Prevention of Iron Deficiency Anemia in Adolescent and Adult Pregnancies

Clinical Medicine & Research
Volume 1, Number 1: 29 - 36
©2003 Clinical Medicine & Research
www.mfldclin.edu/clinmedres
Original Research
Prevention of Iron Deficiency Anemia in Adolescent
and Adult Pregnancies
Paul R. Meier, MD, Departments of Obstetrics and Gynecology, Marshfield Clinic, Marshfield, Wisconsin
H. James Nickerson, MD, Pediatrics, Marshfield Clinic, Marshfield, Wisconsin
Kurt A. Olson, MS, Departments of Epidemiology and Biostatistics, Marshfield Medical Research Foundation, Marshfield, Wisconsin
*Current Affiliation, Amgen, Thousand Oaks, California
Richard L. Berg, MS, Departments of Epidemiology and Biostatistics, Marshfield Medical Research Foundation, Marshfield, Wisconsin
James A. Meyer, MD, Adolescent Medicine, Marshfield Clinic, Marshfield, Wisconsin
ABSTRACT
OBJECTIVE
Worldwide attention over iron deficiency anemia (IDA) in pregnancy has shifted recently from providing supplements during
pregnancy to attempting to ensure that women, especially adolescents, have adequate iron stores prior to conception. We sought
to determine whether adolescent and/or adult women still need supplements during pregnancy to avoid IDA, even if iron stores
are adequate, and whether the IDA translates into maternal and/or infant morbidity and mortality.
DESIGN
Randomized, double-blind clinical trial with placebo control.
SETTING
Multicenter clinic setting in central Wisconsin.
PARTICIPANTS
Adolescent women 18 years or less in their first pregnancy, and adult women 19 years or older, who were found to be healthy
and iron sufficient at their first prenatal visit.
METHODS
Participants were randomized to receive iron supplementation (60 mg/day elemental iron) or placebo. Serum ferritin of 12 ng/mL
or less with simultaneous hemoglobin of 11 g/dL or less defined IDA. When IDA occurred at the second trimester, a therapeutic
supplement of 180 mg of elemental iron per day was initiated.
RESULTS
Forty-seven percent of all placebo-supplemented and 16% of all iron-supplemented patients exhibited IDA (p<0.001); 59% of
adolescent placebo-supplemented and 20% of adolescent iron-supplemented patients exhibited IDA (p=0.021). Nausea, vomiting,
diarrhea, and constipation were not significantly different in the iron supplemented group compared to the placebo group, and no
significant differences were seen in maternal or neonatal health, but the number of women studied was limiting for analysis of
these adverse events.
CONCLUSION
IDA is common in healthy, iron-sufficient adolescent pregnant women during the second trimester, and body stores of iron
decline in both adolescent and adult pregnancies. The incidence of IDA during adolescent and adult pregnancies is substantially
reduced with 60 mg of elemental iron per day. However, there remains no clear evidence that maternal or neonatal health will
benefit from correcting these deficits.
RECEIVED:
February 15, 2002
REVISED AND ACCEPTED:
September 27, 2002
REPRINT REQUESTS:
KEYWORDS:
H. James Nickerson, MD
Iron deficiency anemia (IDA); Iron deficiency; Iron supple-
Department of Pediatrics
ments; Pregnancy
Marshfield Clinic
1000 North Oak Avenue
GRANT SUPPORT:
Marshfield, WI 54449
Research was supported by BRSG S07 RR05960-01 awarded
Email: nickerson.harlan@marshfieldclinic.org
by the Biomedical Research Support Grant Program, Division
of Research Resources, National Institutes of Health and in
part by a grant 128-01-06 from the Marshfield Medical
Research Foundation, the Mead-Johnson Nutritional Division,
and Hybritech, Inc, San Diego, California.
29

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INTRODUCTION
Adolescence is a time of intense physical, psychosocial, and
cognitive development. Increased nutritional needs at this
Anemia during pregnancy, particularly iron deficiency ane-
juncture relate to the fact that adolescents gain up to 50% of
mia (IDA), continues to be of world-wide concern.1-16 Iron
their adult weight, more than 20% of their adult height, and
supplementation in pregnancy is a widely recommended prac-
50% of their adult skeletal mass during this period. The iron
tice, yet intervention programs have met with mixed success
needs are high in adolescent girls because of the increased
and controversies abound. Should supplements be given on a
requirements for expansion of blood volume associated with
weekly or daily basis?4 Should supplements be given to all
the adolescent growth spurt and the onset of menstruation.29
pregnant women, or only to those with demonstrable
When pregnancy is interposed during this time, problems of
anemia?17,18 Are there health risks associated with adminis-
iron balance are compounded.8,16,19,22,26,27,29 Over half the
tering excess iron to women who don’t need it?4 In contrast
world’s population is under 25 years old, and more than 80%
to severe anemia, does mild to moderate anemia during preg-
of the world’s youth live in developing countries.5 Iron
nancy translate into maternal or neonatal morbidity or mortal-
deficits induced by poor diet and disease, along with difficult
ity?4,5,17-20 Should emphasis be placed on building up iron
logistics associated with supplementation programs in devel-
stores prior to conception?21 Are adolescents at an increased
oping countries, compound the problem of studying the iron
risk of developing anemia as compared to adults?5,22
needs during pregnancy in much of the world’s population.
For these reasons, we felt it important to study a population
The world’s adolescent population (age 10–19 years) is esti-
with adequate diets and normal pre-pregnancy iron stores. We
mated to stand at more than 1 billion, yet adolescents remain
investigated the response to supplemental iron in adolescents
a largely neglected, difficult-to-measure, and hard-to-reach
and adults throughout the course of normal pregnancies.
population in which the needs of adolescent girls, in particu-
lar, are often ignored.5 This area of adolescent health has
METHODS
been difficult to study, and there are many unknown factors
and consequences for iron deficiency during adolescence in
Subjects were recruited from obstetrical patients seen for
terms of standards, measurement indicators and health conse-
their first prenatal visit at Marshfield Clinic, a private group
quences.
practice in central Wisconsin. All patients signed informed
consent approved by the Institutional Review Board of the
In 1993, the World Health Organization (WHO) instituted its
Marshfield Medical Research Foundation.
Safe Motherhood Initiative with a goal of reducing the num-
ber of maternal deaths by half before the year 2000.23-25 A
Patients were divided into two groups consisting of adoles-
key component was to eradicate anemia in pregnancy, focus-
cents 15 through 18 years of age in their first pregnancy, and
ing on the greater risk in younger women. In 1997, WHO
adult women 19 years or older in their first or greater preg-
convened a regional consultation of experts to address malnu-
nancy. While WHO defines adolescents as persons 10-19
trition issues among adolescent girls in South-East Asia.26
years of age,30 we chose to use 19 years as a cutoff in order
Among the recommendations for action was a need for the
to enhance the chances of detecting an effect of the adoles-
development of assessment, advocacy, prevention, and control
cent growth spurt.
initiatives, in most countries, to reduce anemia in adolescent
girls. As an outcome, WHO training programs for adolescent
Adolescent or adult women found to have IDA on their first
nutrition have been initiated.
prenatal visit were excluded and offered treatment. Using ran-
domization stratified by age group, eligible adolescent and
In 1999, a special symposium entitled “Improving Adolescent
adult participants were randomized to receive once daily in a
Iron Status before Childbearing” was convened in
double-blind fashion either an oral iron supplement of 200
Washington DC. The conclusions of this group were that
mg of ferrous sulphate (60 mg elemental iron) or a placebo
many girls are already anemic by the time they become preg-
capsule identical in appearance to the iron supplement. Two
nant (16-55%), and that pregnancy is too short a period of
hundred twenty-five capsules were issued to each study par-
time in which to reduce pre-existing anemia, especially when
ticipant, and the unused iron or placebo capsules were col-
many women do not seek prenatal care until the second or
lected at the conclusion of their pregnancy to estimate adher-
third trimester.27 Thus, they concluded that emphasis needs to
ence. Each participant also received 1 mg of folic acid daily31
be placed on pre-pregnancy programs to increase body iron
and was asked not to take any other vitamin or mineral prepa-
stores.
ration during the pregnancy with the exception of fluoride. At
24 to 28 weeks all participants were interviewed by phone by
Others argue that the iron requirements are highest in the sec-
a research nurse to quantify the patient’s perception of the
ond and third trimesters of pregnancy, and that stores are
occurrence of nausea, vomiting, diarrhea, and constipation in
exhausted in most women at this point.19,28 Therefore, iron
their own pregnancy.
balance at this stage depends more on adequate intakes of
bioavailable iron than on the size of iron stores at
conception.19
30
CM&R 2003 : 1 (January)
Meier, et al.

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Laboratory tests were performed upon enrollment in the pre-
More severe IDA with hemoglobins <10.0 g/dL occurred in
natal program (test 1), again at 24 to 28 weeks (test 2), and
four adults (1 on iron, 3 on placebo) and two adolescents
finally before delivery at 36 to 40 weeks (test 3). Serum fer-
(both on placebo) during the study. Iron deficiency without
ritin and hemoglobin levels were assessed on venous blood as
anemia was developing in both placebo groups by tests 2 or 3
previously described.32,33
as evidenced by significantly lower serum ferritin levels
(table 3 and figure 1).
IDA was defined as a simultaneous serum ferritin of
?12 ng/mL and a hemoglobin of ?11 g/dL. The value of
Adherence to supplements
?11 g/dL of hemoglobin was chosen to allow for the usual
Adherence to supplements was assessed through pill counts,
mild decrease in hemoglobin concentration seen in normal
although results were not available in all patients. Adherence
pregnancies related to the physiologic alterations in blood
was generally high but ranged from 32% to 124% in individ-
volume.34-36
ual patients (table 3). In the iron group, this corresponds to a
range of 19-74 mg/day in women’s average intake of elemen-
All adolescent and adult pregnant women who developed
tal iron during the study period. Among adults, the observed
IDA at the second test period were offered therapeutic ferrous
adherence was significantly higher among those taking iron,
sulfate containing 60 mg of elemental iron 3 times daily.
with medians of 98% and 84% among adults taking iron and
Most adolescent pregnant women were part of the Healthy
placebo, respectively (p=0.036).
Birth Program at St. Joseph’s Hospital.
Side effects
Statistical comparisons between groups with regard to IDA,
Table 4 shows the incidence of side effects for the four stud-
adherence, and side effects were based upon Fisher’s exact
ied symptoms. There were no significant differences between
test, while comparisons of hemoglobin, serum ferritin, and
iron and placebo treated patients or between the adolescents
gestational age were based upon the Wilcoxon rank sum test.
and adults.
Twelve subjects who received therapeutic iron for IDA during
the study were analyzed as randomized (9 on placebo, 3 on
Pregnancy outcomes
iron). Results in this report are deemed statistically signifi-
Mean gestational age at the time of delivery was over 39
cant (p<0.05).
weeks and was not significantly different between iron and
placebo treated patients (table 5). There was no clinically sig-
RESULTS
nificant perinatal morbidity or mortality among any of the
infants delivered as measured by Apgar scores at 1 and 5
Patients
minutes. None of the infants needed admission to the neona-
Over a study period of 29 months, 144 patients were initially
tal intensive care unit. Only three infants were less than 2,500
enrolled on the study. Thirty-three patients were ultimately
g at birth, one from the iron group and two from the placebo
excluded or lost to analysis: 20 had inadequate data or failed
group. The total number of C-sections in all pregnancies was
to comply with the study or medication requirements (10
19, with similar frequencies in the iron and placebo groups
were adolescents and 10 were adults); 3 moved or were lost
(16% and 19%, respectively).
to follow-up; 3 had spontaneous abortions; and 7 were
excluded for other reasons. Of the 111 patients analyzed, 53
Therapeutic iron supplementation
received placebo and 58 received iron supplementation.
A therapeutic supplementation of ferrous sulfate 60 mg 3
Patient characteristics at randomization are shown in table 1
times daily was offered to women who developed IDA during
and were well balanced between the randomized groups.
the second trimester (at test 2 on weeks 24 to 28) and was
accepted by three women in the iron group and nine women
Incidence of anemia in pregnancy
in the placebo group. IDA was resolved by the third test at
Overall, 34 of 111 (31%) women developed IDA, 25 of 53
the end of their pregnancies in all three women in the iron
(47%) receiving placebo and 9 of 58 (15%) receiving iron
group and in six of nine women in the placebo group. This
(p<0.001). In adolescents, 4 of 20 (20%) iron supplemented
part of the study was strictly observational and adherence in
patients, and 10 of 17 (59%) receiving placebo developed
taking supplemental iron was not measured.
IDA (p=0.021). Among adults, 5 of 38 (13%) receiving iron,
and 15 of 36 (42%) receiving placebo developed IDA
DISCUSSION
(p=0.008). Thus, in both age groups the incidence of IDA
was significantly reduced in iron treated patients compared to
Both adolescent and adult women were shown to have signif-
placebo treated patients (table 2). The incidence of IDA was
icantly higher rates of IDA during pregnancy if given placebo
not significantly different comparing adolescent and adult
compared to 60 mg of elemental iron daily. This would sug-
groups (38% vs. 27%, p=0.38).
gest that the growth spurt and onset of menses prior to con-
ception in iron sufficient women does not give adequate iron
stores to prevent IDA without oral supplemental iron during
pregnancy.
Iron def iciency anemia in adolescent pregnancy
CM&R 2003 : 1 (January)
31

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The incidence of IDA in our study was higher in adolescent
times associated with taking iron may be similar to the symp-
than adult pregnancies. Although this was not statistically sig-
toms of normal pregnancies. Similarly, there was no dis-
nificant, the study had low power to detect an effect of this
cernible difference between supplemented and placebo
magnitude, and the difference was observed in both iron and
patients in maternal or newborn infant health status upon
placebo groups (see table 2). The incidence was also much
delivery despite the differences in iron status during pregnan-
higher than in two non-randomized studies of IDA in adoles-
cy (table 5).
cent pregnancy in other developed countries, where the inci-
dence varied from 1.5% in Chile to 14.2% in Brazil.7,37 In
There are many good reasons to strive to eliminate iron defi-
developing countries, additional higher risks for severe IDA
ciency in adolescents worldwide.43 However, our findings
in adolescent pregnancies include the young age at concep-
suggest that even if iron status is elevated to normal levels,
tion before the extra iron needs of maternal growth have been
there may still be need for iron supplementation selectively
met, anemias associated with infectious diseases such as
during pregnancy, if the goal is to maintain serum ferritin and
malaria, and hemoglobinopathies.38-42
hemoglobin levels within normal ranges. For mild to moder-
ate iron deficiency during pregnancy, the importance of this
As seen in other studies, iron supplementation decreased the
goal to maternal and neonatal health remains unclear.
incidence of IDA and enhanced iron status during
pregnancy.16,19 The daily regimen of supplementation result-
Whether or not routine iron supplementation is necessary in
ed in no apparent increase in acute side effects in either
adult pregnancies has been extensively reviewed. Aside from
group, although the number of women studied limited our
the benefits of feeling better and having fewer symptoms
ability to detect such effects, and the four symptoms some-
related to IDA, it is difficult to show benefit for pregnancy
outcome or improvement of the health of the mother or
Table 1. Patient characteristics at randomization by age group and treatment.
Iron
Placebo
N
Median
Range
N
Median
Range
Adolescents
Age (years)
20
18.2
15-18
17
17.7
15-18
Week of pregnancy
20
14.1
8-18
16
12.1
8-18
Serum ferritin (ng/mL)
19
31.1
13-93
17
34.0
9-151
Hemoglobin (g/dL)
20
12.6
11-14
17
13.1
11-14
Adults
Age (years)
38
25.2
18‡-35
36
28.8
21-39
Week of pregnancy
38
10.6
7-17
36
12.3
3-17
Serum ferritin (ng/mL)
38
39.3
6-182
35
37.0
9-163
Hemoglobin (g/dL)
38
13.0
11-15
36
12.9
11-17
‡ One adult patient was enrolled one month prior to her 19th birthday.
Table 2. Incidence of IDA in adolescent and adult pregnancies.
Iron deficiency anemia at test 2 or 3
Total Patients
Test 2
Test 3
Total
Percent
p-value‡
Adolescents
Iron
20
3
1
4
20
Placebo
17
5
5
10
59
0.021
Adults
Iron
38
1
4
5
13
Placebo
36
7
8
15
42
0.008
‡p-values compare iron to placebo in each group.
32
CM&R 2003 : 1 (January)
Meier, et al.

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Table 3. Follow-up results by age group and treatment.
Iron
Placebo
N
Median
Range
N
Median
Range
p-value
Adolescents
Serum ferritin (ng/mL)
24-28 wk
19
10.3
4-161
16
8.9
3-21
0.217
36-40 wk
15
12.0
5-71
15
6.2
2-13
0.010
Hemoglobin (g/dL)
24-28 wk
19
11.7
10-13
16
11.6
10-12
0.267
36-40 wk
15
12.2
11-14
16
11.5
10-14
0.024
Pill count adherence (%)‡
17
95.5
36-124
14
87.4
42-100
0.320
Adults
Serum ferritin (ng/mL)
24-28 wk
30
15.6
2-126
28
9.3
3-63
0.025
36-40 wk
33
12.9
4-141
26
7.6
3-37
0.027
Hemoglobin (g/dL)
24-28 wk
32
12.0
10-14
30
11.6
10-13
0.075
36-40 wk
33
12.1
11-14
28
11.7
10-14
0.135
Pill count adherence (%)‡
20
97.8
32-115
24
83.9
32-110
0.036
‡Percent adherence is defined as 100 (225 pill count) / (days on study).
Table 4. Incidence of side effects at any time in the pregnancy.
Adolescent
Adult
Nausea
Iron
53%
63%
Placebo
65%
53%
Vomiting
Iron
41%
35%
Placebo
41%
21%
Constipation
Iron
29%
24%
Placebo
12%
28%
Diarrhea
Iron
13%
14%
Placebo
17%
24%
No significant differences in iron vs. placebo or adolescents vs. adults.
fetus.44,45 However, in our study only 20% of adolescents and
Our study was not large enough to effectively evaluate the
13% of adults developed IDA if they were on 60 mg/day of
potential association of IDA with fetal morbidity and mortali-
elemental iron. Other research suggests that 65 mg of ele-
ty as suggested in some reports. Other studies have shown a
mental iron per day in the second trimester is sufficient to
larger than 2.5-fold increase in pre-term delivery with
prevent iron deficiency in adult pregnancies and may also
IDA.47-50 Severe anemia (hemoglobin <7 g/dL) occurred in
increase serum ferritins in the cord blood of the newborns.46
56% of pregnancies in one developing country, contributing
Iron def iciency anemia in adolescent pregnancy
CM&R 2003 : 1 (January)
33

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Table 5. Perinatal status of infants.
Iron deficiency anemia at test 2 or 3
Apgar scores of
Length
Gestational age
Birth weight
C-sections‡
Total
7 or less in 1
(cm)
(weeks)
(<2,500 g)
n (%)
n
minute n (%)
Mean ± SD
Mean ± SD
n (%)
Adolescents
Iron
20
6 (30.0)
50.0 ± 2.3
39.9 ± 1.3
0 (0)
4 (20.0)
Placebo
16
4 (25.0)
51.6 ± 1.7
39.8 ± 1.3
0 (0)
1 (6.2)
Adults
Iron
38
11 (29.7)
52.4 ± 2.5
39.2 ± 1.7
2 (5.4)
5 (14.3)
Placebo
36
6 (16.7)
51.8 ± 2.3
39.5 ± 1.9
1 (2.9)
9 (25.0)
‡Two elective repeat C-sections were not included, as they would not be related to adverse effects from pregnancy.
Figure 1. Mean serum ferritin levels (ng/mL) during pregnancy in the study groups.
*Indicates iron supplement and placebo groups differ significantly.
significantly to maternal death rates.51 Iron treated adult
the side effects often attributed to iron supplements are simi-
pregnancies have been associated with increased mean length
lar to those of normal pregnancy, it is hoped that increased
and Apgar scores.52 Prophylactic iron supplementation before
adherence in taking iron supplements will allow further suc-
and during pregnancy reportedly gives the best possible out-
cess in the treatment of IDA during pregnancy.
come for the mothers and children in developed and develop-
ing countries.53-57
ACKNOWLEDGMENTS
Our study indicates that 60 mg/day of elemental iron helps to
The authors wish to thank Marshfield Medical Research
prevent IDA in both adolescent and adult pregnancies.
Foundation for its support through the assistance of Alice
Furthermore, among 12 women who developed IDA during
Stargardt, Doreen Luepke and Graig Eldred, Ph.D. for their
the second trimester and received therapeutic supplementa-
assistance in the preparation of this manuscript.
tion with 180 mg of elemental iron daily, 9 of 12 (75%) had
resolved the IDA by the end of their pregnancies. Given that
34
CM&R 2003 : 1 (January)
Meier, et al.

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REFERENCES
29. Dallman PR. Changing iron needs from birth through adolescence. In:
Fomon SJ, Zlotkin S, editors. Nutritional Anemias. Nestle Nutrition
Workshop Series, Vol. 30, Nestec Ltd. New York, NY: Vevey/Raven
1. Abel R, Rajaratnam J, Kalaimani A, Kirubakaran S. Can iron status be
Press; 1992. p. 29-38.
improved in each of the three trimesters? A community-based study.
30. World Health Organization. Young people’s health – A challenge for soci-
Eur J Clin Nutr 2000;54: 490-493.
ety. WHO Technical Report Series, no. 731, Geneva, Switzerland:
2. Allen LH, Rosado JL, Casterline JE, Lopez P, Munoz E, Garcia OP,
WHO. 1986.
Martinez H. Lack of hemoglobin response to iron supplementation in
31. Huber AM, Wallins LL, DeRusso P. Folate nutriture in pregnancy. J Am
anemic Mexican preschoolers with multiple micronutrient deficien-
Diet Assoc 1988;88: 791-795.
cies. Am J Clin Nutr 2000;71: 1485-1494.
32. Nickerson HJ, Holubets M, Tripp AD, Pierce WE. Decreased iron stores
3. Baynes RD, Cook JD. Current issues in iron deficiency. Curr Opin
in high school female runners. Am J Dis Child 1985;139: 1115-1119.
Hematol 1996;3: 145-149.
33. Nickerson HJ, Holubets MC, Weiler BR, Haas RG, Schwartz S, Ellefson
4. Beard JL. Weekly iron intervention: the case for intermittent iron supple-
ME. Causes of iron deficiency in adolescent athletes. J Pediatr
mentation. Am J Clin Nutr 1998;68: 209-212.
1989;114: 657-663.
5. Brabin BJ, Hakimi M, Pelletier D. An analysis of anemia and pregnancy-
34. Fenton V, Cavill I, Fisher J. Iron stores in pregnancy. Br J Haematol
related maternal mortality. J Nutr 2001;131: 604S-614S.
1977;37: 145-149.
6. Dillon JC. Prevention of iron deficiency and iron deficiency anemia in
35. Cook JD, Finch CA. Assessing iron status of a population. Am J Clin
tropical areas. Med Trop (Mars) 2000;60: 83-91.
Nutr 1979;32: 2115-2119.
7. Fujimori E, de Oliveira IM, de Cassana LM, Szarfarc SC. Iron nutritional
36. Committee on Nutritional Status During Pregnancy and Lactation,
status in pregnant adolescents, Sao Paulo, Brazil. Arch Latinoam Nutr
Institute of Medicine. Nutrition during pregnancy: Part I: weight gain,
1999;49: 8-12.
Part II: nutrient supplements. Washington DC: National Academy
8. Gadowsky SL, Gale K, Wolfe SA, Jory J, Gibson R, O’Connor DL.
Press, 1990.
Biochemical folate, B12, and iron status of a group of pregnant ado-
37. Sloan NL, Jordan E, Winikoff B. Effects of iron supplementation on
lescents accessed through the public health system in southern
maternal hematologic status in pregnancy. Am J Public Health
Ontario. J Adolesc Health 1995;16: 465-474.
2002;92: 288-293.
9. Geissler PW, Shulman CE, Prince RJ, Mutemi W, Mnazi C, Friis H, Lowe
38. Menendez C, Todd J, Alonso PL, Francis N, Lulat S, Ceesay S, M’Boge
B. Geophagy, iron status and anemia among pregnant women on the
B, Greenwood BM. The effects of iron supplementation during preg-
coast of Kenya. Trans R Soc Trop Med Hyg 1998;92: 549-553.
nancy, given by traditional birth attendants, on the prevalence of
10. Milman N, Bergholt T, Eriksen L, Ahring K, Graudal NA. Iron require-
anaemia and malaria. Trans R Soc Trop Med Hyg 1994;88: 590-593.
ments and iron balance during pregnancy. Is iron supplementation
39. Pappagallo S, Bull DL. Operational problems of an iron supplementation
needed for pregnant women? Ugeskr Laeger 1997;159: 6057-6062.
programme for pregnant women: an assessment of UNRWA experi-
11. Milman N, Bergholt T, Byg KE, Eriksen L, Graudal N. Iron status and
ence. Bull World Health Organ 1996;74: 25-33.
iron balance during pregnancy. A critical reappraisal of iron supple-
40. Diejomaoh FM, Abdulaziz A, Adekile AD. Anemia in pregnancy. Int J
mentation. Acta Obstet Gynecol Scand 1999;78: 749-757.
Gynaecol Obstet 1999;65: 299-301.
12. Pita Martin de Portela ML, Langini SH, Fleischman S, et al. Effect of
41. Kapil U, Saxena N, Ramachandran S. Iron deficiency anemia in pregnan-
iron supplementation and its frequency during pregnancy. Medicina (B
cy. Indian Pediatr 1996;33: 606.
Aires) 1999;59: 430-436.
42. Fleming AF, Briggs ND, Rossiter CE. Growth during pregnancy in
13. Preziosi P, Prual A, Galan P, Daouda H, Boureima H, Hercberg S. Effect
Nigerian teenage primigravidae. Br J Obstet Gynaecol 1985;9: 32-39.
of iron supplementation on the iron status of pregnant women: conse-
43. Bruner AB, Joffe A, Duggan AK, Casella JF, Brandt J. Randomised study
quences for newborns. Am J Clin Nutr 1997;66: 1178-1182.
of cognitive effects of iron supplementation in non-anaemic iron-defi-
14. Quintas ME, Requejo AM, Ortega RM, Redondo MR, Lopez-Sobaler
cient adolescent girls. Lancet 1996;348: 992-996.
AM, Gaspar MJ. The female Spanish population: a group at risk of
44. Scholl TO, Hediger ML. Anemia and iron-deficiency anemia: compila-
nutritional iron deficiency. Int J Food Sci Nutr 1997;48: 271-279.
tion of data on pregnancy outcome. Am J Clin Nutr 1994;59: 492S-
15. Roodenburg AJ. Iron supplementation during pregnancy. Eur J Obstet
501S.
Gynecol Reprod Biol 1995;61: 65-71.
45. Routine iron supplementation during pregnancy. Review article. US
16. Zavaleta N, Respicio G, Garcia T. Efficacy and acceptability of two iron
Preventive Services Task Force. JAMA 1993;270: 2848-2854.
supplementation schedules in adolescent school girls in Lima, Peru. J
46. Milman N, Agger AO, Nielsen OJ. Iron status markers and serum ery-
Nutr 2000;130: 462S-464S.
thropoietin in 120 mothers and newborn infants. Effect of iron supple-
17. Allen LH. Anemia and iron deficiency: effects on pregnancy outcome.
mentation in normal pregnancy. Acta Obstet Gynecol Scand 1994;73:
Am J Clin Nutr 2000;71: 1280S-1284S.
200-204.
18. Beaufrere B, Bresson JL, Briend A, Farriaux JP, Ghisolfi J, Navarro J,
47. Scholl TO, Hediger ML, Fischer RL, Shearer JW. Anemia vs iron defi-
Rey J, Ricour C, Rieu D, Vidailhet M. Iron and pregnancy. Arch
ciency: increased risk of preterm delivery in a prospective study. Am J
Pediatr 1995;2: 1209-1218.
Clin Nutr 1992;55: 985-988.
19. Lynch SR. The potential impact of iron supplementation during adoles-
48. Rasmussen KM. Is there a causal relationship between iron deficiency or
cence on iron status in pregnancy. J Nutr 2000;130: 448S-451S.
iron-deficiency anemia and weight at birth, length of gestation and
20. Scholl TO, Reilly T. Anemia, iron and pregnancy outcome. J Nutr
perinatal mortality? J Nutr 2001;131: 590S-601S; discussion 601S-
2000;130: 443S-447S.
603S.
21. Schwartz WJ 3rd, Thurnau GR. Iron deficiency anemia in pregnancy.
49. MacGregor MW. Maternal anaemia as a factor in prematurity and perina-
Clin Obstet Gynecol 1995;38: 443-454.
tal mortality. Scot Med J 1963;8: 134-140.
22. Beard JL. Iron deficiency: assessment during pregnancy and its impor-
50. Brabin BJ, Hakimi M, Pelletier D. An analysis of anemia and pregnancy-
tance in pregnant adolescents. Am J Clin Nutr 1994;59: 502S-508S.
related maternal mortality. J Nutr 2001;131: 604S-615S; discussion
23. DeMaeyer EM, Dallman P, Gurney JM, Hallberg L, Sood SK, Srikantia
614S-615S.
SG. Preventing and controlling iron deficiency anaemia through pri-
51. Sarin AR. Severe anemia of pregnancy, recent experience. Int J Gynaecol
mary health care: a guide for health administrators and programme
Obstet 1995;50(suppl 2): S45-S49.
managers. Geneva, Switzerland: World Health Organization, 1989.
52. Preziosi P, Prual A, Galan P, Daouda H, Boureima H, Hercberg S. Effect
24. World Bank. World Development Report 1993. Investing in Health. New
of iron supplementation on the iron status of pregnant women: conse-
York: Oxford University Press, 1993.
quences for newborns. Am J Clin Nutr 1997;66: 1178-1182.
25. Ronsmans C, Achadi E, Sutratikto G, Zazri A, McDermott J. Use of hos-
53. Kurz KM, Galloway R. Improving adolescent iron status before child-
pital data for Safe Motherhood programmes in south Kalimantan,
bearing. J Nutr 2002;130: 437S-439S.
Indonesia. Trop Med Int Health 1999;4: 514-521.
54. Lynch SR. The potential impact of iron supplementation during adoles-
26. World Health Organization. Adolescent nutrition: a neglected dimension.
cence on iron status in pregnancy. J Nutr 2000;130(2S suppl): 448S-
http://www.who.int/nut/ado.htm (5/31/01).
451S.
27. Kurz KM, Galloway R. Improving adolescent iron status before child-
55. Milman N, Bergholt T, Byg KE, Eriksen L, Graudal N. Iron status and
bearing. J Nutr 2000;130: 437S-439S.
iron balance during pregnancy. A critical reappraisal of iron
28. Barrett JF, Whittaker PG, Williams JG, Lind T. Absorption of non-haem
supplementation. Acta Obstet Gynecol Scand 1999;78: 749-
iron from food during normal pregnancy. Br Med J 1994;309: 79-82.
757.
Iron def iciency anemia in adolescent pregnancy
35
CM&R 2003 : 1 (January)

---

56. Looker AC, Dallman PR, Carroll MD, Gunter EW, Johnson CL.
Prevalence of iron deficiency in the United States. JAMA 1997;277:
973-976.
57. Abel R, Rajaratnam J, Kalaimani A, Kirubakaran S. Can iron status be
improved in each of the three trimesters? A community-based study.
Eur J Clin Nutr 2000;54: 490-493.
36
CM&R 2003 : 1 (January)
Meier, et al.

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