Iron supplementation among pregnant women: results from a population-based survey study

Juraci Almeida Cesar Samuel de Carvalho Dumith Maria Aurora Dropa Chrestani Raul Andrés Mendoza-Sassi About the authors

Abstracts

Objectives:

To measure the prevalence and risk factors associated with iron supplementation among pregnant women in the municipality of Rio Grande, Southern Brazil.

Methods:

All mothers living in this municipality who had children in 2007 were surveyed for demographic, socioeconomic and health care received during pregnancy and childbirth. The statistical analysis consisted of Poisson regression with robust adjustment of variance, and the measure of effect was prevalence ratio (PR).

Results:

Among the 2,557 mothers interviewed (99% of total), 59% were supplemented with iron during pregnancy period. After adjusting for various confounding factors, a higher PR to iron supplementation was observed among teenagers, women with black skin color, primigravidae, who had six or more antenatal visits, who performed prenatal care in public sector and received vitamin during pregnancy.

Conclusion:

There is a clear need to increase the iron supplementation coverage of all pregnant women, especially among those currently considered with low gestational risk.

Iron supplementation; Ferrous sulfate; Prenatal care; Anemia; Pregnancy; Pregnant women


Introduction

Iron deficiency is a major cause of anemia during pregnancy, which is characterized by serum hemoglobin concentrations below 11 g/dL11. Stoltzfus RJ, Dreyfuss ML. International Nutritional Anemia Consultative Group (INACG), World Health Organization (WHO), United Nations Childrens Fund (UNICEF). Guidelines for the use of iron supplements to prevent and treat iron deficiency anemia. Washington: ILSI Press. 1988.. According to the World Health Organization (WHO), it affects at least 4 of every 10 pregnant women and is the underlying cause of approximately 115,000 maternal deaths annually in poor countries22. Benoist B, Mc Lean E, Cogswell M. World Health Organization. Worldwide Prevalence of Anaemia 1993-2005: WHO Global Database on Anaemia. Switzerland: WHO Press; 2008.. In newborns, maternal anemia can result in prematurity and intrauterine growth restriction33. Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008; 62(2): 120-4.

4. Peña-Rosa JP, Viteri FE. Effects and safety of preventive oral iron or iron+folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev 2009; (4): CD004736.
- 55. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20.. The most effective way to correct anemia is through supplementation with ferrous sulfate and an appropriate diet that includes foods rich in iron55. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20.

6. Buttha Z, Ahmed T, Black RE, Cousens S, Dewey K, Giugliani E, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet. 2008; 371(9610): 417-40.

7. Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7.
- 88. Beard JL. Effectiveness and strategies of iron supplementation during pregnancy. Am J Clin Nutr. 2000; 71(5 Suppl): 1288S-94S.. Most studies approaching this disease seek to determine the effectiveness of supplementation with ferrous sulfate on the hemoglobin levels33. Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008; 62(2): 120-4. , 44. Peña-Rosa JP, Viteri FE. Effects and safety of preventive oral iron or iron+folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev 2009; (4): CD004736. , 77. Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7. and identify the risk factors associated with anemia. These factors include younger age, low socioeconomic status and inadequate living and sanitation conditions, lack of prenatal care or late initiation of prenatal consultations, little weight gain during pregnancy, history of previous miscarriages or stillbirths, diet low in protein, comorbidity during pregnancy, particularly verminoses, among others99. Meda N, Mandelbrot L, Cartoux, M Dao B, Ouangré A, Dabis F. Anaemia during pregnancy in Burkina Faso, west Africa, 1995-96: prevalence and associated factors. DITRAME Study Group. Bull World Health Organ 1999; 77(11): 916-22.

10. Ferreira HS, Moura FA, Cabral Júnior CR. Prevalência e fatores associados à anemia em gestantes da região semi-árida do Estado de Alagoas. Rev Bras Ginecol Obstet 2008; 30(9): 445-51.
- 1111. Baig-Ansari N, Badrudin SH, Karmaliani R, Harris H, Jehan I, Pasha O, et al. Anemia prevalence and risk factors in pregnant women in an urban area of Pakistan. Food Nutr Bull 2008; 29(2): 132-9.. Despite these numerous studies, none of them attempted to identify factors associated with intake of ferrous sulfate supplementation in government programs. This is relevant because, in Brazil, this micronutrient supplementation is indicated to all pregnant women1212. Ministério da Saúde. Pré-natal e puerpério: atenção qualificada e humanizada - manual técnico. Direitos Sexuais e Direitos Reprodutivos. Caderno nº 5. Brasília: Ministério da Saúde; 2006.. This research aimed to determine the prevalence and identify factors associated with ferrous sulfate supplementation during pregnancy among all mothers living in the municipality of Rio Grande, RS, who gave birth in 2007.

Material and Methods

The municipality of Rio Grande is located in the southern half of the State of Rio Grande do Sul, about 300 km (186.411 miles) from Porto Alegre. In 2007, it had 195,000 inhabitants, 95% of whom lived in urban areas. The municipality's gross domestic product (GDP) per capita/year reached R$ 19.700; the infant mortality rate was 16/1.000 and the primary health care network consisted of 32 basic units. There were also two general hospitals and five clinics for the care of medical specialties1313. Fundação de Economia e Estatística do Rio Grande do Sul. Resumo estatístico dos municípios do Rio Grande do Sul – Rio Grande, RS. Disponível em http://www.fee.tche. br/sitefee/pt/content/resumo/pg_municipios_detalhe. php?municipio=Rio+Grande (Acessado em 02 de fevereiro de 2010).
Disponível em http:...
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The study included all mothers living in the municipality who gave birth between January 1, 2007, and December 31, 2007, in the only two hospitals in the municipality. However, as the analysis unit was composed of newborns weighing less than or exactly 500 g or with 20 weeks or more of gestation, only mothers of these children were included in this study. The study design was cross-sectional (or prevalence), with a single approach to mothers within 24 hours of delivery. All information in this study were collected using a single precoded questionnaire that sought information as to the family's place of residence, demographic characteristics (age, skin color, marital status), occupation (if exercised paid work in the 12 months prior to or during pregnancy), reproductive history (parity, low weight at birth and prior prematurity) and lifestyle habits of pregnant women (smoking, physical activity, alcohol consumption). Also, information regarding socioeconomic status (maternal education and family income), possession of household appliances (type and quantity available in the household), living (type of construction and floor) and sanitation (type of toilet in the household and access to treated water and sewerage), as well as care received during pregnancy and childbirth (number of visits, trimester of initiation and type of care received) and morbidity during pregnancy (complications in the period and type of treatment received) were collected. Weight at birth was noted from the record book. This weight was obtained by nurses using a pediatric electronic scale accurate to 10 g. Some variables need further clarification: skin color, classified by the very pregnant woman from white, mixed and black; family income, amount received by all residents of the household in the month immediately preceding the interview; low weight at birth, if any previous child was born with less than 2,500g; prematurity, if any previous child was born with less than 37 weeks of gestational age; smoking, if the mother smoked at least one cigarette per day in the last 30 days. The gestational age of the newborns was assessed from the date of last menstrual period (LMP) noted on the prenatal care record.

Ten interviewers were trained to conduct this study. Of these 10, eight were students in the Medicine undergraduate course of FURG (Universidade Federal do Rio Grande) and the other two were social workers. The training consisted of reading the questionnaire and the instruction manual and lessons on how to apply the questionnaire in pairs and before the group of interviewers. During the pilot study, conducted in December 2006, each of the trainees applied at least two complete questionnaires and carried out an anthropometric examination in the children. The identification of pregnant women was made directly in the delivery room and in the maternity, and subsequently confirmed by the Medical Records and Statistics Service (SAME). Upon encountering a postpartum patient resident in the municipality of Rio Grande, she was given a consent form to read and, if she agreed to participate in the study, the questionnaire was then applied. This questionnaire was coded and submitted to the project headquarters for final review and typing.

The questionnaires were double entered by different professionals in reverse order. Every two weeks, the information typed were compared, and any errors were corrected and listed. After that, the consistency of the data was checked, with immediate correction of any differences. Data entry was done using software Epi Info 6.041414. Dean AG, Dean JA, Coulombier D, Brendel KA, Smith DC, Burton AH, et al. Epi-Info, Version 6: A word processing, database, and statistics program for epidemiology on microcomputers. Atlanta: Centers of Disease Control and Prevention; 2002.. The research protocol was submitted to and approved by CEPAS (Research Ethic Committee in the Field of Health) of Universidade Federal do Rio Grande. Moreover, the confidentiality of data was guaranteed, the participation was voluntary and there was the possibility of leaving the study at any time, without the need for justification. Crude and adjusted analyzes were conducted using Poisson regression, with a robust adjustment of variance. The outcome measure was expressed by the prevalence ratio (PR), a confidence interval of 95% (95%CI) and p-value from Wald test for heterogeneity. For the adjusted analysis, a four-level hierarchical model was prepared1515. Victora CG, Huttly SR, Fuchs SC, Olinto MT. The role of conceptual frameworks in epidemiological analysis: a hierarchical approach. Int J Epidemiol 1997; 26(1): 224-7 to determine the order of entry of variables in the model. In the first level, demographic and socioeconomic variables (age, skin color, maternal education and family income) were included; in the second level, reproductive variables (parity, low weight at birth and prior prematurity); on the third level, the variables related to prenatal care (number of visits, trimester of initiation and type of care received); and on the last level, having referred vitamin intake during pregnancy. All variables were taken to the multivariable model, and those with p ≤ 0.20 were maintained. The analyses were conducted using Stata 10.0 software1616. StataCorp. Stata statistical software: release 10.0. College Station: Stata Corporation; 2008. and the level of significance used was 95% for two-tailed tests (Chart 1).

Chart 1
Hierarchical analysis model.

Results

For this study, 2,557 postpartum women were interviewed, representing a response rate of approximately 99% among all those who had children in the municipality of Rio Grande in 2007. The description of the sample with regard to demographic, socioeconomic, and gestational characteristics is in Table 1. A fifth of the mothers consisted of adolescents (< 20 years), 70% were of white skin, 13% had up to four years of education and 40% were primiparous. Just over 10% had, in the past, children with low weight at birth or premature. About 60% received prenatal care in the public health system, 72% completed six or more appointments and 74% initiated prenatal care in the first trimester of pregnancy. A quarter of mothers had referred intake of vitamins, and 59% took ferrous sulfate during pregnancy (Table 1). The distribution of outcomes, as well as the results of crude and adjusted analyzes is presented in Table 2. The prevalence of ferrous sulfate supplementation ranged from 47% among those who had less than six visits during prenatal care to 67% among those who underwent consultation in the public health system. In the crude analysis, the following variables showed a significant association to the outcome: maternal age, skin color, family income, parity, number of visits during prenatal care, type of prenatal care received, if prenatal care was received in the public or private health system and vitamin supplementation.

Table 1
- Description of the sample according to some demographic, socioeconomic and reproductive characteristics. Rio Grande, RS, 2007.

Table 2
- Crude and adjusted analysis for factors associated with iron supplementation during pregnancy. Rio Grande, RS, 2007 (n = 2.557).

In the adjusted analysis, using the previously established hierarchic model, the following variables remained significantly associated with supplementation of ferrous sulfate: aged 20 or younger (teenagers) (PR = 1.12; 95%CI 1.02 - 1.22) compared to those aged 30 or older; black skin color (PR = 1.15; 95%CI 1.05 - 1.25) compared to white skin color; first pregnancy (PR = 1.15; 95%CI 1.05 - 1.27) compared to mothers with three or more children; six or more prenatal visits (PR = 1.28; 95%CI 1.18 - 1.39) compared to the rest; mothers who underwent prenatal care in the public health system (PR = 1.31; 95%CI 1.22 - 1.42) compared to the private network and finally, mothers supplemented with vitamin (OR = 1.17; 95%CI 1.09 - 1.25 ) compared to unsupplemented mothers.

Discussion

This study showed that the prevalence of iron sulfate supplementation is low among the pregnant women studied, particularly among those usually considered as having a lower risk of complications during pregnancy. The highest prevalence of supplementation, after adjustment for potential confounding factors, were observed among adolescent mothers, with black skin color, primiparous, who had six or more prenatal appointments, who received prenatal care in the public health system and who had been supplemented with vitamins. When interpreting these results, one must bear in mind that this is a cross-sectional study, so the situation presented refers to the period of data collection. Moreover, regarding the intake of supplementation, data were based, as in most studies dealing with the subject, only on the account of the mother. Finally, there seems to be no reason for a particular group of mothers to have answered (or remembered) differently from each other regarding their intake (or not) of ferrous sulfate during pregnancy. For these reasons, it is possible to assume that the mentioned limitations do not invalidate the results presented here.

Despite the persisting doubt, for example, about the impact of supplementation with ferrous sulfate in reducing the occurrence of postpartum infections and bleeding33. Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008; 62(2): 120-4. , 44. Peña-Rosa JP, Viteri FE. Effects and safety of preventive oral iron or iron+folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev 2009; (4): CD004736. this supplementation is widely recommended during pregnancy because, in this period, the necessary absorption of iron changes from 0.8 to ≤ 7.5 mg8. Moreover, iron has a low cost, high availability and high acceptability, despite some side effects55. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20.. Finally, there is enough evidence that this intervention can reverse anemia and bring benefits to the mother and especially to the child, such as a lower incidence of prematurity and intrauterine growth restriction and better neuropsychomotor development33. Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008; 62(2): 120-4.

4. Peña-Rosa JP, Viteri FE. Effects and safety of preventive oral iron or iron+folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev 2009; (4): CD004736.

5. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20.

6. Buttha Z, Ahmed T, Black RE, Cousens S, Dewey K, Giugliani E, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet. 2008; 371(9610): 417-40.
- 77. Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7..

For all these reasons, WHO universally recommends iron supplementation to pregnant women1. However, despite this wide recommendation, there are no recent data regarding iron supplementation coverage by country or region. Studies conducted in the 1990s, when several countries received encouragement from WHO and various funding agencies for research and intervention to make such supplementation, showed that coverage of iron supplementation during pregnancy was 22% in Yemen, 32% in Eritrea, 44% in Tanzania and approximately 75% in Ghana, Indonesia and the Philippines1717. Yip R. Iron supplementation: country level experiences and lessons learned. J Nutr 2002:132(4 Suppl): 859S-61S.

18. Cavalli-Sforza T. Effectiveness of weekly iron-folic acid supplementation to prevent and control anemia among women of reproductive age in three Asian countries: development of the master protocol and implementation plan. Nutr Rev 2005; 63(12 Pt 2): S77-80.
- 1919. Galloway R, Dusch E, Elder L, Achadi E, Grajeda R, Hurtado E, et al. Women's perceptions of iron deficiency and anemia prevention and control in eight developing countries. Soc Sci Med. 2002; 55(4): 529-44.. In Thailand and Nicaragua, where there was intervention, anemia rates dropped about 40% over 10 years. In these countries, the coverage rate was approximately 85%77. Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7. , 2020. Winichagoon P. Prevention and control of anemia: Thailand experiences. J Nutr 2002; 132(4 Suppl): 862S-6S.. Whereas these benefits should be extended to all mothers, the goal of the programs is to achieve the greatest possible coverage. However, it was not what was observed for the municipality of Rio Grande. Coverage for all of them was 59%, ranging from 47 to 67% among those who had less than six prenatal visits during and among those who received prenatal care in the public health system, respectively. It is even more interesting to note that the lowest prevalence observed in relation to receiving supplementation with ferrous sulfate occurred almost entirely in mothers known to have the lowest risk of adverse outcomes during prenatal and childbirth, such as mothers who were not in their teens, had white skin, with a higher number of children and supplemented with vitamins, besides, of course, those who received prenatal care in the private health system, who have a higher socioeconomic status99. Meda N, Mandelbrot L, Cartoux, M Dao B, Ouangré A, Dabis F. Anaemia during pregnancy in Burkina Faso, west Africa, 1995-96: prevalence and associated factors. DITRAME Study Group. Bull World Health Organ 1999; 77(11): 916-22.

10. Ferreira HS, Moura FA, Cabral Júnior CR. Prevalência e fatores associados à anemia em gestantes da região semi-árida do Estado de Alagoas. Rev Bras Ginecol Obstet 2008; 30(9): 445-51.
- 1111. Baig-Ansari N, Badrudin SH, Karmaliani R, Harris H, Jehan I, Pasha O, et al. Anemia prevalence and risk factors in pregnant women in an urban area of Pakistan. Food Nutr Bull 2008; 29(2): 132-9. , 2020. Winichagoon P. Prevention and control of anemia: Thailand experiences. J Nutr 2002; 132(4 Suppl): 862S-6S.. This finding is contrary to what was observed in other studies. Generally, patients with higher risks have less access and, therefore, a worse coverage2121. Hart JT. The inverse care law. Lancet 1971; 1(7696): 405-12.. Therefore, this finding requires further investigation. This study did not assess the reasons why the mothers were not supplemented with ferrous sulfate. However, subsequent consultation with the Department of Health of Rio Grande showed that during the years 2006 and 2007, at least in the central region, there was no lack of this supplement, and the amount held in stock was sufficient to serve about 250 new mothers/month when, on average, 220 births occur. However, it was not possible to assess the availability of ferrous sulfate in the same period in basic health units and clinics, where pregnant women received their prenatal care. Anyway, it seems that the most common cause for the unsupplementation was not due to lack of ferrous sulfate, as reported in another study, but the lack of recommendation or selective recommendation from health professionals2222. Wulff M, Ekström EC. Iron supplementation during pregnancy in Sweden: to what extent is the national recommendation followed? Acta Obstet Gynecol Scand 2003; 82(7): 628-35.. Several strategies have been recommended to overcome problems related to reduced coverage of supplementation with ferrous sulfate. Among them are clarification on the undesirable effects of the drug; greater involvement of pregnant women in their treatment; use of a calendar indicating date and period of the supplementation with ferrous sulfate; facilitation of the drug's distribution, for example, through community health agents; further explanation about direct benefits to pregnant women resulting from iron supplementation, such as better physical performance and increased appetite; demystification of the possibility of a very overweight newborn, which would cause difficulties during childbirth; reiteration of the benefits to the newborn; explanation of the consequences of prematurity and low weight at birth, outcomes strongly associated with iron deficiency; improving of the support to healthcare professionals, keeping them motivated to offer this supplement during pregnancy and during the first years of life, and promotion of campaigns prioritizing community involvement55. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20. , 77. Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7. , 88. Beard JL. Effectiveness and strategies of iron supplementation during pregnancy. Am J Clin Nutr. 2000; 71(5 Suppl): 1288S-94S. , 1717. Yip R. Iron supplementation: country level experiences and lessons learned. J Nutr 2002:132(4 Suppl): 859S-61S. , 2020. Winichagoon P. Prevention and control of anemia: Thailand experiences. J Nutr 2002; 132(4 Suppl): 862S-6S..

The results presented in this study show that it is necessary to increase the coverage of ferrous sulfate supplementation among pregnant women of Rio Grande, and future studies should seek to understand why this supplementation has not been universalized among these mothers.

References

  • 1
    Stoltzfus RJ, Dreyfuss ML. International Nutritional Anemia Consultative Group (INACG), World Health Organization (WHO), United Nations Childrens Fund (UNICEF). Guidelines for the use of iron supplements to prevent and treat iron deficiency anemia. Washington: ILSI Press. 1988.
  • 2
    Benoist B, Mc Lean E, Cogswell M. World Health Organization. Worldwide Prevalence of Anaemia 1993-2005: WHO Global Database on Anaemia. Switzerland: WHO Press; 2008.
  • 3
    Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008; 62(2): 120-4.
  • 4
    Peña-Rosa JP, Viteri FE. Effects and safety of preventive oral iron or iron+folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev 2009; (4): CD004736.
  • 5
    Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet 2007; 370(9586): 511-20.
  • 6
    Buttha Z, Ahmed T, Black RE, Cousens S, Dewey K, Giugliani E, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet. 2008; 371(9610): 417-40.
  • 7
    Sanghvi TG, Harvey PW, Wainwright F. Maternal iron-folic acid supplementation programs: evidence of impact and implementation. Food Nutr Bull 2010; 31(2 Suppl): S100-7.
  • 8
    Beard JL. Effectiveness and strategies of iron supplementation during pregnancy. Am J Clin Nutr. 2000; 71(5 Suppl): 1288S-94S.
  • 9
    Meda N, Mandelbrot L, Cartoux, M Dao B, Ouangré A, Dabis F. Anaemia during pregnancy in Burkina Faso, west Africa, 1995-96: prevalence and associated factors. DITRAME Study Group. Bull World Health Organ 1999; 77(11): 916-22.
  • 10
    Ferreira HS, Moura FA, Cabral Júnior CR. Prevalência e fatores associados à anemia em gestantes da região semi-árida do Estado de Alagoas. Rev Bras Ginecol Obstet 2008; 30(9): 445-51.
  • 11
    Baig-Ansari N, Badrudin SH, Karmaliani R, Harris H, Jehan I, Pasha O, et al. Anemia prevalence and risk factors in pregnant women in an urban area of Pakistan. Food Nutr Bull 2008; 29(2): 132-9.
  • 12
    Ministério da Saúde. Pré-natal e puerpério: atenção qualificada e humanizada - manual técnico. Direitos Sexuais e Direitos Reprodutivos. Caderno nº 5. Brasília: Ministério da Saúde; 2006.
  • 13
    Fundação de Economia e Estatística do Rio Grande do Sul. Resumo estatístico dos municípios do Rio Grande do Sul – Rio Grande, RS. Disponível em http://www.fee.tche. br/sitefee/pt/content/resumo/pg_municipios_detalhe. php?municipio=Rio+Grande (Acessado em 02 de fevereiro de 2010).
    » Disponível em http://www.fee.tche.br/sitefee/pt/content/resumo/pg_municipios_detalhe.php?municipio=Rio+Grande
  • 14
    Dean AG, Dean JA, Coulombier D, Brendel KA, Smith DC, Burton AH, et al. Epi-Info, Version 6: A word processing, database, and statistics program for epidemiology on microcomputers. Atlanta: Centers of Disease Control and Prevention; 2002.
  • 15
    Victora CG, Huttly SR, Fuchs SC, Olinto MT. The role of conceptual frameworks in epidemiological analysis: a hierarchical approach. Int J Epidemiol 1997; 26(1): 224-7
  • 16
    StataCorp. Stata statistical software: release 10.0. College Station: Stata Corporation; 2008.
  • 17
    Yip R. Iron supplementation: country level experiences and lessons learned. J Nutr 2002:132(4 Suppl): 859S-61S.
  • 18
    Cavalli-Sforza T. Effectiveness of weekly iron-folic acid supplementation to prevent and control anemia among women of reproductive age in three Asian countries: development of the master protocol and implementation plan. Nutr Rev 2005; 63(12 Pt 2): S77-80.
  • 19
    Galloway R, Dusch E, Elder L, Achadi E, Grajeda R, Hurtado E, et al. Women's perceptions of iron deficiency and anemia prevention and control in eight developing countries. Soc Sci Med. 2002; 55(4): 529-44.
  • 20
    Winichagoon P. Prevention and control of anemia: Thailand experiences. J Nutr 2002; 132(4 Suppl): 862S-6S.
  • 21
    Hart JT. The inverse care law. Lancet 1971; 1(7696): 405-12.
  • 22
    Wulff M, Ekström EC. Iron supplementation during pregnancy in Sweden: to what extent is the national recommendation followed? Acta Obstet Gynecol Scand 2003; 82(7): 628-35.

Publication Dates

  • Publication in this collection
    Sept 2013

History

  • Received
    27 Aug 2011
  • Reviewed
    28 May 2012
  • Accepted
    11 July 2012
Associação Brasileira de Pós -Graduação em Saúde Coletiva São Paulo - SP - Brazil
E-mail: revbrepi@usp.br