Postgraduate Training Course in Reproductive Health/Chronic Disease
Systematic review on the incidence/prevalence of stillbirths
Caracostea Gabriela M.D.
		Department of Obstetrics and Gynecology
		University of Medicine and Pharmacology Iuliu Hatieganu
		Cluj-Napoca, Romania
		Tutors: Ana Betran and Lale Say
		Who/Department of Reproductive Health and Research
See also
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presentation
Abstract
BACKGROUND: Fetal death has been defined by World Health Organization 
		as the death of the conceptus before complete expulsion or extraction from 
		its mother, irrespective of the gestational age. The reported incidence 
		for stillbirths varies from one country to another and can be used as an 
		indicator of antepartum and intrapartum care.
		OBJECTIVE: To provide a tabulation of the incidence of stillbirths in different 
		settings.
		METHODS: A systematic search of the literature was used to identify relevant 
		articles on the incidence of stillbirths. 
		RESULTS: A systematic literature search identified 39 studies. Twelve reports 
		were found to be eligible to be included in the review. All included studies 
		were retrospective. The setting was mentioned in some of them (e.g. large 
		maternity, university hospitals, urban community hospitals).
		The studies were conducted in the following countries: USA - 5 studies, 
		United Kingdom - 4 studies, Canada, Turkey, Sweden and Scotland - each 2 
		studies and 1 study from each of the following countries Australia, Rwanda, 
		Italy, Ukraine, Egypt, Singapore, West Africa, Israel, India and Germany.
		The incidence of stillbirths was between 0.15% and 10%. Developing countries 
		have an incidence of stillbirths between 0.40% and 10%. Most developing 
		countries had an incidence higher than 2%. 
		CONCLUSIONS: The incidence of stillbirths is similar in most settings (around 
		1-2% of the total number of births). 
		In our review more than half of the studies did not stratify the data by 
		antepartum or intrapartum events, type of pregnancy, obstetric history or 
		gestational age. 
		Countries and regions should conduct regular audits of registration practices 
		to determine geographic and temporal trends in the occurrence of live births 
		and stillbirths. 
Background
Fetal death has been defined by World Health Organization 
		as the death of the conceptus before complete expulsion or extraction from 
		its mother, irrespective of duration of pregnancy (1).
		Since the middle of last century, stillbirths (late fetal deaths) and early 
		neonatal deaths (fetal death in the first week of life) have often been 
		combined into a single category of “perinatal” deaths.
		In the past, such a combination was justified by the fact that asphyxia 
		was a common cause of death during labour (intrapartum stillbirth) and shortly 
		after birth. In more recent years, however, the etiologic determinants have 
		diverged sharply, with fewer early neonatal deaths caused by asphyxia and 
		relatively many more caused by congenital anomalies (2).
		Each year, about eight million perinatal deaths occur, 98% of them in developing 
		countries. Perinatal mortality has been more difficult to prevent than infant 
		mortality and has only recently received global attention. Being closely 
		linked to maternal outcomes, perinatal mortality can be used as a proxy 
		indicator for maternal mortality and maternal health care status (5).
		Stillbirths and early neonatal deaths differ substantially with respect 
		to their principal causes although there are conditions such as abruptio 
		placentae and fetal growth restriction that can cause either stillbirth 
		or early neonatal death. However, in most developed countries at the present 
		time, the etiologic differences are far more striking than the similarities.
		Moreover, etiologic determinants differ widely according to whether stillbirth 
		occurs before or during labour. Antepartum stillbirths are often combined 
		with severe maternal, placental or fetal abnormalities, including umbilical 
		cord complications, preeclampsia, intrauterine growth restriction, abruptio 
		placentae and infections . Maternal smoking, advanced maternal age, high 
		parity and obesity are also widely recognized risk factors for antepartum 
		stillbirth.
		Intrapartum fetal death is usually the result of fetal distress and/or obstructed 
		labour and often reflects poor access or poor quality of clinical care during 
		delivery. In developed countries, the vast majority (85–90 percent) of stillbirths 
		occur before labour onset, whereas this proportion is much lower and the 
		overall stillbirth rate is much higher in developing countries. This is 
		particularly true in settings where deliveries occur at home and are attended 
		by untrained people or without having access to emergency obstetric care 
		or where distances to such care pose a risk to fetal survival during labour(2).
		Many previous studies concluded that stillbirths are difficult to prevent 
		because the risk factors had not been adequately identified. Despite efforts 
		to identify the etiological factors contributing to fetal death, a substantial 
		part of fetal deaths are still classified as unexplained intrauterine fetal 
		demise (1). 
		Although the overall perinatal mortality rate has fallen considerably in 
		the past several decades, the number of stillbirths has not decreased as 
		rapidly compared to that of early neonatal deaths.
Objective
To provide a tabulation of the incidence of stillbirths in different settings.
Methods of the review
Criteria for considering studies for this review
Types of participants: Pregnant women or women with at least one stillbirth 
		in the past. 
		Type of study design: Any study in English language providing prevalence 
		or incidence data of stillbirths will be included for assessment, including 
		cross-sectional ,cohort studies and surveys.
		Type of outcome: 
| Incidence of stillbirths = | No of fetal deaths at 20 or more completed weeks of gestation x 100 | 
| No of total births | 
Exclusion criteria:
- studies with no data
- studies with no data about the total number of live births
- studies that provide data on stillbirths related to a very specific risk factor (e.g. fetal malformations, maternal diabetes)
- case-control studies
- reports referring to data collected before 1980
Search strategy
- Medline search (1998 to 2003).
- Textword terms: stillbirth, fetal death, perinatal mortality, and for subheading: epidemiology.
- Articles with data about incidence of stillbirths from the reports identified by the ‘Systematic Review on the Epidemiological Evidence for Maternal Morbidity and Mortality’.
Data extraction form
Standardised forms were used to facilitate the data extraction.
		Regarding stillbirths, the form consists of 3 modules:
- general information
- characteristics of the study
- stillbirth reporting data
This data extraction form was developed and tested for the 
		WHO project A15060: Systematic Review on the Epidemiological Evidence for 
		Maternal Morbidity and Mortality between 1997 and 2002.
		The project aims at providing epidemiological evidence about maternal conditions 
		to support the implementation of maternal and neonatal health programs.
Contents of data extraction form:
Module I includes data on the time and place where the study 
		was conducted.
		Module II includes data on:
- study design
- sampling
- data sources
- lowest unit of data source
- number of eligible subjects (if available)
- sample size
- population studied
- description of the characteristics of the population studied (e.g. socio-economic status, ethnicity, age, etc.)
- description of the health characteristics of the population(e.g. healthy women, women with a specific condition, etc.)
- information about loss to follow-up
- description of the study setting
- place of delivery
- risk factors
Module III. Includes data on:
- 
			incidence of stillbirths 
- 
			incidence of perinatal mortality 
- 
			presence of stillbirth definition, information about stratification of results according to the following criteria: - time of death: ante-or intrapartum
- gestational age
- type of pregnancy: singleton or twins
- obstetric history
- specific age groups: adolescents or women after 35 years
 
Results
The search strategy identified 39 studies, 27 were eligible to be included in the review (table 1). All studies were retrospective. Some of them described the settings (large maternity, university hospitals, and urban community hospitals).
Table 1. Baseline characteristics of included studies.
| Nr | Author | Country | Sample Size | Study period | Study design | Outcomes | 
| 1 | Smith 2000 | Scotland | 466 521 | 1980-1996 | Cohort | Stillbirths, birth weight | 
| 2 | Hefler 2001 | USA | 12 209 | 1993-1994 | Cohort | Stillbirths, postnatal autopsy | 
| 3 | Demissie 2002 | USA | 297 155 | 1995-1997 | Cohort | Stillbirths, neonatal deaths | 
| 4 | Sairam 2002 | UK | 4154 | 1989-1991 | Cohort | Stillbirths | 
| 5 | Joseph 2001 | Canada | 28 442 | 1985-1997 | Cohort | Stillbirths, infant mortality | 
| 6 | Vintzileos 2002 | USA | 10 560077 | 1995-1997 | Cohort | Stillbirths, prenatal care | 
| 7 | Roberts 2002 | Australia | 22346 | 1990-1999 | Cross-sectional | Twins-trends in gestational age, mode of delivery | 
| 8 | Rahlenbeck 2002 | Rwanda | 3497 | 1997-2000 | Incidence survey | Pregnancy outcomes, maternal mortality | 
| 9 | Cotzias 1999 | USA | 659 545 | 1989-1991 | Cohort | Unexplained stillbirths | 
| 10 | Bambang 1999 | West Midlands | 209 780 | 1991-1993 | Cohort | Perinatal deaths, birth weight | 
| 11 | Erdem 2003 | Turkey | 92 587 | 1993 | Cohort | Perinatal deaths | 
| 12 | Lauria 2003 | Italy | 2 824080 | 1989-1993 | Cohort | Stillbirths, infant mortality | 
| 13 | Smith 2001 | Scotland | 10 924 | 1992-1998 | Cohort | stillbirths, preterm delivery | 
| 14 | Bracero 1998 | USA | 20 971 | 1987-1993 | Cohort | Stillbirths, neonatal deaths | 
| 15 | Mogilevkina 2001 | Ukraine | 69782 | 1997-1998 | Cross-sectional | Stillbirths, neonatal deaths | 
| 16 | Stanton 2000 | Egypt | 2123 | 1994-1996 | Incidence survey | Morbidity, mortality of neonates and infants | 
| 17 | Dummer 2000 | England Wales | 8 039269 | 1981-1992 | Incidence survey | Stillbirths | 
| 18 | Huang 2000 | Canada | 115 762 | 1961-1996 | Cohort | Unexplained antepartum deaths | 
| 19 | Tham 1998 | Singapore | 30 270 | 1995-1996 | Cohort | Stillbirths | 
| 20 | Chalumeau 2002 | West Africa | 19 809 | 1994-1996 | Census | Stillbirths | 
| 21 | Mazor 1998 | Israel | 4872 | 1985-1995 | Cohort | Meconium stained amniotic fluid in preterm delivery | 
| 22 | Onderoglu 1998 | Turkey | 25 321 | 1983-1990 | Cohort | Stillbirths | 
| 23 | Agarwal 1998 | India | 6790 | 1988-1992 | Cohort | Stillbirths, abortions | 
| 24 | Cnattingius 1998 | Sweden | 916 745 | 1982-1991 | Incidence survey | Stillbirths | 
| 25 | Winbo 1998 | Sweden | 836 881 | 1983-1990 | Incidence survey | Stillbirths, neonatal deaths | 
| 26 | Kunzel 1998 | Germany | 347 463 | 1990-1995 | Incidence survey | Stillbirths, neonatal deaths | 
| 27 | Hilder 1998 | UK | 171 527 | 1989-1991 | Incidence survey | Stillbirths, neonatal deaths, postneonatal mortality | 
The studies were conducted in the following countries: USA 
		- 5 studies, United Kingdom - 4 studies, Canada, Turkey, Sweden and Scotland 
		- each two studies and one study from each of the following countries: Australia, 
		Rwanda, Italy, Ukraine, Egypt, Singapore, West Africa, Israel, India and 
		Germany.
		The majority of reports (20) did not mention the regional variations (urban 
		or rural) of the population studied (table 2).
Table 2. Baseline characteristics of included studies.
| Characteristics of the population studied | ||||||
| Nr | Population Studied | socio economic status | health | Incidence of stillbirth (%) | Incidence of neonatal death (%) | Definition included | 
| 1 | Unknown | Unknown | Pregnant women | 0.5 | - | Yes | 
| 2 | Unknown | Unknown | Pregnant women | 1.12 | - | Yes | 
| 3 | Unknown | Unknown | Multiple pregnancy | 1.7 | 1.9 | Yes | 
| 4 | Unknown | Unknown | Multiple pregnancy | - | - | No | 
| 5 | Unknown | Unknown | Multiple pregnancy | 2 | - | No | 
| 6 | Unknown | Unknown | Pregnant women | 0.28 | - | Yes | 
| 7 | Unknown | Unknown | Multiple pregnancy | 2.2 | - | No | 
| 8 | Rural | Unknown | Pregnant women | 10 | - | No | 
| 9 | Unknown | Unknown | Pregnant women | 0.9 | - | No | 
| 10 | Unknown | Low socio-economic. level | Pregnant women | 0.5 | 0.09 | No | 
| 11 | Unknown | Unknown | Pregnant women | 1.8 | 1.72 | Yes | 
| 12 | Unknown | Mixed socio-economic level | Pregnant women | 0.51 | 0.79 | Yes | 
| 13 | Unknown | Low socio-ec. Level | Teenagers, non-smokers | 0.5 | 0.2 | Yes | 
| 14 | Urban | Jewish | Pregnant women | 0.3 | 0.5 | Yes | 
| 15 | Mixed | Industrial region | Pregnant women | 0.8 | 1.61 | yes | 
| 16 | Mixed | Households | Pregnant women | 1.6 | 8.52 | Yes | 
| 17 | Mixed | Low socio-economic level | Pregnant women | 0.52 | - | |
| 18 | Unknown | Unknown | Pregnant women | - | 0.71 | No | 
| 19 | Unknown | Unknown | Pregnant women | 0.4 | - | No | 
| 20 | Urban , semi urban | Women permanently living in this area | Pregnant women | 2.59 | 4.18 | Yes | 
| 21 | Unknown | Unknown | Pregnant women,>3 antenatal visits | 0.88 | 0.94 | No | 
| 22 | Unknown | Unknown | Pregnant women | 2.05 | - | No | 
| 23 | Rural | Low income households | Pregnant women | 2.08 | - | Yes | 
| 24 | Unknown | Unknown | Pregnant women | 0.15 | - | No | 
| 25 | Unknown | Unknown | Pregnant women | 0.72 | 0.72 | Yes | 
| 26 | Unknown | Unknown | Pregnant women | 0.34 | 0.2 | Yes | 
| 27 | Unknown | Unknown | Pregnant women | 0.48 | 0.42 | Yes | 
Only two studies were conducted in rural populations (in 
		Rwanda and India) reporting a higher incidence of stillbirths compared to 
		other data (10% and 2.08%).
		Two studies were conducted in urban regions and three studies involved populations 
		from mixed regions.
		Nine studies mentioned the socio-economic characteristics of the population 
		and amongst these four were conducted in populations with low socio-economic 
		level.
		All of the studies mentioned the health characteristics of the population 
		(pregnant women). One of the studies, conducted in 10 924 non-smoking teenagers, 
		reported a 0.5% incidence of stillbirths.
		One study reported for both, stillbirths and early neonatal deaths, the 
		same value (0.72%).
		The incidence of stillbirths varied between 0.15% and 10%. Developing countries 
		reported an incidence of stillbirths between 0.40% and 10%. Most of the 
		studies with an incidence higher than 2% were conducted in developing countries.
Discussion
This review provides tabulation for the incidence of stillbirths 
		in different parts of the world. Aiming at a global estimate is difficult 
		because of differences in the methods used (crude or crude and adjusted 
		estimates). Also, the definition used for stillbirth was different between 
		the studies. Similar, differences in the cut-off limits for the gestational 
		age for miscarriage varied from 20 weeks of gestation (United Kingdom) to 
		28 weeks of gestation (India).
		The data source in most of the studies was medical records. When comparing 
		studies conducted in the same country only Turkey and Scotland reported 
		similar data. The sample size of the studies in other countries varied between 
		2123 (Egypt) and 10,560,077 (USA) which could be the reason for the differences.
		More studies conducted in developed countries were identified (18) compared 
		to developing countries (9).
		Data regarding perinatal mortality in developing countries derived mainly 
		from hospital based studies (5). An important percentage of births in these 
		countries occur at home, attended by relatives or traditional birth attendants 
		making it therefore difficult to distinguish between stillbirths and live 
		born infants who died soon after birth. 
		In our review there were 9 studies conducted in developing countries of 
		which two were conducted in a rural population (Rwanda, India). In almost 
		all of the studies performed in developing countries the incidence was more 
		than 2% compared to studies performed in developed countries where the incidence 
		was mostly less than 2%.
		Many factors could be responsible for the differences in the study results. 
		One of the most important factors is the difference in antenatal and neonatal 
		care in the different settings. Early detection of severe pathologies is 
		more frequent in developed countries where fetal death can be diagnosed 
		before 20 weeks of gestation. In developing countries these cases are rarely 
		diagnosed before the first fetal movements are felt.
		Fertility rates in developed countries are lower than in developing countries 
		and this 
		may be another factor related to the incidence of stillbirths.
		The combination of stillbirths and early neonatal deaths in perinatal mortality 
		rates could be misleading. Stillbirths should be reported separate by gestational 
		age and pregnancy and health characteristics of the women. Furthermore, 
		stillbirths should be separated into antepartum and intrapartum stillbirths, 
		reflecting on the quality of prenatal or delivery care, respectively.
		Also, it is very important to describe the characteristics of the population 
		studied and the characteristics of the settings. In our review more than 
		half of the studies did not report the data for these characteristics. Studies 
		that reported the incidence of stillbirths according to gestational age 
		found that it increased with gestational age. This is more commonly observed 
		in twin pregnancies.
		The risk of stillbirths was increased in specific age groups like teenagers 
		and women aged more than 35.
		Studies that stratified data by antepartum or intrapartum fetal death showed 
		a small increase in antepartum stillbirths relating more causes to antepartum 
		death than intrapartum death .
		The differences between all the studies included in this review regarding 
		the incidence of stillbirths reflects variations in completeness of registration 
		of pregnancy and delivery.
		Countries and regions within countries should conduct regular audits of 
		registration practices to determine geographic and temporal trends in the 
		occurrence of live births and stillbirths near the limit of viability, for 
		example, at 20-25 completed weeks of gestational age. When assessing incidence 
		of stillbirths, prenatal records and delivery records should be reviewed.
Conclusion
The incidence of stillbirths in most settings is around 
		1-2% of the total number of births.
		About 55% of studies reported the definition for stillbirth and the limit 
		between miscarriage and stillbirth varied from 20 weeks of gestation (United 
		Kingdom) to 28 weeks of gestation (India).
		In our review about half of the studies reported antepartum or intrapartum 
		events, type of pregnancy, obstetrical history of the mother or gestational 
		age.
		The majority of the studies (21) involved developed countries and the incidence 
		of stillbirths between these studies varied from 0.15% (Sweden) till 2.2% 
		(Australia). 
		Developing countries have an incidence of stillbirths between 0.40% and 
		10%. Most reports with an incidence higher than 2% were from developing 
		countries.
		Countries and regions within countries should conduct regular audits of 
		registration practices to determine geographic and temporal trends about 
		the occurrence of live births and stillbirths.
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