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Indian Journal of Community Medicine: Official Publication of Indian Association of Preventive & Social Medicine logoLink to Indian Journal of Community Medicine: Official Publication of Indian Association of Preventive & Social Medicine
. 2023 Jul 14;48(4):556–561. doi: 10.4103/ijcm.ijcm_428_22

Impact of COVID-19 Pandemic on Maternofetal Outcome in Pregnant Women with Severe Anemia

Meenakshi Singh 1,, Manju Puri 1, Vidhi Choudhary 1, Aishwarya Kapur 1, GS Triveni 1, Gunjan 1, Manisha Patel 1, Vinita Kumari 1
PMCID: PMC10470568  PMID: 37662118

Abstract

Background:

Anemia is the most common nutritional disease in pregnancy with significant adverse maternofetal outcome. The objective of the present study is to study the impact of COVID-19 pandemic on the pregnancy outcomes of women with severe anemia.

Methodology:

A retrospective observational study was conducted in the Department of Obstetrics and Gynaecology at LHMC and SSK Hospital, Delhi. The study included all antenatal women admitted at a gestational age of >26 weeks (third trimester) with severe anemia and hemoglobin level of 7 g/dL. In our study, a total of 4031 women were included as cases during study period (July to December 2022) and 6659 women as controls from pre-COVID-19 period (July to December 2019).

Results:

In present study, a total of 4031 women delivered during study period as compared to 6659 in control period. In the present study, the prevalence of anemia was observed to be 74.7% in the study group and 51.6% in the control group (P < 0.001). Mean hemoglobin level was significantly lower in study group as compared to the control groups P<0.05. Microcytic hypochromic anemia was the most common morphological type of anemia in both groups. Serum ferritin, serum iron, serum B12, and folic acid levels among cases were significantly (P < 0.05) lower as compared to controls. Odds of fetal growth restriction were 1.4 times higher among study group as compared to control groups. The odds of newborn complications such as low birth weight were 2.49 (95% CI: 1.04–5.91) and need for nursery or NICU admission were 4.84 times (95% CI: 0.48–48.24) higher in cases as compared to controls. Low birth rate was higher in cases and was found to be statistically significant.

Conclusion:

COVID-19 pandemic had indirect impact on adverse maternal and fetal outcome in women with severe anemia.

Keywords: Maternofetal outcome, pandemic, severe anemia

INTRODUCTION

Anemia is the most common and most challenging public health problem of the developing countries. It is the most common nutritional disease in pregnancy with significant adverse impacts on maternal and perinatal morbidity and mortality. In 2019, the global prevalence of anemia in pregnant women was estimated at 36.5%.[1] As per recent National Family Health Survey (NFHS-5) report, the prevalence of anemia during pregnancy in India is 45.7% and 54.3% in urban and rural areas, respectively.[2] The important causes of anemia in developing countries include poor nutrition, inadequate iron in diet, poor absorption of iron due to hookworm infestations, diarrhea, suboptimal screening, and treatment and too early, too soon, and too many childbirths. Routine antenatal and postnatal iron supplementation,which is provided free of cost is an important government initiative to reduce anemia in pregnancy. Despite this, anemia remains unabated due to poor compliance with iron supplementation among beneficiaries and lack of commitment among the healthcare providers to screen and treat pregnant women for anemia. COVID-19 pandemic further disrupted the antenatal care services due to repeated lockdowns and related travel restrictions, loss of jobs, associated financial constraints, and the reluctance of pregnant women to visit health facilities for the fear of contracting infection.[3] The lower socioeconomic strata were the worst affected. As with previous epidemics, there was a sudden rise in demand of medical personnel and redistribution of the workforce towards the management of COVID-19 pandemic and resultant reduction in the provision of routine health services.[4] Although COVID-19 infection did not directly cause any increase in maternal mortality, the pandemic resulted in unsupervised pregnancies and subsequent deliveries that adversely affect maternal health.[5,6]

This study was initiated to study the impact of COVID-19 pandemic on pregnancy outcomes in women with severe anemia.

MATERIALS AND METHODS

This record-based retrospective analytical observational study was conducted in the Department of Obstetrics and Gynaecology at Lady Harding Medical College and Smt. Sucheta Kriplani Hospital, New Delhi, for a duration of six months from July 2020 to December 2020, during COVID-19 pandemic (study group) and six months pre-COVID-19 period from July 2019 to December 2019 (control group). The study included all antenatal women admitted at a gestational age of >26 weeks (third trimester) with severe anemia with a hemoglobin level of 7 g/dL for delivery as per WHO classification for grading of severity of anemia in pregnancy.[7]

The case records of patients having severe anemia due to acute blood loss such as antepartum hemorrhage were excluded from the study.

After obtaining ethical clearance from the institutional ethics committee, eligible subjects were identified from birth entry register and case records were retrieved. A proforma was used to record the relevant demographic details including maternal age, registration status of pregnancy, parity, gestational age in weeks at admission, inter-conception period, and gestational age in weeks at delivery; presence of factors contributing to anemia (such as intolerance to iron, non-availability, and lack of antenatal care); clinical complaints at admission (exercise intolerance, easy fatigability, breathlessness, etc.); clinical management data (such as injectable iron, Vit B12, blood transfusion, platelet transfusion); complications (like abruption, postpartum hemorrhage, need of ICU admission, the need for intubation, maternal death, fetal growth restriction); mode of delivery (vaginal delivery or LSCS); laboratory investigations (hemoglobin level, peripheral smear, serum B12, serum folic acid levels, and fetal outcome (gestational age, live or stillbirth, birth weight, APGAR score, and need of nursery/NICU admission). Platelet transfusion in both groups was given to maintain platelet counts above 50,000/mm3 for vaginal delivery and above 80,000/mm3 for cesarean section.[8]

Statistical analysis

The data was collected during the study period and entered into Microsoft Excel spreadsheet. Statistical package for the social sciences for windows, version 18. Continuous variables were expressed as mean ± standard deviation (SD), and categorical variables were expressed as frequencies and percentages. Normality of the data distribution was assessed with the Kolmogorov–Smirnov test. Depending upon normality of data, Chi-square and students t-test were utilized to see the difference between study and control groups with respect to baseline clinical and laboratory characteristics and outcomes. Univariate logistic regression analysis was applied to assess the association between study group and maternal/perinatal outcomes. A P value of less than 0.05 was considered statistically significant.

RESULTS

In the present study, 4031 pregnant women delivered during the study period as compared to 6659 pregnant women delivered during the control period. Of these, 74.7% (3010/4031) and 51.6% (3436/6659) had anemia in study and control groups, respectively. (P < 0.001). The overall prevalence of severe anemia was 1.27 % (51/4031) and 1.16% (77/6659) among all deliveries in the study and control groups, respectively (P>0.05) [Table 1].

Table 1.

Grading of severity of anemia in women admitted in pandemic and control group

Grading of severity of anemia of delivered women Study group (n=4031) Control group (n=6659) P
No anemia (Hb >= 11 g/dL) 1021 (25.3%) 3223 (48.4%) P< 0.0001
Anemia 3010 (74.7%) 3436 (51.6%)
 • Mild anemia (Hb=10-10.9 g/dL) 1750 (43.4%) 1820 (27.3%) P< 0.0001
 • Moderate anemia (Hb=7-9.9 g/dL) 1207 (29.9%) 1539 (23.1%) P< 0.0001
 • Severe anemia (Hb <7 g/dL) 51 (1.27%) 77 (1.16%) 0.616

In the present study, a total of 51 case records from study group and 77 case records from control group were analyzed. Table 2, shows the comparison of epidemiological details, including the mean age of the pregnant women, their antenatal registration status, inter-conception period, mean gestational age at delivery, and antenatal prophylactic iron supplementation. The mean age of women in the study group (27.9 ± 3.1 years) was significantly higher than that in the control group (24.8 ± 4.0 years). There was significantly higher proportion of women with shorter inter-conception period in study group (86.6%) compared to control group (25.9%). Proportion of women taking oral iron prophylaxis was significantly less in the study group (52.9%) in comparison with control group (84.4%).

Table 2.

Comparison of the epidemiological characteristics of pregnant women with severe anemia in pregnancy

Variable Study group (n=51) Control group (n=77) P
Age (in years) 27.9±3.1 24.8±4.0 P< 0.0001
Parity
 Primigravida 36 (70.6%) 50 (64.9%) 0.504
 Multigravida 15 (29.4%) 27 (35.1%)
Antenatal registration
 Yes 20 (39.2%) 43 (55.8%) 0.065
 No 31 (60.8%) 34 (44.2%)
Inter-conception period# P< 0.0001
 <2 years 13 (86.6%) 7 (25.9%)
 >2 years 2 (13.3%) 20 (74.1%)
Gestational age (in weeks) at delivery 36.9±1.6 37.0±2.1 0.903
Preterm birth (<37 weeks of gestation)
 Yes 31 (61.8%) 43 (55.8%) 0.579
 No 20 (38.2%) 34 (44.2%)
Antenatal iron supplementation
 Yes 27 (52.9%) 65 (84.4%) P< 0.0001
 No 24 (47.1%) 12 (15.6%)

#For study group, N=15, and for the control group, N=27

Table 3, describes the clinical presentation at the time of admission in both the study and control groups. Majority of women were asymptomatic in both the groups at the time of admission. Of the symptomatic women, breathlessness the most common symptom in both groups. There was no difference in the clinical presentation in both the groups.

Table 3.

Comparison of clinical characteristics of severely anemic pregnant women in the two groups

Variable Study group (n=51) Control group (n=77)

Clinical complaints and presentation at time of admission*
Breathlessness 11 (21.6%) 16 (20.8%)
Pedal oedema 0 (0.0%) 5 (6.5%)
Dizziness 0 (0.0%) 2 (2.6%)
Anasarca 2 (3.9%) 0 (0.0%)
Asymptomatic 41 (80.4%) 57 (74.0%)

*Multiple responses

All patients received blood transfusion in both the groups in view of severe anemia, whereas 5.9% of patients in the study group and 2.6% in the control group received platelet transfusion.

Parenteral iron was administered to 9.8% patients in study group, whereas none received in the control groups, while parenteral Vitamin B12 was given to 19.6% and 26.8% of patients in the study and control groups, respectively.

The vaginal delivery rates were higher among control group (83.1%) compared to the study group (76.5%); however, the difference was not significant statistically.

Mean hemoglobin levels were significantly lower in the study group compared to that in the control group. Based on the morphology on peripheral smear, the proportion of women with microcytic, dimorphic, macrocytic anemia was 52.9%, 17.6%, 29.4%, respectively in the study group, while the proportion of microcytic, dimorphic, and macrocytic anemia were 50.6%, 10.4%, 39.0%, respectively, in the control group. Microcytic hypochromic anemia was found to be the commonest morphological type of anemia in both study and control groups. The study group had significantly lower serum iron (P < 0.05), serum ferritin (P < 0.001), serum B12 (P < 0.05), and folic acid levels (P < 0.05), compared to those in the control group [Table 4].

Table 4.

Laboratory parameters related to anemia

Variable Study group n=51 Control group n=77 P
Mean Hb (g/dL) 5.4±0.8 6.1±1.2 0.0004
Peripheral smear (Morphological type of anemia)*

Microcytic hypochromic 27 (52.9%) 39 (50.6%) 0.359
Dimorphic 9 (17.6%) 8 (10.4%)
Macrocytic 15 (29.4%) 30 (39.0%)

Serum ferritin and iron levels in microcytic and dimorphic anemia

Serum ferritin (ng/ml) 5.6±5.2 8.6±4.1 0.0004
Serum iron (µg/dl) 25.3±6.5 36.2±5.8 P< 0.0001

Serum B12 and folate levels in macrocytic and dimorphic anemia

Serum B12 (pg/ml) 110.4±34.5 140.7±42.1 P< 0.0001
Serum folic acid (ng/l) 4.1±1.7 4.8±2.3 0.018

*Multiple responses

The odds of maternal death in study group were 6.46 (95% CI: 0.70–59.63) as compared to control group. The odds of maternal complications such as abruption were 2.34 (95% CI: 0.37–14.54), postpartum hemorrhage were 2.65 (95% CI: 0.99–7.04), and ICU admission were 3.29 (95% CI: 0.78–13.80) times higher in study group as compared to control group, but the difference was statistically non-significant due to the wide confidence intervals. Odds of fetal growth restriction were 1.48 times higher in study group as compared to the control group [Table 5].

Table 5.

Comparison of pregnancy outcome in study and control groups

Pregnancy outcomes Study group (n=51) Control group (n=77) OR 95% CI P
Abruption
 Yes 3 (5.9%) 2 (2.6%) 2.34 0.37-14.54 0.914
 No 48 (94.1%) 75 (97.4%)
Postpartum hemorrhage
 Yes 12 (23.5%) 8 (10.4%) 2.65 0.99-7.04 0.050
 No 39 (76.5%) 69 (89.6%)
ICU admission
 Yes 6 (11.8%) 3 (3.9%) 3.29 0.78-13.80 0.103
 No 45 (88.2%) 74 (96.1%)
Need of intubation
 Yes 6 (11.8%) 3 (3.9%) 3.29 0.78-13.80 0.103
 No 45 (88.2%) 74 (96.1%)
Maternal death
 Yes 4 (7.8%) 1 (1.3%) 6.46 0.70-59.63 0.099
 No 47 (92.2%) 76 (98.7%)
Preterm birth (<37 weeks of gestation)
 Yes 31 (61.8%) 43 (55.8%) 1.22 0.59-2.51 0.579
 No 20 (38.2%) 34 (44.2%)
Fetal growth restriction
 Yes 22 (43.1%) 26 (33.8%) 1.48 0.71-3.08 0.284
 No 29 (56.9%) 51 (66.2%)

The odds of neonatal deaths in study group were 4.84 (95% CI: 0.48-48.24) compared to control group. The odds ratio of neonatal complications such as low birth weight were 2.49 (95% CI: 1.04–5.91) and requirement for nursery or NICU admission were 4.84 (95% CI: 0.48–48.24) times higher in study group as compared to control group. Low birth rate was significantly higher in study group. Odds of stillbirth were 1.05 times higher in study group as compared to control group [Table 6].

Table 6.

Perinatal outcome in pregnant women with severe anemia

Outcome Study group (n=51) Control group (n=77) OR 95% CI P
Birth
 Stillbirth 9 (17.6%) 13 (16.9%) 1.05 0.41-2.68 0.910
 Livebirth 42 (82.4%) 64 (83.1%)
Neonatal death*
 Yes 3 (7.1%) 1 (1.6%) 4.84 0.48-48.24 0.178
 No 39 (92.9%) 63 (98.4%)
Baby birth weight <2500 grams*
 Yes 32 (76.2%) 36 (56.3%) 2.49 1.04-5.91 0.038
 No 10 (23.8%) 28 (43.8%)
5 min APGAR score <7*
 Yes 3 (7.1%) 1 (1.6%) 4.84 0.48-48.24 0.178
 No 39 (92.9%) 63 (98.4%)
Need of nursery/NICU admission*
 Yes 3 (7.1%) 1 (1.6%) 4.84 0.48-48.24 0.178
 No 39 (92.9%) 63 (98.4%)

*For study group, N= 42, and for the control group, N=64

DISCUSSION

Main findings

Anemia ranks as the second most common cause of maternal deaths in India contributing to approximately 80% of the maternal deaths in Southeast Asia.[9-11] Anemia is also a defined risk factor for fetal growth restriction, which can lead to perinatal and neonatal morbidity as well as stillbirths. Anemia during pregnancy increases the risk of antepartum hemorrhage, delivery related complications, postpartum hemorrhage, and and puerperal sepsis in the mother. Pregnancy-related complications, maternal mortality, low birth weight, and adverse birth outcomes are among the major poor maternofetal outcomes of anemia in pregnant women in majority of the developing countries, especially Southeast Asia.[12,13]

Though COVID-19 infection has no direct effect on maternal and fetal outcomes, the present study highlights the direct as well as indirect impact of COVID-19 on pregnancy related outcomes. The overall prevalence of anemia, including severe anemia, was higher in the study group compared to control group. In our study, two-thirds of pregnant women with severe anemia in study group (60.8%) did not have any contact with healthcare provider as they were asymptomatic and due to pandemic-related factors like lack of transport facilities, financial constraint, or fear of spread of infection from healthcare centers. A lower number of antenatal care visits and increased unregistered pregnancies contributed to an increase in pregnancy complications and related morbidity and mortality. Davis et al.[14] observed that women preferred home deliveries instead of hospital deliveries due to the fear of contracting COVID infection from healthcare centers. In a WHO-based survey of 37 facilities of low- and middle-income countries, 18% drop and 32% drop in first antenatal care visits and institutional deliveries respectively were reported in the early months of the COVID-19 pandemic.[15]

The pandemic disrupted the healthcare services resulting in lack of access to these women. The inter-conception period of < 2 years was significantly higher in study group. This difference may be due to an increase in sexual exposure consequent to couples staying home due to lockdown, coupled with inaccessibility to family planning services both with respect to contraception and safe abortion services.[16,17]

It is possible that the number of cases of severe anemia during pandemic in the study group is not reflective of the actual numbers. In the present study, 47.1% of women in study group did not receive antenatal iron and folic acid prophylaxis during pregnancy, resulting in anemia and associated complications. A decreased mean hemoglobin level was observed in study group. Similar observations have been reported in other Indian studies.[18,19]

In a study by Justman et al.,[20] the rate of cesarean deliveries, including emergency cesarean deliveries, was similar between the two periods: 22.1% (164/742) in control group vs. 24.1% (147/610) in the study group. However, contrary to this, the cesarean section rates were higher in study group (23.5%) compared to control group (16.9%) but the difference was statistically not significant. The factors contributing to an increased cesarean section rate in study group might be due to the difficulty in close fetal monitoring while wearing PPE and unexpected delays in decision and delivery intervals due to COVID-19 protocols.

More patients in study group required ICU admission due to an increase in complications like abruption and postpartum hemorrhage. In the present study, the odds ratio of maternal deaths among study group was higher in contrast to control group [OR: 6.46 (95% CI 0.70–59.63)]. Similar findings have been reported in the studies by Kumari et al.,[21] [OR: 1.54 (95% CI 0.56–4.25)] and Lumbreras-Marquez et al., [OR: 1·36 (95% CI: 1·22–1·53)].[22] In the present study, the odds of preterm birth before 37 weeks of gestation were 1.22 times higher (95% CI: 0.59–2.51) in study group as compared to control group. Similar findings were observed in the studies by Khalil et al.,[23] Main et al.,[24] McDonnell et al.,[25] and Sun et al,[26] where odds ratio for study group was higher than control group such as OR: 1.11 (95% CI: 0·85–1·44), OR: 1.01 (95% CI: 0·99–1·03), OR: 1.18 (95% CI: 0·91–1·54), and, OR: 1.03 (95% CI: 0·30–3·51), respectively.

In the present study, odds of stillbirth were 5% higher among study group as compared to control group which was similar to pattern found in study by Kumar et al.,[27] [OR: 1·26, (95% CI: 1·00–1·58)], but was in contrast to the study by Caniglia et al.,[28] where odds of stillbirth were higher in control groups as compared to the study group [OR: 0·96, (95% CI: 0·73–1·26)]. In the study by KC et al.,[29] the stillbirth rate in hospitals increased from 14 per 1000 total births before pandemic lockdown to 21 per 1000 total births during lockdown (P = 0·0002). They also reported an increase in neonatal mortality from 13 per 1000 livebirths to 40 per 1000 livebirths (P = 0·0022) during lockdown period.

Only 2 out of 51 women among cases were COVID-19 positive and none of these two required intensive care and had livebirths. The findings of this study show that COVID-19 in itself did not affect the maternofetal outcome.

Recommendations

As India continues to implement public health measures to control the spread of COVID-19, at the same time there is felt need to be prepared for another wave of pandemic to avoid any disruption in maternal health services in these situations. Large surveys are not required to know how healthcare delivery during pandemic can be improved. Instead, there should be adequate preparedness for continuous and effective healthcare delivery during these situations. With the resurgence of COVID-19 cases, it is crucial to be prepared to address the situation. Various programs and interventions such as Ayushman Bharat program,[30] Anemia Mukt Bharat health,[31] and wellness centers,[32] should be nested into ongoing health initiatives. They may be strengthened to the extent that even during pandemics essential healthcare services such as antenatal anemia prophylaxis and treatment are not affected.

Strengths and limitations

The present study was carried out in a government setup of a developing country reflecting the true face of disrupted antenatal care during the COVID-19 pandemic. Despite the setup catering free-of-cost services to the pregnant woman, the pandemic hindered adequate service provision.

One of the limitations of the study is that it is a single-center study at a tertiary hospital so the results cannot be generalized. Second, the analysis includes only those women who were admitted to the facility, while pregnant women with anemia attending outpatient department were not enrolled. Lastly, as it is a retrospective, observational study with a small sample size, and it does not take into account other independent factors affecting delay in patient seeking antenatal care and influencing maternofetal outcomes and few of the data could not be retrieved and analyzed, e.g., dose of prophylactic iron being taken by women before admission.

Interpretation

As is the situation in any pandemics, the healthcare system of India faced a great challenge during the COVID-19 pandemic, exerting indirect effects on the vulnerable antenatal group and an increase in adverse maternofetal outcomes of pregnant women.

CONCLUSIONS

The indirect effects of COVID-19 pandemic on pregnancy outcome were observed. The study showed lower mean Hb levels, lower iron reserves and B12 levels, increased cesarean section rate, increased perinatal mortality rate, increased number of stillbirths together with the increased likelihood of abruption in the study group. This indicates towards interruption in the provision of antepartum care and compromised quality of antenatal care.

Contribution to authorship

Author’s contribution: MS contributed in planning, carrying out, analyzing, and writing up of the work, MP contributed in the conception and final proof check of the manuscript, VC, AK, TG, G, MP, and VK contributed in data collection and analysis.

Details of ethics approval

Ethical approval is taken by the Institutional Ethics Committee of Lady Harding Medical College, New Delhi.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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