrient deciency is high, given
that diets are still heavily cereal based, with little diversity. This constitutes a risk, particularly in children, as their developmental potential could be affected. For example, in follow-up studies of formerly
iron-decient anaemic or chronically iron-decient individuals from
the period of infancy, poorer outcomes were evident in terms of IQ,
motor and cognitive scores and poor academic performance in
spite of iron therapy during infancy.2 This suggests, rst, that lower
micronutrient (in this case, iron) status has long-lasting functional
consequences and, second, that identifying sub-clinical deciencies
and treating them earlier in life is important, rather than tackling it
when severe or chronic symptoms appear. This is particularly
relevant in poorer economies such as India, where the problem is
long term and exacerbated by poverty.

It is very likely that several micronutrient deciencies are related

to functional decits. The objective of this review is to highlight
the extent of micronutrient deciency in children in India, and, in
particular, to focus on the effect of deciencies of micronutrients,
such as the B vitamins (thiamine (B1), riboavin (B2), niacin (B3),
folate, pyridoxine (B6) and cyanocobalamin (B12) and iron on
cognitive and physical performance.

PREVALENCE OF B-VITAMIN AND IRON DEFICIENCIES IN INDIA

Most of the literature relating to the Indian scenario focuses on
the micronutrient deciencies of iron, vitamin A and iodine. Less
attention has been given to vitamin B deciencies. Although the
prevalence of iron deciency has been widely studied by
population-level haemoglobin estimations for anaemia, along
with the use of serum ferritin or soluble transferrin receptor
measurements to dene iron deciency, the study of sub-clinical
deciencies of the B vitamins through evaluation of blood or other
biomarkers are less common. Plasma or serum folate, red blood
cell folate, plasma or serum B12, homocysteine and methylmalonic
acid have been used to assess folate and vitamin B12 status.3
Erythrocyte transketolase activity is used as a functional indicator
of thiamine deciency; erythrocyte glutathione reductase
activation test is used for riboavin and plasma pyridoxal
phosphate for vitamin B6.4

Division of Nutrition, Department of Physiology, St Johns Medical College and Research Institute, St Johns National Academy of Health Sciences, Bangalore, India.
Correspondence: Dr AV Kurpad, Division of Nutrition, Department of Physiology, St Johns Medical College and Research Institute, St Johns National Academy of Health Sciences,
Bangalore 560034, India.
E-mail: a.kurpad@sjri.res.in
Contributors: All authors drafted, interpreted the data and critically reviewed the manuscript.
Received 3 January 2013; accepted 4 January 2013; published online 13 February 2013

Micronutrient deciency and performance in Indian children

S Swaminathan et al

468
Specically with regard to the B vitamins, a recent study
revealed a large number of paediatric cases of deciency over a
period of 3 years with overlapping features of Leigh disease and of
thiamine deciency, thus throwing light on the prevalence of
infantile thiamine deciency in Indian populations.5 A few Indian
studies show biochemical evidence of riboavin deciency in
470% of children from low-income groups,6 largely attributed to
the inadequacy of riboavin in the diet.4 Reports of prevalence of
deciencies of niacin and pyridoxine in Indian children are scarce,
although a deciency of pyridoxine alone is relatively uncommon
and often occurs in association with other B vitamins.7 A study
on middle-income school-aged children (616 years) revealed
low red blood cell folate in most children,8 with signicant
levels of sub-clinical folate deciency reported in semi-urban
school children.9 Although clinical manifestations of Vitamin B12
deciency are uncommon, sub-clinical deciency has been shown
to be widely prevalent.8 In some studies, the prevalence of
B-vitamin deciencies in children from middle-income groups
obtained from blood biochemical analyses indicated that about
99% of children were folate decient, 12% were B1 decient, 66%
were B2 or B6 decient and 44% were B12 decient.8,10
Anaemia is a major public health problem in India, with high
prevalence reported (Table 1). Estimates of prevalence of anaemia
among children below 3 years of age, obtained through the third
National Family Health Survey covering all 29 states in India, is
about 78%.11 In rural preschool children and adolescent girls from
eight states in India, the National Nutrition Monitoring Bureau
reported prevalences of 67 and 70%, respectively.12 Moderate to
severe anaemia was reported in 43% of preschool children and
23% of adolescent girls.12 Urban middle- and high-income groups
also have a high prevalence of anaemia, and children aged 618
years from ve cities had a wide range of anaemia prevalence
between 19 and 88%.10 Presumably, over half of this prevalence of
anaemia could be attributed to iron deciency and low
bioavailability. Other causes include dietary deciencies of folic
acid and vitamin B12. Repeated infections, as well as low-grade
systemic inammation observed in overweight and obese
individuals,13 could result in an increased hepcidin secretion,
which is a key iron regulator, from the liver and adipose tissue.14
The release of cytokines during inammation could also impair
normal physiological systems for transporting iron to target
tissues, probably mediated by hepcidin.15,16

MATERIALS AND METHODS

A search of publications in the past 10 years, which included intervention
studies, cohort studies, cross-sectional studies and review papers on the
micronutrients of interest, as well as their association or effect on cognitive
and/or physical performance of children (118 years), was performed.
Databases searched included PubMed, Google-Scholar, Cochrane library,
SpringerLink and some non-indexed Indian journals. The key search terms
used included micronutrients, multi-micronutrients, vitamins B1, B2, B6, B12,
folate, B-complex vitamins and iron, in combination with any of the
following terms: physical performance, physical endurance, neuromotor

Table 1.

MICRONUTRIENT DEFICIENCY AND COGNITIVE PERFORMANCE

Nutrient deciencies, particularly of micronutrients, affect brain
growth and neurodevelopment largely during the third trimester
of gestation and during infancy, by affecting cell proliferation and
myelination.1719 Myelination begins in the spinal cord and cranial
roots at 16 weeks gestation, followed by the vestibule-acoustic
system, then the parietal cortex and nally the hippocampus,
which matures at about the rst year of infancy and is responsible
for encoding and retrieval of memories. Myelination of left
temporal lobe occurs at 18 months of age and aids in the
acquisition and understanding of language, whereas that of other
brain structures needed for focus and maintenance of attention
occurs through infancy and childhood.19,20 The frontal cortex
myelinates through infancy from 6 months of age up to adulthood
and inuences higher-order cognitive functioning such as
problem solving and higher-order aspects of memory.19 The
psychological processes of memory, learning, reasoning, attention,
language and coordination of motor outputs are classied broadly
under the term cognition. With nutritional inuences being only
one of the inuences on cognitive function, the effects are likely to
be subtle.19 Iron deciency affects memory and impairs learning,
contributing to low cognitive scores and development; deciencies of thiamine, folate and B12 affect episodic memory and
language ability.21
The metabolically active brain requires a continuous supply of
glucose and adequate supplies of micronutrients, which act as
coenzymes or form structural parts of the enzymes required for
metabolic activity. Nutrient deciencies may act by restriction of
myelination, dendritic arborization and synaptic connectivity that
occur early in life.17,2123 Alterations in the tissue levels of
neurotransmitters such as serotonin, dopamine, acetylcholine
and norepinephrine could cause anatomical, chemical or
metabolic changes in the nervous system. Functional consequences depend on the specic deciency and timing of the
deciency relative to the development of the neurological
processes.22,23 There are sensitive and critical stages during
which period cognitive development is facilitated through a
specic type of environmental stimulation. Consequently, a lack of
stimulus during the critical period may make expression of the
specic aspect of functioning difcult or probably impossible,
although during a sensitive period a skill such as language
prociency can still be acquired but less prociently.17
Iron deciency, both in utero and in early postnatal life, could
lead to a decrease in dendrite arborization that decreases the
number and complexity of inter-neural connections. Morphological
alteration in the location and functioning of oligodendrocytes

Prevalence of anaemia in India

Age group, years

0.53
15
1214
1517

performance, motor development, physical work capacity, muscular

performance, cognitive development or performance, mental performance
or development, academic performance or memory. We excluded studies
conducted on animals or adults, those conducted outside India and studies
published more than a decade ago.

Population

Urban and rural

Rural
Rural
Rural

Gender

Girls and boys

Girls and boys
Girls
Girls

Reference

11

NFHS 3
NNMB12
NNMB12
NNMB12

Anaemia (%)
Mild (1011 g/dl)

Moderate (710 g/dl)

Severe (o7 g/dl)

Total

25.7
23.7
46.8
47.0

49.4
41.1
20.8
20.9

3.7
2.1
1.1
1.8

78.9
66.9
68.7
69.7

Abbreviations: NFHS, National Family Health Survey; NNMB, National Nutrition Monitoring Bureau, India.

European Journal of Clinical Nutrition (2013) 467 474

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Micronutrient deciency and performance in Indian children

S Swaminathan et al

469
responsible for myelination occurs during early life, the effects of
which may be irreversible in later life. Animal models have
indicated that dopamine and norepinephrine metabolism is
altered by iron deciency, although limited evidence is available
from human studies.24
The B vitamins function as coenzymes in several metabolic
processes of the body. Vitamins B1, B2, B6, B12 and folate are
required for neurotransmitter synthesis and functioning, brain
energy metabolism and myelination of the spinal cord and brain.
Vitamin B12 deciency could affect cognition by demyelination,
and shared metabolism with folic acid in the process of
myelination or in the synthesis of methionine from homocysteine
could have a role in cognitive processes.22 The homocysteine
hypothesis proposes an indirect and probably long-term effect of
folate, B12 and B6 on brain functioning through affecting the
cerebral vasculature, as high levels of homocysteine that are
largely attributable to low levels of these vitamins are associated
with an increased risk of vascular disease.25
Cognitive function is evaluated by tests that are dependent on the
age of the child, in which different domains such as the assessment
of attention, speed of information processing, learning and memory,
executive functions, intelligence and academic achievement are
assessed. Many of these are adapted culturally to local needs, and a
set of psychological assessments are usually used to evaluate the
effect of nutritional interventions on cognitive performance in
children. For infants and young children, measurements of general
mental and psychomotor development, for example, the Bayley
Scales of Infant Development, are used. In children above 2 years of
age, as cognitive abilities start to differentiate, more specic tests are
used. However, up to 5 years of age some cognitive abilities such as
reasoning and speed of processing are difcult to assess. Intelligence
is usually assessed by sets of short tests such as the Kaufman
Assessment Battery for Children and Wechsler Intelligence Scales for
Children measuring various cognitive abilities, and a general score of
intelligence is obtained.
The fact that micronutrients have subtle effects is known, and at
least two recent reviews have shown this. A meta-analysis of trials
on 516-year-old children receiving micronutrient supplementation for a period of X4 weeks reported benets on uid
intelligence and academic performance, but not on crystallized
intelligence.26 Another review highlighted 13 randomized controlled trials that reported improved intelligence scores, attention,
concentration and short-term memory after micronutrient
supplementation.21 Overall short-term memory, uid intelligence
(reasoning abilities) and mental processing index improved
signicantly, but the effect on crystallized intelligence and other
cognitive performance measures was minimal. It is also important
to note that all of the trials reviewed involved multiple
micronutrient supplementations, and hence it is difcult to point
out single nutrient effects of the B vitamins on cognitive
performance. In addition, the methods used to assess cognitive
performance vary across studies making comparisons with regard
to outcomes difcult to assess.
Eleven studies conducted in India (Table 2) assessing micronutrient status and cognitive performance were retrieved. Of
these, two cohort studies have assessed maternal plasma B12
concentrations (one with B12 and folate) and cognition in the
offspring at 9 years of age. In one study, maternal folate
concentrations predicted cognitive ability while no such association was evident with maternal B12 concentrations.27 However, in
the Pune Maternal Nutrition Study offspring at 9 years of age of
mothers with very low plasma vitamin B12 concentrations had
much lower attention and short-term memory compared with
offspring of mothers with high plasma Vitamin B12
concentrations.28 The former cohort study looked at a
continuum of plasma vitamin B12, whereas the latter looked at
very low versus a very high maternal plasma B12 concentration,
indicating that cognitive performance is probably affected only
& 2013 Macmillan Publishers Limited

when plasma concentrations are extremely low. Among

preschoolers, only one cross-sectional study assessed the effect
and behaviour in terms of social interactions and found that in
anaemic children there was lower social or emotional
development.29 Haemoglobin concentrations were positively
related to the mental processing index in 610-year-olds in a
cross-sectional study.30
In the ve intervention trials conducted on school children,3135
two were conducted with multiple micronutrient supplementation32,34 and three with multiple micronutrient fortication (two
fortied with rice and 1 with salt).31,33,35 All trials were conducted
on school children with normal haemoglobin values or mild
anaemia, with no trial involving children o5 years of age, which
raises the question of whether results would differ in decient
children and/or children under 5 years of age. However, as stated
above, tests of cognition are also difcult to assess below 5 years
of age. Modest changes in short-term memory and no changes in
intelligence were evident in most studies in the supplemented or
fortied group whether the intervention was for a short duration
of 3 months or 1 year. This could probably be due to either the
stage of life at which intervention was provided or due to the
duration of the study. In addition, as multiple micronutrients were
used, it is difcult to pinpoint which micronutrient contributed to
this subtle effect.
MICRONUTRIENT DEFICIENCY AND PHYSICAL PERFORMANCE
B vitamins also have a key role in the energy synthesis process by
modulating carbohydrate, fat and protein metabolism in the
body.36 Among them, B1, B2, B3 and B6 are involved in energy
metabolism and are relevant to muscle function and performance.
B1 functions as a coenzyme for pyruvate dehydrogenase that
catalyses the conversion of pyruvate to acetyl CoA, for
oxoglutarate dehydrogenase in the tricarboxlyic acid cycle, and
for branched-chain decarboxylase involved in the catabolism of
the branched-chain amino acids. A deciency of thiamin can
cause pyruvate accumulation and increase circulating lactate
levels during physical work and reduce physical performance.37
Riboavin is required for the synthesis of the avoenzymes of the
respiratory chain, whereas niacin is required for the synthesis of
nicotinamide adenine dinucleotide (NAD), which has an important
role as a coenzyme in redox reactions, particularly in the process
of oxidative phosphorylation, and it is possible that their
deciency could impair physical performance.38 In addition,
niacin-derived NAD(P)H can act as an antioxidant, and therefore
reduce oxidative damage while facilitating mitochondrial function.39 Vitamin B6, which comprises a group of six related compounds, is used as a coenzyme by aminolevulinate synthasethe
rst enzyme in haeme biosynthesis36as well as in
glycogenolysis.40 Both these actions may be linked to physical
performance. Other B vitamins such as pantothenic acid and
biotin are also important, but are not reviewed here. Overall, a
deciency of one or a combination of these B vitamins could
impair physical performance, and presumably, if the deciency is
corrected, performance should improve. There is a broader
context for the need to improve physical tness and aerobic
capacity in children, particularly in those who are nutritionally
compromised. For example, performance may be related to
physical tness. Physical tness begins to track early in
childhood41 and into adulthood,42 and cardiovascular tness
relates more closely than physical activity to cardiovascular
disease risk factors in healthy children and adolescents.43
Physical activity levels are also generally low in Asian Indian
children,44 and it is possible to speculate that low physical activity
levels in children and adults may be because of low tness levels,
which in turn are due to low endurance and a general feeling of
tiredness when undertaking physical activity. This would restrict
physical activity, and this framework is not entirely unreasonable,
European Journal of Clinical Nutrition (2013) 467 474

European Journal of Clinical Nutrition (2013) 467 474

598

258

610 years
Low SES
school
based

612 years
Low SES
school
based

611 years
Low SES
urban
school
based

610 years
Low SES
school
based

Eilander et al.30

Thankachan
et al.31

Umamaheshwari
et al.32

Muthayya et al.33

598

100

238

4768
months
urban

Lozoff et al.29

108

536

9 years
urban

910 years
urban

Sample

Bhate et al.28

27

Not severely
undernourished children
with
WAZ and HAZ 4  3 s.d.;
Hb 480 g/l

Iron deficient/zinc deficient/

combined (iron and zinc)
deficient/normal
Group 1: 68 years (n 40)
Group 2: 911 years (n 60)

Weight-for-age Z-score
(WAZ) and height-for-age
Z-score (HAZ) 4  3
Hb 490 g/l

WAZ and HAZ 4  3 s.d.;

Hb 480 g/l

Gestational age:
36 weeks
Birth weight below the 10th
percentile for gestational
age
No congenital problems,
disabilities or chronic
illnesses

Group 1: children born to

mothers with low antenatal
B12 concentration (n 57)
Group 2: children born to
mothers with high B12
concentration (n 61)

Children of women with no

history of diabetes before
pregnancy, singleton
pregnancy of o32 weeks of
gestation

Inclusion criteria

Micronutrients and cognitive performance

Veena et al.

Study

Table 2.

Doubleblind RCT

Intervention

Doubleblind RCT

Crosssectional

Crosssectional

Prospective
follow-up
study

Prospective
birth cohort
study

Study design

Wheat biscuit and flavoured milk powder drink

fortified with
1: High MN (100% RDA), high n-3 PUFA
2: Low MN (15% RDA), high n-3 fatty acid
3: High MN (100% RDA),

Iron (2 mg/kg bodyweight in two divided doses) and

zinc (5 mg once a day) supplementation for children
in the deficient group

Lunch with multiple MN-fortified rice with:

Group 1: low-iron (6.25 mg)
Group 2: high-iron (12.5 mg)
Group 3: unfortified rice

Baseline data of a clinical study were used

No supplementation Group 1: Anaemic (n 74)

Group 2: non-anaemic (n 164)

No supplementation

No supplementation

Supplementation/fortification

12 months

3 months

6 months

Duration

High MN treatment significantly improved shortterm memory at 6 months (0.11 s.d.; 0.01, 0.20), but
was less beneficial on fluid reasoning at 6 months
(  0.10 s.d.;  0.17,  0.03) and at 12 months
(  0.12 s.d.;  0.20,  0.04) compared with low
micronutrient treatment.

Memory deficits were observed in children with iron

and zinc deficiency in both the age groups.
In Group 1, with either iron deficiency or combined
deficiency, non-verbal form of memory (P 0.02)
was affected.
Children in Group 2 with combined deficiency had a
severe degree of affectation in verbal (Po0.01) and
non-verbal memory (Po0.01), which improved after
supplementation (P 0.05 and Po0.01,
respectively).

No between-group differences in cognitive function

were observed.

WAZ and HAZ were positively related to mental

processing index MPI (P 0.0006 and 0.002,
respectively).
Hb status was positively related to MPI (P 0  0008),
whereas Vitamin B12 levels were inversely associated
with short-term memory, retrieval ability and MPI
(b (95% CI)  0.124 (  0.224,  0.023), P 0.02).

Children in the anaemic group were 98% more likely

than those in the non-anaemic group to fall within
the half who looked relatively less to their mothers
(OR 1.98, CI: 1.213.49, Po0.05).
The median time (or latency) to approach the
mother was similar (15.32.7 s for the anaemic
group and 12.94.4 s for the non-anaemic group).

Group 1 children performed slower than group 2

children on the colour Trail A test (sustained
attention, 182 vs 159 seconds; Po0.05) and the Digit
Span Backward test (short term memory, Po0.05)
after controlling for age, sex, head circumference,
education, SES and vitamin B12 status at 6 years.
No differences were observed between the groups
in tests of intelligence and visual agnosia.

Increase in cognitive test scores by 0.10.2 s.d. per

s.d. increase in maternal folate concentrations
(Po0.001) during pregnancy was seen.
Increased maternal folate concentrations were
positively associated with learning, long-term
storage/retrieval, visuo-spatial ability, attention and
concentration after controlling for parental
education, SES, religion, the sex, age and current
size of the child, and folate and vitamin B12
concentrations of child at 9.5 years of age.
Maternal vitamin B12 and homocysteine
concentrations were not significantly associated
with childhood cognitive performance.

Main cognitive outcomes

Micronutrient deciency and performance in Indian children

S Swaminathan et al

470

& 2013 Macmillan Publishers Limited

Micronutrient deciency and performance in Indian children

S Swaminathan et al

& 2013 Macmillan Publishers Limited

Abbreviations: CI, confidence interval; HAZ, height-for-age Z score; MN: Micronutrient; MPI, mental processing index; OR, odds ratio; PUFA, Polyunsaturated fatty acid; RCT, randomized controlled trial; RDA,
recommended dietary allowance; SES, socio-economic status; WAZ, weight-for-age Z score.

Significant improvement (Po0.05) in memory tests

in the experimental group when compared with the
control group was seen.
9 months
Experimental group: iodized salt fortified with
vitamins A, B1, B2, B6, B12, folic acid, niacin, iron and
zinc
Control group: iodized salt
100% RDA provided
Provided through all meals and snacks in a day
RCT
All children with Hb 480 g/l
402
518 years
Low SES
urban
residential
school
Vinodkumar
et al.35

All children with Hb 480 g/l

711 years
Low SES
urban
residential
school
Vinodkumar and
Rajagopalan34

123

RCT

A multiple MN daily food supplement (MMFS)

containing chelated ferrous sulphate and
microencapsulated vitamin A, B2, B3, B6, B12, folic
acid, calcium pantothenate, vitamin C, vitamin E,
lysine and calcium

12 months

No differences were observed on retrieval ability,

cognitive speediness and overall cognitive
performance.
Mean change in scores in 5 out of 7 memory tests
and in the letter cancellation test for attention was
significantly higher in the experimental group
(Po0.05) than in the control group.
At end-line, no significant improvement in the
overall intelligence was seen in the Ravens
progressive matrices between the experimental and
control groups.
low n-3 fatty acid
4: Low MN (15% RDA), low n-3 fatty acid

Inclusion criteria
n
Sample
Study

Table 2.

(Continued )

Study design

Supplementation/fortification

Duration

Main cognitive outcomes

471
given that studies on causal factors of low physical activity, in
general, reveal that a feeling of tiredness is an important
barrier.45,46 This is relevant to the nding that South Asians who
undergo a nutritional and epidemiological transition experience
cardiac events at a lower age compared with individuals from
other countries.47 It would be important to optimize physical
tness as early in life as possible, and if micronutrient deciencies
are part of the cause, they are worth addressing. This may also
relate to economic productivity, as even in those who depend on
manual work for their living, B vitamin deciencies (in addition to
generalized undernutrition) may be associated with functional
disadvantages including decreased work capacity.48 However, it is
important to assess whether these vitamins act similarly to
improve performance in otherwise normal, well-fed children. From
the viewpoint of athletic performance, vitamin supplementation
to an athlete on a well-balanced diet has not been shown to
improve performance.49
Despite the prevalence of iron and B-vitamin deciencies in
India, there is limited research on the relationship between these
micronutrient deciencies and physical performance in Indian
children. However, it has been reported that moderate and severe
iron deciency anaemia adversely affects motor development and
physical performance4,50 and mild-to-moderate iron deciency,
even without anaemia, can adversely affect work capacity, work
output and endurance, although the effects may be less obvious.
Anaemic children also fatigue easily owing to their reduced
aerobic capacity increasing stress of exercise,51 and concentrations of haemoglobin have been positively associated with
cardiorespiratory and muscular tness in adolescents.52 The
metabolically important B vitamins have not received adequate
attention because their deciencies are not very well pronounced
and are more often sub-clinical. However, low riboavin levels
have been reported to be associated with impaired psychomotor
performance in school children.4,6,50 Deciencies of vitamin B12
and folate and their link with homocysteinaemia and megaloblastic anaemia53 can also impair performance in young children.
Low intakes of thiamine, riboavin and vitamin B6 have been
associated with overall decreases in physical performance
measures such as aerobic power, onset of blood lactate accumulation and oxygen consumption.54
Intervention studies of iron and the B vitamins with relation to
physical performance in Indian children were few, and four studies
were retrieved31,5557 (Table 3), out of which three were
intervention studies and one was cross-sectional. In all the three
intervention trials, a positive effect of multiple micronutrients on
physical performance outcomes, which included whole-body
endurance, aerobic capacity, speed, muscle strength, endurance
capacity, forearm endurance and visual reaction time, was shown.
These interventions were performed on school children of both
sexes, aged between 6 and 15 years. They differed in the way the
micronutrients were provided, ranging from a fortied beverage
powder to fortied cereal (rice). The amount of vitamins provided
was between 13 and 188% of RDA per serving, and the studies
ranged in duration from 4 to 6 months. All the three trials were
performed on clinically normal children with normal micronutrient
status, which may have attenuated the response to the micronutrient supplementation. The one cross-sectional design study
found haemoglobin levels to be positively related to endurance
capacity in rural adolescent girls.57 Overall, all the 4 studies
indicated improvements in physical performance, more specically physical endurance measures and aerobic capacity of children,
although attributing this benecial effect to B vitamins is difcult,
even though a physiological framework for their effects exists.
NUTRIENT DENSITY OF CHILDRENS DIETS IN INDIA
The micronutrient density of the diet helps in evaluating the risk
of decient intakes in the individual or population, and the need
European Journal of Clinical Nutrition (2013) 467 474

Micronutrient deciency and performance in Indian children

S Swaminathan et al

472
Table 3.

Micronutrients and physical performance

Study

Sample
Sample
characteristics size

Inclusion
criteria

Study
design

Supplementation

Thankachan
et al.31

612 years
Low SES
urban
school based

258

HAZ and WAZ

43

Doubleblind
RCT

Vaz et al.55

710.5 years
Low SES
urban school
based

300

HAZ and WAZ Doublebetween 0 and blind

X3
RCT

Subramani56

710.5 years

200

HAZ and WAZ RCT

between 0 and
X  3 s.d.

Group 1: multiple
6 months
MN-fortified rice with
low-iron (6.25 mg)
Group 2: multiple MNfortified rice with
high-iron (12.5 mg)
Group 3: control
group with unfortified
rice.
Group 1: multiple
120 days
MN-fortified chocomalt beverage
powder
Group 2: matched
energy equivalent
unfortified placebo
Group 3: untreated
control
Group 1: multiple
6 months
MN-fortified chocomalt beverage
powder
Group 2: matched
energy equivalent
unfortified placebo

Panjikkaran
and Usha57

1315 years
rural

150

Girls

CrossNo supplementation
sectional involved

Duration

Main physical performance outcomes

Physical endurance measures
differed between the groups
at end point (P 0.02).
In paired analysis, physical
endurance was enhanced after
6 months in children in Group 1
(4615; P 0.06) and Group 2
(5420; Po0.01) but not in
Group 3 (4516; P 0.86).
An increase in aerobic capacity
and whole-body endurance
(Po0.05) seen in Group 1 compared
with the other two groups.

In the shuttle test, children

receiving supplementation
improved their performance by
about 11 shuttles compared with their
baseline values (P 0.01).
Mean VO2 peak increased from
31.574.31 to 39.124.30 and
mean sprint timing improved from
8.961.31 s to 8.601.07 from
baseline to end-line, respectively.
Girls with acceptable haemoglobin
levels(412 g/dl) had high average
endurance capacity (r 0.96 at 1%
significance).
Two-way frequency analysis
confirmed a consistent increase
in the endurance capacity with
acceptable levels of haemoglobin.

Abbreviations: HAZ, height-for-age Z score; MN: Micronutrient; RCT, randomized controlled trial; SES, socio-economic status; WAZ, weight-for-age Z score.

for dietary diversication, fortication or supplementation.

National-level data on nutrient intakes obtained using a 24-h
recall are available for rural children from 8 states in India,58 and
Table 4 compares these intakes with the estimated average
requirement for each nutrient.4,59 The highest decits in intake for
the various age groups are with folic acid, with all groups
indicating a risk of decient intake in all children. This was
followed by iron and riboavin, with the lowest proportion of risk
of decient intake observed in the younger years, while markedly
increasing during the adolescent period. The proportion at risk for
decient thiamine and niacin intake was also signicant. Overall,
with rural diets being poor in iron and B vitamins, diet
diversication with available local foods such as vegetables,
particularly green leafy vegetables, legumes and milk products is
the main solution to improving intakes, especially with a
substantial section of the population being vegetarian owing to
either cultural or economic reasons. Depending on the age group
(from lower to higher), about 925 mg of iron, 76178 mg of
folate, 0.20.5 mg of thiamine, 0.350.78 mg of riboavin and
1.511 mg of niacin should be provided daily, to reach a more
acceptable proportion (10%) of the population at risk of
decient intakes of these micronutrients. With current costs
and current amount of foods consumed daily in rural India,58
the average cost of the diet would be about Rs.16 per day.
Diversifying and increasing the quality of the diet, for example,
by increasing the fruit and vegetable intake by about 100 g and
milk by about 300 ml per day, would enhance this daily
European Journal of Clinical Nutrition (2013) 467 474

expenditure per caput by about 50%. As an immediate economic

burden, this will perhaps preclude this expenditure as an individual
or family choice. A possible short-term, cheaper solution to meet
adequate levels of micronutrient intake could be through the
fortication of staple foods that are taken through the day. The
benets may not be visible immediately, but this could ensure
adequate intakes of some micronutrients. However, further research
is required to ascertain the effectiveness of these interventions to
improve the status of these micronutrients, as well as body
functionality. As incomes increase and food expenditure increase
and diversify, the problem may also become one of excess, if many
staples and commercial foods are fortied. Therefore, upper limits of
micronutrient intake are also relevant to dene in India at this point.
SYNTHESIS
It appears that, in the small number of studies reviewed, B
vitamins and iron have a role in improving both motor and
cognitive function in decient children. However, several questions remain. First, the methods that are used to measure
functional effects may not be sensitive, and certainly will have
problems with specicity, as they require full cooperation and
understanding from the subject. In the case of cognitive
assessements, oor and ceiling effects may be observed. Second,
these are generally school-based studies, as functional effects are
easier to measure in this age group. Third, the interventions and
exposures measured vary in terms of the mixture of
& 2013 Macmillan Publishers Limited

Micronutrient deciency and performance in Indian children

S Swaminathan et al

473
Table 4.

Recommended dietary intakes and mean nutrient intakes in Indian rural children diets

Age group

Iron
a,4

13 years
Boy and girls
46 years
Boy and girls
79 years
Boy and girls
1012 years
Boys
1012 years
Girls
1315 years
Boys
1315 years
Girls
1617 years
Boys
1617 years
Girls

Thiamine
59

59

Riboflavin
58

59

Niacin
58

59

Folic acid
58

a,4

EAR
(mg/day)

Intake
(mg/day)

EAR
(mg/day)

Intake
(mg/day)

EAR
(mg/day)

Intake
(mg/day)

EAR
(mg/day)

Intake
(mg/day)

EAR
(mg/day)

Intake58
(mg/day)

9.0

5.7 (74)

0.4

0.5 (37)

0.4

0.3 (63)

5.0

5.2 (47)

80.0

20.3 (100)

13.0

8.6 (76)

0.5

0.7 (31)

0.5

0.4 (69)

6.0

7.9 (30)

100.0

28.8 (100)

16.0

10.2 (79)

0.5

0.8 (23)

0.5

0.4 (69)

6.0

9.7 (18)

120.0

34.9 (100)

21.0

12.0 (84)

0.7

0.9 (35)

0.8

0.5 (84)

9.0

11.4 (30)

140.0

40.7 (100)

27.0

11.5 (97)

0.7

0.9 (35)

0.8

0.5 (84)

9.0

11.1 (32)

140.0

39.3 (100)

32.0

13.3 (99)

1.0

1.1 (43)

1.1

0.6 (95)

12.0

13.3 (41)

150.0

47.3 (100)

27.0

13.0 (95)

0.9

1.0 (42)

0.9

0.5 (91)

11.0

12.7 (37)

150.0

45.0 (100)

28.0

16.4 (87)

1.0

1.3 (31)

1.1

0.7 (91)

12.0

15.6 (31)

200.0

56.5 (100)

26.0

13.5 (93)

0.9

1.1 (35)

0.9

0.6 (84)

11.0

12.8 (36)

200.0

47.5 (100)

Abbreviation: EAR, estimated average requirement. Values in parentheses are the rounded-off percentage of the studied population who are at risk of a
deficient intake. Vitamin B12 intakes are not reported. Therefore, these data have been excluded. aThe term used in the referenced document is RDA, although
the reported values are the daily average physiological requirement of iron (adjusted for 5% bioavailability) and folate (adjusted assuming 33% bioavailability);
therefore, these values have been taken to represent the EAR.

micronutrients, their dose and the duration. Fourth, it is also

important to understand whether these vitamins and iron have a
role in normally nourished children consuming a normal diverse
diet. In general, these studies are conducted on children from
average to poor schools, where it is more possible that
micronutrient deciences exist. Fifth, as most intervention studies
have also assessed the provision of a fortied supplement in the
form of a product or a cereal, but in a format that offered this
supplement for one meal provided in school, it is worth
considering whether supplementations would be more effective
if provided at a lower level, but with every meal. For example,
providing one RDA of a micronutrient in a single meal requires
that the micronutrient is adequately absorbed. Then, the
effectiveness of RDA doses of micronutrients given as a single
serving (as in proprietary foods that are being increasingly
marketed to children) is arguable. One may also argue that in
many rural areas children do not attend school regularly or even
not at all, as they work for the family; a school-based intervention
is only effective if children get to school regularly. Sixth, in studies
showing no functional effect, it may be because the window for
change has passed, and that interventions might have been
benecial in early stages of life. It may be important to study the
effects of micronutrient deciency on cognitive and physical
performance in normal, undernourished and overweight children
to understand relationships much better. However, even with
caveats, the physiological framework is strong enough to suggest
that sub-clinical B-vitamin and iron deciencies may be quite
rampant and that they are likely to have functional effects that
track into adulthood, such that general long-term health and
productivity is affected.
CONFLICT OF INTEREST
AVK consults for McCain Foods, and his honoraria go entirely to charity. The
remaining authors declare no conict of interest.

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