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. Author manuscript; available in PMC: 2014 Jul 17.
Published in final edited form as: Matern Child Health J. 2012 Dec;16(9):1913–1925. doi: 10.1007/s10995-011-0938-y

Relationship of maternal knowledge of anemia with maternal and child anemia and health-related behaviors targeted at anemia among families in Indonesia

Ellie S Souganidis 1, Kai Sun 1, Saskia de Pee 2, Klaus Kraemer 3, Jee-Hyun Rah 3, Regina Moench-Pfanner 4, Mayang Sari 5, Martin W Bloem 2, Richard D Semba 1
PMCID: PMC4101891  NIHMSID: NIHMS496970  PMID: 22241619

Abstract

Objectives

Our specific aim was to characterize maternal knowledge of anemia and its relationship to maternal and child anemia and to behaviors related to anemia reduction.

Methods

We examined the relationship between maternal knowledge of anemia and anemia in the mother and the youngest child, aged 6–59 mo, in 7,913 families from urban slums and 37,874 families from rural areas of Indonesia. Knowledge of anemia was defined based upon the mother’s ability to correctly name at least one symptom of anemia and at least one treatment or strategy for reducing anemia. Hemoglobin was measured in both the mother and the child.

Results

In urban and rural areas, respectively, 35.8% and 36.9% of mothers had knowledge of anemia, 28.7% and 25.1% of mothers were anemic (hemoglobin <12 g/dL), and 62.3% and 54.0% of children were anemic (hemoglobin <11 g/dL). Maternal knowledge of anemia was associated with child anemia in urban and rural areas, respectively, (Odds Ratio [O.R.] 0.90, 95% Confidence Interval [C.I.] 0.79, 1.02, P = 0.10; O.R. 0.93, 95% C.I. 0.87, 0.98, P = 0.01) in multivariate logistic regression models adjusting for potential confounders. There was no significant association between maternal knowledge of anemia and maternal anemia. Maternal knowledge of anemia was significantly associated with iron supplementation during pregnancy and child consumption of fortified milk. There was no association of maternal knowledge of anemia with child deworming.

Conclusions

Maternal knowledge of anemia is associated with lower odds of anemia in children and with some health behaviors related to reducing anemia.

Keywords: anemia, children, knowledge, mothers, Indonesia

Introduction

Iron deficiency anemia is the leading cause of anemia worldwide, accounting for approximately 50% of the total prevalence (1,2). Iron deficiency can result in impaired cognition, decreased physical capacity, and reduced immunity as well as impaired psychomotor and cognitive development in children (3–5). Pregnant women are particularly at risk for iron deficiency anemia because of blood volume expansion during pregnancy (6) and the need to support the fetus and placenta (7). In women of childbearing age, blood loss due to childbirth or menses can also be a contributing factor to the development of iron deficiency anemia (8).

The increased risk of iron deficiency anemia during pregnancy has motivated government ministries in many developing countries to implement policies providing iron supplementation for pregnant and lactating women (9). In Indonesia, it is a government recommendation for women to receive iron supplements during pregnancy and the post-partum period (9). The most recently available national survey data from Indonesia indicate that the prevalence of anemia has declined in pregnant women and women of reproductive age to rates of 40% and 27.9%, respectively. However, the anemia prevalence in children aged 0–59 months has increased from 40% to 48.1%, with a prevalence rate of greater than 55% in children less than 24 months of age (10).

Despite the implementation of large-scale programs targeted towards pregnant women and women of reproductive age, the prevalence of anemia remains high (11). Factors that limit the success of iron supplementation include inadequate supply, delivery, and distribution systems, limited access to health care providers and prenatal care, ineffective social marketing, and overall poor monitoring and evaluation of supplementation programs (11–13). The knowledge and attitudes women hold regarding anemia may also play a role in the limited success of these programs. In a survey conducted in eight developing countries, anemia was more commonly recognized by its symptoms instead of by a disease name or clinical diagnosis (9). Only half of women considered these symptoms to be of concern, and many women who took iron supplements, primarily provided through prenatal care, did not understand the reason for treatment (9). Negative attitudes towards iron supplementation, derived from side effects, concerns with the tablet’s bad taste, or fears of adverse outcomes, could facilitate non-compliance, even if the benefits of iron supplementation are known.

Maternal knowledge of anemia is important because of its potential to encourage women to take iron supplements during pregnancy and after childbirth, affecting the iron status of both the mother and the child. In a small study in southern Israel, the presence of anemia in infants and level of maternal knowledge were inversely related, with low knowledge of anemia leading to a 12-fold increase in prevalence of anemia in infants compared to women with higher levels of knowledge (14).

Increased consumption of animal source foods is an additional health-related behavior that could be encouraged by maternal knowledge of anemia. Benefits of consuming animal source foods include dietary diversity, relatively higher bioavailable forms of micronutrients, and overall better maternal nutrition affecting both the mother and child during pregnancy and lactation (15–17).

Strategies to reduce the prevalence of anemia in children have focused on consumption of fortified milk by the child and administration of deworming medications. Consumption of fortified milk has already proven to be an effective strategy to reduce anemia in children and has been the basis for mandatory fortification of powdered milk with iron, vitamins, and other minerals in Indonesia in the mid-1990s (18). The use of deworming medications in endemic areas has also been shown to help improve iron status in children at high risk for anemia-related morbidity and mortality by reducing the chronic intestinal blood loss associated with hookworm and other parasitic infections (19). There is currently no nationwide deworming policy in Indonesia for children under the age of five. However, deworming medications are administered by small pilot projects in some areas or by parents who suspect that their child is infected.

Our specific aim was to characterize mother’s knowledge of anemia and its relationship to anemia in mothers and children and to behaviors related to the reduction of anemia. We hypothesized that women with greater knowledge of anemia would be less likely to be anemic themselves and to have anemic children. We also hypothesized that women with greater knowledge of anemia would be more likely to adopt behaviors aimed at reducing anemia, such as taking iron supplements during pregnancy, having their children consume fortified milk, having their children take deworming medication, and having higher consumption of animal-source foods in the household. To address these hypotheses, we examined the relationship between a mother’s knowledge of anemia with the prevalence of anemia in mothers and their children from rural areas and urban slums in Indonesia. We also examined the relationship between a mother’s knowledge of anemia and health behaviors that are known to reduce anemia.

Subjects and methods

The study subjects consisted of mothers and children from rural areas that participated in the Nutritional Surveillance System (NSS) in Indonesia from March 1999 to August 2003 and mothers and children from urban slum areas that participated in the NSS from January 1999 to July 2003. The present study was based upon a secondary data analysis of existing NSS data. The NSS was established by the Ministry of Health, Government of Indonesia, and Helen Keller International in 1995 (20). The nutritional surveillance system was based upon UNICEF’s conceptual framework on the causes of malnutrition (21) with the underlying principle to monitor public health problems and guide policy decisions (22). The NSS used stratified multistage cluster sampling of households in subdistricts of administrative divisions of the country in rural areas and slum areas of large cities. Data were collected from approximately 40,000 randomly selected households every quarter and involved five major urban poor populations from slum areas in the cities of Jakarta, Surabaya, Makassar, Semarang, and Padang, and the rural population from the provinces of Lampung, Banten, West Java, Central Java, East Java, the island of Lombok (West Nusatenggara), and South Sulawesi. The present study involved households during a period of the NSS in which specific questions were included regarding maternal knowledge of anemia. The analyses are derived from surveys that specifically contained information on anemia in the mother and child and information on maternal knowledge of anemia.

For each child in the family, data were collected on whether the child had consumed industrially produced milk products in the previous week, the commercial brand of the product, and how much money was spent on the milk product in the previous week. Data were also collected on whether the child received a deworming medication in the previous six months. Hemoglobin was measured in mothers and children in the family using a HemoCue© instrument (HemoCue AB, Angelholm, Sweden) and women were also asked whether they took iron supplementation during their last pregnancy.

In each household, data were gathered regarding the expenditures in the previous week. Expenditure and price variables were collected in Indonesian rupiah. For this analysis, expenditures are presented in US dollars using monthly exchange rates from 2000–2003 available through the Bank of Canada (23). Expenditure on food in this analysis was grouped into three categories: plant source foods (fruit, vegetables, and other plant sources), animal source foods (beef, chicken, poultry, fish, eggs, and milk), and grain source foods (rice and other non-processed staple foods).

The study protocol complied with the principles enunciated in the Helsinki Declaration (24). Written, informed consent was obtained from all participants. The nutritional surveillance system in Indonesia was approved by the Ministry of Health, Government of Indonesia. The plan for secondary data analysis was approved by the Institutional Review Board of the Johns Hopkins University School of Medicine.

The study was limited to children aged 6–59 months because the interpretation of low hemoglobin in children under the age of 6 months is difficult (25). For families with more than one child, aged 6–59 months, the analysis was limited to the youngest child only (i.e. families with more than one child were not counted more than once, since anemia tends to cluster within families). Anemia was defined as hemoglobin <11 g/dL in children and <12 g/dL in non-pregnant women according to World Health Organization criteria (1,26). Pregnant women were not included in the study.

Weekly per capita household expenditure was used as the main indicator of socioeconomic status. Crowding was defined as households where more than four individuals were eating from the same kitchen. Maternal smoking was not used in the analyses because the prevalence of maternal smoking in Indonesia was <0.7% (26). Paternal smoking was included in the analysis as it is known to divert precious household income from food to tobacco and exacerbate malnutrition among women and children (27, 28).

Mothers were asked “Have you ever heard about anemia?” and additional questions regarding anemia if they answered in the affirmative. Mothers were asked to name symptoms of anemia and how the symptoms ought to be addressed. Participants were scored as having knowledge of anemia if they mentioned one of the following symptoms: pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache. Mothers were also scored as knowing about anemia if they were able to provide one of the following treatments: take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker.

Chi-square tests were used to compare categorical variables between groups. Multivariate logistic regression models were used to examine the relationship between risk factors and anemia clustering. Variables were included in the multivariate models if significant in univariate analyses. P < 0.05 was considered significant. Covariance matrices were used to examine for multicollinearity among independent variables in the models. In multivariate models, maternal education but not paternal education was used because of high collinearity between maternal and paternal education. Data analyses were conducted using SAS Survey (SAS Institute, Cary, NC).

Results

The prevalence of anemia in mothers (hemoglobin <12 g/dL) and children (hemoglobin <11 g/dL) from urban slums and rural areas are displayed in Table 1. In urban slums, 28.7% of mothers and 62.3% of children were anemic whereas in rural areas, 25.1% of mothers and 54.0% of children were anemic. The prevalence of anemia in mothers and children from urban slums and rural areas in relation to demographic, socioeconomic, and health-related factors are shown in Tables 2 and 3, respectively. Of 7,913 mothers from urban slums, 35.8% had knowledge of anemia whereas 36.9% of 37,874 rural mothers had knowledge of anemia.

Table 1.

Sample demographics, socioeconomic, and health-related factors in mothers and children from urban slums and rural areas1

Characteristic2 URBAN RURAL
N % or Mean (SD) N % or Mean (SD)
Mother anemic Yes 2127 28.7 9066 25.1
No 5274 71.3 27006 74.9
Child anemic Yes 4922 62.3 20885 55.2
No 2982 37.7 16916 44.8
Mother heard about anemia Yes 6886 87.0 30823 81.4
No 1027 13.0 7051 18.6
Mother knows symptom of
anemia3 		Yes 3526 51.2 18754 60.8
No 3366 48.8 12097 39.2
Mother knows treatment of
anemia4 		Yes 5155 74.8 21163 68.6
No 1738 25.2 9674 31.4
Maternal age, y ≤24 2103 26.6 10874 28.7
25–28 1982 25.0 9247 24.4
29–32 1748 22.1 8246 21.8
33+ 2080 26.3 9487 25.1
Maternal education, y 0 357 4.5 1936 5.1
1–6 3530 44.7 19624 52.1
7–9 1917 24.3 8168 21.7
≥10 2090 26.5 7928 21.1
Paternal education, y 0 154 2.0 1409 3.9
1–6 2674 34.7 16791 46.7
7–9 1916 24.9 7198 20.0
≥10 2965 38.4 10585 29.4
Maternal body mass index
(kg/m2)		 18.5 to <25 4870 62.2 25912 68.8
<18.5 919 11.7 4595 12.2
≥25 to <30 1645 21.0 6117 16.2
≥30 398 5.1 1060 2.8
Number of children,
6–59 months of age		 1 6719 84.9 33277 87.9
2 1146 14.5 4451 11.7
3+ 48 0.6 146 0.4
Age of youngest child,
6–59 months of age		 6–11 1402 17.7 7157 18.9
12–23 2468 31.2 11824 31.2
24–35 1934 24.4 9245 24.0
36–47 1360 17.2 6074 16.5
48–59 749 9.5 3571 9.4
Sex of youngest child,
6–59 months of age		 Male 4127 52.2 19591 51.7
Female 3786 47.8 18283 48.3
Child consumes fortified
milk		 Yes 3496 48.2 13534 35.7
No 3755 51.8 24339 64.3
Father is a smoker Yes 5649 72.5 27437 73.9
No 2141 27.5 9712 26.1
Household has improved
latrine		 Yes 6586 83.3 18733 49.5
No 1319 16.7 19131 50.5
Mother took supplements
in last pregnancy		 Yes 1821 85.6 9642 84.2
No 307 14.4 1803 15.8
Weekly per capita
expenditure		 Grain source
food		 7905 .33
(.29)		 37816 .38
(.39)
Animal source
food		 7905 .35
(.32)		 37824 .28
(.30)
Plant source
food		 7904 .45
(.32)		 37805 .35
(.26)
Number of household
members eating from same
kitchen		 2–4 4297 54.4 20590 45.6
>4 3608 45.6 17232 54.4
Weekly per capita
household expenditure,
quintile		 1 795 10.0 6018 15.9
2 1004 12.7 6340 16.8
3 1345 17.0 7211 19.1
4 1847 23.4 8218 21.7
5 2914 36.9 10037 26.5
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1

Total of 7,401 mothers and 7,904 children from urban areas and 36,072 mothers and 37,801 children from rural areas.

2

Missing data for selected variables (urban/rural): maternal age (0/20), maternal education (19/218), paternal education (205/1891), maternal BMI (81/190), age of youngest child (0/3), child consumes fortified milk (662/1), father is a smoker (123/725), household has improved latrine (8/10), mother took supplements in last pregnancy (5785/26429), number of household members eating from same kitchen (8/52), weekly per capita household expenditure, quintile (8/50)

3

Mother can name one of the following symptoms: pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache

4

Mother can name one of the following treatments of anemia: take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker

Table 2.

Demographic, socioeconomic, and health-related factors associated with anemia in mothers from urban slums and rural areas

Characteristic URBAN RURAL
Mother anemic Mother not anemic P Mother anemic Mother not anemic P
N % or Mean
(SD)		 N % or Mean
(SD)		 N % or
Mean
(SD)		 N % or
Mean
(SD)
Mother
knows about
anemia1 		Yes 730 34.3 1924 36.5 0.08 3235 35.7 10111 37.4 0.003
No 1397 65.7 3350 63.5 5831 64.3 16895 62.6
Maternal age,
y		 ≤24 547 25.7 1401 26.6 0.005 2429 26.8 7954 29.5 <0.0001
25–28 504 23.7 1345 25.5 2094 23.1 6649 24.6
29–32 447 21.0 1182 22.4 1901 21.0 5912 21.9
33+ 629 29.6 1346 25.5 2636 29.1 6479 24.0
Maternal
education, y		 0 114 5.4 224 4.3 0.08 587 6.5 1263 4.7 <0.0001
1–6 968 45.6 2320 44.1 4880 54.2 13880 51.7
7–9 502 23.6 1282 24.4 1848 20.5 5926 22.1
≥10 541 25.5 1431 27.2 1691 18.8 5787 21.5
Paternal
education, y		 0 52 2.5 91 1.8 0.01 425 5.0 930 3.6 <0.0001
1–6 709 34.5 1781 34.6 4159 48.5 11883 46.3
7–9 550 26.8 1260 24.5 1659 19.3 5198 20.2
≥10 745 36.2 2018 39.2 2331 27.2 7679 29.9
Maternal
body mass
index (kg/m2)		 18.5 to <25 1353 64.0 3206 61.5 <0.0001 6413 71.0 18289 68.1 <0.0001
<18.5 309 14.6 576 11.0 1330 14.7 3145 11.7
≥25 to <30 361 17.1 1163 22.3 1132 12.5 4579 17.1
≥30 90 4.3 271 5.2 161 1.8 839 3.1
Number of
children, 6–59 months of
age		 1 1750 82.3 4515 85.6 0.0008 7689 84.8 24002 88.9 <0.0001
2 358 16.8 731 13.9 1323 14.6 2921 10.8
3+ 19 0.9 28 0.5 54 0.6 83 0.3
Age of
youngest
child, 6–59
months of
age		 6–11 439 20.6 926 17.6 0.004 1995 22.0 5048 18.7 <0.0001
12–23 625 29.4 1694 32.1 2921 32.2 8452 31.3
24–35 506 23.8 1281 24.3 2021 22.3 6681 24.7
36–47 345 16.2 916 17.4 1363 15.0 4301 15.9
48–59 212 10.0 457 8.7 765 8.4 2523 9.3
Sex of
youngest
child, 6–59
months of
age		 Male 1091 48.7 2771 47.5 0.33 4650 51.3 13987 51.8 0.41
Female 1036 51.3 2503 52.5 4416 48.7 13019 48.2
Child
consumes
fortified milk		 Yes 923 46.9 2329 48.4 0.26 2807 31.0 9940 36.8 <0.0001
No 1047 53.1 2486 51.6 6259 69.0 17065 63.2
Father is a
smoker		 Yes 1540 74.0 3723 71.5 0.03 6655 74.9 19484 73.6 0.01
No 540 26.0 1481 28.5 2225 25.1 7005 26.4
Household
has improved
latrine		 Yes 1729 81.3 4434 84.2 0.003 4192 46.3 13686 50.7 <0.0001
No 397 18.7 833 15.8 4871 53.7 13314 49.3
Mother took
iron
supplements
in last
pregnancy		 Yes 468 84.6 1246 86.0 0.4 2355 82.2 6785 85.2 0.003
No 85 15.4 202 14.0 508 17.8 1182 14.8
Weekly per
capita
expenditure		 Grain source food 2125 .32
(.27)		 5269 .33
(.29)		 0.17 9057 0.38
(.38)		 26963 0.38
(.39)		 0.53
Animal source food 2125 .35
(.30)		 5269 .36
(.33)		 0.17 9057 .26
(.28)		 26967 .29
(.30)		 <0.0001
Plant source food 2125 .42
(.29)		 5268 .47
(.33)		 <0.0001 9054 .32
(.24)		 26951 .36
(.26		 <0.0001
Number of
household
members
eating from
same kitchen		 2–4 1083 51.0 2316 44.0 <0.0001 5417 59.8 14227 52.8 <0.0001
>4 1042 49.0 2953 56.0 3639 40.2 12739 47.2
Weekly per
capita
household
expenditure,
quintile		 1 258 12.1 490 9.3 <0.0001 1700 18.8 4036 15.0 <0.0001
2 308 14.5 627 11.9 1683 18.6 4372 16.2
3 375 17.6 877 16.6 1770 19.5 5134 19.0
4 469 22.1 1268 24.1 1868 20.6 5976 22.2
5 715 33.6 2007 38.1 2036 22.5 7449 27.6
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1

Mother’s knowledge of anemia based upon the ability to name a symptom of anemia (pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache) and a treatment of anemia (take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker).

Table 3.

Demographic, socioeconomic, and health-related factors associated with anemia in children from urban slums and rural areas

Characteristic URBAN RURAL
Child anemic Child not anemic P Child anemic Child not anemic P
N % or
Mean
(SD)		 N % or
Mean
(SD)		 N % or
Mean
(SD)		 N % or
Mean
(SD)
Mother knows
about anemia1 		Yes 1745 35.5 1088 36.5 0.35 7692 36.8 6264 37.0 0.69
No 3177 64.5 1894 63.5 12193 63.2 10652 63.0
Maternal age,
y		 ≤24 1386 28.2 714 23.9 <0.0001 6518 31.2 4343 25.7 <0.0001
25–28 1217 24.7 762 25.6 5084 24.4 4135 24.5
29–32 1088 22.1 657 22.0 4432 21.2 3801 22.5
33+ 1231 25.0 849 28.5 4841 23.2 4627 27.4
Maternal
education, y		 0 224 4.6 132 4.4 <0.0001 1167 5.6 763 4.5 <0.0001
1–6 2309 47.0 1219 41.0 11118 53.5 8463 50.3
7–9 1191 24.3 722 24.3 4483 21.6 3669 21.8
≥10 1186 24.1 902 30.3 4000 19.3 3921 23.3
Paternal
education, y		 0 108 2.2 45 1.5 <0.0001 870 4.4 535 3.3 <0.0001
1–6 1752 36.6 918 31.6 9456 47.9 7290 45.1
7–9 1180 24.6 734 25.2 3951 20.0 3235 20.0
≥10 1752 36.6 1211 41.6 5466 27.7 5107 31.6
Maternal body
mass index
(kg/m2)		 18.5 to <25 3099 63.6 1764 59.8 <0.0001 14378 69.1 11482 68.3 <0.0001
<18.5 624 12.8 294 10.0 2864 13.8 1722 10.2
≥25 to <30 931 19.1 713 24.2 3080 14.8 3027 18.0
≥30 219 4.5 179 6.1 478 2.3 580 3.5
Number of
children, 6–59
months of age		 1 4056 82.4 2657 89.1 <0.0001 17834 85.4 15377 90.9 <0.0001
2 831 16.9 313 10.5 2942 14.1 1503 8.9
3+ 35 0.7 12 0.4 109 0.5 36 0.2
Age of
youngest child,
6–59 months of
age		 6–11 1057 21.5 343 11.5 <0.0001 5295 25.4 1845 10.9 <0.0001
12–23 1716 34.9 748 25.1 7720 37.0 4079 24.1
24–35 1149 23.3 782 26.2 4468 21.4 4762 28.2
36–47 684 13.9 676 22.7 2315 11.1 3748 22.2
48–59 316 6.4 433 14.5 1087 5.2 2479 14.7
Sex of
youngest child,
6–59 months of
age		 Male 2630 53.4 1493 50.1 0.004 11326 45.8 8224 48.6 <0.0001
Female 2292 46.6 1489 49.9 9559 54.2 8692 51.4
Child
consumes
fortified milk		 Yes 1989 43.9 1502 55.5 <0.0001 6479 31.0 7040 41.6 <0.0001
No 2545 56.1 1206 44.5 14405 69.0 9876 58.4
Child received
deworming		 Yes 995 20.2 702 23.6 0.0004 3313 15.90 3451 20.4 <0.0001
No 3925 79.8 2275 76.4 3451 84.1 13433 79.6
Father is a
smoker		 Yes 3582 73.8 2060 70.4 0.001 15359 74.9 12027 72.5 <0.0001
No 1272 26.2 867 29.6 5135 25.1 4556 27.5
Household has
improved
latrine		 Yes 4017 81.7 2561 85.9 <0.0001 9936 52.4 8761 51.8 <0.0001
No 899 18.3 419 14.1 10944 47.6 8150 48.2
Weekly per
capita
expenditure		 Grain
source
food		 4916 0.33
(0.28)		 2980 0.34
(0.31)		 0.21 20856 0.38
(0.38)		 16887 0.39
(0.40)		 0.02
Animal
source
food		 4916 0.35
(0.32)		 2980 0.37
(0.32)		 0.004 20859 0.27
(0.29)		 16892 0.29
(0.31)		 <0.0001
Plant
source
food		 4916 0.44
(0.31)		 2979 0.48
(0.33)		 <0.0001 20850 0.34
(0.25)		 16882 0.36
(0.27)		 <0.0001
Number of
household
members
eating from
same kitchen		 2–4 2287 46.5 1319 44.3 0.05 11521 55.2 9027 53.4 0.0005
>4 2629 53.5 1661 55.7 9335 44.8 7866 46.6
Weekly per
capita
household
expenditure,
quintile		 1 522 10.6 272 9.1 0.007 3687 17.7 2317 13.7 <0.0001
2 654 13.3 350 11.7 3641 17.5 2678 15.6
3 855 17.4 488 16.4 4046 19.4 3145 18.6
4 1125 22.9 720 24.2 4389 21.0 3819 22.6
5 1760 35.8 1150 38.6 5096 24.4 4933 29.2
Open in a new tab
1

Mother’s knowledge of anemia based upon the ability to name a symptom of anemia (pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache) and a treatment of anemia (take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker).

For both urban and rural mothers, factors that were associated with higher odds of anemia in the mother included older maternal age, lower paternal education, mother being underweight, greater number of children in the family, younger child age, paternal smoking, and more than four members sharing the same kitchen. Lower maternal education was also associated with higher odds of anemia in the mother in rural areas. For both urban and rural families, factors associated with lower odds of anemia in the mother included mother being overweight or obese, presence of an improved latrine in the household, greater consumption of plant source foods, and high quintile of per capita household expenditure. Maternal knowledge of anemia, consumption of fortified milk by the child, iron supplementation by the mother during her last pregnancy, and greater consumption of animal source foods were also associated with lower odds of anemia in the mother in rural areas.

For both urban and rural mothers, factors that were associated with a higher odds of anemia in the child included older maternal age, lower maternal and paternal education, mother being underweight, greater number of children in the family, younger child age, female gender of the child, paternal smoking, and more than four members sharing the same kitchen. Greater consumption of grain source foods was also associated with higher odds of anemia in the child in rural areas. For both urban and rural families, factors associated with a lower odds of anemia in the child included mother being overweight or obese, consumption of fortified milk by the child, deworming of the child, presence of an improved latrine in the household, greater consumption of plant source and animal source foods, and high quintile of per capita household expenditure.

Separate multivariate logistic regression models were used to examine the relationship between maternal knowledge of anemia and anemia in the mother in both rural and urban environments (Table 4). In the final multivariate logistic regression models, maternal knowledge of anemia was not significantly associated with anemia in the mother in either rural or urban areas, when adjusting for other covariates. Factors associated with higher odds of anemia in mothers from rural areas and urban slums in the multivariate models included mother being underweight, greater number of children in the family, and more than four individuals eating from the same kitchen. Older maternal age was also associated with higher odds of anemia in the mother in rural areas. Factors associated with lower odds of anemia in mothers from rural areas and urban slums included mother being overweight or obese and older child age. Higher maternal education and consumption of fortified milk by the child were also associated with lower odds of anemia in mothers from rural areas. Increased consumption of plant source foods was associated with lower odds of anemia in mothers from urban areas.

Table 4.

Multivariate model describing the odds of anemia associated with maternal knowledge of anemia and other potential risk factors in mothers from urban slums and rural areas

Characteristics Urban Rural
O.R 95% C.I P O.R 95% C.I P
Mother knows about anemia1 0.90 0.78, 1.02 0.10 0.96 0.90, 1.03 0.24
Maternal
age, y		 ≤24 1.00 --- --- 1.00 --- ---
25–28 0.94 0.79, 1.12 0.51 1.08 0.99, 1.18 0.09
29–32 0.93 0.77, 1.12 0.44 1.11 1.01, 1.21 0.03
33+ 1.12 0.93, 1.35 0.24 1.47 1.34, 1.61 <0.0001
Maternal
education, y		 0 1.00 --- --- 1.00 --- ---
1–6 0.87 0.64, 1.18 0.36 0.91 0.78, 1.06 0.21
7–9 0.90 0.65, 1.24 0.50 0.86 0.73, 1.01 0.07
≥ 10 0.86 0.62, 1.19 0.36 0.84 0.71, 0.99 0.04
Maternal
body mass
index
(kg/m2)		 18.5 to <25 1.00 --- --- 1.00 --- ---
<18.5 1.43 1.18, 1.73 0.0003 1.24 1.13,1.36 <0.0001
≥25 to <30 0.75 0.64, 0.89 0.0008 0.75 0.68, 0.82 <0.0001
≥30 0.86 0.64, 1.16 0.32 0.57 0.46, 0.70 <0.0001
Number of
children, 6–59
months of
age		 1 1.00 --- -- 1.00 --- ---
2 1.22 1.01, 1.47 0.04 1.27 1.15, 1.40 <0.0001
3+ 1.60 0.70, 3.68 0.27 2.03 1.27, 3.23 0.003
Age of
youngest
child, 6–59
months of
age		 6–11 1.00 --- --- 1.00 --- ---
12–23 0.74 0.62, 0.88 0.001 0.87 0.80, 0.95 0.002
24–35 0.90 0.74, 1.09 0.30 0.79 0.72, 0.87 <0.0001
36–47 0.86 0.69, 1.06 0.16 0.86 0.77, 0.96 0.008
48–59 1.06 0.82, 1.37 0.66 0.81 0.71, 0.92 0.001
Child consumes fortified
milk		 1.01 0.89, 1.15 0.90 0.88 0.82, 0.94 0.0004
Father is a smoker 1.04 0.90, 1.20 0.57 1.01 0.94, 1.09 0.81
Household has improved
latrine		 0.86 0.73, 1.01 0.07 0.96 0.89, 1.02 0.21
Weekly per capita animal
source food expenditure		 0.90 0.72, 1.12 0.34 0.93 0.82, 1.06 0.30
Weekly per capita plant
source food expenditure		 0.65 0.51, 0.82 0.0004 0.86 0.72, 1.01 0.06
More than 4 individuals
eating from same kitchen		 1.17 1.01, 1.36 0.03 1.21 1.12, 1.29 <0.0001
Weekly per
capita household
expenditure,
quintile		 1 1.00 --- --- 1.00 --- ---
2 0.95 0.73, 1.24 0.70 1.04 0.93, 1.16 0.52
3 0.97 0.75, 1.26 0.82 1.03 0.92, 1.15 0.62
4 0.88 0.68, 1.14 0.34 1.00 0.89, 1.13 0.98
5 0.93 0.71, 1.21 0.56 0.97 0.85, 1.11 0.68
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1

Mother’s knowledge of anemia based upon the ability to name a symptom of anemia (pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache) and a treatment of anemia (take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker).

Similarly, separate multivariate logistic regression models were used to examine the relationship between maternal knowledge of anemia and anemia in the child in urban and rural settings (Table 5). In the final multivariate model, maternal knowledge of anemia was significantly associated with lower odds of anemia in the child in families from rural areas (P=0.01) but not in children from urban slums (P = 0.10). Factors associated with higher odds of anemia in the child in both rural and urban environments included greater number of children in the family and children who were female. Older maternal age and maternal underweight were also associated with higher odds of anemia in the child in rural areas. Factors associated with lower odds of anemia in the child from rural areas and urban slums included older child age and consumption of fortified milk by the child. Higher maternal education and mother being obese were also associated with lower odds of anemia in children from rural areas. Mother being overweight and households with an improved latrine were associated with lower odds of anemia in children from urban areas.

Table 5.

Multivariate model describing the odds of anemia in children from urban slums and rural areas in association with maternal knowledge of anemia and other potential risk factors

Characteristics Urban Rural
O.R 95% C.I P O.R 95% C.I P
Mother knows about anemia1 0.90 0.79, 1.02 0.10 0.93 0.87, 0.98 0.01
Maternal age, y ≤24 1.00 --- --- 1.00 --- ---
25–28 0.96 0.82, 1.12 0.60 0.96 0.89, 1.04 0.31
29–32 1.04 0.88, 1.24 0.63 0.99 0.91, 1.07 0.79
33+ 0.87 0.73, 1.04 0.13 0.89 0.82, 0.96 0.004
Maternal
education, y		 0 1.00 --- --- 1.00 --- ---
1–6 1.08 0.80, 1.45 0.63 0.90 0.78, 1.04 0.14
7–9 0.87 0.64, 1.18 0.37 0.85 0.72, 0.99 0.03
≥ 10 0.74 0.55, 1.02 0.06 0.76 0.64, 0.89 0.0006
Maternal body
mass index
(kg/m2)		 18.5 to <25 1.00 --- --- 1.00 --- ---
<18.5 1.07 0.88, 1.29 0.51 1.23 1.12, 1.34 <0.0001
≥25 to <30 0.77 0.67, 0.89 0.0003 1.00 0.93, 1.08 0.96
≥30 0.82 0.64, 1.07 0.14 0.82 0.70, 0.96 0.01
Number of
children, 6–59
months of age		 1 1.00 --- --- 1.00 --- --
2 1.46 1.21, 1.76 <0.0001 1.24 1.13, 1.36 <0.0001
3+ 0.99 0.40, 2.45 0.98 1.30 0.78, 2.14 0.31
Age of youngest
child, 6–59 months
of age		 6–11 1.00 --- --- 1.00 --- ---
12–23 0.79 0.66, 0.94 0.009 0.71 0.65, 0.77 <0.0001
24–35 0.57 0.47, 0.69 <0.0001 0.37 0.34, 0.40 <0.0001
36–47 0.38 0.31, 0.47 <0.0001 0.25 0.22, 0.27 <0.0001
48–59 0.29 0.23, 0.37 <0.0001 0.17 0.15, 0.19 <0.0001
Sex of youngest
child, 6–59 months
of age		 Male 1.00 --- --- 1.00 --- ---
Female 1.19 1.06, 1.33 0.003 1.27 1.21, 1.35 <0.0001
Child consumes fortified milk 0.68 0.60, 0.76 <0.0001 0.76 0.72, 0.81 <0.0001
Father is a smoker 1.03 0.91, 1.17 0.63 1.02 0.96, 1.09 0.49
Household has improved
latrine		 0.79 0.67, 0.93 0.004 0.96 0.90, 1.02 0.19
Weekly per capita animal food
expenditure		 0.91 0.75, 1.11 0.34 0.95 0.85, 1.06 0.35
Weekly per capita plant food
expenditure		 0.81 0.65, 1.01 0.06 0.93 0.82, 1.07 0.31
More than 4 individuals eating
from same kitchen		 0.98 0.85, 1.12 0.76 1.04 0.98, 1.11 0.21
Weekly per capita
household
expenditure,
quintile		 1 1.00 --- --- 1.00 --- ---
2 1.00 0.77, 1.39 0.98 0.98 0.88, 1.09 0.71
3 1.14 0.89, 1.46 0.30 1.10 0.99, 1.22 0.08
4 1.07 0.84, 1.37 0.59 1.05 0.95, 1.17 0.34
5 1.10 0.85, 1.42 0.48 1.07 0.95, 1.17 0.24
Open in a new tab
1

Mother’s knowledge of anemia based upon the ability to name a symptom of anemia (pale face, weakness/fatigue, pale eyes, pale arm/nail, or headache) and a treatment of anemia (take iron tablet/capsule/vitamin, consume iron-fortified foods, or visit a doctor/midwife/other health worker).

We examined the relationship between maternal knowledge of anemia and four behaviors related to reducing the risk of anemia: iron supplementation during pregnancy, consumption of fortified milk by the child, deworming of the child, and higher consumption of animal source foods. In urban slums, 85.7% of mothers used iron supplementation during pregnancy, 21.5% of children received deworming medication, and 47.9% of children consumed fortified milk. In rural areas, 84.0% of mothers took iron supplementation during pregnancy, 17.9% of children received deworming medication, and 35.3% of children consumed fortified milk. Separate multivariate logistic regression models were used to examine the relationship of maternal knowledge of anemia to maternal iron supplementation, deworming, child consumption of fortified milk, and consumption of animal source foods in families from urban slums and rural areas (Table 6). In both urban and rural areas, maternal knowledge of anemia was associated with higher odds of consumption of fortified milk by the child and iron supplementation during the mother’s last pregnancy. Maternal knowledge of anemia was also associated with higher odds of per capita consumption of animal source foods by families in rural areas.

Table 6.

Multivariate logistic regression models describing the relationship of maternal knowledge of anemia with health-related behaviors targeted at anemia.1

Health-related behavior Urban Rural
O.R 95% C.I P O.R 95% C.I P
Mother took iron supplementation
in last pregnancy		 1.65 1.16, 2.35 0.005 1.41 1.20, 1.65 <0.0001
Child consumes fortified milk 1.20 1.07, 1.35 0.002 1.21 1.13, 1.28 <0.0001
Child received deworming
medication		 1.02 0.88, 1.17 0.82 1.03 0.96, 1.11 0.41
Consumption of animal source
foods		 1.07 0.94, 1.21 0.31 1.13 1.06, 1.22 0.0004
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1

All models adjusted for maternal age, maternal education, child age, child sex, number of household members eating from same kitchen, weekly per capita household expenditure, and province.

Discussion

The present study shows that maternal knowledge of anemia is not protective against anemia in the mother herself but was found to be protective against anemia in the child in rural families and of borderline significance in urban families. There are other factors in addition to maternal knowledge that may play an important role in anemia among mothers and children. For example, the study also showed an association between the consumption of fortified milk and availability of improved latrines with anemia. This study also shows that maternal knowledge of anemia was associated with the consumption of fortified milk by the child and iron supplementation during the mother’s last pregnancy in rural and urban families, but not with the use of deworming medication in the child. Maternal knowledge of anemia was also significantly associated with consumption of animal source foods in rural families but not in urban families.

To our knowledge, this is the first population-based study to address the relationship between maternal knowledge of anemia and anemia in the mother. The lack of a protective effect of maternal knowledge of anemia may suggest that although women may understand the consequences of anemia on their health, they may not have the means to effectively reduce their risk for developing anemia. Although there were multiple risk factors associated with higher odds of anemia in the mother, weight was the only variable that could be more directly controlled by the mother.

Maternal knowledge of anemia was associated with the use of iron supplements during pregnancy in both urban and rural areas. In the present study, 85.7% of mothers in urban slums and 84.0% of mothers from rural areas used iron supplementation during their last pregnancy. As previously described, barriers to iron supplementation can have a marked effect on adherence, warranting new efforts to develop more accessible and well-accepted supplementation programs. The use of sprinkles of microencapsulated ferrous fumarate was examined in a controlled trial in Ghanaian children as a potential method to increase adherence by reducing unpleasant side effects associated with ferrous sulfate drops (29). Additional follow-up studies suggested that the sprinkles were as equally efficacious as traditional iron supplementation (30). However, there are similar challenges regarding distribution of the sprinkles, suggesting the need for large-scale distribution programs, more effective health policy, and stronger social marketing strategies. Information, education and communication (IEC) programs have also been developed in an effort to improve the effectiveness of iron supplementation and have been implemented in Indonesia (31,32).

Consumption of fortified milk by the child was also protective against anemia in the child in both rural and urban areas and was significantly associated with maternal knowledge of anemia. These results are consistent with previous interventional studies showing a decrease in the prevalence of anemia in children who consume fortified milk (33,34). Increased efforts to distribute fortified milk could be accomplished by reinforcing its effectiveness through IEC programs or through other forms of social marketing. Efforts could also be made to increase the bioavailability of iron in fortified milk. In the past, ascorbic acid at concentrations between 100–800 mg/l was shown to enhance the effectiveness of iron absorption in fortified milk (35). Similar advancements could allow for children to benefit from fortified-milk even if they are only able to consume a smaller volume or are less compliant.

Maternal knowledge of anemia was significantly associated with consumption of animal source foods in rural areas. However, resource-poor settings make increased consumption of animal source foods a difficult strategy to implement. Household food-processing and preparation methods such as thermal processing, mechanical processing, soaking, fermentation, and germination/malting have been shown to enhance the bioavailability of micronutrients in plant source foods (36). Therefore, a diet consisting of modified plant source foods combined with a small portion of animal source foods could be an effective strategy to improve micronutrient bioavailability and dietary diversity (37).

In rural areas, maternal knowledge of anemia was protective against anemia in children. These findings are consistent with results from a study in Southern Israel, which found an inverse relationship between maternal knowledge of anemia and the presence of anemia in the child (14). Maternal knowledge of anemia and its associated health risks in children also motivated women to tolerate negative side effects associated with iron supplements (9). This further supports the value of maternal knowledge of anemia and suggests that there could be a variety of ways a mother’s knowledge could impact a child’s serum iron status.

The strengths of the present study include the large sample size, the population-based sampling, the general corroboration of findings between families from rural areas and urban slums, and the availability of detailed health surveillance data from each family. The limitations of the study are the cross-sectional design, which limits causal interference. As with any epidemiological study, it is not possible to measure all factors that may influence a mother’s knowledge of anemia or the prevalence of anemia in mothers and their children, and there may be unmeasured confounding factors. In the future, a controlled intervention study of improving maternal knowledge of anemia might yield the strongest evidence for a putative effect of maternal knowledge of anemia on both maternal and child anemia. The wording of the survey may also have been a limitation of the study because knowledge of anemia was only assessed in mothers who claimed to have previously heard of anemia; this suggests that some mothers were never asked about their knowledge of anemia even though it may have been relevant. Furthermore, the survey did not address the mothers’ access to health care in general and specifically for screening and treatment of anemia or the availability of services in the nearest primary health care center to each household. Finally, the findings from this study cannot necessarily be extrapolated to other settings in developing countries, as the present study was conducted in areas that were not endemic for malaria, except for one small area of Lombok.

The apparent protective effect of maternal knowledge of anemia on the prevalence of anemia in the child suggests that further insight is needed into whether increased education of mothers regarding anemia will reduce anemia in the child. The Indramayu Project, a social marketing campaign previously conducted in two sub-districts of Central Java, was aimed at improving the availability of iron supplements, conducting monthly health days, and promoting iron supplementation during pregnancy through maternal education (38). A significant increase in the average number of tablets taken during pregnancy was observed following the two-year campaign, suggesting that educational and social marketing techniques such as posters, leaflets, counseling cards, and local radio broadcasts may have played a role in improving iron supplementation rates (38).

The significant association of maternal knowledge of anemia with both consumption of fortified milk by the child and consumption of animal source foods by the mother also suggest two important focus areas for treatment and prevention of anemia. Further research is needed to determine whether there are other health-related behaviors targeted at anemia that are associated with maternal knowledge of anemia and whether these behaviors are effective strategies that can influence the prevalence of anemia in the population at large.

Acknowledgements

The present paper was supported by a writing workshop at Kappel-am-Albis, Switzerland, funded by Sight and Life, the humanitarian initiative of DSM. R.D.S. was funded in part by a Lew Wasserman Merit Award from Research to Prevent Blindness. E.S.S. was supported in part by the Scholarly Concentration Program of the Johns Hopkins University School of Medicine and an internship with the World Health Organization Reduction of Micronutrient Malnutrition Unit in Geneva, Switzerland.

References

  • 1.Benoist B, McLean E, Egli I, Cogswell , editors. Worldwide Prevalence of Anaemia. 1993–2005. Geneva, Switzerland: World Health Organization; 2008. Available at: whqlibdoc.who.int/publications/2008/9789241596657_eng.pdf. [Google Scholar]
  • 2.World Health Organization. Iron deficiency anaemia: assessment, prevention, and control. A guide for programme managers. Geneva: World Health Organization; 2001. WHO/NHD/01.3. [Google Scholar]
  • 3.UNICEF/UNU/WHO/MI. UNICEF/UNU/WHO/MI technical workshop. Boston and Ottawa: International Nutrition Foundation and The Micronutrient Initiative, 1998; 1998. Oct 7–9, Preventing iron deficiency in women and children. Technical consensus on key issues. [Google Scholar]
  • 4.Walter T, Kovalskys J, Stekel A. Effect of mild iron deficiency on infant mental development scores. J Pediatr. 1983;102:519–522. doi: 10.1016/s0022-3476(83)80177-2. [DOI] [PubMed] [Google Scholar]
  • 5.Walter T, De Andraca I, Chadud P, Perales CG. Iron deficiency anemia: adverse effects on infant psychomotor development. Pediatrics. 1989;84:7–17. [PubMed] [Google Scholar]
  • 6.Dallman PR. Tissue effects of iron deficiency. In: Jacobs A, Worwood M, editors. Iron in biochemistry and medicine. London: Academic Press; 1974. [Google Scholar]
  • 7.Allen LH. Pregnancy and iron deficiency: unresolved issues. Nutr Rev. 1997;55:91–101. doi: 10.1111/j.1753-4887.1997.tb06460.x. [DOI] [PubMed] [Google Scholar]
  • 8.Bothwell TH, Charlton RW, Cook JD, et al. Iron metabolism in man. Oxford, UK: Blackwell Scientific; 1979. [Google Scholar]
  • 9.Galloway R, Dusch E, Elder L, et al. Women’s perceptions of iron deficiency and anemia prevention and control in eight developing countries. Soc Sci Med. 2002;55:529–544. doi: 10.1016/s0277-9536(01)00185-x. [DOI] [PubMed] [Google Scholar]
  • 10.Atmarita. "Nutrition problems in Indonesia," An Integrated and International Seminar and Workshop on Lifestyle. Yogyakarta: Gadja Mada University; 2005. [Google Scholar]
  • 11.Gillespie S, Kevany J, Mason J. United Nations Administrative Committee on Coordination/Sub-Committee on Nutrition, State-of-the-Art Series Nutrition Policy Discussion Paper 9. Geneva: World Health Organization; Controlling iron deficiency. [Google Scholar]
  • 12.Galloway R, McGuire J. Determinants of compliance with iron supplementation: supplies, side effects, or psychology? Soc Sci Med. 1994;39:381–390. doi: 10.1016/0277-9536(94)90135-x. [DOI] [PubMed] [Google Scholar]
  • 13.Yip R. Iron supplementation during pregnancy: Is it effective? Am J Clin Nutr. 1996;63:853–855. doi: 10.1093/ajcn/63.6.853. [DOI] [PubMed] [Google Scholar]
  • 14.Bilenko N, Yehiel M, Inbar Y, et al. The association between anemia in infants, and maternal knowledge and adherence to iron supplementation in southern Israel. Isr Med Assoc J. 2007;9:521–524. [PubMed] [Google Scholar]
  • 15.Neumann CG, Harris DM, Rogers LM. Contribution of animal source foods in improving diet quality and function in children in the developing world. Nutr Res. 2002;22:193–220. [Google Scholar]
  • 16.Neumann CG, Bwibo NO, Sigman M. Kenya Project Final Report Phase II –1989–1992. University of California, Los Angeles: Human Nutrition Collaborative Research Support Program, USAID; 1992. Diet quantity and quality: Functional effects on rural Kenyan families. [Google Scholar]
  • 17.Neumann CG, Harrison G. Onset and evolution of stunting in infants and children. Examples from the Human Nutrition Collaborative Research Support Program, Kenya and Egypt studies. Eur J Clin Nutr. 1994;48:S90–S102. [PubMed] [Google Scholar]
  • 18.Semba RD, Moench-Pfanner R, Sun K, et al. Iron-fortified milk and noodle consumption is associated with lower risk of anemia among children aged 6–59 mo in Indonesia. Am J Clin Nutr. 2010;92:170–176. doi: 10.3945/ajcn.2010.29254. [DOI] [PubMed] [Google Scholar]
  • 19.Stolzfus R, Albonico M, Chwaya HM, et al. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr. 1998;68:179–186. doi: 10.1093/ajcn/68.1.179. [DOI] [PubMed] [Google Scholar]
  • 20.Bloem MW, Moench-Pfanner R, Panagides D, editors. Health & Nutritional Surveillance for Development. Singapore: Helen Keller Worldwide; 2003. [Google Scholar]
  • 21.United Nations Children’s Fund (UNICEF) The State of the World’s Children 2010: Celebrating 20 Years of the Convention on the Rights of the Child. New York: UNICEF; 2009. [Google Scholar]
  • 22.de Pee S, Bloem MW. Assessing and communicating impact of nutrition and health programs. In: Semba RD, Bloem MW, editors. Nutrition and Health in Developing Countries. Totowa, NJ: Humana Press; 2001. pp. 483–506. [Google Scholar]
  • 23.Bank of Canada. [Accessed December 18, 2005];Exchange rates: monthly average rates: 10-year look-up. Available at: http://www.bankofcanada.ca/en/rates/exchange-avg.html.
  • 24.World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. Bull World Health Organ. 2001;79:373–374. [PMC free article] [PubMed] [Google Scholar]
  • 25.de Pee S, Bloem MW, Sari M, Kiess L, Yip R, Kosen S. High prevalence of low hemoglobin concentration among Indonesian infants aged 3–5 months is related to maternal anemia. J Nutr. 2002;132:2115–2221. doi: 10.1093/jn/132.8.2215. [DOI] [PubMed] [Google Scholar]
  • 26.World Health Organization. Nutritional anemia: report of a WHO Scientific Group. Geneva: World Health Organization; 1968. [Google Scholar]
  • 27.Semba RD, Campbell AA, Sun K, et al. Paternal smoking is associated with greater food insecurity among poor families in rural Indonesia. Asia Pac J Clin Nutr. 2001;20:618–623. [PubMed] [Google Scholar]
  • 28.Best CM, Sun K, de Pee, et al. Paternal smoking and increased risk of child malnutrition among families in rural Indonesia. Tob Control. 2008;17:38–45. doi: 10.1136/tc.2007.020875. [DOI] [PubMed] [Google Scholar]
  • 29.Zlotkin S, Arthur P, Antwi KY, et al. Treatment of anemia with microencapsulated ferrous fumarate plus ascorbic acid supplied as sprinkles to complementary (weaning) foods. Am J Clin Nutr. 2001;74:791–795. doi: 10.1093/ajcn/74.6.791. [DOI] [PubMed] [Google Scholar]
  • 30.Zlotkin S, Schauer C, Christofides A, et al. Micronutrient sprinkles to control childhood anemia. PLoS Medicine. 2005;2:24–28. doi: 10.1371/journal.pmed.0020001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Kodyat B, Kosen S, de Pee S. Iron deficiency in Indonesia: current situation and intervention. Nutr Res. 1998;18:1953–1963. [Google Scholar]
  • 32.Mora J. Iron supplementation: overcoming technical and practical barriers. J Nutr. 2002;132:853–855. doi: 10.1093/jn/132.4.853S. [DOI] [PubMed] [Google Scholar]
  • 33.Olivares M, Walter T, Hertrampf E, Pizarro F, Stekel A. Prevention of iron deficiency by milk fortification. The Chilean experience. Acta Paediatr Scand Suppl. 1989;361:109–113. doi: 10.1111/apa.1989.78.s361.109. [DOI] [PubMed] [Google Scholar]
  • 34.Torrejón CS, Castillo-Durán C, Hertrampf ED, Ruz M. Zinc and iron nutrition in Chilean children fed fortified milk provided by the Complementary National Food Program. Nutrition. 2004;20:177–180. doi: 10.1016/j.nut.2003.10.013. [DOI] [PubMed] [Google Scholar]
  • 35.Stekel A, Olivares M, Pizarro F, et al. Absorption of fortification iron from milk formulas in infants. Am J Clin Nutr. 1986;43:917–922. doi: 10.1093/ajcn/43.6.917. [DOI] [PubMed] [Google Scholar]
  • 36.Hotz C, Gibson R. Traditional food-processing and preparation practices to enhance bioavailability of micronutrients in plant-based diets. J Nutr. 2007;137:1097–1110. doi: 10.1093/jn/137.4.1097. [DOI] [PubMed] [Google Scholar]
  • 37.Gibson RS, Yeudall F, Drost N, et al. Experiences of a community-based dietary intervention to enhance micronutrient adequacy of diets low in animal source foods and high in phytate: a case study in rural Malawian children. J Nutr. 2003;133(Suppl 2):3992S–3999S. doi: 10.1093/jn/133.11.3992S. [DOI] [PubMed] [Google Scholar]
  • 38.The World Bank. [Accessed 12/15/2011];Appendix A. Examples of Nutrition CBC Projects that had Measurable Impact. [ http://web.worldbank.org/WBSITE/EXTERNAL/TOPICS/EXTHEALTHNUTRITIONANDPOPULATION/EXTNUTRITION/0,,contentMDK:20205536~menuPK:282580~pagePK:148956~piPK:216618~theSitePK:282575,00.html]

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