Decreased

preschool
Imelda

rate of stunting
children
through

T Angeles,

ABSTRACT
hematological

Werner

J Schultink,

among anemic Indonesian

iron supplementation12

Paul

Effects of iron supplementation

status
of Indonesian
anemic

Matulessi,

Rainer

Gross,
Chwang
physical

on growth
and
preschool
children

with low weight-for-age

were investigated.
A treatment
group
(n
=
39) received
daily supplements
of3O mg Fe and 20 mg vitamin

both

C, whereas

anism

a control

food
were

and

(P

of iron

vitamin

Nutr

supplementation
as well

group
group.

school

<

0.01).

<

in the treatment
increase
in the control

the

on linear

growth

were larger
The positive

was

not

caused

Subjects
The

Iron supplementation,

anemia,

growth

rate,

anemia

reduced

and

decreased

problems

among

1 , 2).

Anemia
capacity
and

learning

(6).

Decreased

growth

is associated

with

achievement

(2-5).

in infancy

compared

with
rate

in

increased

are

two

children

A child

risks

protracted

peers

having

children

who

in

(WFA)

HFA

(8).

in developing

lack

is highly

countries.

Stunting

ifleft

untreated

(11,

which

has

in children

can

usually
after

of nutrients

Stunting

implies

that

lead

to a low

The

area

study

a childs

from

time,

an early

no catching

age

occurrence

ofanemia

among

J C/in Nutr

preschool

1993:58:339-42.

and

reduced

children.
Printed

growth
Aukett

and

in USA.

al

to in-

itself.
and

study

reduced

investigated

significantly
status,

improve

ofanemic

pre-

WFA.

out
that

109000

in Jakarta.

covered
and

a population

group
comprised
no stable jobs).
was

Indonesia,

at two

neighborhoods

with

density

sub-

a total

of 38000/

the lower socioeconomic

class
and environmental
hygiene
in

poor.

process
sequentially
and then as anemic.

identified
children,
aged 2The selection
criteria
were

to define
anemia
(2). All subjects
records
at the health centers,
which

were identified
contained
only

data on WFA.
From
the health
centers
list 2 16 children
were
selected
who met the anthropometrical
criteria.
All 2 16 children
to the health
their

a low

tration

center

hemoglobin
hemoglobin

was measured.

at the

request

concentration

ofhealth

could

concentration,
Finally.

center

be analyzed.
serum

84 children

met

femtin

staff

so

For those
concen-

the hematological

criteria.
The parents
of 80 children
gave written
consent
for
their childrens
participation
in the study.
Stool samples
of the
subjects
were examined
for the presence
of parasitic
infections
(ascariasis
and trichuriasis).
Children
with parasites
received
antreatment

(14) before

starting

iron

are often
(3)

1993 American

From
of

Indonesia,

the SEAMEO-TROPMED
Jakarta,

Indonesia

Center

Jakarta

and

Gesellschaft

Zusammenarbeit,
Eschborn,
Germany.
2 Address
reprint requests to WJ Schultink,
3852, 10038 Jakarta.
Indonesia.
Received
November
20. 1992.
Accepted
for publication
March 18, 1993.

be possible

rate
et

of iron

present

would

this

morbidity,

of anemia

the

mech-

supplementation,

genetic

onward,

up may

the
In theory,

as follows:
WFA Z score between
-2 and -3. hemoglobin
concentration
between
80 and 1 10 g/L, and serum
ferritin
< 12 g/
L. The upper
limits
of the hematological
measures
are usual

tihelminthic

communities

(9), and it may negatively

affect
life because
of smaller
body size

develops
some

will
in many

carried

of

the

with

reduced

effect

as hematological

a low

offices

study
have

that

12).

associated

was

health

km2. The
(25-30%

came

iron

developing

risk and

performance

prevalent

is not fully expressed

work capacity
in later

(10).

.4,ii

A chronic

(stunting),

potential
physical

study

district

values
used
from existing

develbetter

in

morbidity

(7). Growth

rate

in children
is associated
growth,
impaired
immune

capacities

anemic

disadvantages

growth
preschool

Asia,

elusive.

and methods

The selection
5 y. as low WFA

be assessed
by measuring
weight,
height,
and age, and can be
classified
by combining
the measurements
to form the indicators
weight-for-height
(WFH),
height-for-age
(HFA),
and weight-forage

with

direct

prevalences

in Southeast

children

population

iron-deficient

scholastic

rate

high

improves
supple-

influencing

However,

to decreased

or to the

the

iron

of positively
rate.

be due

iron

developing
countries
with decreased
physical

status

intake,

effect
growth
remains

growth,

nutrition-related

countries

may

supplementation
Therefore,

growth

physical

(P

Indonesia

opmental

food

dual
and

whether

Iron-deficiency

been

in growth

Considering

1993:58:339-42.

and

the

status

ofiron-enhanced

creased

Introduction

system,

have

0.001).
Height
and
Increases
in height

KEY WORDS

major

may

hematologic

that iron
children.

(P

values

supplementation

preschoolers,

mentation

increase

double
height,

by increased
food intake,
but seems to be influenced
by decreased
morbidity.
Iron supplementation
may be a relatively
inexpensive
way to help decrease
the high prevalence
of stunting.
Am
C/in

et al ( 1 3) reported
growth
in anemic

growth

Z score

height-for-age
0.001)
than

20 mg

Sastroamidjojo

hemoglobin
and serum
femtin
concentrations
Only the treatment
group showed
a significant

in all hematological
of all children
increased

effect

37) received

of 2 mo. Supplement
allocation
was
and finish of the study,
body weight,

intake.
and
determined.

increase
weight

(n

Soemilah

and
Society

for Clinical

Nutrition

at the University
f#{252}rTechnische

SEAMEO/GTZ,

P0 Box

339

Downloaded from ajcn.nutrition.org by guest on August 12, 2015

only for a period

blind.
At the start

group

and

340
so as to remove
and

helminthiasis

hematological

dom

to a treatment

None

of the

ferrous
dered

The

group

(ii

children

diseases.
The treatment
for a period

status.

prepared

Daily
supplement
locations,
between
closely

from

a control

(n

acute

supervised

daily
iron

C. both in powthe control

group

Farma,

Jakarta,

health

height,

workers

packages.
finish
of the

and

food

2-mo

intake

by using

perature
or more

the

incidence

daily by the researcher

The children
were
and

hemoglobin,

mean

weighing

Germany).

(16).
intake

3 alternate

was

by using generic
Energy
intakes

determined

(one

day

platform-

SECA,

were

by using

of sex and

by the

24-h

recall

the

days

of data

collected

Electronics

Ltd.

age

method

on
over

collection)
size.
food-

Japan).

by radioimmunoassay
kit (Ramco
Laboratories,

analysis

carried

Serum

procedure
Houston).

out at the
University

was

via venipuncture

out

by

between-subjects
subject
factor.
the differences

factor

and

time

by using unpaired
were not normally

differences

within

matched-pairs
were tested

signed-rank
test, and
by using the Mann-Whitney
transformation

groups

the

failed

tested

to give

de-

Pathol-

and
10.5

MANOVA

re-

Chicago)
C) as a

as a within-

interaction
groups

were

(P

<

0.05),
further

I tests, respectively.
as for serum
ferritin,
by

using

Wilcoxons

differences
between
test (20), because
a normal

children

and

group.

Four

and

groups

to treat

19 female)

of the

were,

period

male

subjects

and

1 8 female)

selected

an Islamic
holiday
on
relatives
outside
Jakarta.
control
mo.

in the control

a 2-mo

37 (19

Review
At the end

80 subjects

which
Mean

their
parents
(SD)
age in

respectively,

37.4

9.5

Results
Stool
and
with

examination
showed

before

that

70.3%
of the
parasites
(no

56.5%

the

start

ofthe

children
significant

of the

children

supplementation

in the treatment

group

in the control
group
were
difference
by chi-square

infected
test). At

the start of the study.

no significant
differences
existed
in hematological
values
(Table
1) nor in weight and height (Table
2)
between
the treatment
and control
groups.
During
the supplementation
period
limits, indicating

WBCs
absence

ofall children
were
ofserious
infectious

have influenced
the serum
After
the supplementation

the

group

(Table

within
diseases

ferritin
concentration.
period
the mean

(P

group
for hemoglobin
ferritin
(P = 0.001)

control

were

the normal
that might

values

of

the

0.001),
MCV (P = 0.02),
higher
than the values
for

1 ), whereas

there

was

no significant

for the mean values of weight,

height,
and the Z scores
HFA, and WFH
(Table
2). With respect
to the change

difference
ofWFA,

in the variables,
the before-after
differences
for the treatment
group
were significantly
greater
than those for the control
group
for hemoglobin
(P = 0.00 1 ), serum
femtin
(P = 0.02), MCV (P
=
0.02),
change

the

height
(P - 0.00
in WFH
Z score

ment

group

dicate

anemia.

were

HFA Z score
control
group

1 ), and
in the

change
in the treatment
After supplementation

TABLE
1
Hematological

above

(P

the cutoff

Within-group

increases

point

0.00 1 ). The
higher
than

was

group
(P = 0.02).
all hernatological
values

of the

concentrations
in body

values

before

distribution.

groups
a logTo

and after

weight

treatthat

and

in-

height

2 mo supplementation*

Before
Iron

vs after)

and paired
distributed,
were

was

4.0 (SPSS Inc.

C vs vitamin

When there was a significant

between
and within
treatment

investigated
When
values

ferritin

of Clinical

using

(before

control

18) by using a cornAll hematological

Department
of Indonesia.

peated-measures
design
of SPSS/PC+
(19) with treatment
(iron
and vitamin

in the

the

39 (20 male

group

Ethical

Jakarta.

over

groups

used.

between

concentration,
MCV,
and WBCs
counter
(Sysmex
CC-l 80: TOA

Kobe.

subjects

treatment
and serum

Hamburg,

0. 1 cm

designed
to identify
portion
by using the Indonesian

Hemoglobin
by electronic

analyses
were carried
ogy, Medical
Faculty,

arithmic

0900

table ( 1 7). Intake

at the start and finish ofthe
supperiod
was calculated
as the average
intake
of the

Medical

Data

alpha:

for effects

between

food models
were calculated

and 1 1 30.
determined

termined
mercial

an electronic,

to the nearest

to correct

3 d ofdata
collection.
Blood samples
(3 mL)
0830
were

770

measured

data

days

composition
plementation

tern-

of the indicators
WFA,
HFA,
and WFH
by using the National
Center
for Health
Statistics

reference

growth
Food

(body

diarrhea
(four
and recorded

Z scores

a microtoise.
were calculated
(NCHS)

(SECA

was

of fever

of sup-

or the district
health
worker.
without
clothing
between

0. 1 kg by using

scale

Height

duration

period

infections
(1 5), and
per 24 h) were checked

(ITA.)
weighed

1 100 to the nearest

model

and

37 #{176}C),
respiratory
loose, watery
stools
>

iron-treatment

was

by the

period

supplements

set included

in the

period

ofoccult

plementation,

approved
of Indonesia,

supplementation

their anemia.
The final data

period
Furthermore,

the entire

was

University

iron

between
test

researchers

blind

the

Over

received

iron-treated
and 37.2

volume
(MCV),
and serum
ferritin
concentration.
cell counts
(WBCs)
were carried
out to determine
infections.

2-mo

at central
was super-

corpuscular
White
blood
presence

ofthe
group

Indonesia).

ofthe

recorded.

to determine

proposal

of the

dropped
out after
took them to visit

supplementation

were

collected

one

was double

research

ofhelminthiasis

the chi-square

+ vitamin
(n = 39)
Hemoglobin
Serum ferritin
MCV (ft.)
Vitamin
C (n =
Hemoglobin
Serum ferritin
MCV (if.)
*

After

Difference

C
(gIL)
(tg/L)
37)
(gIL)
(ig/L)

SD. MCV,

mean

102
6.2
78.2
103
7.1
77.6

corpuscular

9
1.7
7.2

1 12
15.0
82.5

8
2.5
7.0

104
10.0
77.9

9t
lO.2t
5.4

10
8.8
4.0

I
10.9
9.2

1
2.9
0.3

l0t

9.5j
4.9

12
10.7
8.0

volume.

t Significantly
greater than the related value ofthe vitamin C group:
=
0.001, P < 0.02.
Significant
difference
between
start and finish of supplementation
period, P = 0.001 (within-group
change).
tP

Downloaded from ajcn.nutrition.org by guest on August 12, 2015

were

and

supplements

which
iron

in prevalence

of enrollment,

Committee

supplements

C alone.
containing

The

40).

infectious

as 8 1 mg hydrated

of 20 mg vitamin
to the supplement

ofthe

samples

group

obvious,

by PT Kimia

by district

coded
supplement
At the start and
blood

at the time

ingestion
by subjects
took
place
meals
from 0900 to 1 1 30 h, and

Allocation

weight.

test the difference

at ran-

with 20 mg vitamin
same period
oftime,

supplements
appearance

(supplements

vised

growth

were

of 2 mo of 30 mg elemental

received
daily
was of similar

(ITA.).

of both
assigned

received

sulfate.
combined
form.
During
the

AL

as a confounder

suffered

group

ET

80 subjects
40) and

ANGELES

GROWTH
TABLE 2
Weight, height, and Z scores
after 2 mo supplementation*

AND

IRON

STATUS

OF

During
of anthropometric

Before

indicators

before

After

and

both
This

+ vitamin

10.6
86.2
-2.53
-2.33
1.48

10.6
86.6
-2.54
-2.18
-1.56

1.2
6.5
0.42
0.83
0.55

11.1 1.4
88.9 5.9
-2.37 0.49
-1.96 0.73
1.57 0.50

1.3
6.9
0.34
0.96
0.60

1 1.2 1.5
88.1 6.9
-2.33 0.54
-2.10 0.92
-1.36 0.68

0.50.5t
2.7 l.Stt
0.17 0.33
0.37 0.4ltt
-0.06
0.46
0.6
1.5
0.21
0.07
0.21

Significantly
P

were

higher

significant

in the

than

the related

in both

treatment

groups

group

was

scores

significantly
ofWFA

period.
Energy

450 1 1045

(Table

2.7

whereas

and

intake

WFH

at the

kJ/d

significant

in the

increased
start

for the

changes

Episodes
control
group
respectively,

before

the

vitamin

vitamin

during

iron-treated

start

of the

whereas

period
and

No

data

was

4 1 1 3 1 187

groups.
and

were

diarrhea
more
group

in the

frequently,
(Table
3).

about
the same
in both
for fever,
respiratory
available

on

was

reflected

morbidity

study.

height

this

weight

of

may

be

gain

in a higher

was

WFA

group
received

infection

control
more

on growth
unlikely

resulted

group.

the

with parasites.
treatment,

at the end

treatment
given
there would
have
in the control

start

in the control

were infected
antihelminthic

to have

in an increase

Before

children

was made

influences

Z score for the treatment

Z score changed
in the control

in HFA

did not change

in the

ences

ofthe

of the

group

than

The children
but no recheck

supplementation

before
supplementation
been especially
negative

group.

happened

However,

such

considering

the

in both groups.
supplementation

influ-

sufficient

on growth

of

anemic
children
have been reported
elsewhere
(3. 1 3). The children in those studies
had initial
HFA Z scores
of -0. 14 (3) and
I .66 ( 1 3), which
does not classify
them
as being stunted,
and

an effect

of the supplementation
and control
groups
were
respectively.
There
were no

infections,

The

the WFA

period

they were not

present
study.

group

to which

study.

comparable
increases
in weight
The enhancing
effects of iron

the supplementation

group

of the illnesses
was
and 1 . I d, respectively,
diarrhea.

increase

extent

rise

Z score

HFA

Z score

are

the

in this
and

fact that

period.
If the worm
had been ineffective,

end

of the two

respiratory

and

height

while

for parasite

0.001)

C-only

occurred
1 .7, 2.5, and 3.0 times
than
in the iron-supplemented

duration
1 .5, 3.5,

infections,

(P

of the supplementation

in either

of fever,

2). The

1.5 cm

kJ/d for the control

group.
At the
period
the intakes
for the treatment
44 1 8 840 and 4368 99 1 kJ/d,

Average
groups:

of the iron

group

in the treatment
in both groups

0.81
0.36
0.23
0.5lII

group
was 1.5 1.8 cm (P = 0.001).
the Z scores
of WFA
and HFA
in-

the increase
in the control
In the iron-treated
group
creased

value

The

and

for growing
children.
influenced
by the de-

change
in height
in the treatment
group
was
than the height
change
in the control
group,

supplementation

0.02.

only.

weight

underweight
Two studies

of iron

due to the low

in methodology

as opposed
among
Thai

supplementation

to the
children

children
in the
did not show

on growth,

but

this

may

be

amount
of supplemented
iron or to differences
(22, 23). Normally,
a child 37 mo of age with

a height similar
to the median
ofthe
NCHS
reference
(16) would
need to grow
1.4 cm in 2 mo to remain
equal
to the median.
An average
increase
in height ofthe
treatment
group
in the present study
was 2.6
dicating
a marked

cm. or 1 86%
acceleration.

of the median
growth
rate, inIn a study in which
daily food

supplements
were
provided
to stunted
children
for a period
of 90 d (24), HFA
-2.34
found
growth

preschool
changed
from

to -2.24.
which
reflects
a smaller
increase
than the one
in this study. Effects offood
supplementation
on physical
are reported
to be most effective
when children
are aged

1 y (25, 26). In the present

<

Indonesian

Z scores

but only iron

it is interesting
improvement
In the

study,

in which

no food

were distributed
and all children
to note that the treatment
group
in linear

growth.

study,

energy

present

intake

was

supplements

were aged > 2 y,

showed
a marked

sufficient

for the chil-

drens
actual
weight
according
to WHO
daily
intake
recommendations
of 397 kJ/kg
(95 kcal/kg)
(9). Treating
anemia
is
reported
to increase
appetite
in adults
(27). However,
the treat-

Discussion
Both
Indonesia
milieu

and growth
are considered

of multiple

vestigate
and

anemia
and

conditions,

the effect

physical

growth

children.
The iron dosage,
ganization
(WHO)
The

substantial

supplementation
cantly
larger
C-only

group.

of iron

the

are
health
aim

supplementation

variables

ofanernic,

which
was
recommendations

increases
than

retardation
public

in line

in hematological

highly
prevalent
in
problems.
In this

of this

study

was

on the blood
underweight,

to invalues

preschool

with World
Health
Or(2), proved
to be effective.
values

over

TABLE
3
Episodes
of fever. respiratory
infections,
and diarrhea
supplementation
period in the two groups

the 2-mo

period
of the iron-treated
group
were signifithe small changes
that occurred
in the vitamin

Iron
Type

of morbidity

(n

vitamin
39)

during

the

Vitamin
C
(n = 37)

%
Fever
Respiratory
Diarrhea*
*

Defined

7.7
10.3
5.1

infections

as four or more

loose,

watery

13.5
27.0
16.2
stools

per 24 h.

Downloaded from ajcn.nutrition.org by guest on August 12, 2015

II

groups

the

be expected
positively

(2 1), but

to a significant

group

in WFH

t Significant
difference
between start and finish of supplementation
period (within-group
change) tP < 0.0 1 , P < 0.05.
:j: Significantly
higher than the related value of the vitamin C group,
P= 0.001.
group,

in both

leading

0.6t

period

be estimated

score. The marked

1 .8 times
greater

SD.

treatment

cannot

similar

(n = 39)
Weight(kg)
Height (cm)
Weight-for-age
Height-for-age
Weight-for-height
Vitamin
C (n = 37)
Weight (kg)
Height (cm)
Weight-for-age
Height-for-age
Weight-for-height

the supplementation

worming

Difference

341

groups
increased
as would
increase
may have been

true
Iron

CHILDREN

342
ment

group

did

plementation
growth

rate

food

increased

energy

suggests

that

in the

treatment

group

was

During

the

diseases

in the treatment

ofinfectious
rate
iron

have
This

intake.

control

not
period.

group.

This

intake
the

may

have

caused

period
group
the

study
indicate
that
role in overcoming

iron

I 0. Spurr GB. Effects of chronic energy deficiency

on stature, work capacity and productivity.
In: SchOrch B, Scrimshaw
NS, eds. Chronic
energy deficiency:
consequences
and related issues. Lausanne:
International
Dietary Energy Consultative
Group,
1987:95-134.
1 1 . Billewicz WZ, McGregor
IA. A birth to maturity
longitudinal
study
ofheights
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villages. Ann
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A, Pollitt E. Iron supplementation
and physical
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children.
Am J Clin Nutr 1988:47:496-

suplinear

incidence

less than

increased

in the treatment
group.
Furthermore
the
on oxidative
processes
may have stimulated

The results
of this
may play an important

the

by higher

the

was

influenced

ET

increased

not

supplementation

after

ANGELES

in the
growth

direct
action
of
growth
rate.

supplementation
both growth
retar-

dation
and anemia
in preschool
children.
It is recommended,
therefore.
that consideration
be given to providing
iron supplementation
women,

but

not only to existing

target
also to preschool
children.

on effective
would
need
cost

supplementation
to be conducted.

ofiron

treatment

example,

is relatively

treatment

for one

Traditionally,

it is believed

between
micronutrients
tamin
A (30). Furthermore,
that

stunting

because

was

not

infectious

leads

to growth

this

WFA

cost

may

the
the

is caused

is too limited
effects
of mibut also zinc.
the interaction

indicator

2 1.

to growth

retar-

this study
increased

did confirm
morbidity,

that
which

and

1990.

20.

of malnutrition

contribute

in children,

and
about

for

one between
iron and viworking
group
concluded

also

It is necessary
malnutrition,

study,

$0.18.

or HFA

be considered,
(28, 29) and

an appropriate

depression

indicator,
knowledge

low

as the
a WHO

(3 1 ). However,
may cause

indirectly
to stunting.
beliefs
about
chronic
appropriate
Increased

such

diseases

dation
of children
lack of micronutrients

1 mo

energy.
This assumption
taking
into account
the

cronutrients.
Not only should
iron
which
is reported
to enhance
growth

children
that the

In the present

for

that

preschool
to note

14. World Health Organization.

The treatment
and management
of severe protein-energy
malnutrition.
Geneva:
WHO, 198 1.
15. World Health Organization.
Case management
ofacute
respiratory
infections
in children
in developing
countries:
report of a working
group meeting. Geneva:
WHO, 1986.
16. National
Center for Health Statistics.
NCHS growth curves for children, birth-18
years, United States. Washington,
DC: US Department ofHealth,
Education
and Welfare,
1977. (PHS 78-1650.)
17. Directorate
ofNutrition.
Food composition
table. Jakarta: Ministry
of Health. RI, 1990.
18. International
Nutritional
Anemia
Consultative
Group.
Measurements ofiron
status. Washington,
DC: INACG,
1985.
19. Norusis Mi. SPSS/PC+
advanced
statistics 4.0. Chicago: SPSS Inc.

may

therefore

to reconsider
the
the use of stunting

selection
of suitable
role of micronutrients

lead
existing
as an

treatment.
is vital

in

#{163}3

aspect.

22.

23.

We thank Poppy Hendrawan,

director
of Tebet Community
Health
Center,
for her excellent
cooperation.
The valuable
recommendations
of Noel Solomons
and Gustaaf Sevenhuysen
are highly appreciated.

24.

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by a lack ofprotein
and/or
and should
be reviewed,

low.

child

501.

groups
such as pregnant
Therefore,
further
study

systems
for
It is important

AL