Abstract
Background
We report on late gestation stillbirth rate (SBR) and impact of COVID-19 pandemic in a nationally representative mortality survey in nine Indian states.
Methods
Detailed verbal autopsy (VA) interviews using PHMRC VA tool were undertaken for stillbirths reported between 2019 and 2022 from the adult most knowledgeable about the circumstances in a nationally representative population sample of one million. Late gestation stillbirth was defined as a fetal death with gestation period of ≥ 7 months where the fetus did not show any sign of life. We estimated overall SBR, and pre-, during and post-COVID-19 periods per 1000 births for India. We also report on stillbirth registration, last rites, and whether the mother was able to see and hold her baby.
Results
We identified 878 stillbirths in 59,639 births from 240,975 households (87.1% participation) covering an average population of 1,002,098. The annualised SBR between 2019 and 2022 was 14.7 (95% CI 13.8–15.7) per 1,000 births. The SBR in post-COVID-19 period (18.3; 95% CI 16.1–20.8) was significantly higher than pre-COVID-19 period (12.7; 95% CI 11.2–14.4) and COVID-19 period (14.4; 95% CI 13.0-15.9). The annualised antepartum SBR was estimated at 6.1 (95% CI 5.5–6.7) and intrapartum SBR at 5.0 (95% CI 4.5–5.6) per 1,000 births. Stillbirth certificate was available for only 8 stillbirths; last rites were performed for nearly all stillbirths (98.9%) and burial was the most commonly reported practice (90.9%). Only 187 (25.5%) mothers had seen and held their stillborn baby, 194 (26.4%) had only seen their baby, and 353 (48.1%) had neither seen nor held their baby.
Conclusions
This study documents an increase in SBR post COVID-19 pandemic as compared with the pre- and pandemic periods in India. Findings could contribute to monitoring of SBR, development of bereavement guidelines, and strengthening of stillbirth registration to address the burden of stillbirths in India.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12884-026-08650-z.
Keywords: Stillbirth, India, COVID-19 pandemic, Antepartum, Intrapartum, Registration, Last rite, Bereavement
Background
India accounted for the highest number of stillbirths globally in 2021 estimated at 567,000 stillbirths at ≥ 20 weeks gestation and 397,300 at ≥ 28 weeks gestation as per the recent estimates from the Global Burden of Disease Study [1]. The estimated stillbirth rate (SBR) for India in 2021 was 24·7 (95% confidence interval [CI] 20·4 to 30·3), 24 (95% CI 19·8 to 29·5), and 17·4 (95% CI 14·4 to 21·3) per 1,000 births for ≥ 20 weeks, ≥ 22 weeks, and ≥ 28 weeks gestation period cut-offs, respectively [1]. The other modelled estimates for SBR available from the UN-IGME report estimated SBR ≥ 28 weeks gestation at 12.2 (95% CI 9.9–15.1) for India in 2021 [2].
India’s commitment to a single-digit SBR for ≥ 28 weeks gestation period under the India Newborn Action Plan (INAP) by 2030 [3], requires robust and timely estimation of stillbirths on a routine basis, for which challenges have been identified previously [4–8]. Furthermore, there is mixed evidence of COVID-19 pandemic’s impact on SBR, with reports of both increase and no change across the high-income countries (HICs) and low- and middle-income countries (LMICs) [9–11]. Also, significant literature has dealt with changes in SBR among women who had Covid-19 during pregnancy but little evidence is available on pregnancy outcomes at the population level for births during the Covid-19 pandemic irrespective of Covid-19 during pregnancy, including from India [12–16]. In this background, we report on changes in SBR ≥ 28 weeks gestation as a result of COVID-19 pandemic in India documented as part of a nationally representative survey of deaths for all ages in India between 2019 and 2022 [17]. Given the substantial burden of stillbirths in India, we also present data that could contribute towards developing national bereavement guidelines for stillbirth affected parents in India.
Methods
This study was part of an all-cause mortality survey that was approved by the Institutional Ethics Committee of the Public Health Foundation of India. All participants provided written informed consent, and for those who could not read or write, the participant information sheet and consent form were explained by a trained interviewer and a thumb impression was obtained.
Detailed sampling methods for the survey were reported previously [17], and the methods relevant to this paper are described here. Nine states—Assam, Gujarat, Haryana, Jharkhand, Kerala, Maharashtra, Odisha, Tamil Nadu, and Uttar Pradesh—were selected as per the sampling criteria described elsewhere [17]. The sample size for deaths was estimated 25,800 deaths for a 1,000,000 population sample based on the crude death rate for each of the sampled state. We used a multi-stage sampling procedure to select 1,000 clusters from 50 districts in the nine sampled states with the aim of having a sample representative of the population of India [17]. Based on the Census 2011 data [18], 20 study clusters of about 1,000 population each were sampled in each district using stratified systematic sampling technique, with the proportion of rural-urban clusters similar to the proportion of rural-urban population in each district. All households in the sampled cluster were mapped and listed in a serpentine pattern starting from the north-east corner and ending in the opposite corner. A household was defined as people eating from the same kitchen.
Data collection was undertaken from January to August 2023. A total of 279 trained interviewers enumerated the number of current usual residents, in-migration and out-migration, births, deaths, and stillbirths that occurred between January 2019 and December 2022 in each sampled household across the nine states. Relevant to this paper, date of birth, sex of the baby born and whether it was a livebirth or stillbirth was documented for each birth in the sampled households in the enumeration. Stillbirths were documented by confirming that none of the three signs of life were present (did not cry, breathe, and move) to differentiate stillbirths and early neonatal deaths.
All households with at least one stillbirth born to a usual resident woman between January 2019 and December 2022 were considered eligible for the detailed survey. We made at least three attempts to reach all eligible stillbirth interviews. The interview data were captured across the nine states using Open Development Kit software in hand-held tablets by 208 interviewers trained in standardised study procedures [19]. In the survey, the interviewers re-confirmed for the absence of the signs of life and then undertook confidential interviews in local language with the mother of the baby or most knowledgeable adult if mother was not available. A verbal autopsy (VA) interview was done using the Population Health Metrics Research Consortium (PHMRC) VA questionnaire which includes close-ended questions followed by an open narrative [20–23]. Interview documented socio-demographic details for the household and mother, place of delivery, gestation period at the time of delivery, and when the baby’s last movements were felt by the mother. If a woman had reported to a health provider for delivery but she was sent back by the health provider to come later for delivery was considered as a deferred delivery; and if a woman had gone to another facility for delivery prior to delivering where she delivered was termed as a referred delivery [16, 24]. The reason(s) for deferred and referred deliveries were documented as well. The reason(s) for stillbirth was documented only if communicated by the health care provider to the mother/family. Details and place of last rites, availability of stillbirth certificate, and the reason(s) for not registering the stillbirth were documented. Lastly, the mother was also asked if she had seen and/or held the baby, and the reasons for not seeing and/or holding the stillborn baby. The interview tool was developed in English and was translated into the local languages of the sampled states, and then back-translated into English to ensure accurate and relevant meaning and intent of the questions. Pilot testing of the tool was carried out in each state and modifications made as necessary.
Data analysis
The late gestation stillbirth was defined as a foetal death with gestation period of ≥ 7 months (≥ 28 weeks) wherein the baby did not show any sign of life (did not cry, breathe, and move). Data on gestation period was reported in months by the respondents as is the practice in India; we assumed 1 month as 4 weeks to identify stillbirths for this analysis. We use the term stillbirth from here on indicating late term stillbirths. Before the analysis, open narratives from interviews of all stillbirths and day 0 neonatal deaths were reviewed by two authors (MA and SSPD) to re-confirm the baby’s status at the time of birth. A total of four stillbirths were reassigned as neonatal deaths and 11 neonatal deaths were reassigned as stillbirths in this exercise.
We report annualised stillbirth rate (SBR) per 1,000 births using enumeration data from 2019 to 2022 for both sexes combined, by sex, and by place of residence, and the change in overall SBR between 2019 and the other years for India. The study period was categorised into three periods - pre-COVID-19 (January 2019 to March 2020), COVID-19 (April 2020 to February 2022), and post-COVID-19 (March 2022 to December 2022) [25]. We estimated SBR separately for these three time periods. SBR by the type of stillbirth is also reported, wherein antepartum and intrapartum classification was undertaken based on the baby’s last movement felt by the mother as an indication of the time of death as described in detail elsewhere [16, 24]. Distribution of deferred and referred deliveries with the reasons for the same, and of the cause of stillbirth as indicated by the health provider is reported. The reported causes of stillbirth were categorised as mother- and baby-related for meaningful interpretation.
The coverage of stillbirth registration is reported with the reason(s) for not registering stillbirth by state. We report on the patterns of last rite practice for stillborn babies by state, and the distribution of the place of burial by sex of the baby, place of residence, wealth index quartile, place of delivery, type of stillbirth, and state. The distribution of having seen and/or held the stillborn by the mother is reported by sex of the baby, place of residence, wealth index, place of delivery, and state. The reason(s) for the mother not seeing and/or holding the stillborn baby for India and by state.
Wealth index quartiles were calculated using the standard methods used in the National Family Health Survey to calculate wealth index [26, 27]. We report chi-square test of significance as relevant; and 95% confidence interval (CI) are reported for all estimates. All analyses were performed using STATA V.13.1 software (StataCorp, USA).
Role of the funding source
The funders had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.
Results
A total of 59,639 births including 878 stillbirths between year 2019 and 2022 were identified during the enumeration from 240,975 households (87.1% participation) covering an average population of 1,002,098. Distribution of 878 stillbirths identified among all births is shown in Appendix Table 1 for select socio-demographic characteristics. A little over half the stillbirths were boys (502, 57.2%) and 740 (84.3%) were in rural areas. Stillbirths accounted for 0.28% of all births in Tamil Nadu to 2.60% in Uttar Pradesh between 2019 and 2022 among the sampled states. A total of 251 (1.3%), 389 (1.4%), and 235 (1.8%) births were stillbirths in the pre-COVID-19, COVID-19, and post-COVID-19 period, respectively. A total of 197 (22.4%) stillbirths were reported with a gestation period of 7 months, 182 (20.7%) with 8 months, and 494 (56.3%) 9 months or more (Additional file Fig. 1).
Stillbirth rate
The annualised overall SBR was estimated at 14.7 (95% CI 13.8–15.7) per 1,000 births for India between 2019 and 2022, and was significantly higher for boys than girls, and in rural than in the urban areas (Table 1). The overall SBR in pre-COVID-19 period (12.7; 95% CI 11.2–14.4) was similar to the COVID-19 period (14.4; 95% CI 13.0–15.9) but it was significantly lower than the SBR in post-COVID-19 period (18.3; 95% CI 16.1–20.8) as shown in Table 1. The SBR in post-COVID-19 period was significantly higher than the pre-COVID-19 SBR for boys and in the rural areas and was higher but of borderline significance for girls and in the urban areas.
Table 1.
Annualised stillbirth rate between 2019–2022, and stillbirth rate in three time periods based on COVID-19 for India
| Annualised stillbirth rate (95% confidence interval) |
Stillbirth rate (95% confidence interval) |
||||
|---|---|---|---|---|---|
| Pre-COVID-19 period* | COVID-19 period* | Post-COVID-19 period * | |||
| Overall | 14∙7 (13∙8–15∙7) | 12∙7 (11∙2–14∙4) | 14∙4 (13∙0–15∙9) | 18∙3 (16∙1–20∙8) | |
| Sex of the baby | Boy | 16∙3 (14∙9–17∙8) | 14∙4 (12∙2–16∙9) | 15∙9 (13∙9–18∙1) | 20∙1 (17∙0–23∙8) |
| Girl | 12∙5 (11∙2–14∙7) | 10∙5 (8∙6–12∙7) | 12∙4 (10∙6–14∙4) | 15∙3 (12∙5–18∙7) | |
| Place of residence | Rural | 16∙4 (15∙3–17∙6) | 14∙0 (12∙2–16∙0) | 16∙5 (14∙9–18∙4) | 19∙8 (17∙2–22∙8) |
| Urban | 9∙5 (8∙0–11∙2) | 8∙8 (6∙5–11∙9) | 7∙6 (5∙8–10∙0) | 14∙0 (10∙5–18∙7) | |
*Pre-COVID-19 period is January 2019 to March 2020; COVID-19 period is April 2020 to February 2022; and post COVID-19 period is March to December 2022
The annualised antepartum SBR was estimated at 6.1 (95% CI 5.5–6.7) and intrapartum SBR at 5.0 (95% CI 4.5–5.6) per 1,000 births; and the rest could not be classified. Additional file Table 2 provides the distribution of type of stillbirths in India between 2019 and 2022. The proportion of intrapartum stillbirths was significantly higher in girls (p < 0.001) and in the year 2020 (p = 0.034), however this needs to be interpreted within the proportion of unclassified stillbirths across the variable categories.
Stillbirth distribution by place of delivery
Detailed interview was available for 745 (84.9% participation) stillbirths. Among these stillbirths, 333 (44.7%) were delivered at a public health facility, 282 (39.2%) at a private health facility, and 120 (16.1%) were delivered at home. Distinct pattern for place of delivery was seen by state with Kerala (66.7%), Gujarat (60.0%) and Haryana (50.0%) having a higher proportion of stillbirths in a private health facility whereas Odisha (72.6%), Assam (69.6%), Maharashtra (54.8%) and Tamil Nadu (54.6%) in a public health facility (p < 0.001; Additional file Fig. 2). Nearly 60% of all stillbirths in the public and private sector health facilities were in a higher-level facility (Additional file Fig. 3), and this distribution was similar irrespective of the study period.
Stillbirth characteristics and cause
A deferred delivery was reported for 53 (7.11%) of all stillbirths, with no deferred deliveries were reported in Kerala, Maharashtra, Odisha, and Tamil Nadu. Majority of the mothers were told to go back as there was still time for delivery (43, 81.1%) and 7 (13.2%) had to go back as the health provider was not available for delivery. Referred delivery was reported for 140 (22.4%) of all stillbirths delivered in a health facility; 56 (88.9%) and 43 (56.3%) of the stillbirths delivered at the higher-level facilities were referred deliveries in public sector and private sector heath facilities, respectively. A total of 197 responses were available for the reason for referral (67.6% provided one reason and the rest multiple), and the major reason cited for referral was complicated delivery (72.9%) as shown in Additional file Fig. 4.
The health care provider had informed of a reason for 257 (34.5%) of the 745 stillbirths, with 119 (46.3%) reporting a mother-related reason and 137 (53.3%) baby-related reason. Issues related to the uterus, placenta, or amniotic fluid (30.3%), and maternal health conditions (30.3%) including high blood pressure infection, anaemia, jaundice were informed the most under the mother-related reasons (Additional file Fig. 5). Baby died in womb (40.2%) and Meconium Aspiration Syndrome (21.9%) were informed as the most common baby-related reasons (Additional file Fig. 5). A significantly higher proportion of respondents who delivered in the private health facilities (133, 45.6%; p < 0.001) reported being informed by the healthcare provider about the reason for the stillbirth compared to those who delivered in public health facilities (117, 35.1%) or a home (7, 5.8%).
Stillbirth registration and last rites
Data on stillbirth certificate was available for all but one case. Stillbirth certificate was available for only 8 (1.1%) stillbirths. Among the 736 not registered stillbirths, the major reason cited was because the baby was born dead (656; 89.1%) followed by no need for it (119; 16.2%).
Performing of last rites was reported for nearly all stillbirths (98.9%). Burial was the most commonly reported practice accounting for 90.9% of the cases (Fig. 1). Among those who were buried, one-third were buried at a graveyard, 24.8% in an agricultural land, 20.5% near a waterbody, 10.6% at home, and 9% in the health facility premises (Table 2). State-level variations were reported in the place of burial with graveyard reported for majority in Kerala (100%) and Haryana (72.6%), home in Assam (57.7%) and Tamil Nadu (45.5%), health facility premises in Odisha (40.9%), and agricultural land in Uttar Pradesh (31.1%). The proportion of burial at graveyard was significantly higher in urban area (p < 0.001), in wealth quartile 2 (p = 0.002), in home delivery (p = 0.003), and in unclassified stillbirths (p < 0.001).
Fig. 1.
Distribution of the last rite practice followed for stillborn babies by state. Other included thrown into the bushes/forest/outskirts of the village and given to hospital staff
Table 2.
Distribution of the place of burial of stillbirths for those who were buried by select socio-demographic characteristics
| Variable of interest | Variable category | Number of stillbirths buried | Place of burial (% of variable category) | Chi-square test of significance p-value | ||||
|---|---|---|---|---|---|---|---|---|
| Graveyard/ crematorium |
Near waterbody | Health facility premises | Home | Agricultural land | ||||
| Overall | 677 | 237 (35∙0) | 39 (20∙5) | 61 (9∙0) | 72 (10∙6) | 168 (24∙8) | ||
| Sex of baby | Boy | 383 | 125 (32∙6) | 84 (21∙9) | 35 (9∙1) | 43 (11∙2) | 96 (25∙1) | 0∙895 |
| Girl | 291 | 111 (38∙1) | 54 (18∙6) | 26 (8∙9) | 29 (10∙0) | 71 (24∙4) | ||
| Don’t know | 3 | 1 (33∙3) | 1 (33∙3) | 0 | 0 | 1 (33∙3) | ||
| Place of residence | Rural | 570 | 173 (30∙4) | 127 (22∙3) | 54 (9∙5) | 59 (10∙4) | 157 (27∙5) | < 0∙001 |
| Urban | 107 | 64 (59∙8) | 2 (11∙2) | 7 (6∙5) | 13 (12∙2) | 11 (10∙3) | ||
| Wealth index quartile | Q1 | 224 | 60 (26∙8) | 52 (23∙7) | 20 (8∙9) | 33 (14∙7) | 59 (26∙3) | 0∙002 |
| Q2 | 187 | 63 (33∙7) | 39 (20∙9) | 13 (7∙0) | 19 (10∙2) | 53 (28∙3) | ||
| Q3 | 147 | 38 (25∙9) | 27 (18∙4) | 14 (9∙5) | 53 (36∙1) | 15 (10∙2) | ||
| Q4 | 119 | 18 (15∙1) | 21 (17∙7) | 14 (11∙8) | 61 (51∙3) | 5 (4∙2) | ||
| Place of delivery | Public facility | 304 | 71 (23∙4) | 57 (18∙8) | 29 (9∙5) | 109 (35∙9) | 38 (12∙5) | 0∙003 |
| Private facility | 259 | 60 (23∙2) | 54 (20∙9) | 31 (12∙0) | 96 (37∙1) | 18 (7∙0) | ||
| Home | 114 | 37 (32∙5) | 28 (24∙6) | 1 (0∙9) | 32 (28∙1) | 16 (14∙0) | ||
| Timing of stillbirth | Antepartum | 267 | 66 (24∙7) | 63 (23∙6) | 19 (7∙1) | 95 (35∙6) | 24 (9∙0) | 0∙008 |
| Intrapartum | 334 | 89 (26∙7) | 66 (19∙8) | 26 (7∙8) | 115 (34∙4) | 38 (11∙4) | ||
| Unclassified | 76 | 27 (35∙5) | 10 (13∙2) | 16 (21∙1) | 10 (13∙2) | 13 (17∙1) | ||
| State | Assam | 52 | 4 (7∙7) | 12 (23∙1) | 3 (5∙8) | 30 (57∙7) | 3 (5∙8) | < 0∙001 |
| Gujarat | 36 | 20 (55∙6) | 3 (8∙3) | 3 (8∙3) | 3 (8∙3) | 7 (19∙4) | ||
| Haryana | 51 | 37 (72∙6) | 4 (7∙8) | 1 (2∙0) | 11 (2∙0) | 8 (15∙7) | ||
| Jharkhand | 112 | 51 (45∙5) | 21 (18∙8) | 4 (3∙6) | 1 (0∙9) | 35 (31∙3) | ||
| Kerala | 2 | 2 (100) | 0 | 0 | 0 | 0 | ||
| Maharashtra | 57 | 19 (33∙3) | 4 (7∙0) | 13 (22∙8) | 14 (24∙6) | 7 (12∙3) | ||
| Odisha | 44 | 6 (13∙6) | 9 (20∙5) | 18 (40∙9) | 1 (2∙3) | 10 (22∙7) | ||
| Tamil Nadu | 11 | 3 (27∙3) | 0 | 2 (18∙2) | 5 (45∙5) | 1 (9∙1) | ||
| Uttar Pradesh | 312 | 95 (30∙5) | 86 (27∙6) | 17 (5∙5) | 17 (5∙5) | 97 (31∙1) | ||
Seeing and holding stillborn baby
A total of 187 (25.5%) mothers reported having seeing and held their stillborn baby, 194 (26.4%) only having seen the baby, and 353 (48.1%) mothers reported neither having seen nor holding their baby (Fig. 2). A slightly higher proportion of mothers delivering at home reported seeing and holding the baby than the facility deliveries, and variations were observed across the states in the pattern of seeing and holding the baby, however, these differences were not statistically significant (p = 0.095 and p = 0.322, respectively). One-third of the mothers in Haryana and Kerala reported seeing and holding baby, and neither seeing nor holding the baby ranged from 43.1% in Odisha to 72.7% in Tamil Nadu. No significant difference in this pattern was seen by sex of the baby (p = 0.379), place of residence (p = 0.609), or wealth index quartile (p = 0.307). The major reasons for neither seeing nor holding the stillborn baby included family refused to show (40.2%), followed by the mother was unconscious (25.8%) as shown in Fig. 3. Among the 194 mothers who saw but did not hold the baby, 108 (55.7%) reported that family and 51 (26.3%) reported that health provider suggested to not to hold the baby (Additional file Fig. 6).
Fig. 2.
Distribution of mother having seen the baby, having held the baby, and neither for stillbirths in India between 2019 and 2022 by select characteristics
Fig. 3.
Distribution of reasons why the mother neither saw or nor held the stillborn baby born between 2019 and 2022 in India. Reasons are not mutually exclusive
Discussion
To the best of our knowledge, these are the first nationally representative study of ≥ 28 weeks gestation SBR estimates for India based on primary data allowing for an understanding of trends in SBR in the context of the COVID-19 pandemic. We found an increase of 44% in SBR between the pre- and post-COVID-19 pandemic time periods, a high proportion of mothers reported neither seeing or holding their stillborn baby and significant differences in this proportion by the place of delivery, and distinct state-level patterns of stillbirth by place of delivery and place of burial.
The potential implications of COVID-19 on SBR including SBR in pregnant women with COVID-19, SBR in pregnant women without COVID-19, and population-level SBR in pre-pandemic and pandemic periods has been captured in various settings [9, 10, 16, 28]. We have previously reported a 24% increase in SBR from the Indian state of Bihar [16], however such an understanding of impact of COVID-19 pandemic reported in this study from population-representative data at the country-level is not readily available. A recent systematic review has reported substantial disruptions to antenatal care, facility-based deliveries and emergency obstetric care primarily during the first wave of the pandemic in 2020 and highlighting the dearth of high-quality population-representative data on these services across SEAR countries including India [29]. Similar findings have been reported from the Health Management Information System (HMIS) in India [30]. The increase in SBR due to COVID-19 has been attributed to reduced antenatal surveillance, a reluctance to access in-hospital care due to increased stress and anxiety, and missed appointments due to rapid changes in maternity services during the pandemic from elsewhere [14, 31–35]. We have also previously reported on increased SBR in the Indian state of Bihar along with a significant shift for deliveries towards the private sector facilities during the pandemic as many public sector facilities were treating COVID-19 patients, and with some changes in risk factors for stillbirth during the pandemic [16]. This shift, though countered the access-related issues for maternal and newborn services as noted elsewhere as well [36, 37], it also possibly resulted in an increase in SBR as the newborn survival is known to be poor in the private sector in comparison to the public sector in India [38]. Nearly 30% of all institutional deliveries were documented to be in a private facility in India as per the most recent round of the National Family Health Survey (NFHS-5) documenting births primarily between 2014 and 2019, with this share at 43.2% in urban areas and 24.3% in rural areas [26]. There are no recent national level data to understand the trends in place of delivery during and post the COVID-19 pandemic. Though it is not possible for us to comment specifically on the role of private sector for increased SBR in this study as we did not document the place of delivery for all births, it is important to note that there were state-level variations in the proportion of stillbirths by the place of delivery. Furthermore, deferred and referred deliveries were reported for 7% and 22% of stillbirths, respectively, which are also reported to be significant risk factors for stillbirth from the Indian state of Bihar [16, 24]. Almost 90% and more than half of stillbirths delivered at the higher-level facilities were referred deliveries in public sector and private sector heath facilities in this study, with complicated delivery as the most common reason. Poor quality obstetric referral services, higher odds of adverse birth outcomes in referral deliveries, and low competence of health staff providing emergency obstetric care in India have been documented previously [39–43]. Significant efforts are underway in India survival using innovative strategies evolved under the national programme to deliver evidence-based interventions to improve the newborn survival, including the labour room and quality improvement initiative and ensuring linkages and referrals to create a continuous care pathway [44, 45]. Such efforts are likely to further strengthen the quality of care during labour and childbirth in deliveries with complications and will likely result in the significant numbers of stillbirths averted [6, 46].
The annualised antepartum and intrapartum SBR was similar in this population over the study period and one-fourth of the cases could not be classified, with intrapartum stillbirths significantly higher in girls and in the year 2020. The SBR by type of stillbirth needs to be interpreted with caution within the context of unclassifiable cases and that the classification is based on baby’s movement [24, 47–49], and not perinatal autopsy. Only one-third of the mothers reported being informed of the cause of stillbirth by their healthcare provider. Importantly, baby died in the womb was also indicated as a cause of stillbirth without any details of the actual cause of stillbirth. The poor availability of clinical data during pregnancy, labour and delivery remains a major barrier in understanding the causes and risk factors for stillbirths as the dependence on mother’s self-report in surveys has limited consequent understanding [48, 50]. Urgent investments are needed in electronic individual records for improved clinical documentation that can facilitate targeted interventions for stillbirth reduction [51]. Also, the proportion of complete diagnostic autopsy for stillbirths conducted in India is dismal due to sociocultural, religious, technical, financial and infrastructure issues [52, 53]. Efforts are being explored with minimally invasive autopsy and minimally invasive tissue to support establishing accurate cause of stillbirth as these are less invasive, non-disfiguring, quicker and cheaper compared to the standard autopsy in resource-limited settings [54–58].
Comprehensive and timely accounting of levels and trends of stillbirths is crucial for monitoring progress towards INAP SBR target and to identify priorities for further stillbirth reduction at the national and sub-national levels [3, 6]. The challenges with SBR estimation in India in the Sample Registration System and HMIS have been previously detailed [5, 8], and will have to be addressed appropriately to facilitate SBR reduction. Vital registration is another source to understand the magnitude of stillbirths as stillbirth registration is mandatory in India [59]. However, we found negligible stillbirth registration at 1% in our study. The major reason cited for not registering the baby was because the baby was born dead, which seems understandable from the community perspective wherein birth registration is linked to the need for school admission. There is evidence of increased birth registration with increase in facility deliveries in India, which has not translated for stillborn babies despite the majority of these babies being born in health facilities highlighting missed opportunity [60, 61]. Furthermore, details on the place of last rites documented in this study also offer an opportunity to improve upon the stillbirth registration. Nearly 3 in 10 stillborn babies were buried in a graveyard, which could also facilitate improvement in stillbirth registration as is the case with death registration. Broadly, relevant efforts are needed to change the mindset about stillborn babies as a loss of life from a baby born without life in the community and at all levels of the health system and policy-making for a meaningful difference in stillbirth registration [7].
Accelerating progress to address stillbirth also includes offering quality, respectful and supportive bereavement care support services for bereaved parents and families. Countries such as UK, Ireland, and Australia have developed national bereavement care guidelines to support the bereaved families [62–64]. A growing body of evidence suggests beneficial effects for parents who received supportive care including the option to see and hold their baby, especially from HICs [65, 66], with a mixed evidence from LMICs [67–71]. Only one-fourth of the mothers in this study reported having seen and held their stillborn baby, a quarter reported only having seen the baby, and nearly half reported neither having seen nor holding their baby. Importantly, family and healthcare provider were the two most cited stakeholders for making the decision as to the mother seeing or holding her baby. Given the burden of stillbirths in India and recognising the influence of socio-cultural contexts on grief and coping processes, it is critical to comprehend the experiences and unmet needs of bereaved families in India towards the development of a culturally appropriate bereavement care package that can be integrated within the current maternal health services to support bereaved parents and families across all levels of care. Such an effort in India is being led by the Indian Council of Medical Research [72, 73], and findings from this large-scale national study can directly contribute to that effort.
There are many strengths of this study. Data from India has contributed little to the published pooled analysis reporting on population-based estimates on pregnancy outcomes as a result of COVID-19 [74]. This large-scale nationally representative study allows for a detailed understanding of epidemiology of stillbirths by place of delivery and by type pre-, during, and post-pandemic periods comparable across urban and rural settings. Importantly, this was a population-based study of pregnancy outcomes over a time-period and did not evaluate the difference in outcomes between those women who tested positive for COVID-19 or were symptomatic and those women who tested negative. Our SBR estimates were strengthened by documenting all in/out migration among the reproductive age women who had a pregnancy outcome in the period of interest to provide an appropriate denominator of all births. We also strengthened the numerator for SBR estimates by confirming stillbirth at three points in time from enumeration through the analysis by confirming signs of life, which is different from the DHS surveys [75]. There are some limitations to the study findings. The gestational age was captured in months instead of weeks as the pregnancy length in India is reported in months. The last menstrual period forms the basis for most gestational age estimates and is considered a reliable estimate for measuring gestational age [76, 77]. To classify stillbirths as antepartum or intrapartum, we preferred the baby’s movement over the description of stillborn baby because appearance is reported to be a less accurate proxy for death-to-delivery interval [24, 47–49, 78–80]. Lastly, we did not capture early gestation stillbirths in this report, thereby, underestimating the overall SBR for India [1].
In conclusion, beyond documenting the rise in stillbirths, our study underscores that further health system strengthening for maternal and newborn health is an urgent priority in the post-pandemic period to achieve stillbirth reduction in India. The findings also not only underscore the strengthening of stillbirth registration for tracking and monitoring the stillbirths, but also that parental experiences can provide critical insights for developing context-appropriate bereavement care services.
Supplementary Information
Abbreviations
- CI
Confidence interval
- HMIS
Health Management Information System
- HICs
High-income countries
- INAP
India Newborn Action Plan
- LMICs
Low- and middle-income countries
- PHMRC
Population Health Metrics Research Consortium
- SBR
Stillbirth rate
- UN-IGME
United Nations Inter-Agency Group for Child Mortality Estimation
- VA
Verbal autopsy
Authors’ contributions
RD, GAK and LD conceptualised the study and designed the study methods. RD and GAK verified the data underlying this study. RD wrote the first draft of the manuscript. GAK performed data analysis with contributions from RD, MA, SSPD, and MM. LD and RM provided critical input on the interpretation. All the named authors agreed with the final version of the paper, accept the responsibility to submit for publication. RD is the guarantor for overall content of the paper.
Funding
The all-cause mortality survey was made possible by the support of the American people through the United States Agency for International Development (USAID), in collaboration with the Ministry of Health and Family Welfare, Government of India. The publication costs were supported by the Indian Council of Medical Research, New Delhi, India. The funders had no role in study design, data collection, data analysis, or writing of the report. The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.
Data availability
All data and materials relevant to the study are included in the article or uploaded as supplementary information.
Declarations
Ethics approval and consent to participate
The survey was approved by the Institutional Ethics Committee of Public Health Foundation of India (study numbers TRC-IEC 493/22, TRC-IEC 493.1/22 and TRC-IEC 493.2/22). All participants provided written informed consent, and for those who could not read or write, the participant information sheet and consent form were explained by a trained interviewer and a thumb impression was obtained. The study adhered to the Declaration of Helsinki.
Consent for publication
Not applicable.
Competing interests
RM is employee of ICMR. RD is Vice Chair of the International Stillbirth Alliance. Other authors declare no completing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
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