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. 2016 Jan 1;12(1):95–102. doi: 10.2217/whe.15.91

Assessment of Iron Deficiency and Anemia in Pregnant Women: An Observational French Study

Thierry Harvey 1, Asmaa Zkik 2,*, Marie Auges 2, Thierry Clavel 3
PMCID: PMC5779562  PMID: 26693881

Abstract

Aim:

We explored the prevalence and management of iron deficiency and anemia among pregnant women in France.

Patients & methods:

In this prospective, observational, multicenter registry study, randomly selected investigators (gynecologists/obstetricians/midwives registered in the CEGEDIM® database) assessed pregnant women presenting for a consultation. Participants completed a questionnaire at study inclusion.

Results:

A total of 1506 patients were enrolled by 95 investigators. Overall, investigators estimated a moderate or significant risk of iron deficiency in almost 60% of women. The overall prevalence of anemia (15.8%) increased with longer pregnancy duration. Medication (mainly iron-based) was prescribed to 57.3% of patients.

Conclusion:

In French clinical practice, the estimated risk of iron deficiency and prevalence of anemia during pregnancy align with expectations and are managed according to national/international recommendations.

Keywords: anemia, iron deficiency, oral ferrous sulfate, pregnancy, prevention

Anemia is one of the main causes of disability worldwide and consequently, at an international level, represents a serious public health problem. In 2010, the global anemia prevalence was estimated to be 32.9%, resulting in 68.4 million years lived with disability [1]. Iron deficiency anemia, ranked as the fifteenth leading cause of disability-adjusted life years (DALYs) by the WHO in 2012, is the most common etiology [1], and WHO data estimate that iron deficiency anemia in children and adults results in 19.7 million DALYs, or 1.3% of global total DALYs [2]. From the European perspective, a small UK study reported that approximately 40% of women of reproductive age were iron deficient (ferritin <10 μg/l) and 70% had ferritin <20 μg/l [3]. In France, almost 30 and 4% of children aged less than 2 years had iron deficiency and iron deficiency anemia, respectively [4].

Due to different lifestyles and socioeconomic conditions between cultures, the prevalence of anemia during pregnancy is highly variable. According to a WHO review of nationally representative surveys from 1993 to 2005, anemia affects approximately 42% of pregnant women worldwide (52 and 23% in developing and developed countries, respectively) [5,6]. Although an estimated 1.6 billion individuals worldwide have anemia, it is generally assumed that 50% of cases of anemia are due to iron deficiency and about twice as many individuals are estimated to be affected by iron deficiency [7].

Anemia and iron deficiency are common during pregnancy [8,9]. A small decrease in hemoglobin (Hb) is a normal physiological consequence of the increase in blood plasma volume during pregnancy. Normally, after an initial increase (due to the cessation of menstruation), Hb levels decrease by around 20 g/l and reach their lowest level during the second trimester, returning to pre-pregnancy levels as the pregnancy advances toward term [8,10]. The increase in iron requirements during pregnancy results from increased total blood cell volume, the requirements of the fetus and placenta and, during labor, blood loss [9,10].

In the case of iron deficiency anemia during pregnancy, there are several possible risks to the mother, including increased fatigue, short-term memory loss, decreased attention span and decreased performance at work, increased pressure on the cardiovascular system due to insufficient Hb and low blood oxygen saturation levels, lower resistance to infections and a reduced tolerance to significant blood loss and to surgical interventions during labor [4,11]. The presumed risks of iron deficiency for the fetus relate to the fact that low iron levels increase the risk of reduced Hb levels, and therefore oxygen, to the uterus, placenta and the fetus during development [11]. Moreover, iron-deficient neonates have been shown to have a statistically significant increment in both cognitive and behavioral abnormalities up to 10 years after iron repletion [12]. Iron deficiency anemia, even if mild to moderate, can be associated with unfavorable obstetric outcomes, notably, premature birth, low birth weight and fetal death [8,10–11].

Daily supplementation with oral ferrous sulfate is effective in preventing maternal anemia and iron deficiency during pregnancy, and reducing the risk of low birthweight [13,14]. Indeed, international guidelines recommend universal iron supplementation for the management of iron deficiency and iron deficiency anemia during pregnancy [15–17].

Although iron deficiency and anemia lead to serious consequences for health and well-being, as well as social and economic repercussions [11], there is currently a lack of available French data on the prevalence of these conditions in pregnancy. The objective of the current observational study (PRECAM) was to explore the prevalence of iron deficiency and anemia among pregnant women in France according to French practitioner daily practice and to identify reasons for the prescription of medication for iron deficiency and anemia in this population. The PRECAM study consisted of two parts: first, a registry study (monitoring program) was performed to explore the prevalence of iron deficiency with or without anemia during pregnancy; consequently, a cohort study was performed to assess how treatment was chosen and the impact of treatment on patient's quality of life. The results of the cohort study are not presented in this publication.

Patients & methods

PRECAM was a prospective, observational study conducted at 95 centers in France between March 2013 and June 2014. Study investigators (gynecologists/obstetricians and midwives) were asked to include the first 15 pregnant women who presented for a consultation. The randomly selected investigator sample consisted of physicians/midwives registered in the CEGEDIM® (CEntre de GEstion, de Documentation, d'Informatique et de Marketing) database [18]. CEGEDIM, a global technology and services company specializing in the healthcare field, supplies services, technological tools, specialized software, data flow management services and databases, to healthcare industries, life sciences companies, healthcare professionals and insurance companies.

At study inclusion, each patient who agreed to participate in the study received a questionnaire consisting of one section to be completed by the clinician and a second section to be completed by the patient (self-assessment). Data collected on the patient questionnaire included age, gestation week, laboratory values (e.g., Hb, ferritin), type and reason for the prescription of medication and/or lifestyle/dietary advice. The duration of pregnancy was defined, in gestation weeks, as <16 weeks (first trimester of pregnancy), ≥16 and ≤28 weeks (second trimester) and >28 weeks (third trimester). Anemia was defined as Hb <11 g/dl (in the first and third trimesters) or <10.5 g/dl (second trimester) [19,20]. Iron deficiency was defined as serum ferritin <15 μg/l.

The study was strictly anonymous; there was no possible link between the patients' or clinicians' identities through the questionnaire. Additionally, the study was strictly noninterventional and care was never modified as a result of patient participation.

Statistical analyses were performed using SAS® software for PC (release 9.3, SAS Institute). Quantitative variables were described by the mean and standard deviation. Qualitative variables were described by frequency and percentage. Descriptive statistics were performed on the documented data and no weightings were applied since the sample was representative.

Estimated risks of iron deficiency were based on physician knowledge and expertise; no specific criteria were defined.

Results

One thousand five hundred and six patients were enrolled by 95 investigators (55% male, 99% gynecologists, 17.4% hospital-based from across France); data were analyzed for 1478 patients. A total of 28 patients were removed from the analysis because they were receiving folic acid alone during the first trimester of pregnancy, for the prevention of neural tube defects and therefore deemed to be outside the scope of assessing the prevention/treatment of iron deficiency. The mean age of the study population was 29.9 ± 5.1 (range: 15−45) years. 31.9, 43.6 and 24.5% of women were in the first, second and third trimesters of pregnancy, respectively.

Estimated risk of iron deficiency

Overall, investigators estimated that almost 60% of women were at moderate or significant risk of iron deficiency (59.3 vs 40.7% [no risk]). Of note, the proportion of women classified with a moderate or significant risk of iron deficiency increased with increasing duration of pregnancy (48.4% [first trimester] vs 68.4% [third trimester]) (Figure 1).

Figure 1.

Figure 1.

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Iron deficiency risk by duration of pregnancy in the PRECAM study.

In patients estimated to have a significant or moderate risk of iron deficiency, treatment (any) was prescribed in 97.8 and 73.6% of patients, respectively. In line with the increased estimated risk of iron deficiency with more advanced pregnancy, more patients received a prescription for treatment in the final trimester than in the first trimester (Figure 2).

Figure 2.

Figure 2.

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Proportion of women with an estimated iron deficiency risk who were prescribed treatment in the PRECAM study.

Prevalence of anemia

Overall, data regarding Hb levels were available for the majority (88.8%) of all pregnant women (80.2, 89.7 and 97.4% at the first, second and third trimesters, respectively) and 15.8% of these women were determined to have anemia. The prevalence of anemia increased with increased pregnancy duration (8.8, 13.7 and 26.0% at the first, second and third trimesters, respectively). A total of 2.9, 17.3 and 56.4% of pregnant women who were estimated by their physician to have no, moderate or significant risk of iron deficiency, respectively, had anemia. Medication (any, 98.5%) and/or lifestyle/dietary advice (90.2%) was prescribed to the vast majority of anemic women. Interestingly, nonanemic women were also prescribed lifestyle/dietary advice (78.4%). More than three-quarters of the nonanemic women were in the second (48.3%) or third (30.0%) trimesters and the majority (78.9%) were estimated by their physician to have moderate or significant risk of iron deficiency.

Exploratory assessment of iron deficiency

Overall, complete data regarding ferritin levels were available for 605/1300 (46.5%) women (57.3, 42.7 and 39.9% at the first, second and third trimesters, respectively) and were similar regardless of estimated risk of iron deficiency (46.9, 45.7 and 53.7% with no, moderate or significant risk, respectively). For women with determined ferritin levels (n = 605), ferritin was <15 μg/l in 30.9% of individuals (18.7, 31.7 and 51.2% at the first, second and third trimesters, respectively), increasing with increased estimated risk of iron deficiency (12.7, 38.1 and 64.6% with no, moderate or significant risk, respectively).

Medication for iron deficiency was prescribed to 812/1417 (57.3%) patients, with the specific treatment documented for 795 patients (Table 1). Lifestyle/dietary advice was prescribed in 80.1% of patients. Iron formulations alone were prescribed to 686/795 (86.3%) of pregnant women, of which 83.4% were specific ferrous sulfate formulations with or without folic acid (Table 1). Iron/folic acid combinations and food supplements with/without iron were prescribed to 1.1 and 12.6% of women, respectively. Figure 3 presents the use of the various medications by duration of pregnancy (Figure 3A) and by estimated risk of iron deficiency (Figure 3B). Prescription of iron alone increased from 75.7% (first trimester) to 94.0% (third trimester), whereas prescription of food supplements with/without iron decreased from 23.7% (first trimester) to 4.4% (third trimester). Similarly, prescription of iron alone increased from 65.3% (no estimated risk of iron deficiency) to 95.3% (significant risk), whereas prescription of food supplements with/without iron decreased from 34.7% (no risk) to 1.56% (significant risk).

Table 1.

Medications prescribed to pregnant women with iron deficiency in the PRECAM study.

Treatment Patients, n (%)
Ferrous sulfate/folic acid (Tardyferon® B9) 504 (63.4)
Ferrous sulfate 80 mg (Tardyferon 80) 41 (5.16)
Ferrous sulfate (Tardyferon) 118 (14.84)
Other iron formulations 23 (2.89)
Folic acid + Tardyferon 8 (1.01)
Folic acid + other iron formulations 1 (0.13)
Food supplements 80 (10.06)
Food supplements + Tardyferon 12 (1.51)
Food supplements + other iron formulations 8 (1.01)
Total 795 (100)
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Tardyferon®: Prolonged-release oral ferrous sulfate.

Figure 3.

Figure 3.

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Medication prescription by (A) duration of pregnancy (n = 782) and (B) estimated risk of iron deficiency (n = 751).

Iron alone (95.8%) represented virtually all prescribed treatment in patients with anemia, whereas iron/folic acid combinations and food supplements (with/without iron) represented only 2.6 and 1.6% of all treatments in this population. A similar trend was observed in nonanemic patients, although food supplements (with/without iron) represented a slightly higher proportion of treatments prescribed to these patients (14.8%).

Data relating to the reason for prescribing treatment were available for 556 pregnant women (478 of whom [86%] received iron alone; iron/folic acid combination or food supplements with/without iron were prescribed to 6 and 72 women, respectively) (Figure 4). Almost half of all 478 patients treated with iron alone had clinical signs of anemia (206 patients, 43.1%) and a similar proportion (39.6%) received iron alone for ‘systematic prevention, pregnancy or supplementation’ reasons. Virtually none of the pregnant women received iron alone for dietary problems, abnormal biology, hemorrhage/blood loss or due to nausea, hot flushes, diabetes or asthma (Figure 4).

Figure 4.

Figure 4.

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Reasons for prescribing iron alone, iron/folic acid combinations or food supplements with/without iron in 556 pregnant women in the PRECAM study.

†Nausea, hot flushes, diabetes, asthma.

Discussion

It is well documented that the prevalence of iron deficiency and anemia is particularly elevated in pregnant women. Based on historical data (published between 1985 and 1998), the prevalence of iron deficiency anemia in pregnant women in Europe ranged from 6 to 30% [4]. The current study (PRECAM) provides a real-life clinical view, from the perspective of gynecologists and midwives in France, of the estimated risk of iron deficiency among pregnant women and explores reasons for the prescription of medications for the management of iron deficiency and anemia.

Many pregnant women in the current study were estimated, by their gynecologist or midwife, to have a moderate or significant risk of iron deficiency throughout the course of their pregnancy. Given the known increased need for iron during pregnancy, resulting from the increased total cell volume, the needs of the fetus and placenta [10], these observations were in line with medical expectations.

Furthermore, our study showed that clinicians estimated the risk of iron deficiency to be moderate or significant during more advanced stages of pregnancy. Patient management guidelines in France require a pregnant woman's individual risk to be evaluated as early as possible in the pregnancy in order to prevent anemia from occurring [21]; indeed, despite the absence of iron deficiency anemia, undiagnosed iron deficiency may already be present in an individual prior to confirmation of pregnancy and it is estimated that up to 50% of women do not have adequate iron stores before pregnancy [22]. There are many potential negative consequences of iron deficiency anemia for pregnant women including increased fatigue, decreased work/daily life performance, increased pressure on the cardiovascular system due to insufficient Hb, reduced resistance to infections and death in cases of hemorrhage during labor) and for the developing fetus (resulting from an insufficient supply of Hb, and therefore oxygen, to the uterus, placenta and the fetus) [11]. Indeed, even mild or moderate iron deficiency anemia during pregnancy can be associated with unfavorable outcomes at birth, including preterm birth, low birth weight and fetal death [8,10–11].

Although a recently updated US Preventive Services Task Force review reported inconclusive evidence regarding screening for iron deficiency [23], international guidelines acknowledge the importance of serum ferritin in diagnosing iron deficiency at the beginning of pregnancy [24]. The risk of iron deficiency was determined by serum ferritin levels in about 50% of cases in PRECAM, with the proportion decreasing slightly with increasing duration of pregnancy. Current French guidelines recommend targeted screening for anemia risk factors and, if necessary, by measuring Hb levels at the beginning of pregnancy, and obligatory screening at the sixth month of pregnancy [21]. While our data are encouraging, these observations indicate that there is room for improvement in routine screening in France. In contrast, serum iron levels alone are of little clinical interest because they are subject to daily variations depending on dietary intake and erythropoietic needs; indeed, serum iron levels should not be used to diagnose iron deficiency [16,25–26], and our analysis showed that very few pregnant women are screened for serum iron alone. These observations indicate that routine screening in France is generally being conducted appropriately, with an evaluation of iron deficiency at the beginning of pregnancy and an evaluation of anemia during the third trimester of pregnancy. However, as is common during pregnancy, there appears to be a lack of screening for iron deficiency in the absence of anemia.

Iron deficiency during pregnancy can be prevented or controlled by counseling individuals and families about sound iron nutrition and iron supplementation during pregnancy, by screening persons on the basis of their risk for iron deficiency and by treating and monitoring individuals with presumed iron deficiency [4]. This may help to reduce the manifestations of iron deficiency and, consequently, improve public health. A recent longitudinal study conducted in more than 380 pregnant women in Switzerland showed that mild iron deficiency anemia and depleted iron stores detected early in pregnancy are not risk factors for adverse maternal or perinatal outcomes in women receiving iron supplements [27]. Using data from national surveys from 46 countries during 2003 and 2009, Lutter and colleagues reported that an estimated 52–75% of women had received any iron tablets/syrup during pregnancy, with the majority receiving iron for less than 90 days [28]. Our data demonstrate that, in the event of an estimated elevated risk of iron deficiency, the choice of iron treatment was most often an oral ferrous sulfate-based product. Our analysis showed that, out of the women receiving iron/folic acid combinations, the highest proportion received them during the earlier stages of pregnancy but, with increasing duration of pregnancy, the proportion of women receiving combination therapy reduced and a greater proportion of women received iron alone. These observations are in line with current French recommendations for the management of iron deficiency [21].

The lack of ferritin and Hb levels in some patients is a limitation of the current study. Indeed, ferritin levels were only measured in 605 of 1300 patients because data were unavailable for the remainder. However, one of the objectives of this trial was to evaluate the practices of French obstetricians, for example, in identifying the reasons for the prescription of medications for iron deficiency and anemia. Determination of serum ferritin is not yet usual practice in developed countries such as France. The future study cohort following this trial will estimate the iron status of anemic pregnant women. In addition, severity thresholds for the risk of iron deficiency were left free to be chosen by individual physicians. The results of this study demonstrate that the thresholds identified by physicians vary from one physician to another.

When interpreting the results from PRECAM, one must bear in mind that this is a descriptive observational study, and the outcomes presented relate to the period of data collection. Moreover, although more individuals are estimated to have iron deficiency than iron deficiency anemia in the general population, some cases of anemia are due to causes other than iron deficiency (e.g., nutritional deficiencies other than iron, genetic traits, renal insufficiency or chronic inflammation), and anemia is not an optimal indicator of iron status in some populations [7]. The current study does not attempt to differentiate the underlying cause of iron deficiency.

Conclusion & future perspective

The PRECAM study demonstrates that, in metropolitan France, the risk of iron deficiency during pregnancy is being managed in accordance with current Haute Autorité de Santé (HAS) and WHO recommendations. Anemia screening (Hb level) is practically systematic (>80% of patients) and is higher than the estimated risk of iron deficiency (59% of patients estimated to have a moderate or significant risk). This practice is in line with current French recommendations [21], which advise screening risk factors of anemia at the beginning of pregnancy and obligatory screening for anemia from the sixth month of pregnancy. Conversely, iron deficiency screening via blood ferritin levels at the beginning of pregnancy (first trimester), and the transferrin saturation coefficient (throughout pregnancy, but particularly in the second and third trimester of pregnancy), is not yet regular practice in France. This evaluation was conducted in around 50% of the pregnant women included in PRECAM; future efforts are needed in order to establish this screening into routine standard practice. Prescribed treatments are in line with French (HAS) and international (WHO) recommendations, which advise anemia treatment (HAS and WHO) based on ‘high’-dose oral ferrous sulfate and an iron deficiency prevention regimen (WHO) based on oral ferrous sulfate with or without folic acid.

We believe that the current insight from the PRECAM study into how gynecologists/obstetricians and midwives approach the risk and management of iron deficiency in pregnant women in France is of general interest to clinicians elsewhere; indeed, due to the fact that anemia may represent a ‘red flag’ for general disease in pregnancy, early diagnosis and management of iron deficiency should improve the overall maternal and fetal prognosis.

Executive summary

graphic file with name 10.2217_whe.15.91-fig5.jpg

  • Anemia, a leading cause of disability worldwide, represents one of the most serious public health problems globally.

  • Although anemia and iron deficiency are common during pregnancy, there is a lack of current data regarding the prevalence of iron deficiency and anemia among pregnant women in France.

  • This observational study explored the risk of iron deficiency and anemia among more than 1500 pregnant women in France and identified reasons for the prescription of medication.

  • Investigators (gynecologists/obstetricians and midwives) estimated that almost 60% of women were at moderate or significant risk of iron deficiency, with the risk increasing with increased pregnancy duration.

  • Treatment (any) was prescribed to virtually all (97.8%) pregnant women who were estimated to have a significant risk of iron deficiency. Iron alone (95.8%) represented virtually all prescribed treatment in patients with anemia.

  • Overall, data regarding hemoglobin levels were available for the majority of all pregnant women and, of these, 15.8% were determined to have anemia. Data regarding ferritin levels (assessment of iron deficiency) were available for approximately half of the pregnant women.

  • In real-life clinical practice in France, the risk of iron deficiency during pregnancy is managed in accordance with current national/international recommendations.

Acknowledgement

The authors thank C Taieb, for providing scientific input into the study.

Financial & competing interests disclosure

This study was granted an unconditional grant by Pierre Fabre Médicament, Castres, France. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

The authors thank DP Figgitt, Content Ed Net, for providing medical writing assistance, with funding from Pierre Fabre SA, Paris, France.

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