Original Research

The iron status of rural Nigerian women in the second and third trimesters of pregnancy: implications for the iron endowment and subsequent dietary iron needs of their babies

AUTHORS

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Bennett Chima Nwanguma
1 PhD, Professor * ORCID logo

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Herietta Chinonso Odo
2 MSc, Researcher

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Bravo Udochukwu Umeh
3 MSc, Lecturer ORCID logo

name here
Amarachukwu Vivian Arazu
4 MSc, Lecturer ORCID logo

CORRESPONDENCE

*Prof Bennett Chima Nwanguma

AFFILIATIONS

1, 2 Department of Biochemistry, University of Nigeria, Nsukka, Enugu State, Nigeria

3 Department of Genetics and Biotechnology, University of Nigeria, Nsukka, Enugu State, Nigeria

4 Department of Science and Laboratory Technology, University of Nigeria, Nsukka, Enugu State, Nigeria

PUBLISHED

13 February 2024 Volume 24 Issue 1

HISTORY

RECEIVED: 6 October 2022

REVISED: 2 August 2023

ACCEPTED: 4 October 2023

CITATION

Nwanguma BC, Odo HC, Umeh BU, Arazu AV.  The iron status of rural Nigerian women in the second and third trimesters of pregnancy: implications for the iron endowment and subsequent dietary iron needs of their babies. Rural and Remote Health 2024; 24: 7906. https://doi.org/10.22605/RRH7906

AUTHOR CONTRIBUTIONSgo to url

This work is licensed under a Creative Commons Attribution 4.0 International Licence


abstract:

Introduction:  The aim of the study was to determine the iron status of rural-dwelling pregnant Nigerian women in the second and third trimesters, and to predict their risk of giving birth to babies with suboptimal iron endowment.
Methods:  This was a prospective cohort study conducted between April and August 2021. A total of 174 consecutive and consenting pregnant rural dwellers, who met the inclusion criteria, were recruited by convenience sampling from the antenatal clinic of a public hospital in Nsukka, a semirural town in south-east Nigeria. The study participants were aged 21–40 years, and their iron status was determined by measuring blood haemoglobin (Hb) and serum ferritin (SF) concentration. Hb concentration was determined by the cyanmethemoglobin method and the SF concentration was determined by enzyme immunoassay method.
Results:  Almost half (47.7%) of the participants had Hb concentrations below 11 g/dL, while about two out of every five (40.8%) had SF concentrations less than 15 µg/L. The prevalence of iron deficiency, iron deficiency anaemia (IDA) and non-iron deficiency anaemia were 40.8%, 23.6% and 24.7%, respectively. The mean SF levels varied with maternal age, gestation stage, pregnancy intervals and the intake of iron supplements. The mean SF concentration was higher in the second trimester than in the third. The mean SF concentration ± standard deviation (37.10±3.02 µg/L) was higher in the group that took iron supplements than in the group that did not (20.76±2.11 µg/L). However, two out of five participants in both groups had SF concentrations less than 15.0 µg/L.
Conclusion:  The prevalence of IDA was quite high among the participants in both trimesters even with the widespread intake of the recommended oral iron supplements. About four out of 10 of the participants had SF concentrations of less than 15 µg/L and were thus judged at risk of giving birth to babies with poor iron deposits. Therefore, more effective strategies are needed to monitor and prevent IDA among pregnant women in rural populations of Nigeria and, by inference, other parts of tropical Africa.

Keywords:

anaemia, babies, ferritin, haemoglobin, iron, Nigeria, pregnancy.

full article:

Introduction

Iron deficiency anaemia (IDA) is a common health problem in persons of all physiological groups. However, pregnant women face a higher risk of IDA because additional iron is needed to meet the iron needs of the growing fetus and supply the increased iron requirement for the expanding maternal red blood cell mass1,2. Suboptimal levels of iron during pregnancy are associated with a number of adverse outcomes, including low birth weight, preterm birth3,4 and, in more severe cases, maternal fatality5. Thus, the iron status of pregnant women is widely considered an important determinant of pregnancy outcome around the world.

Reducing the burden of IDA during pregnancy has, therefore, become an important aspect of global efforts to reduce the burden of maternal–infant mortality, especially in rural populations in developing countries where reported figures of maternal–infant mortality remain relatively higher5,6. The strategies widely advocated to address this burden include improved dietary supply of iron, regular intake of iron and folic acid supplements and the periodic evaluation of the iron status of pregnant women7-9. In Nigeria and other countries of the tropics, additional preventive strategies are advocated and implemented for reducing the burdens of endemic parasitic diseases, such as malaria and helminthiasis, which are associated with increased risk of IDA in pregnant women10,11.

In addition to its implications on pregnancy outcome, there are strong concerns that suboptimal iron status in pregnant women also affects the ability of neonates to accumulate sufficient iron stores before birth12,13. This is because the iron endowment of newborns is determined to a great extent by the iron status of their mothers, especially in the second and third trimesters when most of the accretion of foetal iron occurs14-16. These foetal iron deposits are important because newborns rely on them in the first months of life to compensate for shortfalls in their dietary iron intake and to protect against anaemia and its associated far-reaching consequences, which includes the impairment of brain development16. How soon these iron deposits are depleted is determined by the concentration at birth, as well as the dietary iron intake in the early months of life. By inference, children born with inadequate iron deposits would face an increased risk of anaemia in the early months of life, because the deposits may not last long enough to continue to compensate for shortfalls in their dietary iron intake. Another plausible inference is that the risk of anaemia will be higher in exclusively breastfed infants because breast milk is a poor source of iron12.

Although orally administered iron and folic acid supplements are widely recommended for pregnant women attending antenatal clinics, a number of problems, including poor absorption and non-compliance, which could be common in rural dwellers, are believed to affect the effectiveness of these supplements in preventing IDA in pregnant women. Therefore, there is need for studies of this type to determine if the supplements are effective in reducing the burden of IDA. The aim of this article is therefore to determine the iron status of pregnant women attending an antenatal clinic and to ascertain if they face the risk of giving birth to babies with suboptimal iron deposits. This study is important because although prevailing socioeconomic conditions, characterised by poor nutrition and a predisposition to a number of endemic parasitic diseases10, combine to increase the risk of IDA in pregnant women in rural populations, the prevalence and severity of IDA in pregnant women in rural populations of Nigeria and other parts of the tropics deserve further investigation. In this study, we used a combination of haemoglobin (Hb) concentrations and SF levels to determine the iron status of pregnant women attending an antenatal clinic at a public hospital in Nsukka, a semi-urban town in south-east Nigeria. The choice of SF and Hb levels as markers of iron status is informed by their reported suitability for clinical and population-wide studies such as this5,17. Besides, combining both parameters gives a better picture of the iron status of pregnant women than Hb concentration alone, which is commonly used to assess the iron status of pregnant women attending antenatal clinics in rural and semirural populations Nigeria.

Methods

This was a prospective cohort study conducted between April and August 2021 at Bishop Shanahan Hospital, Nsukka, Enugu state, Nigeria. Nsukka is a semi-urban town and the hospital is a public hospital that is run by the Roman Catholic Mission and is attended by rural populations around Nsukka. The study participants were recruited by convenience sampling, and a total of 174 consecutive and consenting pregnant rural dwellers in the second and third trimesters and aged 21–40 years, who met the inclusion criteria, were recruited from the antenatal clinic of the hospital for the study. The gestational stages were obtained from the clinics and were determined through ultrasound. Participants who admitted to being smokers or diagnosed with known conditions, such as sickle cell anaemia, HIV and untreated malaria, which could affect the results of study, were excluded from the study.

Determination of haemoglobin concentration

Hb concentration was determined by the cyanmethemoglobin method18. Anaemia was defined as Hb concentration less than 11.0 g/dL.

Determination of serum ferritin concentration

Serum ferritin (SF) concentration was determined by the enzyme immunoassay method19. The AccuBind Ferritin Assay Kit was used for the determination. An SF concentration of 15 µg/L was used as the cut-off point for iron deficiency. Participants with SF concentrations less than 15 µg/L were diagnosed as having iron deficiency. Such participants were identified and offered treatment in line with the practice of the antenatal clinic.

Diagnosis of iron deficiency, iron deficiency anaemia and non-iron deficiency anaemia

Iron deficiency was diagnosed as serum SF<15 µg/L, IDA was diagnosed as Hb<11 mg/dL and SF<15 µg/L, while non-iron deficiency anaemia was diagnosed as Hb<11 mg/dL and SF³15 µg/L.

Demographics

Demographic data of the participants, including age, stage of pregnancy, consumption of iron supplements and obstetrical history (such as parity and number of previous pregnancies), were obtained through a questionnaire. The questionnaire was written in English and was administered by the researchers with the help of staff of the clinic.

Data analysis

Data were analysed using Statistical Package for Social Sciences v22.0, for Windows (IBM Corp; https://www.ibm.com/products/spss-statistics). Comparison of means was prepared by one-way ANOVA test and Pearson correlation. The test was performed to assess the correlation between the Hb concentration and SF levels with other variables.

Ethics approval

This study was conducted according to the guidelines laid down in the Declaration of Helsinki. The procedures involving human participants/patients were approved by the ethics authorities in the Faculty of Biological Sciences, University of Nigeria, Nsukka, and Bishop Shanahan Hospital, Nsukka. Written and signed informed consent was obtained from all participants.

Results

Demographics

The demographic data of the 174 participants are shown in Table 1. The participants were aged 21–40 years. A total of 58 (32.7%) of the participants were in the second trimester, while 116 (67.2%) were in the third trimester. The participants were further categorised in terms of interpregnancy intervals and on the consumption of iron supplements. The most common interpregnancy intervals were 21–40 months (49.2%) and 0–20 months (46.5%). A high proportion of the participants (85.6%) admitted to the regular consumption of iron supplements, while the rest (14.3%) did not.

Table 1:  Demographics of study participantstable image

Prevalence of anaemia, iron deficiency, iron deficiency anaemia and non-iron deficiency anaemia

Data on the iron status of the participants are shown in Table 2. The prevalence of anaemia was 48.0%, while the prevalence of iron deficiency was 40.8%. In addition, the prevalence of iron deficiency anaemia was 23.6%, while the prevalence of non-iron deficiency anaemia was 24.7%.

Only 33.9% (59/174) of the participants met the criteria of Hb concentration and SF levels set for normal iron status. A higher percentage (38.8%) of the participants in the third trimester than those in the second trimester (24%) met these criteria.

Table 2:  Iron status of study participantstable image

Effect of maternal age, gestational stage, interpregnancy interval and consumption of iron supplements on serum ferritin concentrations

The serum concentration of ferritin varied with maternal age (Table 3). The highest mean SF concentration (41.02±4.01 µg/L) was observed in the 31–35 year age group, while the lowest mean concentration (20.04±3.76 µg/L) was observed in the 21–25 year age group, which was the youngest age group. The mean SF concentration also varied with the gestational stages of the participants. Participants in the second trimester had a mean SF concentration of 43.87±3.76 µg/L, while those in the third trimester had a significantly (p>0.05) lower mean SF concentration of 30.31±3.89 µg/L.

Similarly, the mean SF concentration of the participants varied with the interpregnancy intervals. The highest mean concentration of SF (63.87±4.93 µg/L) was recorded in the group with an interpregnancy interval of 41–60 months, while the lowest mean SF concentration (25.82±2.92 µg/L) was recorded in the group with an interpregnancy interval of 0–20 months. The consumption of iron supplements also affected the mean SF concentration of the participants. The mean SF concentration recorded in the group that regularly consumed iron supplements (37.10±3.02 µg/L) was significantly (p≤0.05) higher than the mean concentration of the group that did not consume the supplements (20.76±2.11 µg/L).

Table 3:  Influence of maternal age, gestation stage, interpregnancy interval and intake of iron supplementation on serum ferritin concentrations of study participantstable image

Discussion

This study set out primarily to investigate the iron status of a population of rural Nigerian women in the second and third trimesters of pregnancy, with a view to establishing the percentage of the participants with poor iron status and, therefore, who are at risk of giving birth to babies with suboptimal iron deposits. The study is necessitated by the concern that maternal iron status determines the concentration of foetal iron deposits, which newborns depend on to compensate for shortfalls in dietary iron intake in the first few months of life14. Exclusively breast-fed babies rely on these deposits to meet their daily iron needs since the iron supply from breast milk falls far short of the recommended daily iron requirement at this stage of life13-15.

The 40.8% prevalence of iron deficiency observed in this study is quite high, but is comparable to the prevalence figures reported previously in studies on iron deficiency in Nigeria20,21. Such high prevalence figures are common in rural and semirural populations in developing countries of tropical Africa and are partly attributable to poor nutrition linked to poor socioeconomic status and a higher predisposition to malaria and other infectious diseases, such as helminthiasis22.

The prevalence of 23.6% reported for IDA in this study is almost double the prevalence of 12.3% reported by Ajepe et al21 in a study of pregnant women in an urban Nigerian population. The lower prevalence of IDA reported by Ajepe et al21, could be partly because their study was conducted in the more metropolitan city of Lagos and at a teaching hospital, where people of higher socioeconomic status are more likely to attend. As shown in Table 2, the prevalence of anaemia, ID and IDA were all higher in the second trimester than in the third trimester. This is probably because of the higher rate of consumption of iron supplements in the third trimester than in the second trimester.

The SF concentration of 15 µg/L used as the benchmark for the diagnosis of ID in this study was recently identified as the critical threshold for identifying pregnant women who would be unable to accrete their foetuses with sufficient iron deposits23. Curiously, the SF level of up to 40.8% of the participants fell below this threshold. This implies that babies born to four out of 10 of the participants would be at risk of being born with a compromised iron status. Based on the lower benchmark of 13.6 µg/L recommended by Sweet et al24, the percentage of the participants that would be at risk of giving birth to babies with a compromised iron status would still be as high as 38% (66/174). This implies that a relatively high percentage of these participants would give birth to children with suboptimal iron concentrations. These projections are supported by the findings of a study25 that reported low SF levels in the cord blood of more than half a population of newborns in Nigeria.

The current advocacy for exclusive breastfeeding for up to 6 months is based on the projection that the iron deposits of full-term babies would last this long and will continue to compensate for the deficits in iron intake from breast milk12,13,26. From the foregoing, this may not be the case in a high percentage of babies born in rural parts of Nigeria and other countries of tropical Africa. It is worthy of note that such low levels of SF were observed in the participants in spite of the regular consumption of iron supplements, especially in the third trimester. Our concern about the ability of such children to meet their iron needs when exclusively breast fed for 6 months is strengthened by new evidence that suggests that the concentration and bioavailability estimates previously reported for iron in breast milk may have been overstated26,27. In light of this new information, it can be argued that foetal iron deposits are far more important in supplying the iron needs of babies than was previously thought. This, in turn, implies that foetal iron deposits play a more critical role in preventing anaemia in the early months of life than was previously believed.

About one in four of the participants (24.7%) was diagnosed with non-iron deficiency anaemia, or anaemia of inflammation. The relatively high prevalence of this form of anaemia among the participants is attributable to the endemicity of several inflammatory tropical infectious diseases in Nigeria. The most common of these diseases is malaria, whose prevalence in pregnant women in south-eastern Nigeria could be very high28. In a study on the prevalence of malaria in pregnant women in south-eastern Nigeria, malaria parasitaemia was reported in 99% of the study population28.The plasmodium parasites that are responsible for malaria usually cause the rapid destruction of red blood cells, resulting in a significant reduction in Hb concentrations in the patients. It is possible at such times, therefore, for the rate of destruction of red blood cells to exceed the rate at which they can be replaced. The physiological implication of non-iron deficiency anaemia is not yet known, and it is not thought to adversely affect the iron endowment of newborns29. However, the physiological attempt to restore normal Hb levels in the affected participants would require additional iron and this may have an impact on their iron status.

From the results (Table 2), only 33.9% of the participants met the criteria of normal iron status based on their blood Hb concentration and SF levels. A significantly higher percentage of the participants in the third trimester (38.8%) met this criterion in comparison to only 24% of the participants in the second trimester. The difference between the two trimesters could be attributed in part to the fact that a much higher proportion of the participants in the third trimester (96.5%) admitted to the regular consumption of iron supplements than those in the second trimester (65%).

A number of factors were found to affect the mean SF levels of the participants. Participants in the lowest age group (21–25 years) had the lowest mean SF of all the groups. This is thought to be because this group is more likely to include a higher number of first-time mothers, as opposed to participants in the older age groups, such as those aged 31–35 years, who had a significantly higher mean SF concentration of 41.02±4.01 µg/L. Being first-time mothers implies they may not be aware of the need for additional iron requirements in pregnancy. The gestational stage also affected the mean SF concentrations of the participants. Participants in the second trimester had a significantly (p≤0.05) higher mean SF concentration of 43.87±3.76 µg/L than those in the third trimester, who had a mean concentration of 30.31±3.89 µg/L. Such lower concentrations of SF in the third trimester are thought to be due to the increased accretion of foetal iron, which occurs at this stage of pregnancy. A physiological mechanism that gives priority to the accretion of foetal iron at the expense of maternal iron is thought to operate in humans30. This observation is remarkable considering that a much higher percentage of the participants in the third semester admitted to the consumption of iron supplements than those in the second trimester.

The SF levels were also found to be affected by interpregnancy intervals as well as the consumption of iron supplements. Participants who allowed a longer interpregnancy interval of up to 41–60 months had a significantly (p≤0.05) higher mean SF concentration (63.87±4.93 µg/L) than those who allowed a shorter interval of 0–20 months (25.82±2.92 µg/L). This is because longer interpregnancy intervals allow more time for women to rebuild their iron stores and therefore be more able to meet the iron demands of the next pregnancy31.

The high percentage of the participants (40.8%) with suboptimal SF levels in spite of the regular intake of oral iron supplements casts doubts on the compliance and effectiveness of the supplements in achieving the desired improvement in the iron status of the participants. Adanikin et al32 and Zhao et al33, made similar observations on the ineffectiveness of iron supplements at improving the iron status of pregnant women and their babies. This has been blamed on poor compliance, poor absorption of iron due to morbidities and the possibility of interference by other food components34. A variety of gastrointestinal perturbations have also been associated with oral iron supplements35. The problem of counterfeit and substandard drugs, which is more widespread in rural communities, may also affect the effectiveness of iron supplementation in pregnant women in rural populations. The reported ineffectiveness of oral iron supplementation in preventing iron deficiency and associated anaemia in pregnancy has led to recent recommendations that the intravenous administration of iron be considered for all pregnant women in the third trimester35-38. Such a strategy is needed more urgently in developing countries of the tropics, where a combination of socioeconomic factors and the endemicity of some tropical infectious diseases predispose pregnant women in rural areas to a higher risk of iron deficiency anaemia2,20.

The fact that this study was conducted at a single health facility constitutes a limitation, as does the population size of 174. In addition, participants who did not take supplements were underrepresented.

Conclusion

A very high proportion of the participants drawn from the rural communities were diagnosed with IDA. In addition, the SF concentration in as many as one-quarter of the participants fell below the threshold of 15.0 µg/L recommended for defining those at risk of giving birth to babies with low iron stores. Thus, additional efforts are needed to reduce the burden of IDA in rural Nigerian populations. These efforts need to recognise and address some of the prevailing socioeconomic factors, which include low levels of literacy, poverty, and poor standards of nutrition and hygiene, which are common among rural dwellers in Nigeria and many other African countries. The current clinical practice of relying mostly on Hb levels to monitor anaemia in pregnant women in Nigeria may not reveal the true burden of IDA, and fails to detect the existence of non-iron deficiency anaemia during pregnancy. Thus, in addition to a more effective method of supplementation, we recommend the routine use of both Hb and SF levels to monitor the iron status of pregnant women during antenatal care. The close monitoring of the iron status of exclusively breast-fed children is also advocated in rural populations to prevent IDA and its consequences at this delicate stage of life.

Funding

No funding was received for this research.

Conflict of interest

The authors declare no conflicts of interest.

references:

1 McMahon LP. Iron deficiency in pregnancy. Obstetric Medicine 2010; 3: 17-24. DOI link, PMid:27582835
2 Cerami C. Iron nutriture of the fetus, neonate, infant, and child. Annals of Nutrition and Metabolism 2017; 71(Suppl 3): 8-14. DOI link, PMid:29268254
3 Figueiredo ACMG, Gomes-Filho IS, Silva RB, Pereira PPS, Mata FAFD, Lyrio AO, et al. Maternal anemia and low birth weight: a systematic review and meta-analysis. Nutrients 2017; 10(5): 601. DOI link, PMid:29757207
4 Beckert RH, Baer RJ, Anderson JG, Jelliffe-Pawlowski LL, Rogers EE. Maternal anemia and pregnancy outcomes: a population-based study. Journal of Perinatology 2019; 39(7): 911-919. DOI link, PMid:30967656
5 Daru J, Zamora J, Fernández-Félix BM, Vogel J, Oladapo OT, Morisaki N, et al. Risk of maternal mortality in women with severe anaemia during pregnancy and post partum: a multilevel analysis. Lancet Global Health 2018; E548-E554. DOI link, PMid:29571592
6 Meh C, Thind A, Ryan B, Terry A. Levels and determinants of maternal mortality in northern and southern Nigeria. BMC Pregnancy and Childbirth 2019; 19(1): 417. DOI link, PMid:31718572
7 World Health Organization. Guideline: daily iron and folic acid supplementation in pregnant women. 2012. Available: web link (Accessed 19 December 2023).
8 Bauerman M, Lokangaka A, Thorsten V, Tshefu A, Goudar SS, Esamai F, et al. Risk factors for maternal death and trends in maternal mortality in low- and middle-income countries: a prospective longitudinal cohort analysis. Reproductive Health 2015; 12(Suppl 2): S5. DOI link, PMid:26062992
9 Dorsamy V, Bagwandeen C, Moodley J. The prevalence, risk factors and outcomes of anaemia in South African pregnant women: a protocol for a systematic review and meta-analysis. Systematic Reviews 2020; 9: 209. DOI link, PMid:32912318
10 Gunn JKL, Ehiri JE, Jacobs ET, Ernst KC, Pettygrove S, Kohler LN, et al. Population-based prevalence of malaria among pregnant women in Enugu State, Nigeria: the Healthy Beginning Initiative. Malaria Journal 2015; 14: 438. DOI link, PMid:26542777
11 Moorthy D, Merrill R, Namaste S, Lannotti L. The impact of nutrition-specific and nutrition-sensitive interventions on hemoglobin concentrations and anemia: a meta-review of systematic reviews. Advances in Nutrition 2020; 11(6): 1631-1645. DOI link, PMid:32845972
12 Meinzen-Derr JK, Guerrero ML, Altaye M, Ortega-Gallegos H, Ruiz-Palacio GM, Morrow AL. Risk of infant anemia is associated with exclusive breast-feeding and maternal anemia in a Mexican cohort. Journal of Nutrition 2006; 136(2): 452-458. DOI link, PMid:16424127
13 Rao R, Georgieff MK. Iron in fetal and neonatal nutrition. Seminars in Fetal and Neonatal Medicine 2007; 12(1): 54-63. DOI link, PMid:17157088
14 Shao J, Lou J, Rao R, Georgieff MK, Kaciroti N, Felt BJ, et al. Maternal serum ferritin concentration is positively associated with newborn iron stores in women with low ferritin status in late pregnancy. Journal of Nutrition 2012; 142: 2004-2009. DOI link, PMid:23014493
15 Kumar JK, Asha N, Murthy DS, Sujatha M, Majunath V. Maternal anemia in various trimesters and its effect on newborn weight and maturity: an observational study. International Journal of Preventive Medicine 2013; 4: 193-199.
16 Best CM, Pressman EK, Cao C, Cooper E, Guilet R, Yost OL, et al. Maternal iron status during pregnancy compared with neonatal iron status better predicts placental iron transporter expression in humans. FASEB Journal 2016; 30(10): 3541-3550. DOI link, PMid:27402672
17 Georgeieff MK. Nutrition and the developing brain: nutrient priorities and measurement. American Journal of Clinical Nutrition 2007; 85(2): 614S-620S.
18 Sari M, de Pee S, Martini E, Herman S, Sugiatmi, Bloem MW, et al. Estimating the prevalence of anaemia: a comparison of three methods. Bulletin of the World Health Organization 2001; 79: 506-511.
19 Conradie JO, Mbhele BE. Quantitation of serum ferritin by enzyme-linked immunosorbent assay (ELISA). South African Medical Journal 1980; 57: 282-287.
20 Okafor IM, Okpokam DC, Antai AB, Usanga EA. Iron status of pregnant women in rural and urban communities of Cross River State, South-South Nigeria. Nigerian Journal of Physiological Sciences 2017; 31: 121-125.
21 Ajepe AA, Okunade KS, Sekumade AI, Daramola ES, Beke MO, Ijasan O, et al. Prevalence and foetomaternal effects of iron deficiency anaemia among pregnant women in Lagos, Nigeria. PLoS One 2020; 15(1): e0227965. DOI link, PMid:31971986
22 Brooker S, Hotez PJ, Bundy DAP. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Neglected Tropical Diseases 2008; 2(9): e291. DOI link, PMid:18820740
23 Daru J, Allotey J, Pena-Rosas JP, Khan KS. Serum ferritin thresholds for the diagnosis of iron deficiency in pregnancy: a systematic review. Transfusion Medicine 2017; 27(3): 167-174. DOI link, PMid:28425182
24 Sweet D, Savage G, Tubman TR, Lappin TR, Halliday HL. Study of maternal influences on fetal iron status of term using cord blood transferrin receptors. Archives of Disease in Childhood – Fetal and Neonatal Edition 2001; 84: F40-F43. DOI link, PMid:11124923
25 Adediran A, Gbadegesin A, Adeyemo TA, Akinbami AA, Akanmu AS, Osunkalu V, et al. Haemoglobin and ferritin concentrations in cord blood in a tertiary health centre in Nigeria. Nigerian Quarterly Journal of Quarterly Medicine 2011; 21(4): 284-289. DOI link, PMid:27579114
26 Cal C, Harding SV, Firel JK. Breast milk iron concentrations may be lower than previously reported: implications for exclusively breastfed infants. Maternal and Pediatric Journal 2015; 2: 1-4. DOI link
27 Friel J, Qasem W, Cai C. Iron and the breastfed infant. Antioxidants 2018; 7(4): 54. DOI link, PMid:29642400
28 Gunn JKL, Ehiri JE, Jacobs ET, Ernst KC, Pettygrove S, Kohler LN, et al. Population-based prevalence of malaria among pregnant women in Enugu State, Nigeria: the healthy beginning initiative. Malaria Journal 2015; 14: 438. DOI link, PMid:26542777
29 Abioye AI, Park S, Ripp K, McDonald EA, Kurtis JD, Wu H, et al. Anemia of inflammation during human pregnancy does not affect newborn iron endowment. Journal of Nutrition 2018; 148: 427-436. DOI link, PMid:29546300
30 Cao C, O’Brien KO. Pregnancy and iron homeostasis: an update. Nutrition Reviews 2013; 71: 35-51. DOI link, PMid:23282250
31 Sanga LA, Mtuy T, Philemon RN, Mahande MJ. Inter-pregnancy interval and associated adverse maternal outcomes among women who delivered at Kilimanjaro Christian Medical Centre in Tanzania, 2000–2015. PLoS One 2020; 15(2): e0228330. DOI link, PMid:32027674
32 Adanikin AI, Awoleke JO, Olofinbiyi BA, Adanikin PO, Ogundare OR. Routine iron supplementation and anaemia by third trimester in a Nigerian hospital. Ethiopian Journal of Health Sciences 2015; 25: 305-312.
33 Zhao G, Xu G, Zhou M, Jiang Y, Richards B, Clark KM, et al. Prenatal iron supplementation reduces maternal anemia, iron deficiency, and iron deficiency anemia in a randomized clinical trial in rural China, but iron deficiency remains widespread in mothers and neonates. Journal of Nutrition 2015; 145: 1916-1923. DOI link, PMid:26063068
34 Reveiz L, Gyte GM, Cuervo LG, Casasbuenas A. Treatments for iron-deficiency anaemia in pregnancy. Cochrane Database of Systematic Reviews 2011; 10: CD003094. DOI link
35 Toikien Z, Stecher L, Mander A, Powell JJ. Ferrous sulfate supplementation causes significant gastrointestinal side-effects in adults: a systemic review and meta-analysis. PLoS One 2015; 10(2): e0117383. DOI link, PMid:25700159
36 Achebe M. Gafter-Gvili A. How I treat anemia in pregnancy: iron, cobalamin and folate. Blood 2017; 129(8): 940-949. DOI link, PMid:28034892
37 Auerbach M. Commentary: Iron deficiency of pregnancy – a new approach involving intravenous iron. Reproductive Health 2018; 15(Suppl 1): 96. DOI link, PMid:29945649
38 Garzon S, Cacciato PM, Certelli C, Salvaggio C, Magliarditi M, Rizzo G. Iron deficiency anemia in pregnancy: novel approaches for an old problem. Oman Medical Journal 2020; 35(5): e166. DOI link, PMid:32953141
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