European Journal of Cardiovascular Medicine

Anemia is one of the most common nutritional and haematological disorders affecting women of reproductive age and is defined in pregnancy by the World Health Organization (WHO) as a haemoglobin (Hb) concentration below 11 g/dL. Globally, an estimated 38% of pregnant women, or nearly 32 million, were anemic in 2011, with the highest burden in South Asia and sub-Saharan Africa [1,2]. In low- and middle-income countries, anemia during pregnancy is driven mainly by inadequate dietary intake of iron and other micronutrients, repeated pregnancies with short birth intervals, infections and parasitic infestations, and poor access to antenatal care [3].

India continues to carry one of the highest burdens of anemia in pregnancy in the world. The National Family Health Survey-4 (2015–16) reported that 50.3% of pregnant women aged 15–49 years were anemic [4], despite decades of implementation of the National Nutritional Anaemia Prophylaxis Programme and, later, the National Iron Plus Initiative [5]. Facility-based and community-based Indian studies have often reported far higher figures, ranging from 50% to well over 80% depending on the region, the socio-economic profile of the population and the haemoglobin cut-off used [6,7,8,9]. The problem is therefore not merely one of prevalence but also of severity, since a large proportion of women reach tertiary hospitals only late in pregnancy with moderate or severe anemia.

The physiology of pregnancy predisposes to anemia. Plasma volume expands by nearly 40–50% while red cell mass increases by only 20–30%, producing haemodilution, and the total iron requirement of a singleton pregnancy is approximately 1000 mg, of which the greater share is needed in the second and third trimesters [10]. Iron deficiency accounts for the majority of cases, but deficiencies of folate and vitamin B12, chronic infections, hookworm infestation, malaria and inherited haemoglobin disorders such as thalassemia and sickle cell disease are important additional contributors, particularly in India where predominantly cereal-based, vegetarian diets provide poorly bioavailable iron and little vitamin B12 [11,12,13].

The consequences of anemia are serious for both mother and baby. Maternal complications include reduced work capacity, cardiac decompensation, pre-eclampsia, postpartum haemorrhage, puerperal sepsis and, in severe cases, death [14]. Foetal and neonatal risks include preterm birth, intrauterine growth restriction, low birth weight, poor Apgar scores, perinatal mortality and iron deficiency in infancy [15,16,17,18]. Anemia is also a recognised indirect cause of a considerable share of maternal deaths in India.

A combined clinical and pathological (haematological) profile, correlated with etiology and with maternal and foetal outcomes, is useful for clinicians and pathologists alike, because it guides the choice of investigations and treatment and identifies women who need early referral. The present hospital-based study was therefore undertaken to describe the clinicopathological profile of anemia in pregnant women attending a tertiary care hospital.

AIMS AND OBJECTIVES

To estimate the prevalence and grade the severity of anemia among pregnant women attending a tertiary care hospital. To study the socio-demographic, dietary and obstetric factors associated with anemia in pregnancy. To describe the clinical presentation and the haematological (peripheral smear and red cell indices) profile of anemic pregnant women. To classify anemia etiologically and to assess maternal and foetal outcomes in relation to the severity of anemia.

This was a hospital-based, prospective, observational study carried out in the Departments of Obstetrics and Gynaecology and Pathology of a tertiary care teaching hospital in India over a period of 18 months, comprising 12 months of enrolment and follow-up of the enrolled women until delivery and the puerperium. Approval of the Institutional Ethics Committee was obtained before the start of the study and written informed consent was taken from every participant.

Sample size

The sample size was calculated using the formula n = Z²pq/d², taking the prevalence of anemia in pregnancy as 50.3% from NFHS-4 [4], a confidence level of 95% and an absolute precision of 5.7%, which gave a minimum of 296 women. The sample was rounded up to 300 women, enrolled by consecutive sampling.

Inclusion and exclusion criteria

Inclusion criteria: pregnant women aged 18–40 years with a singleton pregnancy, of any gestational age and parity, who gave consent and were willing for follow-up until delivery.

Exclusion criteria: multiple gestation; known chronic renal disease, chronic liver disease, malignancy or overt haemorrhagic disorder; history of blood transfusion or parenteral iron in the preceding three months; women who had already been treated for anemia in the current pregnancy; and women who delivered elsewhere or were lost to follow-up.

Data collection

Data were collected on a pre-tested structured proforma. It recorded age, residence, education, occupation, socio-economic status (modified Kuppuswamy scale [19]), dietary habit (vegetarian or mixed), gravidity, birth interval, gestational age, antenatal registration (booked if registered before 20 weeks with at least four antenatal visits), and intake of iron-folic acid tablets (regular if at least 100 tablets had been consumed as advised under the national programme [5]). Detailed clinical examination included pallor, koilonychia, glossitis, angular stomatitis, oedema, pulse rate, blood pressure, cardiac auscultation and abdominal and obstetric examination.

Laboratory investigations

Venous blood (3 mL) was collected in an EDTA vial and analysed within two hours on a five-part automated haematology analyser to obtain Hb, packed cell volume (PCV), red blood cell count, mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH), mean corpuscular haemoglobin concentration (MCHC) and red cell distribution width (RDW). Peripheral blood smears were stained with Leishman stain and examined by two pathologists for red cell morphology, and reticulocyte counts were performed by supravital staining [20]. Serum ferritin (chemiluminescence immunoassay), vitamin B12 and folate were estimated in women with a dimorphic or macrocytic picture or where the diagnosis was doubtful; a ferritin level below 15 ng/mL was taken as confirming iron deficiency [21,22]. Haemoglobin variant analysis (HPLC) and a sickling test were performed in women with persistent microcytosis and a normal or raised ferritin. Urine routine examination and stool examination for ova and cyst were done in all anemic women.

Classification of anemia

Anemia was diagnosed when the Hb was below 11 g/dL and graded as mild, moderate or severe as shown in Table 1 [5,21]. Trimester-specific cut-offs [23] were not applied so that results remain comparable with national survey data. On the smear, anemia was classified as microcytic hypochromic, normocytic normochromic, macrocytic (megaloblastic) or dimorphic. Etiological categories were assigned by integrating the smear, red cell indices, ferritin, B12/folate levels and haemoglobin variant analysis.

Table 1: WHO criteria used for grading anemia in pregnancy

Outcome variables and management

Maternal outcomes recorded were pregnancy-induced hypertension/pre-eclampsia, antepartum haemorrhage, mode of delivery, postpartum haemorrhage (blood loss >500 mL after vaginal delivery), puerperal sepsis, need for blood transfusion and maternal death. Foetal outcomes were preterm birth (<37 completed weeks), low birth weight (<2.5 kg), stillbirth and admission to the neonatal intensive care unit. All anemic women were managed as per the departmental protocol: oral iron with folic acid for mild and moderate anemia, parenteral iron sucrose for those intolerant to or non-responsive to oral iron or presenting late, vitamin B12 for documented deficiency, deworming after the first trimester, and packed cell transfusion for severe anemia near term or with decompensation.

Statistical analysis

Data were entered in Microsoft Excel and analysed with SPSS software (version 25). Continuous variables are expressed as mean ± standard deviation and categorical variables as numbers and percentages. The chi-square test (Fisher's exact test where expected counts were below five) was used for categorical variables and one-way ANOVA for comparison of means across severity groups. A p value below 0.05 was considered statistically significant

A total of 300 pregnant women fulfilled the criteria and were analysed. Their mean age was 25.4 ± 4.3 years (range 18–39 years) and the mean gestational age at enrolment was 29.6 ± 7.8 weeks. The overall mean haemoglobin was 9.8 ± 1.9 g/dL, and 9.0 ± 1.6 g/dL among the anemic women.

Prevalence and severity of anemia

Anemia was present in 213 of the 300 women, giving a prevalence of 71.0%. Mild anemia was the most frequent grade, followed closely by moderate anemia, while 25 women (8.3% of all women; 11.7% of anemic women) had severe anemia (Table 2, Figure 1). No woman had very severe anemia (Hb <4 g/dL).

Table 2: Prevalence and severity of anemia in pregnant women (N = 300)

Socio-demographic and obstetric factors

The prevalence of anemia was highest in women below 20 years (81.5%) and in those aged 35 years or more (75.0%), but the difference across age groups was not significant (p = 0.71). In contrast, anemia was significantly more common among rural women (80.1% vs 58.9%), among illiterate or poorly educated women, and with declining socio-economic status; it was 87.8% in the lower class compared with 46.3% in the upper and upper-middle classes (Table 3).

Table 3: Association of anemia with socio-demographic characteristics

NS: not significant.

Table 4 shows the dietary and obstetric factors. Anemia increased progressively from the first (52.6%) through the second (67.3%) to the third trimester (77.8%) (p = 0.005). Primigravidae had a lower prevalence (65.3%) than women of gravidity four or more (80.0%), although this trend did not reach significance (p = 0.14). Among multigravidae, an interpregnancy interval of less than 24 months was associated with a higher prevalence (81.3% vs 71.2%), but again without statistical significance. Vegetarian women, unbooked women and women who took IFA tablets irregularly or not at all had significantly higher rates of anemia; only 47.1% of women who had taken IFA regularly were anemic, compared with 97.4% of those who had taken none (p <0.001).

Table 4: Association of anemia with dietary and obstetric factors

NS: not significant.

Clinical profile of anemic women

Among the 213 anemic women, pallor (93.0%) and easy fatigability or generalised weakness (82.6%) were the commonest findings, followed by breathlessness on exertion (43.2%), dizziness (33.3%) and palpitations (30.0%). Pedal oedema was seen in 27.2%, and signs of chronic iron deficiency such as angular stomatitis or glossitis (16.0%) and koilonychia (12.7%) were noted in a minority. Pica was reported by 9.9%. Tachycardia was present in 23.0% and a functional systolic murmur in 14.6% (Table 5). Symptoms and signs became more frequent and more marked as the Hb fell; all 25 women with severe anemia were symptomatic and 17 had breathlessness at rest or on minimal exertion.

Table 5: Clinical features in anemic pregnant women (n = 213)

Multiple features could be present in the same woman; percentages therefore exceed 100.

Haematological (pathological) profile

Red cell indices fell significantly and RDW rose progressively with increasing severity of anemia (all p <0.001 by ANOVA, Table 6). The mean MCV declined from 88.4 fL in non-anemic women to 70.3 fL in those with severe anemia, and the mean RDW increased from 13.4% to 18.7%, reflecting increasing anisocytosis.

Table 6: Haematological parameters according to severity of anemia (mean ± SD)

On the peripheral smear, microcytic hypochromic picture was the commonest (56.8%), followed by a dimorphic picture (27.2%), normocytic normochromic (9.4%) and macrocytic anemia with macro-ovalocytes and hypersegmented neutrophils (6.6%) (Table 7). Pencil cells and target cells were frequently seen in the microcytic smears, and a few women showed leucocytosis with eosinophilia (n = 19), which prompted stool examination. Stool examination detected ova of hookworm in 17 women (8.0% of anemic women).

Table 7: Peripheral smear morphology in anemic women (n = 213)

Etiological classification

Iron deficiency anemia was the most frequent etiological type (66.7%). A further 21.6% had combined deficiency of iron and folate and/or vitamin B12 (dimorphic anemia), and 6.6% had pure megaloblastic anemia due to folate or vitamin B12 deficiency, the latter being more frequent among strict vegetarians. Anemia of chronic disease or infection accounted for 2.8%, and haemoglobinopathies (β-thalassemia trait in three and sickle cell trait in two women) for 2.3% (Table 8).

Table 8: Etiological classification of anemia (n = 213)

Maternal and foetal outcomes

Adverse outcomes were more frequent in anemic than in non-anemic women (Table 9). Low birth weight (28.6% vs 13.8%, p = 0.007) and need for blood transfusion (17.8% vs 3.4%, p = 0.001) were significantly higher among anemic women. Preterm delivery (15.0% vs 6.9%) was borderline (p = 0.055), while pre-eclampsia, postpartum haemorrhage, puerperal sepsis, stillbirth and NICU admission were numerically higher in anemic women without reaching statistical significance in this sample. One maternal death occurred in the anemic group in a woman with severe anemia who developed cardiac failure in the immediate postpartum period.

Table 9: Maternal and foetal outcomes in anemic and non-anemic women

NS: not significant. *Fisher's exact test; other p values by chi-square test.

The risk of adverse outcome rose steeply with the severity of anemia (Table 10, Figure 2). Among women with severe anemia, 56.0% delivered low-birth-weight babies, 32.0% delivered preterm and 68.0% required blood transfusion, compared with 13.8%, 6.9% and 3.4%, respectively, in non-anemic women (p <0.001, p = 0.004 and p <0.001).

Table 10: Selected outcomes according to severity of anemia

Treatment received

Oral iron with folic acid was the primary modality in 151 of 213 anemic women (70.9%), parenteral iron sucrose in 24 (11.3%) and blood transfusion in 38 (17.8%) (Table 11). In addition, all 60 women with megaloblastic or dimorphic anemia (28.2% of anemic women) received parenteral vitamin B12, and hookworm-positive women received albendazole after the first trimester. Of the 25 women with severe anemia, 17 were transfused, mostly after 34 weeks of gestation.

Table 11: Primary treatment modality in anemic women (n = 213)

Vitamin B12 (n = 60) and deworming (n = 17) were given in addition to the above.

Anemia remains a leading obstetric problem in India, and the present hospital-based study confirms this. The prevalence of 71.0% is higher than the national estimate of 50.3% for pregnant women in NFHS-4 [4] and the global estimate of about 38% [1,2], but it lies within the wide range of 50–90% reported by Indian hospital and community studies [6,7,8,24]. Our figure is expected to be higher than population-based estimates because a tertiary hospital receives referred, late-booking and high-risk women, and because a large part of its catchment is rural and of lower socio-economic status. Similar high figures have been reported from hospital-based studies in Maharashtra and Karnataka [25,26], and from neighbouring South Asian countries [27,28].

The severity profile shows that mild and moderate anemia together made up 88.3% of anemic women, whereas severe anemia constituted 11.7%. A substantial share of moderate and severe anemia has likewise been documented in the ICMR multi-centre survey of pregnant women in India [8]. The importance of severe anemia lies in its consequences: 68.0% of our severely anemic women needed transfusion and there was one maternal death, in keeping with the strong association between severe anemia and maternal mortality reported in earlier analyses [6,14].

Socio-demographic and obstetric determinants

We found no significant relation between anemia and maternal age, although the youngest women (below 20 years) had the highest prevalence. Adolescent pregnancy compounds the iron needs of growth with those of pregnancy, and high figures among adolescents have been noted in Indian district surveys [7,9]. The significant association with rural residence, low education and low socio-economic status agrees with the findings of Lokare et al. in Aurangabad and Viveki et al. in North Karnataka [25,26], and with multi-country analyses of low- and middle-income countries [3]. Poor education limits awareness of the need for iron supplementation and a balanced diet, while poverty restricts access to iron-rich foods, and the two act together with early marriage, early childbearing and low autonomy in health decisions.

Anemia increased with advancing gestation, being present in 52.6% of women in the first trimester and 77.8% in the third trimester. This is explained by the progressive rise in iron demand and haemodilution in the later half of pregnancy, when requirements can no longer be met from diet and depleted stores [10,29]. Although primigravidae had the lowest prevalence and grand multigravidae the highest, the trend was not statistically significant, as also observed in some Indian reports, suggesting that nutritional status and supplementation matter more than parity alone. A short interpregnancy interval (<24 months) showed a higher prevalence of anemia, consistent with incomplete replenishment of iron stores between pregnancies [11].

Dietary habit was a strong correlate: 81.3% of vegetarian women were anemic against 62.7% of women on a mixed diet. Non-haem iron in cereal- and pulse-based diets has low bioavailability because of phytates and tannins, and vegetarian women are also at risk of vitamin B12 deficiency, which is widespread in India [11,12]. The most striking association, however, was with antenatal care and IFA use. Only 47.1% of women who took IFA regularly were anemic, while 97.4% of those who took none were, and unbooked women had a much higher rate than booked women. Poor compliance with IFA tablets in India is attributed to gastrointestinal side effects, forgetfulness, lack of counselling and inadequate supply, as documented in a study from coastal Karnataka [30]. These findings underline that the availability of the National Iron Plus Initiative and Anemia Mukt Bharat is not enough unless tablets are actually consumed [5,31], and that a Cochrane review has shown daily oral iron to reduce the risk of maternal anemia at term and of iron deficiency [32].

Clinical profile

Pallor and fatigue were the most consistent features, seen in 93.0% and 82.6% of anemic women. Pallor is a simple bedside sign and remains the mainstay of screening in peripheral facilities, but its sensitivity for mild anemia is limited, and 15 anemic women in our series (7.0%) had no clinically obvious pallor. This supports routine laboratory estimation of Hb at every antenatal visit rather than reliance on clinical examination [6,24]. Symptoms of cardiovascular strain, such as exertional dyspnoea, palpitations and pedal oedema, were commoner with lower Hb levels, and features of chronic iron deficiency such as koilonychia, glossitis and pica were seen in a minority, as is usual in clinical descriptions of iron deficiency in pregnancy [29,33].

Haematological profile and etiology

The gradual fall in MCV, MCH and MCHC and the rise in RDW with increasing severity is the expected biochemical footprint of progressive iron-restricted erythropoiesis, and a raised RDW was the earliest indicator of anisocytosis even in mild anemia [20,33]. Microcytic hypochromic morphology was the predominant smear pattern (56.8%) and iron deficiency was the leading cause (66.7%), which agrees with Indian and international literature identifying iron deficiency as responsible for the majority of anemia in pregnancy [6,11,24]. The high proportion of dimorphic smears (27.2%) deserves emphasis. In a population with cereal-based vegetarian diets, iron deficiency commonly coexists with folate and vitamin B12 deficiency, and treating with iron alone may fail to correct the anemia. Pure megaloblastic anemia was seen in 6.6%, a relatively small share, possibly because the routine prescription of folic acid in antenatal clinics masks folate deficiency while vitamin B12 deficiency goes undetected [12].

Hookworm infestation was found in 8.0% of anemic women. Chronic intestinal blood loss from hookworm is a recognised contributor to anemia in pregnancy in endemic areas and is preventable by deworming after the first trimester [13]. Haemoglobinopathies contributed 2.3%, which is small, but is important because these women do not respond to iron and require genetic counselling and partner screening. In our practice, red cell indices, peripheral smear and ferritin were sufficient to sort out most cases, and HPLC needs to be reserved for women with unexplained microcytosis who are not iron deficient [20,22].

Maternal and foetal outcomes

Anemic women had a higher requirement for blood transfusion and more frequent postpartum haemorrhage, puerperal sepsis and pre-eclampsia, although only transfusion reached statistical significance in this sample. A larger series would be needed to confirm the other maternal differences. The rise in low birth weight from 13.8% in non-anemic women to 56.0% in severely anemic women fits the dose–response relationship reported in a large systematic review of low- and middle-income countries [17], and in earlier Indian and Pakistani studies [18,34]. Haider et al. showed that the risks of low birth weight and preterm birth increase as maternal Hb falls below about 9.5–10 g/dL [16], and the cohort of Patel et al. from rural Maharashtra similarly related maternal anemia to poor pregnancy outcomes [35]. A direct correlation between maternal haemoglobin concentration and birth weight has also been demonstrated [36], and iron deficiency has been linked to impaired placental function and hypoxia-driven growth restriction [15]. The borderline association with preterm delivery (p = 0.055) is likely to reflect the modest sample size, since the gradient across severity grades was clearly significant.

Implications for prevention and control

Our findings point to several actionable measures. First, anemia should be identified before pregnancy or at the earliest antenatal visit; anemia in the first trimester in more than half of our women shows that many begin pregnancy already depleted. Second, regular IFA intake should be supported by counselling, side-effect management and supply assurance, since regular users had much lower rates of anemia. Third, women with moderate or severe anemia, late presentation or poor tolerance of oral iron should be offered parenteral iron, which allows faster correction than oral therapy and reduces the need for transfusion [22,33]. Fourth, women with dimorphic or macrocytic pictures should be screened for vitamin B12 and folate deficiency. Finally, the broader package of nutrition education, deworming, delayed first pregnancy, adequate birth spacing and improved female education is needed for a sustained decline, as reviewed in the evidence base for maternal nutrition interventions [37,38].

Limitations of the study

This was a single-centre, hospital-based study, and its findings may not be generalisable to the community. Serum ferritin, vitamin B12 and folate could be estimated only in selected women, which may have led to some misclassification of etiology. Dietary intake was recorded by history and not by quantified dietary recall, and IFA compliance depended on self-report. Some outcome comparisons were underpowered because of the small number of events.

Anemia was present in seven out of every ten pregnant women in this hospital-based study and was mainly nutritional, with iron deficiency and combined iron-folate/B12 deficiency accounting for nearly nine-tenths of cases. Rural residence, low education and socio-economic status, vegetarian diet, late gestation, unbooked pregnancy and irregular or absent IFA intake were the important correlates, and the risks of low birth weight, preterm delivery and need for transfusion increased steadily with the severity of anemia. A simple laboratory panel comprising Hb, red cell indices and a peripheral smear reliably classifies most anemia in pregnancy and guides therapy. Early registration, universal Hb screening, assured and monitored IFA supplementation, correction of B12 deficiency, deworming and use of parenteral iron in selected women should be strengthened to reduce this preventable burden.

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