European Journal of Cardiovascular Medicine

Stillbirth is defined as dead fetus of 1000 g or more at birth, or after 28 completed weeks of gestation, or attainment of at least 35 cm crown-heel length according to WHO.(1) The Perinatal Mortality Surveillance Report (CEMACH)3 defined stillbirth as ‘a baby delivered with no signs of life known to have died after 24 completed weeks of pregnancy (RCOG).(2)Stillbirths constitute a major part of perinatal deaths, yet they largely remain invisible.(3) Every stillbirth is a tragedy and a potential life lost. There are, in addition, many psychosocial consequences for parents, including anxiety, long term depression, posttraumatic stress disorder and stigmatisation.(4)Sadly, woman who have experienced a stillbirth are more likely to experience this again in subsequent pregnancies than those who have not.(5) 

According to a study by Jacob P. Koshy et al, the incidence of stillbirth in 1995 was 3.3 million and this decreased to 2.6 million in 2009.(6) Thus from 1995 to 2009, the stillbirth rate had declined by 14%. Therefore, the stillbirth rate had reduced by 1.1% per year (according to world stillbirth rate). At least 2.65 million cases of annual stillbirths were calculated worldwide in 2008, with 1.2 million of these fetal deaths occurring intrapartum. Because of developments in diagnostic and therapeutic modalities in the last few decades, there has been a marked reduction in stillbirth in developing countries, including India. In spite of this, our stillbirth rate is still much higher than that of the developed countries.

This is a complex situation too, as a probable cause and contributing factors involved are to be identified and a suitable method of termination of pregnancy has to be suggested. Data suggests that most of these deaths could have been prevented.If these factors are identified early implementation of effective and timely interventions could prevent the preventable stillbirths, thus improving maternal and perinatal outcomes.

There are only a few studies in India which have studied these aspects of stillbirths. We therefore, wanted to find out the various factors associated with stillbirth among patients admitted in our hospitalusing the existing ReCoDe system of classification.

This is Cross sectional observational study conducted at the Department of Obstetrics and Gynaecology, Government Medical College, Thrissur. Data was collected from antenatal women who were admitted with Intrauterine foetal demise in labour room/ ward of Obstetrics and Gynaecology Department or who were admitted for other conditions and had Intrauterine foetal demise during their stay in the ward of Obstetrics and Gynaecology Department at Government Medical College Thrissurduring the study period of 12 months, i.e., from 1^stJanuary 2022 to 31^st December 2022. All the study subjects were evaluated for inclusion and exclusion criteria. Data was then collected using a semi-structured interview after obtaining informed and signed consent from the study subjects. The questionnaire included detailed clinical history regarding age, socioeconomic status, parity, body mass index, regularity of ANC, presence of other risk factors, past and present medical and surgical history, any relevant drug intake, gestational age at diagnosis of IUFD (Intra Uterine Fetal Death) and if gestational age was not known all stillbirths weighing more than 500gms were included). The relevant investigations, ultrasonography (growth parameters, liquor, biophysical profile, doppler parameters) were noted.

After delivery, the stillborn baby was examined for foetal weight, morphology, skin staining, maceration, colour and other details were recorded. Placenta was weighed and examined for blood clots, meconium staining, infarcts, oedema, hydropic changes, structural abnormalities like circumvallate placentae or accessory lobes. Umbilical cord was examined for entanglement, knots (true or false), hematomas, strictures, assessment of Wharton’s jelly, number of vessels and insertion abnormalities. Amniotic fluid was noted for volume colour and odour.

Data was coded and entered in Microsoft excel spreadsheet and analysed using SPSS Version 25. Qualitative variables were expressed as proportions and quantitative variables was depicted as mean and median values with its standard deviation and interquartile range respectively. 

A total of 134 study subjects had stillbirthduring the study period of 12 months. These women with intrauterine fetal death were studied to assess the risk factors that may have been associated with stillbirth. Majority of the study participants were in the age group of 20 – 25 years (52, 38.8%), and 25 patients were included in the high-risk group in which 10 (7.5%) were below 20 years and 15 (11.2%) were above 35 years. 76.1% of the study participants were unemployed, while 53% were educated up to or below high school level. Out of the 134 study participants 61.9% belonged to BPL (below poverty line) socioeconomic class and 10.4% were tribal women, with a large majority hailing from rural areas. Among the study participants, 51 (38.1%) were overweight and 27 (20.1%) were obese. (Table no.1)

Table No 1General details of the study participants

There were 58 (43.3%) primigravida women and majority were in the gestational age 31-37 weeks (72, 53.7 %).10 (7.5%) women had a Bad Obstetric History.Majority of the patients 90 (67.2%) were referred from other peripheral centres. There were 4 (3.0%) women who were unbooked, while 20(14.9%) women had irregular antenatal care. 21.6 % of the study subjects with still birth had history of infertility treatment. 25 (18.7 %) had previous history of abortion and out of 76 participants who were multigravida, 43 (56.6%) participants had a previous vaginal delivery while 33 (43.4%) were delivered by caesarean section in their previous pregnancy.10 (7.5 %) study subjects had Bad obstetric history and Previous history of IUD. (Table No.2)

Table No.2 Distribution of study subjects based on maternal factors

In our study, 60 (44.8%) participants had hypertensionwhile 49 (36.6%) of the women had gestational diabetes and 47 (35.1%) study subjects had hypothyroidism. 15 of the participants had maternal infection in the antenatal period of which 5 (3.7%) had viral and 10 (7.5%) had bacterial infection. 47(35.1%) patients had anemia in our study. 11 (8.2%) participants had taken drugs which included antiepileptics, immunosuppressants, 5 (3.7%) had viral maternal infection during pregnancy, 10 (7.5%) had bacterial infection including urinary tract infection, vulvovaginal infections etc. 4 (3.0%) of the study participants were diagnose to have bicornuate congenital uterine anomalies while 9 (6.7%) had cervical incompetence.

The congenital anomalies seen in the foetus included 6 (4.5%) fetuses showed syndromic anomalies, 2 (1.5%) had facial anomalies, 1 (0.7%) had limb anomalies, 4 (3.0%) had gastrointestinal tract anomalies and 4 (3.0%) had neural tube. In our study, out of 134 participants, 2 (1.5%) had birth asphyxia and 1 (0.7%) had birth trauma. MSAF grade I was seen in 3 (22.2%) participants, grade II in 3 (2.2%) and grade III in 6 (4.5%). There was no unidentified cause. (Table No.3)

Table No.3 Distribution of study subjects based on risk factors

Out of 134 study subjects 29 (21.6%) of the women had oligohydramnios, while in 15 (11.2%) polyhydramnios was present. Out of 134 study participants, 31 (23.1%) had experienced placental abruption and 3 (2.2%) had placenta previa. There were 22 (16.4%) foetuses who had cord around neck and meconium-stained liquor was noticed in 12 (8.9%) cases. Among the fetuses majority of the fetus were between 1 – 1.5kg (38, 28.4%) and most of them were male fetuses (73, 54.5%) and macerated stillborn (76, 56.7 %). (Table No.4)

Table No.4 Distribution of study subjects based on characteristics of placenta, amniotic fluid, umbilical cord and foetus

Table No. 5  Frequency and Percentage distribution according to ReCoDe.

IUGR was present in 51 (38.1%) of the study participants, and this was the second most common cause identified, resulting in stillbirth. (Table No.5)

There were a total of 2877 live births and 139 stillbirths during the study period of one year from January 1st 2022 to December 31^st2022 at Government Medical College Thrissur. Being a tertiary referral centre, most (67.2%) of the participants were referred to our hospital after confirming stillbirth from other peripheral centres.

Age Of the Patient

Out of 134 women recruited in the study majority 52 patients (38.8%) were between the age group of 20 – 25 years.  18.7% of the women belonged to the high-risk group. This included 10 women below 20 years and 15 women above 35 years. This was similar to the finding of Murali Paul Kannan in their study conducted at JIPMER Pondicherry, which found that stillbirth rate was higher when maternal age was less than 20 years.(7) In a study conducted by Das Lucy et al, it was found that the largest number of fetal deaths occurred when the maternal age was more than 35 years.(8)There is a felt need for improving family welfare measures to delay the age at first pregnancy, thereby reducing the multiple complications that may occur in the young mother and her new-born baby.

Educational Status

Educated mothers assume greater responsibilities in planning their families and also availing timely and good maternal services. In our study, stillbirths were seen most among women who were not educated beyond high school level (53%).  Those who were illiterate constituted 20.9% of the study population. In a study conducted by Auger N etal in NCBI edition about relation between education and stillbirth, found that low levels of education was associated with stillbirth.(9) This study also found that education beyond high school reduced the risk of perinatal mortality by 20% among the white population.Countries or regions with high female literacy rates have lower birth rates and mortality rates. According to NFHS survey – 3 female literacy rates in Kerala was 93.91% compared with the whole of India (74.04%). Stillbirth rate is less in Kerala compared to the rest of India.(10)

Socioeconomic Status

In our study, 83% of the participants were below poverty line (BPL) as per the ration card issued by the state government of Kerala. Similar findings were reported by Erdem et al in his study from Turkey which showed that stillbirths and neonatal deaths were high among those who had a poor socioeconomic status.(11)In our study, 10.4 % were tribal women. In a study conducted by Sophie L P et al, socioeconomic inequalities in neonatal mortality in eastern India remained high and PVTGs (previously known as Primitive tribal group) are most severely affected.(1)

BMI

Out of 134 study participants, 51 (38.7%) were overweight and 27 (20.1%) were obese. Similar observations were found by Vickflendy et al.(12) They found that overweight and obesity were the leading factors for gestational hypertension and diabetes which if not well controlled, finally led to stillbirth and other maternal complications.

BOH (Bad Obstetric history)

BOH is said to be present in those with a history of at least one stillbirth or more than 2 abortions or at least one perinatal mortality. In our study out of 134 study participants, 10 (7.5%) women had BOH. In a study by Beegum SFs et al they found that in those with a history of previous stillbirth or abortions, gestational diabetes and obstructed labour the most important contributory factors resulting in adverse perinatal outcomes.(13)

OBSTETRIC HISTORY

Out of 134 study participants, 58 (43.3%) were nullipara, 47 (35.1%) were parity two, 24 (17.9%) were parity three while 5 (3.7%) women had a parity of more than 3. Similar observations were found in a study done by Nazia Hashim.(14)Other observations included a previous history of stillbirth was present in 7.5% of the study population, previous history of abortion was seen in 19%, while 43% had a previous history of caesarean section. Previous mode of delivery has been shown to influence fetal outcome. Caesarean delivery in a first pregnancy has been associated with an increased risk of stillbirth in the second pregnancy.(15)Previous history of still birth has been seen to be a risk factor for another stillbirth.(16)

GESTATIONAL AGE

Out of 134 study participants, majority 72 (53.7%) were between 31 and 37 weeks of gestational age. According to a study conducted by Melissa G Rosenstein, the risk of stillbirth after 32 weeks of gestation increases with gestational age, and half of the late fetal deaths occurred at term.(17)

Antenatal Visit Status

Proper antenatal care is essential for a favourable fetal outcome. Antenatal care is reflected by the number of antenatal visits. At least 3 visits are recommended by the National child survival and Safe Motherhood Programme, for the enhancement and expansion of MCH Programme of Govt of India. Majority of the patients in our study had undertaken regular antenatal check-up with a minimum of 3 visits. 90 (67.2%) were referred from other centres while 20 (14.9%) were booked at our institution. 20 (14.9%) participants had irregular ANC. According to a study conducted by Trhas Tadesse Berhe et al in Ethiopia, having a good quality of ANC significantly reduced antepartum stillbirth.(18)

Maternal Infections

Maternal infections like respiratory tract infection, urinary tract infection and other infections associated with fever can contribute to stillbirth. There were 15 (11.1%) women who had fever during their antenatal period among the study subjects. Similar observations were found in a study conducted by Robert et al.(19) In a study conducted by Indu Lata et al, the incidence of poor pregnancy outcome was higher in bacterial vaginosis, with UTI (urinary tract infection).(20)

Anemia In Pregnancy

Anemia is one of the major public health problems globally. Anaemia can be associated with an increased incidence of stillbirths, perinatal deaths, low birth weight babies and prematurity. There were 47 (35.07%) patients who had anemia in our study, which is similar to a study conducted by Pretty P et alat Baroda where they confirmed that anaemic mothers were more prone for preterm delivery and IUGR.(21)

Gestational Hypertension

Out of the 134 study subjects 44.8% had gestational hypertension. Das Lucy et al in their study from Orissa on perinatal mortality reported that gestational hypertension accounted for 21.9% of perinatal mortality.(22)Similar outcomes have been observed in other studies on women with medical complications in pregnancy. In a WHO antenatal care trial analysis of 39615 pregnancies it was found that fetal deaths were higher in pre-eclampsia (2.2%) in comparison to gestational hypertension (1.4%).(16) In a study conducted by Indu Verma et al Preeclampsia-eclampsia was associated with increased risk of adverse perinatal outcomes as compared to Gestational and Chronic Hypertension, necessitating screening, vigilant antenatal care, timely intervention, and referral.(23)

Gestational Diabetes

Diabetes was present in 36.6% of stillbirth which contributed to the third most common cause of stillbirth in our study. According to Johnston et al gestational diabetes with elevated glucose levels is at high risk of unexplained stillbirth. Earlier studies have shown the rate of stillbirths to be 1.5% in diabetic pregnancies. This is five times that of a non-diabetic pregnant population.(24)

Thyroid Disease

Pregnant women with thyroid disease generally have poor obstetric outcome, if the metabolic control is poor. According to Davis et al there is increased incidence of preterm delivery, IUGR and stillbirth associated with thyroid disorders in pregnancy. In our study hypothyroidism was present in 35.1 % of the study participants.(25) 

Iugr And Low Birth Weight

In our study, 38.1 % women had babies with IUGR which was significant, contributing to the second most common cause of stillbirth. 28.4% babies had a birth weight between 1 kg and 1.5kg, while 26.9% babies weighed below 1 kg. Birth weight is one of the most significant factors for adverse fetal outcome. Stillbirth is strongly associated with fetal growth restriction. The risk factors and potential causes of stillbirth and fetal growth restriction mostly overlap. Other studies have shown a strong relationship between stillbirth and growth retardation with half the stillborn being less than 10 percentiles for weight.Data from Brimingham COGS project 2009 reported that stillbirth rate is 7 times higher when fetus have intrauterine growth restriction. In our study 26.9% babies weighed less than 1 kg.(26)

Cord Around Neck

16.4% of stillborn babies had cord around neck in the present study and tight cord around neck can affect the outcome of delivery. A study on perinatal mortality conducted by V Bangal et al found that some of the umbilical cord accidents can be prevented by identifying risk factors like malpresentation, cephalopelvic disproportion, polyhydramnios and multiple pregnancy during the antenatal visits.(27) 

Antepartum Hemorrhage (Aph)

In our study, APH occurred in 23.1% of mothers who delivered stillborn babies. Bhandari S et al in their study reported that pregnancies complicated by APH of unknown origin are at a greater risk of stillbirth and adverse maternal outcome. Abruptio placentae was associated with adverse perinatal outcomes too.There were 3 cases of placenta previa and 2 cases of uterine rupture, all being women with previous caesarean section in our study.(28)

Meconium-Stained Liquor

Meconium-stained liquor was seen in 9% of the stillbirths in our study. Erum et al reported, in their study that meconium-stained liquor is associated with fetal mortality as it is a sign of hypoxia.(29)

Sex Of Baby

There were 54.4% male babies compared to 44% females in the presentstudy. In a study conducted by Debapriya Mondal et al, risk of stillbirth in males is elevated by about 10%.(30) There were 2 cases where the sex of the stillborn babies could not be unidentified. Gender was not a significant risk factor for stillbirth according to a study conducted by Sonal et al.(31)

Congenital Anomalies

Congenital anomalies were present in 12.7% of the stillborn babies in our study. Among them 4.5% babies had syndromic congenital malformations. 3% of the stillborn babies had both neural tube defects as well gastro intestinal tract anomalies. A very high percentage (25%) of stillbirths were attributed to congenital malformations.(16)

Liquor Abnormalities

In our study 21.6% (29 women) patients had oligohydramnios where as 11.2 % (15 women) participants had polyhydramnios. 11.2 % patients had PPROM out of which 3 women had features of chorioamnionitis. 

ReCoDeSYSTEM

The ReCoDe system is an important step towards understanding the causes of still births. In our study, hypertensive disorder accounted for the commonest (44.8%) cause for stillbirth followed by IUGR (38.1%) and diabetes complicating pregnancy (36.6%). In our study we can identify the cause of stillbirth in almost 100% of cases and the factor which contributes maximum was taken into consideration.

In a study by Jason Gardosi et al in 2003 by the conventional Wigglesworth classification 66.2%of the stillbirths were unexplained. The proportion of stillbirths that were unexplained was high regardless of whether a post-mortem examination was carried out or not. By the ReCoDe classification, the most common condition was fetal growth restriction (43%) and only 15.2% remained unexplained. ReCoDe identified 57.7% of Wigglesworth unexplained stillbirths as growth restricted. The size of the category for intrapartum asphyxia was reduced from 11.7% (Wigglesworth) to 3.4%.(32)

In a study conducted by Ajini et al in 2017 which studied 177 cases of stillbirth, the SBR was 38.56 per 1000 live births and this study could explain the cause of stillbirths in 87.58% of cases by using ReCoDe system. In this study, they found that Intrauterine Growth Restriction (41.8%) was the commonest cause for stillbirth. It was followed by hypertensive disorders (27.68%), oligohydramnios (23.16%), congenital anomalies (12.42%), diabetes (14.68%) as the other causes.(16)

The new ReCoDe (Relevant Condition at Death) system is currently the only classification system specifically developed for classification of causes of stillbirths. With the help of new ReCoDe system we can identify the factors leading to stillbirth in our institution. It was seen that the factors leading to stillbirth included socio demographic factors like age of the patient, education, income, occupation, obstetric factors like parity, BMI, maternal medical disorders like gestational hypertension, gestational diabetes, maternal infections and fetal factors like IUGR, Oligamnios, and congenital anomalies of the fetus.

In our study 44.8% stillbirths were associated with hypertensive disorders contributing to the largest number stillbirths. Therefore Preeclampsia-eclampsia has been associated with increased risk of adverse perinatal outcomes, necessitating screening, vigilant antenatal care, timely intervention, and referral. IUGR fetuses were associated with a high stillbirth rate. Prenatal recognition of IUGR will improve pregnancy outcomes by allowing close monitoring and timely delivery. The third most common cause of stillbirth was diabetes and it is recognized to be a major risk factor for stillbirth beyond 32 weeks, where timely intervention could reduce the stillbirth rate. Stillbirth was high in women who had lower levels of education, had a low socioeconomic status and when there were maternal factors like overweight and obesity. Other factors involved were cord around neck, antepartum haemorrhage, prolonged labour and meconium-stained amniotic fluid.

Thus,maternal and child death reviews, tracking of all deaths in the hospitals and simultaneously expanding it to the community in which most births occur will help in sharper understanding of the preventable causes and their management. So, to conclude, for improved perinatal outcomes it is imperative that the strategies should aim to improve quality of antenatal and intrapartum care with timely referral wherever necessary.

Funding Statement: No external funding

Conflict Of Interest: Nil

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