quantitative research proposal on anaemia in pregnancy pdf

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• Published: 09 December 2014

Prevalence and associated factors of anemia among pregnant women of Mekelle town: a cross sectional study

• Abrehet Abriha 1 ,
• Melkie Edris Yesuf 1 &
• Molla Mesele Wassie 1  

BMC Research Notes volume  7 , Article number:  888 ( 2014 ) Cite this article

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Nutritional anemia is the most common type of anemia worldwide and mainly includes iron, folic acid, vitamin B 12 and vitamin C deficiencies. Anemia is a global public health problem affecting people in all age groups but the burden of the problem is higher in pregnant women. The study aimed to assess prevalence of anemia and associated factors among pregnant women attending antenatal care in governmental health institutions in mekele town.

Institution based cross-sectional study was employed. Systematic random sampling procedure was employed to select 619 study subjects. Pretested questionnaire were used to collect the data. The predictive value of the variable to Anemia was identified by bivariate and multiple logistic regression analysis.

The overall prevalence of anemia among pregnant women was 19.7%. Meal frequency less than two per day [AOR 3.93 95% CI (2.0,7.9)], Low Dietary Diversity score [AOR 12.8 95% CI (6.4,25.6)], Medium Dietary Diversity score [AOR 2.4 95% CI (1.2,4.8)], Parity [AOR 2.3 95% CI (1.4,3.8)] and Meat consumption less than once per week [AOR 2.2 95% CI (1.0,4.9)] were found to be factors affecting Anemia in pregnant women.

Anemia among pregnant women is found to be mild public health problem in the study area. Parity, meal frequency, dietary diversity and meat consumption were significantly and independently affect anemia of pregnant women. Using family planning methods and improved meat consumption contributes for decreasing prevalence of anemia. Moreover, Diversifying food intake and increasing meal frequency of pregnant women is highly recommended.

Anemia is affecting 1.62 billion people globally [ 1 ]. The prevalence of anemia in developing countries is estimated to be 43% and that of developed countries is 9%. Anemia is estimated to contribute to more than 115 000 maternal deaths and 591 000 prenatal deaths globally per year [ 2 ]. Anemia occurs at all stages of the life cycle but its risk is higher in state of pregnancy due to an increased iron requirement, physiological demand, loss of blood and due to infections [ 1 , 3 ].

Nutritional anemia is the most common type of anemia worldwide and mainly includes iron, folic acid, vitamin B 12 and vitamin C deficiencies [ 1 , 3 – 5 ]. Iron deficiency contributes for half of the burden of anemia globally [ 6 ]. Iron deficiency affects 1.3 to 2.2 billion persons out of those 50% are women of reproductive age [ 7 ]. In Ethiopia nearly 17% of women with age 15–49 are anemic of these 22% are pregnant women [ 8 ].

The contextual factors contributing for anemia among pregnant women are different. Interaction of multiple factors like women’s’ socio-demographic, socio- economic, nutritional and health related factors cause anemia in pregnant women. There is no adequate information on factors leading to anemia in pregnant women in Ethiopia and Mekele town in particular. Hence this study aims to provide evidence-based estimates of the magnitude and associated factors of anemia among pregnant women attending ANC in Mekelle governmental health institutions in the town.

Facility based quantitative cross-sectional study was employed from February to April, 2014 at Mekelle town which is located at a distance of 783 km from Addis Abeba (capital of Ethiopia). The total number of women with in reproductive age was 68,093. Among these 11,011 were pregnant. There were five Governmental Hospitals, nine health centers and 4 private hospitals in mekele town and surrounding community which were giving ANC service in the study period [ 9 ].

Study population

All pregnant women attending ANC in governmental health institutions of Mekelle town were target for the study. All pregnant women who attend ANC for the first time in the selected governmental health institutions during the data collection period were included in the study. Pregnant women who were seriously ill during the data collection period and pregnant women with repeated visits were excluded from the current study.

Sample size and sampling

Sample size was determined by taking prevalence of anemia in a study done on Shalla woreda which was 12% [ 10 ], with 5% marginal error, design effect of 2, 95% CI and a non response rate of 10%. Based on this assumption, the final sample size was 632. Multistage sampling was employed to select pregnant women. Two Governmental hospitals and five health centers were selected randomly by using lottery method. The average number of pregnant women who visit ANC in health institutions in one month time was obtained by referring the client registration books to calculate the sampling interval which was 3. The calculated sample size were used to recruit study subjects from health Institutions proportional to their size. Finally study subjects were selected by using systematic random sampling technique.

The questionnaire, which was administered in the local language included questions that assessed socio-economic and demographic factors, pregnancy related characteristics, dietary diversity and meal frequency.

Blood Hemoglobin level was used to assess anemia status of pregnant women and women with <11 g/dl of blood hemoglobin level were considered as anemic. Meal frequencies for selected food items were asked for their habit one week prior to data collection. Dietary diversity score (DDS) was calculated by gathering information on dietary intake using single 24 hour dietary recall method. The score was categorized as Low (DDS ≤ 3), medium (DDS = 4 or 5) and high (DDS ≥ 6). Pregnant women taking at least one additional meal per day in addition to regular meal were considered as having good meal frequency. Value 0 was given for those having anemia and 1 for with no anemia in the analysis.

Data collection tools, procedures and data quality management

Interviewer administered questionnaire was used to collect information about pregnant women. Data on hemoglobin level were collected by reviewing charts of pregnant women.

Seven nurse data collectors and two supervisors were trained for one day before the actual data collection. The structured questionnaire were translated in to Tigrigna (local language) and retranslated back to English to ensure accuracy of translation in to Tigrigna language. Questionnaire were pre-tested in Quiha health center which includes 32 pregnant women. After the pretest questions, ambiguous words or anything wrong was corrected before the final questionnaire is printed and distributed.

Data Processing and Analysis

Data were entered in to Epi Info version 3.5.3 and analyzed using SPSS version 20 statistical software. Proportion and summary statistics was done to describe the study participants in relation to relevant variables. Both Bivarate and multivarate analysis were carried out. Variables with p value less than 0.2 in Bivariate analysis were entered in to multivariate logistic regression model. Variables P value less than 0.05 were taken as statistically significant and adjusted odds ratio with 95% CI was considered to see association.

Ethical Consideration

The proposal was reviewed and approved by the Institutional Review Board (IRB) of University of Gondar. Health institutions were communicated and permission was obtained to proceed on the study. After the purpose and objective of the study have been informed, verbal informed consent were obtained from each pregnant women included in the study. Participants were informed as participation is on voluntary basis. In order to keep confidentiality of any information the data collection procedure was anonymous.

Socio-demographic characteristics

A total of 632 respondents were included in the study with 97.9% response rate. The mean age of the respondents was 27.4 ± 5.5 years. More than two third of the respondents were married and 484 (78%) were orthodox Christian followers. Majority (85.1%) of the respondents were Tigre in ethnicity followed by Amhara 41 (6.6%). Majority of respondents were urban dwellers (88.2%) and 262 (42.3%) were housewife. Majority of the respondents were unable to read and write 223 (36%), 224 (36.2) were in the age group 26–30 and 215 (34.7%) of respondents earned (Table  1 ).

Pregnancy related Characteristics

Two hundred ninety-seven of the respondents were in the second trimester pregnancy. More than half (53.8) of the respondents were with parity of two and above, and 78% pregnant women were using contraceptive prior to current pregnancy (Figure  1 ).

Pregnancy related characteristics of pregnant women attending ANC in Mekelle town, Northern Ethiopia, 2014.

Nutritional Characteristics

Injera and wet was the staple diet for 418 pregnant women. Around half of the pregnant women ate three times per day. More than half of pregnant women (57.8%) took meat once per week, about 210 (33.4%) of women took milk twice per week. Two hundred eighty three (45.7%) of the respondents reported that they took egg twice per week. similarly around half of pregnant women ate fruits once per week. Majority of pregnant women took vegetables twice per week 452 (73%), two hundred seventy one (43.8%) of pregnant women were with medium dietary diversity score. The mean dietary diversity score of the respondents were 4.9 (Table  2 ).

Prevalence of Anemia

The mean ± SD hemoglobin concentration was 11.7 g/dl ± 2.32 and an overall prevalence rate of anemia with hemoglobin level < 11 g/dl was 19.3% (CI:19.1, 19.5). In terms of severity, mild anemia was 13.7%, moderate anemia was 4.4% and severe anemia was 1.6%.

Anemia is found to be a mild public health problem in the study groups. This finding is consistent with study conducted in Gondar town and Nine regional states of Ethiopia with the prevalence of 21.6% [ 11 ] and 18% [ 12 ] respectively. The result of this study was lower than the previous studies done on pregnant women at ANC clinic in Shalla Worda, in Urban Pakistan, in rural Uganda, in rural Vietnam and Ghana [ 3 , 13 – 16 ] but higher than a study done in Iran and Awassa where the prevalence was found to be 13.1% and 15% respectively [ 17 , 18 ].

Socioeconomic and geographical variations may be the reasons for different prevalence's of anemia in pregnant women across countries. Using different cutoff points for anemia may also resulted varied prevalence of anemia.

Multiple logistic regression analysis revealed that number of pregnancy, Meal frequency, Dietary diversity and frequent consumption of meat were significantly associated with anemia at p-value ≤ 0.05. Age category, Family monthly income, Marital status and occupational status of pregnant women showed significant association by bivariate analysis but not on the multivariate analysis (Table  3 ).

Pregnant women with lower level of Dietary diversity score were around 13 times more likely to develop anemia than those with higher dietary diversity score. This finding is consistent with a study done in nine regional states of Ethiopia [ 12 ]. Studies conducted in Pakistan and Turkey also suggested consumption of fruit two or more times per week is associated with a decreased risk of anemia [ 14 , 19 ]. Poor dietary diversity leads to deficiency of minerals and vitamins which may increase bio-availability of iron then affects Iron status [ 20 ]. Pregnancy is the most nutritionally demanding period in a woman’s life. Consequently, pregnant women are advised to eat more diversified diet than usual [ 12 ] .

Consumption of meat were also another factor which showed significant association with Anemia in pregnant women. Pregnant women with habit of eating meat once per week were 2.2 times at higher risk of developing anemia than pregnant mothers who ate meat more than twice per week. This finding is consistent with other studies in which pregnant women who ate red meat two or more times a week had higher mean hemoglobin concentrations [ 6 , 12 , 14 , 15 , 19 ]. The increased concentration of hemoglobin is with the fact that red meat is an important source of heme iron [ 10 , 21 ].

The present study also identified that, the odds of repeated pregnancies more than two or more were 2.3 times greater among pregnant mothers as compared to those who have less than two number of pregnancies. This result is consistent with the study done in Pakistan [ 14 ].This is due to the fact that Short intervals between births may not provide women with enough time to replenish lost nutrient stores before another reproductive cycle begins [ 22 ]. The risk is considerably exacerbated in those conditions where balanced diets is not available [ 5 ].

Pregnant women who had meal frequency less than two times per day were 3.9 times at higher risk of developing anemia than those whose meal frequency was more than three times per day. This might be due to the fact that pregnancy is a special period with increased energy and nutrient requirement which can be fulfilled with increased meal frequency.

Limitation of the study

There will be a recall and/or social desirability bias while subjects were requested to give dietary information and monthly income. Exclusion of patients with severe anemia may lower the prevalence in the study groups. Moreover, cross sectional nature of the study limits measuring the cause and effect relationship.

Anemia is found to be a mild public health problem in the study area. Number of pregnancy, Meal frequency, Food diversity and frequent consumption of meat were variables affecting anemia in pregnant women. Awareness creation on contraceptive use, nutritional counseling on consumption of iron-rich foods and Iron/foliate supplementation are recommended to prevent anemia in pregnant women.

Abbreviations

Antenatal care

Adjusted odds ratio

Confidence interval

Crude odds ratio

Dietary diversity score

Ethiopia demographic health survey

Iron deficiency anemia

Middle upper arm circumference

Statistical package for social science

World Health Organization.

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Acknowledgment

The authors are grateful for university of Gondar for financial support for data collection. Furthermore we extend our heartfelt gratitude to Tigray regional state health bureau, Mekele health centers and hospitals. We also want to thank all respondents, data collectors and supervisors for their active participation during the data collection process.

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Abrehet Abriha, Melkie Edris Yesuf & Molla Mesele Wassie

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Authors’ contributions

AA, MEY, and MMW conceived and designed the study. AA and MMW analyzed the data. MMW wrote the draft manuscript. AA & MEY commented on the draft and approved the final manuscript. All authors approve the manuscript.

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Abriha, A., Yesuf, M.E. & Wassie, M.M. Prevalence and associated factors of anemia among pregnant women of Mekelle town: a cross sectional study. BMC Res Notes 7 , 888 (2014). https://doi.org/10.1186/1756-0500-7-888

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Received : 03 September 2014

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DOI : https://doi.org/10.1186/1756-0500-7-888

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• v.14(2); 2021 Jun

Iron deficiency anaemia in pregnancy: A contemporary review

Charlotte s benson.

1 Department of Obstetrics, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK

Akshay Shah

2 Department of Medicine, University of Oxford, Oxford, UK

3 Nuffield Department of Anaesthesia, John Radcliffe Hospital, Oxford, UK

Matthew C Frise

4 Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK

5 Intensive Care Unit, Royal Berkshire Hospital, NHS Foundation Trust, Reading, UK

Charlotte J Frise

6 Fetal Maternal Medicine Unit, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK

7 Queen Charlotte’s and Chelsea Hospital, Imperial College Healthcare NHS Trust, London, UK

Associated Data

Supplemental material, sj-pdf-1-obm-10.1177_1753495X20932426 for Iron deficiency anaemia in pregnancy: A contemporary review by Charlotte S Benson, Akshay Shah, Matthew C Frise and Charlotte J Frise in Obstetric Medicine

Iron deficiency anaemia is a global health problem, which particularly affects pregnant women. Iron deficiency anaemia during pregnancy is associated with increased maternal and perinatal morbidity and mortality. Maternal iron deficiency may also be associated with neurocognitive deficits in infants. Iron requirements increase during pregnancy and are influenced by hepcidin, the master regulator of iron homeostasis. The enduring global burden of maternal anaemia suggests that currently employed iron supplementation strategies are suboptimal. Recent developments in our understanding of systemic and placental iron homeostasis may improve therapeutic effectiveness by altering the dose and frequency of oral iron. Intravenous iron appears to be a safe treatment to correct maternal anaemia rapidly but research on patient-centred outcomes and cost-effectiveness is needed. Future trials should be adequately powered to assess outcomes relevant to pregnant women.

Introduction

Approximately 1.24 billion people worldwide are affected by iron deficiency anaemia (IDA). 1 It is one of the leading global causes of years lived with disability, particularly affecting women, low–middle social demographic groups and populations of Asia and sub-Saharan Africa. 1 Maternal anaemia is thought to affect 32 million women worldwide. 2 , 3 A large, UK cohort study reported that 46% of women were anaemic at some point during pregnancy. 4 Iron deficiency (ID) is by far the most common cause of maternal anaemia but other causes include haemoglobinopathies, such as sickle-cell anaemia and thalassaemia; deficiencies of folate, B12 or both; hookworm infection; schistosomiasis and HIV infection.

The association between anaemia and poor maternal, fetal and neonatal outcomes is now well established. 5 , 6 Anaemia is increasingly recognised as a potentially modifiable risk factor for postpartum haemorrhage – a leading cause of maternal morbidity and mortality. 7 – 9 Adverse fetal and neonatal outcomes include preterm labour, growth restriction and increased mortality.

This review discusses iron homeostasis and current definitions of IDA in pregnancy, adverse maternal and neonatal outcomes associated with anaemia, and the most recent treatment recommendations for IDA during pregnancy and the postpartum period. Management of other causes of anaemia is beyond the scope of this review and is reviewed elsewhere. 10 – 14

We searched MEDLINE, PubMed, Cochrane Central Register of Controlled Trials, EMBASE and Google Scholar. Titles and abstracts were screened and references of all identified systematic reviews, randomised controlled trials, observational studies, review articles and current treatment guidelines were checked for further relevant literature. The search was restricted to literature from 1 January 2000, but older important publications were not excluded. The end date of the literature search was 12 January 2020. Topics beyond the scope of this review were referenced by relevant narrative reviews, systematic reviews or clinical guidelines where applicable. The literature searches included the following terms: iron; anaemia/anemia; haemoglobin/haemoglobin; outcomes; pregnancy; obstetric; neonatal; fetal/foetal; and parturient. The results are shown in Supplementary Figure 1.

Iron homeostasis during pregnancy

Iron requirements during pregnancy.

Iron is an essential element required by almost all organisms due to the indispensable roles it plays in processes such as DNA synthesis, cell growth and differentiation, immunity, mitochondrial function and responses to hypoxia. 15 – 19 Iron requirements increase approximately 10-fold during pregnancy from 0.8 mg/day in the first trimester to 7.5 mg/day in the third trimester in order to support the increase in maternal red cell mass, sustain placental and fetal growth, and accommodate blood loss during delivery. 20 , 21 The placenta requires around 90 mg of iron in its own right and transports approximately 270 mg of iron to the fetus over the course of a normal pregnancy. 22

The role of hepcidin

Systemic iron homeostasis is controlled by hepcidin – a peptide hormone predominantly produced in the liver and excreted by the kidneys. 16 Hepcidin works by regulating the activity of ferroportin – the sole mammalian iron transport protein. 16 Ferroportin delivers stored, dietary or recycled iron to blood plasma and is expressed at all sites involved in iron–plasma exchange, including the basolateral membrane of duodenal enterocytes, macrophages, hepatocytes and the basal surface of placental syncytiotrophoblasts facing the fetal circulation. 16 , 23 At each of these sites hepcidin causes intracellular degradation of ferroportin, thereby preventing iron export to blood plasma ( Figure 1 ). Changes in hepcidin levels can lead to rapid fluctuations in plasma iron concentrations.

Hepcidin–ferroportin interaction and major systemic iron pathways. Hepcidin expression results in degradation of ferroportin which impairs release of iron from macrophages and duodenal enterocytes. Reduction in hepcidin during pregnancy increases the availability of iron for placental transfer.

Fe-TF: iron-transferrin; FPN: ferroportin; RBC: red blood cell.

Expression of hepcidin is increased in response to inflammation, infection, malignancy and iron overload. 19 Hepcidin-mediated degradation of ferroportin causes iron to remain trapped within macrophages and duodenal enterocytes and therefore unavailable for those tissues that require it. Inhibition of duodenal absorption of iron – known as the ‘hepcidin block’ – may explain why oral iron is ineffective in inflammatory states. Hepcidin expression is reduced in states of ID, anaemia, hypoxaemia and increased erythropoietic drive. 19

In healthy pregnancy, hepcidin increases in the first trimester when compared with the non-pregnant state, but then decreases in the second and third trimesters ( Figure 2 ). 24 , 25 It is presumed that this pattern facilitates increased absorption of dietary iron and release of iron from stores. However, the mechanism underlying maternal hepcidin suppression as pregnancy progresses is still unknown. 22 The development of ID may be the key driver, although low hepcidin concentrations are reported even in women who are iron replete at delivery. 26

Serial changes in serum hepcidin and ferritin concentrations during pregnancy and postpartum. (a) Median (IQR) serum hepcidin concentrations in 31 women during pregnancy and postpartum. ***Compared with first-trimester values, P < 0.0001. (b) Geometric mean ± SEM serum ferritin concentrations during pregnancy in women given oral iron supplementation (filled circles; n = 63) compared with controls (open circles; n = 57).

Source: Reproduced with permission from van Santen et al. 25

Placental and fetal iron homeostasis

The majority of iron transfer to the fetus occurs during the third trimester, which coincides with the period of lowest hepcidin expression. 22 This transfer is unidirectional. Iron is bound to transferrin in the maternal circulation and is taken up by transferrin receptor 1 located on the apical membrane of the syncytiotrophoblast. 22 This complex is then endocytosed and eventually exported to the basal surface of the syncytiotrophoblasts where, through ferroportin, iron enters the fetal circulation. 21 , 22 Relatively little is known about fetal hepcidin and the responses of the maternal–placental–fetal unit to changes in maternal iron status. A recent study evaluating mechanisms in murine and in vitro trophoblastic models of severe ID observed an unexpected response that prioritised placental iron retention over fetal iron transfer. 23 This response may have an evolutionary benefit to protect iron-dependent placental processes, and may provide overall benefit for the fetus despite diminishing fetal iron availability. This work also suggests that the fetus may be unable to compensate for maternal ID by increasing placental iron transfer. 23 Further studies are required to clarify the significance of these findings.

Changes in other markers of iron status during pregnancy

Concentrations of serum ferritin and iron, along with transferrin saturation, gradually fall to a nadir in the third trimester. 22 , 24 The decrease is less marked in pregnant women receiving iron supplementation. 22 However, since ferritin is an acute phase protein, and transferrin a negative acute phase protein, these parameters become unreliable as indices of iron status in pregnancies complicated by inflammatory pathologies. 16

Defining IDA in pregnant women

IDA is a composite diagnosis based on haemoglobin (Hb) and ferritin concentrations. The World Health Organisation (WHO) has defined anaemia in pregnancy as a Hb concentration less than 110 g/L irrespective of trimester, but recognises that Hb may fall physiologically by around 5 g/L during the second trimester. 27 This is due to a rise in plasma volume of ∼50%, disproportionate to the concomitant ∼25% rise seen in red cell mass. 28 , 29

The WHO definition has been questioned as it is derived from studies conducted in the 1950s and 1960s that did not include pregnant women and used now superseded methods for measuring Hb. Recent evidence has also questioned the validity of the figure of 5 g/L for the physiological fall in Hb during the second trimester. A large, multi-ethnic, observational study of 7054 pregnant women found that the fall in Hb was in the order of 14 g/L, or 11% of the first trimester value. 27 Such findings have significant implications for the diagnosis and management of maternal anaemia. 30 , 31 The use of a lower Hb threshold compared with men for the diagnosis of anaemia in non-pregnant women has been recently challenged, 32 and guidelines now recommend targeting an Hb > 130 g/L in patients undergoing major surgery, irrespective of sex. 33

The most recent British Committee for Standards in Haematology (BCSH) guidelines on the management of ID have defined anaemia as Hb less than 110 g/L in the first trimester, less than 105 g/L in the second and third trimesters, and less than 100 g/L in the immediate postpartum period. 34 It is recommended that Hb routinely be measured at the initial booking consultation with a healthcare professional in the first trimester and at around 28 weeks’ gestation. Although not supported by high-quality evidence, these timepoints were felt to be practically feasible.

Most stored iron is located in the liver, bound to the iron storage protein ferritin. The most common test of iron status, serum ferritin, provides a convenient measure of storage iron. Current BCSH guidelines recommend using a ferritin of less than 30 µg/L to diagnose ID in pregnancy, but this is not unified globally. 34 , 35 The ferritin threshold of 30 µg/L is derived from two studies published in the 1990s that compared serum ferritin with histochemical assessments of bone marrow iron stores. 36 , 37 These studies had limitations including small sample sizes and inclusion of women with possible coexisting inflammatory conditions. As already mentioned, ferritin is an acute phase protein. Ferritin may even be elevated as a result of pregnancy itself, so while a low ferritin almost invariably indicates ID, a normal ferritin cannot reliably be used to exclude it. To date, no high-quality studies have been undertaken to investigate pregnancy-specific ferritin thresholds.

Most experience with other biomarkers of iron status such as transferrin saturation, soluble transferrin receptor, reticulocyte Hb content, mean cell Hb concentration and hepcidin comes from non-pregnant populations; experience in pregnancy is largely limited to research purposes. 38 – 41

Non-anaemic iron deficiency

Anaemia is the final manifestation of ID as erythropoiesis is often preserved until the advanced stages of ID. 42 Therefore, much of the burden of ID in pregnant women will go unnoticed if the absence of anaemia is taken to imply adequate iron stores. Non-anaemic iron deficiency (NAID) is increasingly being recognised as a disease but the clinical relevance in pregnancy is unclear. 42 A recent study of 102 non-anaemic pregnant women found that 42% had evidence of ID as determined by a ferritin less than 30 µg/L or transferrin saturation less than 20%, but data on maternal and fetal outcomes were lacking. 43

A recent systematic review of iron supplementation in healthy non-pregnant women suffering from NAID showed lower levels of subjective fatigue in participants who received iron. 44 However, there were no improvements in objective measures of physical capacity such as time trials, time to exhaustion tests or maximal oxygen consumption. Furthermore, the overall quality of evidence was judged to be low to moderate. Small exploratory studies in patients undergoing elective colorectal and cardiac surgery have suggested worse postoperative outcomes in patients with NAID when compared with iron-replete individuals. 45 , 46

Relying on the presence of anaemia to prompt assessment of iron status may result in large numbers of pregnant women with ID being missed. Further research into the diagnosis of NAID and its impact on maternal and fetal outcomes is needed. Routine screening of pregnant women using serum ferritin has been suggested; however, cost implications and lack of well-designed prospective studies to support this approach mean that a more targeted approach of identifying and treating at-risk pregnant women is currently recommended. 34

Outcomes associated with maternal anaemia

Maternal outcomes.

The clinical signs and symptoms of IDA include fatigue, pallor, angular cheilitis, weakness, palpitations, shortness of breath, restless legs, pica syndrome, irritability and poor concentration. These may also be present in NAID.

Observational studies 47 , 48 have demonstrated an association between maternal anaemia and mortality, with one study demonstrating a 29% linear increase in maternal mortality with each 10 g/L decrease in maternal Hb. 48 A recent study reported that severe anaemia, defined as Hb < 70 g/L during pregnancy or postpartum, doubled the risk of death. 49 Of particular concern, maternal anaemia – with or without ID – increases the risk of developing postpartum haemorrhage. 7 , 50 A large, two-centre, UK study, involving 10,213 women, found that 62% of women with Hb < 85 g/L developed postpartum haemorrhage, and 26% progressed to develop severe (greater than 1500 mL) postpartum haemorrhage. 51

It is important to note that the majority of these data come from low- and middle-income countries. 48 , 49 The timing of Hb measurement is not always clear and therefore it is difficult to determine whether postpartum haemorrhage led to severe anaemia, or whether severe anaemia during pregnancy increased the risk of postpartum haemorrhage. In addition, despite attempts to control for multiple confounders such as haemorrhage, sepsis and critical care admission, it is possible that a weaker association between anaemia and poor maternal outcomes exists than is initially suggested by such data.

Postpartum anaemia has been linked to depression, 52 – 54 fatigue, 55 impaired cognition, 56 impaired lactation and early cessation of breast feeding. 57 , 58 Trials of postpartum iron therapy have demonstrated improvements in Hb and serum ferritin concentration but data on patient-centred outcomes are lacking. 59

Fetal and neonatal outcomes

Maternal IDA is a recognised risk factor for preterm labour, low birthweight and small-for-gestational age (SGA) babies. 5 , 7 , 60 , 61 The Baby’s Vascular health and Iron in Pregnancy (BABY VIP) study showed that maternal ID in the first trimester was associated with a two-fold increase risk of having a fetus with SGA. Every 10 g/L decrease in maternal Hb before 20 weeks’ gestation was associated with a 30% increase in the relative risk (RR) of SGA. 61 A systematic review of 48 randomised controlled trials (a total of 17,793 women) and 44 cohort studies (a total of 1,851,682 women) found that iron supplementation resulted in a modest increase in birthweight (weighted mean difference (WMD) 41–69 g) with a small reduction in the risk of delivering a low birthweight infant. 60 There was no evidence of an effect on gestation length, preterm birth or SGA infants.

Maternal anaemia is also associated with increased perinatal and neonatal mortality. 4 , 7 A large, multi-ethnic, UK observational cohort study which evaluated over 14,000 pregnant women, found that women with Hb < 100 g/L had a three-fold increased risk of perinatal death and a five-fold increased risk of stillbirth when compared with women who had Hb > 110 g/L. 4 The authors controlled for multiple confounders including advanced maternal age, ethnicity, body mass index, smoking status and a range of medical comorbidities.

There is increasing interest in the impact of maternal ID on the neonatal brain and cognitive development. 62 Fetal brain growth accelerates rapidly in the last trimester and continues for the first 2 years after birth, 63 by the end of which total brain volume reaches 80%–90% of adult volume. 64 The iron-dependent processes occurring during this period include monoamine neurotransmission, myelination and hippocampal development. 65 ID has been shown to alter expression of genes critical for hippocampal development and function. 66 Infants with evidence of ID in utero have been demonstrated to have abnormal neural maturation, poor memory, altered interactions with caregivers and an increased incidence of abnormal neurological reflexes. 65 , 67 Low ferritin levels in utero have also been linked with lower IQ, worse language ability and poorer tractability at up to 5 years of age. 68 Studies addressing the effects of iron supplementation have yielded mixed results. In one study in Nepal, prenatal iron supplementation for women at high risk of developing ID resulted in improved intellectual and fine motor functioning in subsequent children aged 7–9 years. 69 However, in other studies, the effects of iron supplementation on children whose mothers have established ID have been less clear, 70 implying that timing of the intervention is critical; earlier supplementation during the antenatal period may be necessary for a beneficial effect on the developing brain. Future maternal intervention trials should incorporate neurodevelopmental outcomes of offspring.

Treatment strategies

The recommendations from the most recent BCSH guidelines 34 are summarised in Table 1 . Guidelines from other countries make broadly similar recommendations, with some modifications tailored towards their respective population. 71 – 73

Summary of key recommendations from the 2019 UK guidelines on the management of iron deficiency anaemia.

Hb: haemoglobin.

A careful history is required to identify women at risk of developing ID with or without anaemia ( Table 2 ). All women should be offered dietary advice, though this is invariably insufficient to correct established ID. Dietary iron is absorbed in two forms – non-haem (inorganic) iron and haem-bound iron. Non-haem iron exists predominantly in the oxidised ferric (Fe 3 + ) form and needs to be reduced to the ferrous (Fe 2 + ) form in order to be absorbed efficiently. 34

Risk factors for developing iron deficiency anaemia during pregnancy.

Meat, fish and poultry are rich sources of haem iron, which is absorbed much more readily than non-haem iron. Non-haem iron is predominantly derived from plant-based foods, where it is complexed in insoluble forms, which significantly contributes to the high prevalence of ID observed in societies that consume vegetarian diets. Iron absorption is inhibited by tannins in tea and coffee, and phytate, a substance found in cereals and legumes. Co-ingestion of vitamin C (ascorbic acid) significantly increases iron uptake from non-haem sources. 74

Oral iron is an effective, cheap and safe way to treat ID. The large systematic review discussed earlier found that prenatal iron increased maternal Hb by a mean of 46 g/L (95% Confidence Interval (CI): 37–55 g/L), with concomitant reductions in the RR of developing (1) anaemia (RR 0.50; 95% CI: 0.42–0.59); (2) ID (RR 0.59; 95% CI: 0.46–0.79) and (3) iron-deficiency anaemia (RR 0.40; 95% CI: 0.26–0.60). 60

Current pregnancy guidelines recommend 40–80 mg of elemental oral iron once daily each morning, 34 which differs from previous guidance recommending 100–200 mg daily. 74 The WHO recommendations on antenatal care for a positive pregnancy experience recommend 30–60 mg of oral iron once daily or intermittent doses of 120 mg if daily iron is not acceptable due to side effects. 75 , 76 These recommendations have largely been driven by recent advances in our understanding of iron homeostasis. Studies in non-pregnant women have shown that a once daily or alternate day dosing strategy may be more effective and better tolerated by women compared with the traditional higher total daily doses. 77 , 78 Oral ingestion of a single dose of ferrous sulphate results in a rapid rise in circulating hepcidin, which can take up to 48 h to return to normal. 77 Subsequent oral doses may not be absorbed during this period because of this ‘hepcidin block’, and may expose women to well-recognised gastrointestinal side effects such as nausea, constipation and epigastric pain. A recent meta-analysis reported an incidence of up to 70% associated with oral iron. 79 Since hepcidin levels are also lowest in the morning, dosing at this time is advised. 80

Ferrous salts such as ferrous sulphate, ferrous fumarate and ferrous gluconate ( Table 3 ) are preferable to ferric salts due to better oral bioavailability but differ with respect to available elemental iron. Multivitamins and ‘off the shelf’ preparations are not recommended as they contain insufficient amounts of iron and may include other substances, particularly calcium, that impair iron absorption. Slow release and enteric-coated formulations are undesirable as the majority of iron in these preparations is carried past the duodenum and therefore not absorbed. 81

Characteristics of different oral iron formulations.

BNF: British National Formulary; NHS: UK National Health Service.

Once commenced on oral iron, Hb should be measured after 2–3 weeks to assess response. Once Hb has normalised, replacement should continue for three further months, and, if near term, up to 6 weeks postpartum. 34 If the response is poor, compliance should be explored. Other causes for failure to respond to oral therapy include iron sequestration driven by elevated hepcidin as a result of inflammation or infection; ongoing blood loss and other causes of anaemia such as folate deficiency.

Intravenous iron

Intravenous iron is efficacious in replenishing iron stores and treating anaemia in a wide range of clinical situations with or without the presence of inflammation. 82 , 83 Intravenous iron should be considered from the second trimester for women with confirmed IDA who do not respond to, or who fail to tolerate, oral iron. Given the proximity to delivery, it should also be considered for women presenting after 34 weeks’ gestation with Hb < 100 g/L and confirmed ID. 34

Recent systematic reviews have shown intravenous iron to be more effective at improving maternal Hb (WMD 6.6 g/L; 95% CI: 3.1–10.1 g/L) and ferritin (WMD 45.6 µg/L; 95% CI: 26.21–65.16 µg/L) at delivery when compared with oral iron supplementation; intravenous therapy is also associated with fewer mild medication reactions than oral treatment (RR 0.34; 95% CI: 0.20–0.57). 84 , 85 Intravenous iron is also associated with higher neonatal birthweight (WMD 58 g; 95% CI: 6–111 g). However, there was no evidence of an effect of intravenous iron to reduce maternal blood transfusion requirements or improve neonatal Hb. It is worth noting that the majority of the studies included in these systematic reviews were small and of low methodological quality, as evidenced by the wide confidence intervals. There was also heterogeneity with regards to the timing and dosage of iron supplementation and a lack of reporting of maternal and neonatal-centred outcomes.

Four intravenous iron preparations are currently available in the UK. The properties of these are summarised in Table 4 .Newer iron preparations such as ferric carboxymaltose (Ferinject®) and iron isomaltoside (Monofer®) form stable carbohydrate complexes that permit controlled delivery of iron to the reticuloendothelial system (liver macrophages, spleen and bone marrow). 86 , 87 Iron is subsequently delivered in a slow and controlled manner to iron binding proteins such as ferritin. These mechanisms limit the amount of freely available and potentially toxic unbound iron circulating in the bloodstream, while also bypassing the ‘hepcidin block’ in inflammatory states. 87

Characteristics of different intravenous iron formulations available in the UK.

Newer preparations also enable delivery of higher doses of iron over short time frames, typically 15–20 min ( Table 4 ) and are increasingly being offered in an outpatient setting. True anaphylaxis and severe hypersensitivity reactions are rare with these modern intravenous iron preprations, 88 , 89 but facilities and staff trained in the management of anaphylaxis should be present. Common side effects include nausea, headaches, dizziness, hypertension, flushing and injection/infusion site reactions. These are managed by slowing the infusion rate and providing symptomatic care, such as antiemetics. Transient hypophosphataemia has been reported in several studies, and this may be more pronounced in pregnant compared with non-pregnant women. 90 , 91 Whether this hypophosphataemia has any clinically relevant consequences is uncertain. Permanent haemosiderin skin pigmentation has been reported from extravasation, 92 and women should therefore be advised to report any pain at the infusion site. An increased risk of infection was a concern with older intravenous iron preparations, driven by the availability of unbound circulating iron for invading bacterial pathogens. Recent systematic reviews, which have included critically ill patients at high risk of sepsis, have demonstrated no increased risk of bacterial infection. 93 , 94

Intravenous iron preparations are considerably more expensive than oral iron, even without including the costs of administration such as infusion kits and staff time. Although trials have reported costs of treatment, no formal cost-effectiveness analysis has been undertaken comparing intravenous iron with oral iron in pregnant women. Given the improved effectiveness and favourable side-effect profile of newer intravenous iron preparations discussed above, it remains possible that the overall economic cost might favour intravenous therapy in this setting.

During labour and postpartum

Women who enter labour with IDA are at increased risk of postpartum haemorrhage and have lower iron stores in reserve to support compensatory erythropoiesis following significant blood loss. Mode of delivery should be determined by obstetric indications but appropriate intravenous access, availability of a group and screen, birth in an obstetrician-led unit and active management of the third stage of labour should be considered. 34

Appropriate management of IDA in the antenatal period reduces the likelihood of developing postpartum anaemia. Current guidelines recommend measuring Hb within 48 h of delivery in women with uncorrected anaemia in the antenatal period, blood loss of over 500 mL, or signs and symptoms suggestive of anaemia. Oral iron may be sufficient in women without active bleeding and asymptomatic or mildly symptomatic anaemia. The recommended daily dose is 40–80 mg of elemental iron for 3 months. 34

Women requiring urgent correction of symptomatic anaemia, or those who are intolerant of oral iron, should be offered intravenous iron. A recent systematic review demonstrated a mean improvement of 9 g/L (95% CI: 4–13 g/L) at 6 weeks postpartum in women who received intravenous iron compared with oral iron. 59 The reported rate of anaphylaxis in women receiving intravenous iron was 0.6%. Low-quality evidence suggests that intravenous iron may lower fatigue and depression scores at up to 12 weeks postpartum. 95 There is a need for well-designed, adequately powered, randomised controlled trails.

Allogeneic red blood cell transfusion should be reserved for women with severe active bleeding, imminent cardiac compromise or symptoms of anaemia requiring urgent attention. Women should be fully consented regarding the potential risks of transfusion, 96 including being unable to donate blood in the future, and potential alternative treatments.

Conclusion and directions for future research

ID remains the most common cause of maternal anaemia worldwide, with detrimental consequences for both mother and baby. Large-scale epidemiological studies have demonstrated that antenatal anaemia is a risk factor for maternal mortality, perinatal mortality, preterm labour, low birthweight infants and postpartum haemorrhage. Maternal ID may also be associated with poor infant neurodevelopmental outcomes. Postpartum anaemia is linked with lactation failure and low maternal quality of life scores.

The WHO aims to reduce the prevalence of anaemia in women of reproductive age by 50% between 2010 and 2025. 6 Currently, interventions such as oral or intravenous iron do not appear to be working at the scale required to meet the WHO aims. This may be partly due to uncertainty regarding how best to investigate, prevent and treat maternal anaemia. Importantly, few trials so far have reported maternal and neonatal-centred outcomes; the vast majority have instead focused on haematological parameters. Despite this limitation being highlighted in a systematic review in 2012, 97 little progress appears to have been made since. Advances in our understanding of iron physiology have led to the potential for considerable improvement by altering the dosing strategy for oral iron. Newer laboratory indices of iron status such as hepcidin may ultimately help to guide iron therapy, but a recent study found no benefit of using a hepcidin-guided screen-and-treat approach when compared with the WHO’s recommended regimen. 98

Over a 5-year period, the Primary prevention of maternal ANaemia to avoid preterm Delivery and other Adverse outcomes (PANDA) 99 research programme, recently funded by the National Institute for Health Research (NIHR), will attempt to address some of the research uncertainties highlighted in this review. Initial work will include identifying barriers and enablers to iron supplementation, development of a behavioural intervention to promote compliance and a feasibility randomised controlled trial to identify the optimal dosing schedule for oral iron. This will be followed by a larger, two-arm, multicentre trial of oral-iron supplementation versus placebo which will aim to enrol 11,020 pregnant women across 20 maternity units. The primary outcome is a composite of preterm birth, still birth, neonatal death and SGA infants. Long-term maternal and infant neurodevelopmental outcomes will also be evaluated. Future research is also needed to identify effective screening strategies during the antenatal and postnatal periods; determining the optimal dose of oral iron treatments; developing core outcome sets; and exploring the utility of universal iron supplementation to prevent maternal IDA.

Supplemental Material

Declaration of conflicting interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: AS is currently being supported by an NIHR Doctoral Research Fellowship (DRF-2017–10-094).

Ethical approval: Not applicable.

Informed consent: Not applicable.

Guarantor: CSB is the guarantor of the present work.

Contributorship: CJF and MCF conceived the idea for the review. The literature searches, drafting and editing of all article versions were undertaken by CB and AS. All authors have contributed to, reviewed and approved the final version of the draft.

Charlotte S Benson https://orcid.org/0000-0002-3900-1049

Matthew C Frise https://orcid.org/0000-0001-5575-2531

• Research article
• Open access
• Published: 11 December 2019

Prevalence and determinants of anaemia in pregnant women receiving antenatal care at a tertiary referral hospital in Northern Ghana

• Anthony Wemakor   ORCID: orcid.org/0000-0003-0399-8913 1  

BMC Pregnancy and Childbirth volume  19 , Article number:  495 ( 2019 ) Cite this article

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Anaemia during pregnancy is a major public health problem in developing countries. It is important to regularly monitor haemoglobin level in pregnancy and factors associated with it to inform clinical and preventive services. The aim of this study was to assess the prevalence and determinants of anaemia in pregnant women attending antenatal clinic (ANC) of a tertiary referral hospital in Northern Ghana.

An analytical cross-sectional study involving 400 pregnant women receiving antenatal care in Tamale Teaching Hospital was conducted. Using a semi-structured questionnaire and 24-h dietary recall, data were collected on socio-demographic characteristics, health practices, dietary diversity, anaemia knowledge and haemoglobin level of the women. Anaemia was defined as haemoglobin concentration less than 11 g/dl. Chi-square test and logistic regression analysis were used to identify the independent determinants of pregnancy anaemia.

The mean age and haemoglobin of the women were 28.3 (±4.5) years and 10.81 (±1.41) g/dl respectively. About half of the women 50.8% [95% Confidence Interval (CI): 45.8–55.7] were anaemic and the prevalence of anaemia increased with pregnancy trimester. Among a host of socio-demographic, dietary, and preventive health service factors evaluated, the women’s knowledge on anaemia and pregnancy trimester at interview were the independent determinants of anaemia in pregnancy. Compared to women of the highest anaemia knowledge tertile, women belonging to the lowest (AOR = 2.63, 95% CI: 1.50–4.61) and middle (AOR = 1.92, 95% CI: 1.12–3.27) anaemia knowledge tertiles were about 3 and 2 times more likely to be anaemic respectively. Similarly, women in third trimester of pregnancy were about 4 times more likely to be anaemic compared to those in first trimester at the time of interview (AOR = 3.57, 95% CI: 1.91–6.67).

Conclusions

There is a high prevalence of anaemia, which increases with pregnancy trimester, in pregnant women attending ANC in a tertiary referral hospital in Northern Ghana. The women’s knowledge on anaemia and pregnancy trimester at the time of interview are associated with their anaemia status. The high prevalence of anaemia in pregnancy needs urgent intervention to prevent the occurrence of adverse maternal and neonatal outcomes. Education on anaemia should be intensified at ANCs.

Peer Review reports

Anaemia in pregnancy is defined as haemoglobin concentration less than 11.0 g/dl [ 1 ]. Globally, anaemia affects half a billion women of reproductive age. In 2011, 29% of non-pregnant women, and 38% of pregnant women aged 15–49 years were anaemic worldwide but the prevalence was highest in South Asia and Central and West Africa [ 2 ]. In Ghana, 45% of pregnant women were anaemic in 2014 [ 3 ].

Anaemia impairs the capacity of blood to transport oxygen around the body and is an indicator of poor nutrition and health [ 4 ]. Anaemia in pregnancy is a major public health issue throughout the world, particularly in the developing countries where it is an important contributor to maternal morbidity and mortality [ 5 ]. It is also associated with increased risk of miscarriage [ 6 ], prematurity, stillbirth, low birth weight and consequently perinatal mortality [ 7 ].

The main cause of anaemia in women of reproductive age globally is iron deficiency, resulting from prolonged negative iron balance, which accounts for 50% of anaemia in women worldwide [ 2 ]. The negative iron balance may be due to inadequate dietary iron intake or absorption, increased needs for iron during pregnancy, and increased iron losses as a result of menstruation, worm infestation and infections [ 8 ]. Some genetic and socio-demographic and economic characteristics of women also influence the distribution of anaemia [ 9 ] and should be taken into consideration in designing preventive interventions for pregnancy anaemia. The World Health Organisation (WHO) recommends intermittent iron and folic acid supplementation for menstruating women living in settings where the prevalence of anaemia is 20% or higher and daily iron and folic acid supplementation for pregnant women as part of antenatal care in order to prevent anaemia in pregnancy [ 1 ].

The WHO recommended focused antenatal care approach to antenatal clinic (ANC), which involves client- centered individualized care, disease detection and care by a skilled provider, is implemented in Ghana [ 10 ]. In Ghana, all pregnant women are expected to have their haemoglobin measured at first ANC attendance, 28 weeks gestation and 36 weeks gestation to identify and manage anaemia. It is important to assess haemoglobin level of pregnant women and its determinants regularly to inform treatment and preventive services. The objective of this study was to assess the prevalence and determinants of anaemia in pregnant women receiving antenatal care at Tamale Teaching Hospital, a tertiary referral facility in Northern Ghana.

Study design, site, population and subjects

An analytical cross-sectional study involving pregnant women attending ANC of Tamale Teaching Hospital, Northern Region, Ghana, was carried out during February–April, 2016. The Tamale Teaching Hospital is a tertiary level referral hospital for the 4 northern regions i.e., Northern, Savanna, Upper East and Upper West regions. It is located at the north-eastern part of Tamale along the main Tamale-Yendi road in the Tamale South Constituency. The ANC is ran by the maternity department of the hospital. The average daily attendance to the ANC is about 100 women.

Tamale Metropolitan District is located in Northern Region, and has Tamale as its capital. The metropolis has a population size of 371,351 with 274,373 being women and an annual expected number of pregnancies of 4,292 [ 11 ]. The people of Tamale Metropolis predominantly belong to the Dagomba tribe; but other minority tribes like Gonja, Konkomba, and Dagarti can also be found in the Metropolis. The main religion of the Metropolis is Islam but a considerable number of people also practice Christian or Traditional African Religion. The Dagombas practise patrilineal lineage system and most men are polygamous.

Pregnant women in Tamale who attended ANC in Tamale Teaching Hospital were the target population of this study.

Sample size and sampling technique

Sample size was determined using single population proportion formula of Snedecor and Cochran [ 12 ]. Using a margin of error (0.05), critical value at 95% confidence level (1.96), and prevalence of anaemia in pregnancy (45.0%) [ 3 ], a minimum sample of 380 was estimated. The minimum sample size was increased to 400. About 100 pregnant women attended ANC daily but on each day about 30 pregnant women were sampled using systematic random sampling for 14 days spread over the 3-month study period. For each day a sampling interval of 3 was used. This was obtained by dividing the expected number of women 100 per day by the daily sampling size of 30. One of the numbers 1, 2, and 3 was randomly picked to serve as a starting point and the sampling interval was added to select the next participant until the required number for the day was achieved.

Data collection

A semi-structured questionnaire and 24-h dietary recall [ 13 ] were used to collect the data. The semi-structured questionnaire included sections on socio-demographic characteristics, health practices during pregnancy, dietary practices, knowledge on anaemia in pregnancy and haemoglobin level (Additional file 1 ). The questionnaire was administered in face-to-face interviews with the women at the ANC.

Seven (7) statements on general nutrition and anaemia were read to the women and they were to indicate whether each statement was true or false. The statements were based on what pregnant women were taught on iron deficiency and anaemia at ANCs in Ghana and were put together by a team of ANC nurses. The statements are: 1. It is very important to eat a variety of foods during pregnancy 2. Good nutrition before conception is not necessary 3. Eating fruits and vegetables ( e.g. banana and cocoyam leaves) during pregnancy increases the risk of anaemia 4. Iron/folic acid supplements given during ANC are detrimental to blood production in pregnancy 5. Blood loss during pregnancy is normal and hence cannot contribute to anaemia 6. Treating infections ( e.g. malaria) during pregnancy can reduce the risk of anaemia 7. It is advisable for women that are pregnant to stop eating animal source foods ( e.g. poultry, fish).

The most recent results of laboratory tests for haemoglobin, malaria and worm infestation were extracted from the pregnant women’s ANC booklets.

In the 24-h dietary recall, the pregnant women were asked to recall the foods they had consumed in the previous 24 h, first spontaneously then followed by probes to ensure that no meal or snack consumed was left out. The women were then asked to mention all the ingredients of the dishes and snacks they consumed. Using this information, it was indicated whether they ate from the following 10 food groups or not: 1. Grains, white roots and tubers, and plantains, 2. Pulses (beans, peas and lentils), 3. Nuts and seeds, 4. Dairy, 5. Meat, poultry and fish, 6. Eggs, 7. Dark green leafy vegetables, 8. Other vitamin A-rich fruits and vegetables, 9. Other vegetables, and 10. Other fruits [ 13 ].

Study variables

Anaemia was defined at haemoglobin concentration less than 11.0 g/dl [ 4 ]. Anaemia was further divided into mild (haemoglobin = 10.0–10.9 g/dl), moderate (haemoglobin = 7.0–9.9 g/dl) and severe (haemoglobin < 7.0 g/dl) categories [ 4 ].

Minimum dietary diversity - women (MDD-W)

Using data from the 24-h dietary recall, dietary diversity score was calculated. For each food group the women ate from they got a score of “1” otherwise a score of “0”. A count of the number of scores was made to give the dietary diversity score [ 13 ]. Irrespective of the number of foods eaten from one food group, a score of “1” was given and the total score theoretically ranged from 0 to 10. Using the dietary diversity score, MDD-W was derived. MDD-W is an indicator variable on whether a woman has eaten from 5 or more food groups out of 10 designated food groups within the last 24 h, i.e., a dietary diversity score of 5 or more. MDD-W is a measure of adequacy of micronutrient (including iron) intake among women of reproductive age i.e., women who meet the criterion for MDD-W are less likely to be micronutrient deficient [ 13 ].

Iron-rich food group

Given that the main variable of interest was anaemia, the iron-rich food group: flesh foods containing organ meat; flesh meat and fish; and sea food, among the 10 food groups was isolated and its association with anaemia was examined.

Household wealth index

A household wealth index based on possession of 14 household items was derived. This is based on an earlier concept whereby the sum of dummy variables obtained from data on housing quality, availability of electricity, water and toilet to the household, and ownership of household durable goods (e.g. bicycle, television, radio) and possession of livestock were used to construct a household wealth index [ 14 ]. The 14 household items include mattress, TV, satellite dish, animal-drawn cart, mobile phone, radio, sewing machine, car, bicycle, motor bike, computer, electric fan, DVD player and refrigerator. Following exploratory analysis, the percentages of households with mattress, electric fan and mobile phone were above 95% and that of households with animal drawn cart was below 5% so these items were excluded from further analysis. A wealth score was generated for each household using the remaining 10 household items with principal component analysis and the scores for all the households were ordered and divided into 3 categories (tertiles): - lowest, middle and highest.

Anaemia knowledge index

Based on the responses to the seven statements on anaemia, a pregnant woman scored “1” when she correctly identified a “true” or “false” statement otherwise “0”. A count of the scores was made to give the total score which could range from 0 to 7 depending on the number of correct answers given by the woman. The total scores were ranked and divided into tertiles i.e., lowest, middle and highest.

Quality assurance

The questionnaire was first prepared in English, translated into Dagbani and then back translated into English to ensure consistency and accuracy of translation. The questionnaire was also pre-tested on pregnant women seeking antenatal care from another hospital and inconsistencies identified were corrected. A 3-day training was given to data collectors during which they practiced how to ask the questions both in Dagbani and English. Data were collected by 3 final year students of the Department of Nutritional Sciences, University for Development Studies, Tamale. The completed questionnaires were checked for completeness on a daily basis on site and questions that were not answered were answered.

Data entry and analysis

The data were entered into SPSS then transferred into Stata (version 12) for analysis. Descriptive statistics were computed: frequency and percentage for categorical data, and mean and standard deviation for continuous data. Bivariate and multivariate analyses were employed to identify factors associated with anaemia. Factors that were significant in bivariate analyses with Chi-square or Fisher’s exact test were entered into a multivariate logistic regression model to identify the independent determinants of anaemia in pregnancy. In all statistical tests, a probability value ( p -value) less than 0.05 was considered statistically significant.

Ethical consideration

The study received ethics permission from the Joint Ethics Committee of the School of Medicine and Health Sciences and School of Allied Health Sciences, University for Development Studies, Tamale. Written informed consent was obtained from the respondents and they were assured that the information they would provide would be kept confidential and used only for the purposes of the study.

Socio-demographic characteristics of respondents

The age of the women ranged from 18 to 41 years with a mean of 28.3 (±4.5) years. Most of the women were in the age group 25–29 years (40.0%), were traders (39.0%), had secondary education (34.5%), and belonged to the middle household wealth index tertile (36.3%) (Table  1 ). A greater majority of the respondents were married (92.0%), and the majority practiced Islamic religion (61.8%).

Health status and practices in pregnancy

At the time of interview, 16.3, 41.3 and 42.5% of the women were in first, second and third trimesters of pregnancy respectively, Table  2 . About two-thirds of the women (71.0%) initiated ANC in the first trimester. About a third (35.7%) and 9.5% of the women had malaria and worm infestation respectively at one time during the pregnancy, while 2.7% were infected with HIV. Consequently, 25.7 and 9.4% used antimalarial and anti-helminthic drugs during the pregnancy. About a quarter of the women (24.3%) used insecticide treated bed net while a greater majority (98.3%) had used a multivitamin drug containing iron and folic acid. The anaemia knowledge of about a quarter of the women (24.5%) was classified into the highest tertile.

Dietary and pica practices

All respondents ate foods from starchy staples (100.0%) whiles only about a fifth ate foods made from eggs (22.8%) (Table  3 ). A greater majority of the respondents ate flesh foods or foods considered to be rich sources of iron (i.e., meat, poultry, fish) (94.5%) and other vegetables (96.8%) but less than half ate from pulses (beans, peas and lentils) group (43.8%), diary (35.3%), dark green leafy vegetables (44.5%), other vitamin A-rich fruits and vegetables (36.8%) and other fruits (32.8%). However most of the respondents (80.3%) were meeting the minimum dietary diversity of consuming foods from at least five of the ten food groups.

Eighty-six women practiced some form of pica and 81 of these women started the practice in the first trimester (Table  4 ). The pica practices involved chewing the following: stick/wooden sponge, cola nuts, clay, chalk and “pepsodent” tooth paste. The main reasons for practicing pica were to prevent nausea and vomiting. Tea/coffee intake was high (75.3%) among the respondents and among those who reported intake, 47.5% took it sometimes and 44.2% took it once a day. The majority (95.8%) of the respondents were not taking any alcoholic beverage during their pregnancy.

Prevalence of anaemia

The haemoglobin measurements were carried out for most of the women in the second trimester (44.3%), followed by 35.8% in first trimester and 20.0% in third trimester. The mean haemoglobin for the women was 10.81 (±1.41) g/dl and the overall prevalence of anaemia (haemoglobin less than 11.0 g/dl) was 50.8% [95% Confidence Interval (CI): 45.8–55.7]. With respect to the severity of anaemia, 25% each was mildly and moderately anaemic and one woman was severely anaemic. The proportion of anaemic women increased as the pregnancy progressed, with 32.2% in first trimester, 53.7% in second trimester and 77.5% in third trimester.

Determinants of anaemia

Socio-demographic, socio-economic and anaemia knowledge index of the pregnant women were compared with anaemia status. In the bivariate analyses, pregnancy trimester at interview ( p  < 0.001), religion practiced ( p  = 0.009), household wealth index ( p  = 0.043), trimester of ANC initiation ( p  = 0.010), and anaemia knowledge index ( p  = 0.001) were significant (Table  5 ). A multivariate analysis including the significant factors in bivariate analyses found the women’s anaemia knowledge index and trimester of pregnancy at the time of interview statistically significant (Table  6 ). Compared to women of the highest anaemia knowledge tertile, women belonging to the lowest (AOR = 2.63, 95% CI: 1.50–4.61, p  = 0.001) and medium (AOR = 1.92, 95% CI: 1.12–3.27, p  = 0.017) anaemia knowledge tertiles were about 3 and 2 times more likely to be anaemic respectively. Similarly, women in third trimester were about 4 times more likely to be anaemic compared to those in first trimester at the time of interview (AOR = 3.57, 95% CI: 1.91–6.67, p  < 0.001).

The prevalence of anaemia and its determinants in pregnant women attending ANC at a tertiary referral hospital in Northern Ghana were assessed. A high prevalence of anaemia of 50.8% was found among the pregnant women which increased with pregnancy trimester. Following bivariate and multivariate analyses of potential determinants of anaemia, the women’s knowledge on anaemia and pregnancy trimester at interview were identified as the only independent determinants of anaemia.

Most of the study women started ANC visit in the first trimester but the use of insecticide treated bed net was low and consequently a third of them had malaria. Malaria in pregnancy is associated with poor maternal and child health outcomes such as intrauterine growth retardation, preterm birth, low birth weight, and maternal anaemia [ 15 ]. To reduce the prevalence of malaria in pregnancy in Ghana, the intermittent preventive treatment of malaria in pregnancy with sulfadoxine-pyrimethamine is to be implemented in all facilities where antenatal care services are provided. However, the level of malaria prevalence measured suggests low sulfadoxine-pyrimethamine uptake among the subjects although that was not assessed in the current study. A fifth of the women practised some form of pica, which has been associated with iron deficiency and anaemia [ 16 ], starting from the beginning of the pregnancy. This involved the ingestion of non-food items such as chewing stick/sponge and was aimed at preventing nausea and vomiting. It is important that education on this is intensified in ANCs to prevent unwanted pregnancy outcomes.

A higher prevalence of anaemia (50.8%) was measured than reported for pregnant women in Ghana at 45% in the latest demographic and health survey [ 3 ]. Our prevalence rate for anaemia in pregnant women in Northern Ghana is high enough for anaemia to be classified as a severe public health problem according to WHO [ 17 ]. In Ghana, our prevalence is lower than reported for groups of pregnant women in 25 communities in Northern Ghana (70.0%) [ 18 ], and in Sekyere West District in Southern Ghana (57.1%) [ 19 ] but greater than estimated for pregnant women in Sekondi-Takoradi, Western Ghana (34.4%) [ 8 ]. In comparison to other pregnancy populations in Africa, our prevalence rate is lower than estimates made for pregnant women in South Eastern Nigeria (58%) [ 20 ], Eastern Ethiopia (56.8%) [ 21 ], Southern Ethiopia (51.9%) [ 22 ], Kiboga, Uganda (63.1%) [ 23 ], Derna, Libya (54.6%) [ 24 ], and Niger Delta, Nigeria (69.6%) [ 25 ]. However, our anaemia in pregnancy prevalence is higher than estimated for populations in South West Ethiopia (23.5%) [ 26 ], North West Ethiopia (25.2%) [ 27 ], and Mpigi, Uganda (32.5%) [ 28 ]. The differences in the prevalence of anemia in pregnancy in the different population groups might be due to differences in socio-economic circumstances, cultural practices, dietary patterns, preventive health practices and diagnostic tests. However, it is clearly established that the prevalence of anaemia in pregnancy is very high and pregnant women are not obtaining enough iron and other essential nutrients from their diet or from supplement use to produce adequate levels of haemoglobin to support pregnancies.

The high prevalence of anaemia measured in our study population may have a number of potential causes including low or non-compliance with iron folic acid supplementation, low dietary iron intake and the high risk nature of the population studied. WHO recommends oral daily iron and folic acid supplementation for pregnant women because of the high iron requirements in pregnancy which cannot be met from dietary sources alone [ 29 ]. However, many pregnant women redeem the iron folic acid supplement but do not take it as advised because of the side effects of the elemental iron used in the formulation. In a study, anaemia prevalence increased with non-compliance with iron supplementation as pregnancy progressed and the non-compliant pregnant women were 6 times more likely to be anaemic compared to those compliant (Adjusted OR 6.19, 95% CI 2.55–15.02) [ 30 ]. It is also possible that the consumption of iron-rich foods and fruits that aid absorption of iron, zinc and vitamin A needed for hematopoiesis was low in our study population although we found that a high percentage of the women consumed iron-rich foods in the last 24 h before the interviews. Consumption of plant-based foods rich in non-haem iron with low bioavailability underlies this. It is reported that the absorption of non-haem iron may be as low as 5% in plant-based meals with little animal source foods [ 31 ]. Women attending ANC of a hospital that receives referrals of pregnant women with complications including anaemia from the four northern regions of Ghana were studied. Thus, it can be assumed that some of the women in the study population could be referred to receive antenatal care at the study hospital because of anaemia-related pregnancy complications but this was not explored in the present study. Infections such as malaria and HIV increase the risk of anaemia [ 8 ] and may have also contributed to the level of anaemia measured in the study population.

The study evaluated a host of socio-demographic, dietary, and preventive health service use factors in order to identify risk factors of anaemia for planning health services. Among the potential risk factors identified in bivariate analyses, only the women’s knowledge on anaemia and pregnancy trimester at interview remain significantly associated with their anaemia status in multivariate analysis. Even though religion practised, and household wealth index were significant in bivariate analyses, they did not remain significant in multivariate analysis. The finding of a link between anaemia knowledge and anaemia level is similar to the findings of a survey conducted on pregnant women in Malaysia which found that knowledge on anaemia among the pregnant women corresponds to a reduction in the odds of anaemia [ 32 ]. In this study, it is possible that higher levels of anaemia knowledge correspond to more awareness on the causes and preventive strategies of anaemia and this translates into increased adoption of preventive measures hence lower anaemia prevalence rates.

Limitations

Our study has a number of limitations. One important limitation is that a cross-sectional design, which does not allow for the study of causation, was used. The study did not independently carry out haemoglobin estimation on the women but relied on the hospital’s estimate of haemoglobin of the women recorded in the ANC booklets for anaemia diagnosis. In the assessment of dietary diversity of the pregnant women, only one 24-h dietary recall was conducted, and this may not be representative of the usual dietary pattern individually. This study did not have information on compliance to iron-folic acid supplementation and pregnancy outcomes of the women so could not do any analysis relating to these. Also, the questionnaire used to generate the anaemia knowledge index was investigator-constructed and was not fully validated. Despite these limitations, this study provides some important insights into the level of anaemia in pregnancy and its risk factors in the Tamale Metropolis.

Half of pregnant women (50.8%) seeking antenatal care at a tertiary referral hospital in Northern Ghana are anaemic making anaemia in pregnancy a severe public health problem. The prevalence of anaemia increased with pregnancy trimester. The women’s knowledge on anaemia and pregnancy trimester at interview emerged as independent determinants of anaemia among a host of socio-demographic, dietary, and preventive service use factors explored. The high level of anaemia in pregnancy needs immediate action to prevent the occurrence of adverse maternal and neonatal outcomes. Education of pregnant women on anaemia should be intensified in ANCs. Further studies are needed to understand why the prevalence of anaemia in pregnancy remains high despite the availability of preventive health services.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Antenatal Clinic

Adjusted Odds Ratio

Confidence Interval

grammes per deciliter

Minimum Dietary Diversity-Women

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Wemakor, A. Prevalence and determinants of anaemia in pregnant women receiving antenatal care at a tertiary referral hospital in Northern Ghana. BMC Pregnancy Childbirth 19 , 495 (2019). https://doi.org/10.1186/s12884-019-2644-5

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Research Article

Prevention and management of anaemia in pregnancy: Community perceptions and facility readiness in Ghana and Uganda

Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation Department of International Public Health, Liverpool School of Tropical Medicine, Liverpool, United Kingdom

Roles Conceptualization, Methodology, Supervision, Writing – review & editing

Affiliation Department of Family Medicine and Community Practice, Mbarara University of Science and Technology, Mbarara, Uganda

Roles Data curation, Methodology, Writing – review & editing

Affiliation Research, Planning, Monitoring & Evaluation Department, National Blood Service Ghana, Accra, Ghana

Roles Data curation, Investigation, Methodology, Validation, Writing – review & editing

Affiliation Community Health Department, Mbarara University of Science and Technology, Mbarara, Uganda

Roles Data curation, Methodology, Supervision, Validation, Writing – review & editing

Affiliation Department of Health Policy Planning and Management, University of Ghana School of Public Health, Accra, Ghana

Roles Formal analysis, Writing – review & editing

Roles Conceptualization, Funding acquisition, Methodology, Supervision, Writing – review & editing

Roles Conceptualization, Funding acquisition, Project administration, Supervision, Writing – review & editing

Affiliation Department of Medical Laboratory Science, Mbarara University of Science and Technology, Mbarara, Uganda

• Tara Tancred, 
• Vincent Mubangizi, 
• Emmanuel Nene Dei, 
• Syliva Natukunda, 
• Daniel Nana Yaw Abankwah, 
• Phoebe Ellis, 
• Imelda Bates, 
• Bernard Natukunda, 
• Lucy Asamoah Akuoko

• Published: August 26, 2024
• https://doi.org/10.1371/journal.pgph.0003610
• Peer Review
• Reader Comments

Anaemia is one of the most common conditions in low- and middle-income countries, with prevalence increasing during pregnancy. The highest burden is in Sub-Saharan Africa and South Asia, where the prevalence of anaemia in pregnancy is 41.7% and 40%, respectively. Anaemia in pregnancy can lead to complications such as prematurity, low birthweight, spontaneous abortion, and foetal death, as well as increasing the likelihood and severity of postpartum haemorrhage. Identifying and mitigating anaemia in pregnancy is a public health priority. Here we present a mixed-methods situational analysis of facility readiness and community understanding of anaemia in Ghana and Uganda. Quantitative health assessments (adapted from service availability and readiness assessments) and qualitative key informant interviews (KIIs) with district-level stakeholders, in-depth interviews (IDIs) with maternity staff, and focus group discussions (FGDs) with community members were held in 2021. We carried out facility assessments in nine facilities in Ghana and seven in Uganda. We carried out seven KIIs, 23 IDIs, and eight FGDs in Ghana and nine, 17, and five, respectively, in Uganda. Many good practices and general awareness of anaemia in pregnancy were identified. In terms of bottlenecks, there was broad consistency across both countries. In health facilities, there were gaps in the availability of haemoglobin testing—especially point-of-care testing—staffing numbers, availability of standard operating procedures/guidelines for anaemia in pregnancy, and poor staff attitudes during antenatal care. Amongst community members, there was a need for improved sensitisation around malaria and helminth infections as potential causes of anaemia and provision of education around the purpose of iron and folic acid supplementation for preventing or managing anaemia in pregnancy. Anaemia in pregnancy is a persistent challenge, but one with clear opportunities to intervene to yield improvements.

Citation: Tancred T, Mubangizi V, Dei EN, Natukunda S, Abankwah DNY, Ellis P, et al. (2024) Prevention and management of anaemia in pregnancy: Community perceptions and facility readiness in Ghana and Uganda. PLOS Glob Public Health 4(8): e0003610. https://doi.org/10.1371/journal.pgph.0003610

Editor: Marie A. Brault, NYU Grossman School of Medicine: New York University School of Medicine, UNITED STATES OF AMERICA

Received: April 3, 2024; Accepted: July 25, 2024; Published: August 26, 2024

Copyright: © 2024 Tancred et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All data can be found in the manuscript and supporting information files.

Funding: This work was wholly funded by the Medical Research Council, UK (reference MR/T00326X/1) as part of the Public Health Intervention Development scheme, awarded to IB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Competing interests: The authors have declared that no competing interests exist.

Introduction

Anaemia occurs when there are insufficient red blood cells or haemoglobin to carry oxygen to the tissues of the body. The prevalence of anaemia in women of reproductive age has been slow to improve. A review found the pooled prevalence of anaemia across 24 low-resource countries amongst women aged 15–24 was 42% [ 1 ]. Anaemia in pregnant women—sometimes called maternal, obstetric, or prepartum anaemia—is defined as a haemoglobin less than 110 g/L. It is an indicator of both poor nutrition and poor health. Globally, 36.8% of pregnant women are anaemic. The highest burden is in Sub-Saharan Africa and South Asia, where the prevalence of anaemia in pregnancy is 41.7% and 40% respectively [ 2 ].

Anaemia in pregnancy is associated with adverse outcomes for the mother and baby. These include preterm delivery, low birthweight infants, and impaired child development [ 3 ]. Severe anaemia, defined as haemoglobin below 60 g/L, can further result in spontaneous abortions, puerperal sepsis, and foetal death [ 4 , 5 ]. A review of anaemia in pregnancy in low-resource settings found that 12% of low birthweight births, 19% of preterm births, and 18% of perinatal mortalities were attributable to anaemia in pregnancy [ 6 ]. Severe anaemia also presents a risk to the mother, increasing the odds of postpartum haemorrhage by approximately 3.5 times [ 7 ].

Anaemia has multiple causes including: nutritional deficiencies (iron, folate, vitamin A); parasitic infections (malaria, hookworm, schistosomiasis); bleeding; underlying chronic conditions (tuberculosis, human immunodeficiency virus); and haemoglobinopathies such as sickle-cell disease [ 8 ]. The most common cause of anaemia in pregnancy is iron deficiency anaemia, though this may be proportionally less prevalent in malaria-endemic areas [ 5 ]. Iron deficiency can be caused by inadequate iron-rich food in the diet, or by blood loss, including secondary blood loss to helminth infections [ 9 , 10 ]. Women infected with intestinal parasites are 3.59 times more likely than uninfected women to develop anaemia, and women who have no iron and folic-acid supplementation are 1.82 times more likely to develop anaemia than supplemented women. Anaemia tends to worsen as pregnancy progresses, such that women in their third trimester are 2.37 times more likely to develop anaemia than those in the first and second trimesters [ 5 ].

Anaemia in pregnancy is a complex public health challenge, though there are many points from community-to-facility where helpful interventions may be put in place [ 11 ]. During pregnancy, antenatal care (ANC) is the main platform through which anaemia is identified, prevented, and treated. During antenatal visits, anaemia is assessed clinically or through the measurement of haemoglobin. Iron and folate supplements are generally prescribed, and, where appropriate, antimalarial prophylaxis and anti-helminth medication may be advised. With good adherence, this approach can improve iron stores and prevent or resolve anaemia in pregnancy [ 12 ]. Counselling on nutrition and malaria prevention, and encouragement to eat iron-rich foods, are also provided. For severe anaemia unresponsive to oral treatment, iron infusions, and occasionally, blood transfusions, may be warranted [ 5 ]. To meaningfully prevent or manage anaemia in pregnancy, it is critically important that ANC is accessible and of high quality, uptake is consistent, and that adherence to prescriptions and counselling is followed.

To strengthen health systems to catalyse reductions in anaemia in pregnancy, it is crucial to understand both facilitators and bottlenecks of anaemia care from multiple perspectives. With the aim of identifying good practices and areas for improvement, this study focused on perspectives about the prevention and management of anaemia in pregnancy amongst pregnant (or recently pregnant) women, male partners, community influencers, health services staff, and decision-makers who influence anaemia care policy and practice in Ghana and Uganda.

Materials and methods

Study design.

We carried out a cross-sectional mixed methods situational analysis of factors from community-to-district that impact the prevention, management, and treatment of postpartum haemorrhage in Uganda and Ghana from March–May of 2021. The results here are derived from an embedded sub-study that focused on anaemia in pregnancy, given that it is a key and persistent factor influencing the likelihood and severity of postpartum haemorrhage.

Study sites

Ghana and Uganda were selected as our study countries to maximize the diversity of contexts studied. As such, we wanted to select a country from West Africa and one from East Africa with different models of health system financing and governance. Due to longstanding research relationships in Ghana and Uganda across our study team, we selected these two countries. In both countries, we collected data from two districts. We piloted tools in an additional district in Ghana and an additional facility in Uganda. To facilitate the transferability of our findings, these districts were chosen to be “mid-range” in terms of population and geography compared to others in their respective countries. Among all the health facilities within each district—including private, public and faith-based—we selected only those that provided caesarean sections and blood transfusions, as we were interested in understanding readiness to support prevent, manage, and treat postpartum haemorrhage in referral-level facilities which are most likely to receive such cases. Our findings therefore reflect a census across all facilities in each study district meeting these criteria.

Data collection

Quantitative data collection..

The study involved a quantitative health facility assessment based on adapted “health facility service availability and readiness assessments” [ 13 ]. This assessment had three different modules: one for anaemia, one for postpartum haemorrhage management, and one for blood transfusion—the one for anaemia is presented here. This module asked a comprehensive set of questions to determine the availability of appropriate standards or protocols, drugs, equipment, trained staff, and infrastructure to support anaemia prevention and management. Certain practices that are documented—or were expected to be documented—in patient files were also captured, for example, the measurement of haemoglobin at the time of labour. For such measures, we typically assessed all relevant patient files in the preceding three months. Within each health facility, different questions within the module were administered to maternal health care providers, laboratory technicians, or pharmacists as relevant, and where needed, observation (e.g. physically viewing a protocol) took place. No processes of care, however, were observed.

Qualitative data collection.

Qualitative data were derived from community focus group discussions (FGDs), in-depth interviews (IDIs), and key informant interviews (KIIs). FGDs were held in each district with: currently pregnant or recently delivered women; male partners of currently pregnant or recently delivered women; community leaders and elders (referred to hereafter as “community influencers”); and blood donors. FGD participants were recruited from communities within the catchment area of study sites in the health facility assessment. Study information was shared with community leaders, who then advertised it and helped identify prospective participants meeting study inclusion criteria in their communities to ensure 6–10 eligible persons would be available per focus group. Other than the provision of refreshments and transport reimbursements, participants were not unduly incentivised to participate. FGDs explored perceptions about anaemia (how it is locally understood, what causes it, what its consequences are, how it can be prevented or managed) and ANC (why women do or do not attend, what occurs during ANC, its importance, and its role in anaemia prevention and management). IDIs were conducted with maternity in-charges and the heads of the participating health facilities to understand perceived facilitators and barriers to good practice in anaemia prevention and management. Laboratory technicians were also involved in IDIs to understand testing for anaemia and ordering blood for transfusion. There were typically only one or two people fulfilling each role in each participating facility, and we identified and interviewed them where possible. KIIs were carried out with key district- or national-level informants who play a role in supporting maternal and/or blood transfusion services in each participating district, including district health officers, district heads of maternity/reproductive health services, district heads of laboratory services, and regional or zonal blood transfusion leads. IDIs and KIIs were complementary to the health facility assessments, serving also to explain any gaps identified. All participants were purposively sampled based on their role in their community, health facility, or district and their lived experiences. Each participant participated in only one interview or group discussion.

FGDs took 60–90 minutes to complete, and IDIs and KIIs took 20–60 minutes to complete and were audio recorded. FGDs took place in convenient locations in each community where participants were derived from. To minimize the ask on participant time and travel, IDIs took place in the health faciltiies where the assessments were carried out with the relevant members of staff and KIIs were carried out in the offices of the key informants. All IDIs and KIIs were carried out in English, whilst FGDs were carried out in local languages as appropriate (Twi or Ga in Ghana and Runyankore in Uganda). All qualitative data were collected by skilled research assistants. They were registered nurses trained in maternal health, and in Ghana, they were also supported by staff from the National Blood Service for aspects pertaining to blood transfusion. They had at least three-years’ of experience conducting health research within the study districts.

Our study team included clinicians specialising in obstetrics, haematology and blood transfusion, nurses, and social scientists, all with extensive experience in low- and middle-income country health services research. We developed our data collection instruments to explore some of the themes identified in the qualitative review of postpartum haemorrhage prevention by Finlayson et al [ 14 ] and the general processes described in the protocol by Akter et al [ 15 ]. We tailored them to the purpose and context of our study. Since tools needed minimal revision following piloting, we included data from the pilots in our analysis. Our data collection instruments can be found in “ S1 Data Collection Instruments”.

Quantitative data were analysed in Excel to generate basic descriptive statistics (counts, averages, percentages). Qualitative data were read and re-read for familiarity. Framework analysis [ 16 ] was used to generate higher-level categories around specific pre-determined aspects of anaemia in pregnancy prevention and management. Data within each category were analysed thematically, being coded inductively, line-by-line in NVivo. These codes were grouped into increasingly higher-level codes to develop sub-themes to reflect key findings.

Quantitative data from the health facility assessments and qualitative data were then triangulated to present an overall picture of the key strengths and barriers to anaemia in pregnancy prevention and management across our study sites in Ghana and Uganda.

Ethical considerations.

We obtained ethics approvals from the Ghana Health Service Ethics Review Committee and, in Uganda, from the Research Ethics Committee of Mbarara University of Science and Technology and the Uganda National Council for Science and Technology. In the UK, research ethics approval was obtained from the Liverpool School of Tropical Medicine.

Permission to carry out the research was obtained from district health offices and the head of each participating health facility. All participants provided written informed consent before proceeding with data collection.

Data were collected from a total of nine health facilities (inclusive of one pilot facility) in Ghana and seven (also inclusive of a pilot facility) in Uganda. As seen in Table 1 , in Ghana, facilities from District 1 were generally larger than in other districts, with more patient traffic. Health facilities in Uganda had smaller overall patient numbers and tended to have facilities with larger capacity (as reflected by number of beds).

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https://doi.org/10.1371/journal.pgph.0003610.t001

Qualitative data collection is summarised in Table 2 below. Data were collected from 84 participants in Ghana and 63 in Uganda.

https://doi.org/10.1371/journal.pgph.0003610.t002

Diagnosing anaemia in pregnancy

Standard operating procedures or guidelines for assessing anaemia in pregnancy were not present in 7/9 (78%) facilities in Ghana, and in the other two facilities, respondents stated “unsure/don’t know”, or they were reported available but not seen. In Uganda, 5/7 (71%) facilities did not have these in place, and in the two other facilities, they were reported available but not seen ( Table 3 ).

https://doi.org/10.1371/journal.pgph.0003610.t003

The health facility assessments reported various methods for testing women’s haemoglobin concentration. The use of an automated haematology analyser for doing a full blood count was the most common method by far, being stated by participants across all facilities in the assessment in Ghana and in 6/7 (86%) facilities in Uganda. Only two facilities each in Ghana and Uganda also used non-automated methods (e.g. colorimeter, haematocrit) for measuring or estimating haemoglobin concentration. In Uganda, only one facility reported the use of Hemocue and another reported the use of DiaSpect, both of which can be point-of-care tests. However, no facilities in either country reported having haemoglobin measurement that was explicitly for point-of-care use ( Table 3 ).

In the facility assessment, in Ghana, only 5/9 (56%) of facilities had available documentation on assessment of haemoglobin at the time of labour, and this was reportedly done for all women in two of those three facilities (1029/1029 women in one facility, and 6/6 women in another), for 6/10 women coming to the facility for childbirth in the third, and for zero women in the other two. In Uganda, these data were available in 6/7 (86%) facilities, but of the 1161 women presenting during labour in the three months prior to the assessment across these six facilities, only 235 (20%) of women had their haemoglobin assessed at the time of labour. However, most of these came from one facility, where 116/156 (74%) of women had haemoglobin assessed during labour—the range across facilities was 0–74%, with three facilities at roughly 10% and one at 59% of women ( Table 3 ).

Maternity staff in Uganda noted that haemoglobin testing was done at various times and frequencies during pregnancy. Only one IDI participant in Uganda mentioned measuring haemoglobin during labour. At the facilities in Ghana, most or all women had their haemoglobin measured during labour as routine practice, which was confirmed in IDIs.

Yes it’s a routine thing we do here, all [labour] admissions that come, they go through the lab, do full blood count, then we know your haemoglobin level before any other thing. (IDI, matron in-charge, Ghana)

In community FGDs, especially those with women, in both countries, participants did note that their “blood is measured” during ANC.

It was also mentioned in both countries—though considerably more in Uganda—that, in the absence of haemoglobin testing, anaemia would be clinically assessed by pallor. Some district-level key informants in Uganda noted that lab-based haemoglobin testing is not always available, leading to this reliance on clinical assessment, which may not be as objective.

Clinical assessment depends entirely on the clinical acumen of the individual and it is highly subjective, so we want to beef it up, we want to support the clinical assessment with the laboratory confirmation, you cannot depend on just clinical assessment. (KII, district official, Uganda)

In Uganda, some facility-based participants also reported that a barrier to the laboratory diagnosis of anaemia in pregnancy was that sometimes error—human or technical—could lead to inaccuracies, for example, through documentation or equipment errors.

Respondent: When they mix the results, they may end up giving low blood count to the patient who is actually okay… [Or] when the machine for measuring haemoglobin is not working very well, it can give a false haemoglobin and we end up transfusing blood. (IDI, midwife, Uganda)

Anaemia in pregnancy is taken seriously by healthcare providers

In both countries, it was recognised that a woman should not be anaemic at the time of birth. Iron supplementation and nutritional counselling were cited as key ways to prevent or manage anaemia, though it was recognised by many participants that more severe anaemia may require blood transfusion.

When [haemoglobin] is 10 [g/L], they are being given haematinics for one month but when its nine and below, they are being referred to doctor to be given haematinics, mostly tot’hema [oral iron solution]. But if it’s seven, seven and below, they are being counselled on transfusion, yes. (IDI, matron in-charge, Ghana)

In both countries, maternity care providers commented on their commitment to following up with women they have identified as anaemic.

Once we see [anaemia], during the antenatal, we make sure that you don’t go down . Once you come here and I see you , I monitor you seriously . At least every week or two; at-least two weeks or third week , we do the blood test again to see if it has come up . And we have been successful in those cases . (IDI, matron in-charge, Ghana)

These participants noted difficulties in ensuring continuity of care, which acted as a barrier to effective anaemia in pregnancy management, often due to gaps in ANC attendance by pregnant women, including those with anaemia.

…ones who just came with maybe anaemia in pregnancy, those are actually the hardest to come back, but these others to them they think there are justifiable causes, like maybe I ruptured my uterus or something, those ones will come back. (IDI, matron in-charge, Uganda)

To encourage attendance at ANC, providers usually give women the details of their next ANC appointment at their current one so that women are aware of the importance of coming back and know when they should next attend. In Ghana, maternity staff and community members noted that women are provided with midwives’ contact details. This practice enabled better organisation of appointments, shorter waiting times, and provided a communication channel to address women’s needs, particularly for those who struggle to access care.

They also tell her days on which she should keep coming back to the hospital to check the status of her pregnancy until she gives birth. (FGD, community influencers, Uganda) The staff , most of them give their numbers out , and with a good relationship , a client will always call . (KII, district official, Ghana)

Localised understanding of anaemia in pregnancy

Anaemia is understood according to its symptoms..

In Ghana, some community FGD participants had a good understanding of the symptoms of anaemia. In Uganda, the term anaemia was recognised but was again understood in terms of its symptoms. These included being pale, having low energy, and dizziness. Anaemia was generally understood to mean a “low amount of blood” or “low blood volume” and was typically thought to be caused by not eating and sleeping well. In Uganda, community FGD participants also regularly talked about swelling, and in the FGD with pregnant or recently delivered women, anaemia was also linked to weight loss and loss of appetite.

Respondent 4: I know anaemia is when you don’t have enough blood, or your blood level is low. Respondent 3: Please I don’t know. Respondent 2: I haven’t heard of anaemia before. Respondent 1: I haven’t also heard it before. Respondent 5: Same. Respondent 6: Same. Interviewer: What are some of the symptoms of anaemia? Respondent 6: Sometimes you feel dizzy and not feel okay. Respondent 2: Your heart beats faster and you easily get tired. (FGD, pregnant or recently delivered women, Ghana)

Anaemia was seen as dangerous by participants in all community FGDs, especially to the developing fetus, leading to foetal death or premature childbirth. Some participants also noted it was potentially life-threatening to the mother, though this was given less focus. In one FGD in Uganda, a male partner specifically noted anaemia means “less oxygen and nutrients for the baby.”

Most FGD participants were aware of haemoglobin testing as a way to detect “blood volume”—i.e. anaemia. Male partners in Ghana and community influencers in Uganda also noted that there is a normal haemoglobin range or a “cut-off” and that falling below these indicates anaemia.

Reflecting on what was noted by facility- and district-level participants, some women in Uganda also described how a clinical assessment for anaemia is done during ANC.

The doctors instructs you to look up and looks into your eyes and looks into your hands to see if you have blood. (FGD, pregnant or recently delivered women, Uganda)

There is understanding of local foods associated with “improving blood”.

In Ghana, participants across community FGDs could describe many local foods that were useful in combatting anaemia to “help their blood”, including leafy greens, legumes, plantains, cabbage, milk, dried fish, meat, and eggs. Tomato paste and coke were also mentioned. Community influencers in Ghana also made a link between anaemia and vitamin C deficiency, noting the importance of fruit for preventing anaemia. Pregnant or recently delivered women also mentioned multivitamins and “iron 3 [a hematinic oral solution]—it’s a blood tonic” (FGD, pregnant women, Ghana).

Key informants in Ghana described several successful programmes to educate pregnant women and community members about anaemia in pregnancy. These include pregnancy schools—which are educational sessions run outside of routine antenatal appointments—and dietary education provided through two community-based nutrition programmes.

… we used to have anaemia quite bad in pregnant women, so we put in two major programs. Food demonstration and food bazaars. (KII, district official, Ghana)

In Uganda, local foods widely understood to prevent anaemia or to be consumed by women with anaemia in pregnancy are fruits (mango, banana, watermelon, pawpaw, pineapple, avocado), vegetables (eggplant, amaranth leaves and other greens), maize meal porridge, ground nuts, beans, and meat.

ANC and the prevention and management of anaemia in pregnancy

Perceptions towards anc are very positive..

Across all community FGD participants, ANC was seen as important.

There are many diseases that come up in the pregnancy period … the baby can even die at the point of birth if these things are not taken care of, so it is necessary to go for ANC . (FGD, male partners, Ghana)

We are firm in knowing we won’t meet any complications because we have been attending ANC . (FGD, male partners, Uganda)

Across community FGDs in Ghana, services referred to as part of ANC included: checking the baby’s growth and position; checking the mother’s weight, blood pressure, and temperature; as well as doing tests for infections and providing treatment where necessary. The provision of counselling, especially around nutrition and hygiene, was also noted frequently. A few participants in Ghana also mentioned that screening for Rhesus factor and sickle cell disease would be done. Male partners in Ghana were divided into those who were unsure about what ANC entails and those who had more knowledge as they had participated in ANC or asked their wives about it and reviewed ANC booklets. Only community influencers suggested that couples receive preferential treatment if a male partner accompanies a woman to ANC. However, mandatory HIV testing during ANC was mentioned as a deterrent to male partner involvement.

I have no idea…no, because I am not allowed inside. (FGD, male partners, Ghana) My wife said they tested her [haemoglobin] and was told her blood level is low , so I called the nurse and asked her because I didn’t see it in the antenatal book , so the nurse confirmed and said yes , she was told , but they didn’t write it in the book . (FGD, male partners, Uganda)

Community participants in Uganda were quite specific about what ANC covers, including measuring the “quantity of your blood” (to test for anaemia), screening for infections like HIV and syphilis and treating these, providing an expected due date, checking for blood pressure and blood sugar, counselling on nutrition and hygiene, the position and health of the baby, the amount of amniotic fluid, counselling on the place of childbirth, and education on understanding what different pains in pregnancy mean. Some also mentioned “mama kits” that include labour and childbirth supplies as well as newborn necessities that are given depending on the health facility they visited—it was expressed that they would like to see this given at all public facilities.

ANC timing and frequency are not always understood.

Guidelines in both contexts indicate that there should be eight ANC visits throughout pregnancy and that the first visit should be initiated within the first trimester to ensure that interventions are offered at the appropriate time. FGDs with pregnant or recently delivered women in Ghana highlighted variable knowledge about the timing and number of ANC visits, with only one participant noting that there should be “seven or eight” ANC visits throughout pregnancy. Timing of ANC initiation varied from two weeks to six months, though of the 23 pregnant women participating across three FGDs, 16/23 (70%) noted starting ANC in the first trimester. Women who sought care very early (within the first or second month of pregnancy) often commented that they had felt particularly unwell or that they had a history of miscarriage, which prompted them to seek care.

This variability in knowledge about ANC visits was also reflected in male partner FGDs in Ghana, but there seemed to be a stronger sense that going early was not required if there were no issues and that most women went after six months. However, when asked when women should go for ANC, there was consensus that starting at around three months, though a handful of participants noted that ANC attendance should begin as soon as the pregnancy is identified. When asked how often ANC occurs, there was a wide range of responses, from every two or three weeks to monthly, for a total number of visits ranging from 6–18 over the course of pregnancy. There was the sense amongst participants that ANC attendance is increasing, primarily due to policies supporting free care.

In FGDs with community influencers in Ghana, there was broad agreement around the start of ANC being from two-to-three months up until the pregnancy is visible. They expressed that women might delay going so that the pregnancy is more advanced, so they only have to pay for one ultrasound.

Interviewer: How many times [should a pregnant woman attend ANC] …? Number 3. Respondent 3 : 3 times . Interviewer : 3 times . Number 4 how many times … ? Respondent 4 : It can be 6 times . Interviewer : 6 times ? Number 6 how many times ? Respondent 6 : 9 times . (FGD, community influencers, Ghana)

Across all community FGD participants in Ghana, there was the perception that strong women and those with healthy pregnancies do not need ANC, and those who are “weaker” or with obvious health issues are the ones who need ANC earlier.

It depends on the individual. Some people are physically strong when they are pregnant. Others aren’t that strong, so they visit the hospital in their first week. (FGD, community influencers, Ghana)

In Uganda, most participants in the FGD with pregnant or recently delivered women spoke about the timing of the first ANC visit as 1–3 months, and it was clear that “eight ANC visits” was correctly understood as being the desired number of visits. However, in the FGD with male partners and both FGDs with community influencers, this ranged from four-to-eight. There was a shared understanding that most women would be likely to seek out ANC as soon as they have a positive pregnancy test but that there would be women who might go later in the absence of complications.

They go for antenatal on the sixth month of pregnancy…because until then there have not been any complications, so there would not be a need to go for antenatal . (FGD, male partners, Uganda)

However, community influencers suggested that most women start care from three-to-five months’ gestation and associated women coming later with a lack of responsibility.

[Coming at five months for the first ANC] is for a mother that has delayed or…doesn’t care…at three months, a responsible mother should be coming from ANC. (FGD, community influencers, Ghana) Doctors taught them [women in communities] that when you get pregnant , you start coming for ANC . (FGD , community influencers , Uganda)

Persistent barriers to ANC uptake exist.

All community FGD participants in both countries described recurring barriers to ANC care. These largely centred distance to the health facility, difficulty finding and paying for transportation—especially in remote areas—and other financial barriers, including “hidden costs” for equipment or medication that are expected to be free of charge. These barriers are exacerbated when repeated visits are required.

Some pregnant or recently delivered women in Ghana—especially those who already have children—suggested that expenses are increasing. There is a small charge for each visit (10 cedis (~1.7 USD at the time of data collection)) and two cedis (~0.34 USD) for some medications, even with health insurance. Male partners in Ghana agreed that there are many costs associated with ANC and pregnancy, mainly linked to drugs and transportation, and estimated total expenses throughout pregnancy and childbirth as high as 1500 cedis (~255 USD). Although Ghana’s National Health Insurance should cover costs, community-based participants regularly cited cost-related barriers. For example, if medication is required, as they explained, there are hidden costs that can influence the decision to seek care. In Uganda, it was widely agreed across community participants that ANC in public facilities is free, though payment is expected in private facilities. However, costs may still be incurred, as women might be sent to another facility if certain equipment is unavailable (e.g. an ultrasound machine), or they may be asked to buy medications.

They also like to take money too much, whether you have insurance or not. Medicine that will cost 20 cedis you end up spending 100 cedis. (FGD, community influencers, Ghana) Respondent 1: It comes down to a money issue and fatigue. Respondent 3 : I want to buttress that point . If you go today to do laboratory work , you would be expected to pay . After three days’ time , when you are scheduled to come back , you would be asked to go and do another . So if that continues , then you find out that your money is getting finished…if you have money , then you go and give birth . They say it’s free , but it’s actually not . (FGD, pregnant or recently delivered women, Ghana).

Many participants in both countries reiterated that the cost of ANC sometimes results in delays in women seeking and accessing anaemia in pregnancy diagnosis and management.

When they go early they will do so many scans, so if you go late in the last trimester that means you will do like just one scan and you leave. So, I think it’s the financial obligation that makes them stay longer at home. (FGD, community influencers, Ghana)

Poor attitudes of ANC staff were extensively highlighted in both countries by pregnant women and male partners, as well as long wait times in Ghana. These prevented women from taking up ANC and also from giving birth in a health facility. Community influencers also noted that healthcare providers do not consistently provide good quality care and can be unhelpful and unkind. However, some women stated they were satisfied with the care provided and the relationship with their midwives. It was understood that this may affect the reputation of the health facility in positive or negative ways as women share information about their experiences.

If I brought my wife here and if she wasn’t treated well—or even if she was treated well—now they are advising [other women]…which will cause a change of heart on the other person. (FGD, male partners, Uganda)

Local perceptions of having safely had children previously without seeking ANC or skilled attendance at birth may reinforce this idea among those women or women close to them.

Some people have given birth safely without antenatal, so they don’t see the need. (FGD, pregnant or recently delivered women, Ghana)

In Uganda, the perception of having lower socioeconomic status was seen as a barrier to some women. Lack of permission or support from husbands or mothers-in-law was also repeatedly cited across community participants.

Lack of proper clothes to wear to come to the hospital…they fear being seen in torn clothes and decided to keep home. (FGD, pregnant or recently delivered women, Uganda)

The use of traditional care was frequently mentioned by community-based participants in Ghana. Traditional care was appreciated as it lacked many of the barriers of formal ANC, such as cost and distance. Traditional medicine was also sometimes viewed as more effective.

Respondent: It is because sometimes traditional/herbal medicine is more potent than orthodox medicine…that is also a contributing reason. (FGD, pregnant or recently delivered women, Ghana)

Facility-based participants and key informants explained that inadequate staffing is sometimes a barrier to adequate ANC and, therefore, to anaemia in pregnancy diagnosis and management, as laboratory personnel were in particularly short supply.

Interviewer: So currently staff is a challenge? Respondent : It’s a huge problem , it’s a huge problem . (KII, district official, Ghana)

Staff training on anaemia in pregnancy appeared to be infrequent in both countries, though there was training before qualifying and on-the-job. Facility-based participants communicated gaps in training, particularly for training on attitude and conduct.

Apart from training on certain topics, ours have been informal discussions when we go on rounds, we talk a lot and try to educate them on transfusion, that has been my approach, I don’t normally run a lot of formal workshops and those things, we see a patient we just discuss it. (IDI, midwife, Ghana)

Some district-level key informants in Uganda also noted the importance of continuing medical education for anaemia in pregnancy.

Preventing and managing anaemia are well-understood by healthcare providers and less well understood by community members.

In IDIs with maternity staff in both countries, alongside haemoglobin measurement, routine practices during ANC—including preventing and treating malaria, providing deworming medication, giving iron and folate supplements, and providing nutritional counselling—were described as important for preventing and managing anaemia in pregnancy. The use of insecticide-treated bednets was also mentioned by maternity staff and community-based participants. In Ghana, maternity staff reported that women are supervised in taking malaria medication to increase adherence. Women across FGDs in both countries noted that many women did not always like taking antimalarials or iron and folate supplements due to side effects.

Yeah, we are doing it actually in antenatal, we start from antenatal, we first do haemoglobin, then on subsequent visits, we do it, and then that’s why we give them ferrous and folic, whatever we have in place, even the minister of health, that’s what she is advocating for, even the [intermittent preventative treatment for malaria] we are giving, if the woman does not have malaria, if she is dewormed and worms are not sucking blood, if she is given these to supplement her blood, then there is nothing that should stop her from fighting anaemia. Then also advising her on what to eat, nutritional status . (IDI, matron in-charge, Uganda) I want to find out why they give us the malaria drug . When I went , they ask us to take the medicine right there . But when I came home I had adverse reactions; my mouth area was itching and when I touched it , rashes developed . (FGD, pregnant or recently delivered women, Ghana)

These findings are echoed in facility assessments, where intermittent malaria prophylaxis is routinely given to all women across all participating facilities in both countries and iron and folate supplements are provided to all women during ANC. In Ghana, the provision of anti-helminth medications was offered to all women in ANC in 5/9 (56%) facilities and only to women in higher-risk areas in 4/9 (44%) facilities. In Uganda, these medications were offered to all women attending ANC ( Table 3 ).

Participants in the FGDs with pregnant and recently delivered women in Ghana linked iron and folate supplements to the development of the baby’s blood and bones rather than with their own anaemia. “I think folic acid supports blood cells…about iron? I have no idea” (FGD, male partners, Ghana). In Uganda, pregnant or recently delivered women knew pills could be given for anaemia but did not refer to these by name.

They give us those red tablets to increase our blood levels…and…add on our blood levels and [ensure we] have enough blood to take care of the baby in the womb. (FGD pregnant women, Uganda)

Iron and folate supplements were known by a few male partners and community influencers in Uganda to help women “gain blood”. However, it was mostly understood as being important for health in general and not linked to resolving anaemia.

Although malaria and helminth infections were understood as bad for the baby and mother, they were not associated with anaemia in FGDs with pregnant or recently delivered women in Ghana. Only one pregnant or recently delivered participant in Uganda noted, “deworming prevents [pregnant women] from being anaemic”. However, some male partners and community leaders in Ghana did note the association between malaria and “reducing blood”, and one community influencer in Uganda noted malaria causes “blood loss and complications” and was therefore linked to anaemia. Only one male partner in Uganda noted that worms “take nutrients”, resulting in the mother becoming malnourished and then anaemic (Male partner FGD, Uganda).

Blood transfusion was sparingly mentioned in both countries by community participants as a treatment for severe anaemia.

This mixed methods assessment explored facility readiness and diverse stakeholder perspectives to identify many good practices in Ghana and Uganda around the diagnosis, prevention, and management of anaemia in pregnancy, as well as several gaps.

Standard operating procedures or guidelines specific to anaemia in pregnancy were reported as sparingly present in both countries but were never seen. Ensuring that these are available, widely publicised, and used for continuing medical education would help to promote better practice and reduce anaemia in pregnancy and its consequences for the mother and baby. Such guidelines could be adapted from the “World Health Organization recommendations on ANC for a positive pregnancy experience”, which recommend daily (or intermittent if side effects are intolerable) oral iron and folic acid supplementation and for pregnant women to be advised about food sources of vitamins and minerals, and dietary diversity [ 5 ].

Community participants widely understood the use of haemoglobin testing for detecting anaemia. Haemoglobin measurement around the time of labour did not appear to be routine in many facilities in Uganda, but is very important so that anaemia can be corrected prior to delivery, especially where women may have had inconsistent attendance of ANC and do not have a recent measure [ 17 ]. Doing so may reduce the occurrence and severity of peripartum haemorrhage [ 18 ]. In both countries, automated analysers were by far the most common way to measure haemoglobin; this is the recommended method for diagnosing anaemia in pregnancy [ 5 ]. However, the limited availability of laboratory personnel and equipment sometimes necessitated the use of manual haemoglobin measurements or clinical assessment of anaemia, even though clinical examination is inadequately sensitive and specific for diagnosing anaemia [ 19 ]. Point-of-care haemoglobin tests may be useful in this situation as they can be performed by non-laboratory personnel and can yield timely, reliable results for quick decision-making [ 20 , 21 ]. However high volume use of these tests can be expensive [ 20 , 22 ], limiting their availability in many contexts, as was also reflected in our assessment.

Overall, there was a good level of understanding of some critical aspects of anaemia. Community participants in both countries recognised the symptoms and consequences of anaemia but knew less about the causes. Its implications on the developing foetus, and to a lesser extent on the mother, were acknowledged by community participants. There was wide general knowledge about local foods that may help in preventing or reducing anaemia across both countries, including an emphasis on vitamin C-rich foods, which can increase the absorption of iron, especially from plant foods [ 23 , 24 ]. Dietary factors can play an important role in reducing the risk of anaemia [ 25 ]. Positively, it was clearly noted by participants in both contexts that nutrition education for anaemia prevention or mitigation is a common aspect of ANC.

Community participants unanimously understood ANC to be very important. The timing of uptake and frequency of ANC visits were less well-understood, especially among Ghanaian participants. In both countries, initiation of ANC was frequently (and correctly) cited by participants as being within the first three months of pregnancy. However, literature from both Uganda and Ghana suggest this is not typical of most women, for whom early initiation of ANC and regular attendance is a persistent challenge due to gaps in knowledge and social, financial, and geographical barriers to accessing care [ 26 – 29 ]; achieving all eight ANC contacts occurs for a minority of women [ 30 – 32 ]. Community education about the importance of early and consistent ANC uptake may, therefore, be beneficial in managing anaemia in pregnancy [ 33 , 34 ].

Anaemia in pregnancy was taken seriously by maternity staff, with efforts being made to follow-up with patients identified as anaemic, including providing personal phone numbers and appointment reminders. However, despite efforts made, this follow-up was sometimes difficult due to women’s reluctance to take up care. In both countries, there were common barriers around ANC uptake, largely stemming from long distances to the health facilities, difficulty finding or paying for transportation, other costs, especially for medications, and poor staff attitudes. From the health providers’ perspectives, staff shortages and a lack of anaemia in pregnancy-specific training were noted in both countries. All of these resonate with findings from other lower-resource settings [ 35 , 36 ]. Without early and consistent uptake of ANC, women miss opportunities for interventions that can prevent or mitigate anaemia in pregnancy, potentially leading to poorer health outcomes for the mother and the baby [ 37 ]. It is, therefore, important that initiatives to reduce barriers to accessing ANC are implemented. For example, in other African settings, women have been provided with transportation vouchers that they can use in exchange for bus or motorcycle transport, which helps to overcome some of the transportation barriers related to attending ANC [ 38 – 40 ].

Finally, though the provision of antimalarials, iron and folate supplements, and deworming are routine during ANC in both countries, very few community participants understood their link with preventing or managing anaemia in pregnancy. Even where the link was made, it was not fully understood—for instance, helminth infections can cause anaemia due to red cell destruction or intestinal bleeding [ 41 ], but the women associated them with causing malnutrition. Iron and folate supplements are very effective in reducing anaemia if taken consistently during pregnancy [ 42 , 43 ] and ANC clinic consultations are a critical point through which iron and folate supplements are provided. Delays in care may, therefore, exacerbate the risk of developing anaemia [ 44 ]. Further, across many contexts, knowledge about iron and folate supplements and their importance supported significant improvements in adherence throughout pregnancy [ 45 – 47 ]. In a recent systematic review of iron and folate supplement adherence, the most significant contributor to compliance was knowledge of anaemia and the role of iron and folate supplements in preventing or managing it [ 47 ]. As participants highlighted the importance of counselling on various topics in ANC and noted a clear understanding of anaemia as dangerous for the developing foetus and mother, emphasising the link between iron and folate supplements, antimalarials, deworming, and anaemia within this counselling is an easy-to-action and likely highly effective step in promoting adherence to these treatments given during ANC.

Strengths and limitations

This study benefitted from having both quantitative and qualitative components, drawing insights across a wide range of respondents. Collecting data from two countries enabled comparison around the many similarities and few differences. Our study focused on surgery- and blood transfusion-capable facilities, so the findings may not apply to lower-level facilities, which may be less well-resourced and have less experienced or knowledgeable staff. Further, as we only collected data from 2–3 districts (and 16 facilities total) across both countries, our findings may not be generalizable. However, the many similarities across both countries suggest that our findings may be applicable to other facilities providing comprehensive obstetric care across Sub-Saharan Africa.

Conclusions

Limited capacity for haemoglobin testing, difficulties in accessing ANC, and staffing issues were raised by participants in both countries. Improved education for pregnant women, their families, and communities on anaemia, including its importance, causes, treatment and prevention, may support better uptake of anaemia prevention and treatment strategies. Understaffing, insufficient resources, and provision of and training on standards of care for anaemia in pregnancy should be addressed by the health service at the district or national levels.

Supporting information

S1 checklist. checklist—contains our human subject research checklist..

https://doi.org/10.1371/journal.pgph.0003610.s001

S1 Data. Data collection instruments—contains our data collection instruments.

https://doi.org/10.1371/journal.pgph.0003610.s002

Acknowledgments

We thank all of the participating health facilities, staff, and community members for their insights and cooperation.

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