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 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.
References
- Smith GC. Sex, birth weight, and the risk of stillbirth in Scotland, 1980-1996. Am J Epidemiol. 2000 Mar 15;151(6):614-9. [PubMed]
- Hefler LA, Hersh DR, Moore PJ, Gregg AR. Clinical value of postnatal autopsy and genetics consultation in fetal death. Am J Med Genet. 2001 Nov 22;104(2):165-8. [PubMed]
- Demissie K, Ananth CV, Martin J, Hanley ML, MacDorman MF, Rhoads GG. Fetal and neonatal mortality among twin gestations in the United States: the role of intrapair birth weight discordance. Obstet Gynecol. 2002 Sep;100(3):474-80. [PubMed]
- Sairam S, Costeloe K, Thilaganathan B. Prospective risk of stillbirth in multiple-gestation pregnancies: a population-based analysis. Obstet Gynecol. 2002 Oct;100(4):638-41. [PubMed]
- Joseph KS, Marcoux S, Ohlsson A, Liu S, Allen AC, Kramer MS, Wen SW. Changes in stillbirth and infant mortality associated with increases in preterm birth among twins. Pediatrics. 2001 Nov;108(5):1055-61. [PubMed]
- Vintzileos AM, Ananth CV, Smulian JC, Scorza WE, Knuppel RA. Prenatal care and black-white fetal death disparity in the United States: heterogeneity by high-risk conditions. Obstet Gynecol. 2002 Mar;99(3):483-9. [PubMed]
- Roberts CL, Algert CS, Morris JM, Henderson-Smart DJ. Trends in twin births in New South Wales, Australia, 1990-1999. Int J Gynaecol Obstet. 2002 Sep;78(3):213-9. [PubMed]
- Rahlenbeck S, Hakizimana C. Deliveries at a district hospital in Rwanda, 1997-2000. Int J Gynaecol Obstet. 2002 Mar;76(3):325-8. [PubMed]
- Cotzias CS, Paterson-Brown S, Fisk NM. Prospective risk of unexplained stillbirth in singleton pregnancies at term: population based analysis. BMJ. 1999 Jul 31;319(7205):287-8. [Free Full Text]
- Bambang S, Spencer NJ, Logan S, Gill L. Cause-specific perinatal death rates, birth weight and deprivation in the West Midlands, 1991-93. Child Care Health Dev. 2000 Jan;26(1):73-82. [PubMed]
- Erdem G. Perinatal mortality in Turkey. Paediatr Perinat Epidemiol. 2003 Jan;17(1):17-21. [PubMed]
- Lauria L, De Stavola BL. A district-based analysis of stillbirth and infant mortality rates in Italy: 1989-93. Paediatr Perinat Epidemiol. 2003 Jan;17(1):22-32. [PubMed]
- Smith GC, Pell JP. Teenage pregnancy and risk of adverse perinatal outcomes associated with first and second births: population based retrospective cohort study. BMJ. 2001 Sep 1;323(7311):476. [Free Full Text]
- Bracero LA, Byrne DW. Optimal maternal weight gain during singleton pregnancy. Gynecol Obstet Invest. 1998;46(1):9-16. [PubMed]
- Mogilevkina I, Bodker B, Orda A, Langhoff-Roos J, Lindmark G. Using the Nordic-Baltic perinatal death classification to assess perinatal care in Ukraine. Eur J Obstet Gynecol Reprod Biol. 2002 Jan 10;100(2):152-7. [PubMed]
- Stanton B, Langsten R. Morbidity and mortality among Egyptian neonates and infants: rates and associated factors. Ann Trop Med Parasitol. 2000 Dec;94(8):817-29. [PubMed]
- Dummer TJ, Dickinson HO, Pearce MS, Charlton ME, Parker L. Stillbirth risk with social class and deprivation: no evidence for increasing inequality. J Clin Epidemiol. 2000 Feb;53(2):147-55. [PubMed]
- Huang DY, Usher RH, Kramer MS, Yang H, Morin L, Fretts RC. Determinants of unexplained antepartum fetal deaths. Obstet Gynecol. 2000 Feb;95(2):215-21. [PubMed]
- Tham WL, Tan KH, Tee CS, Yeo GS. Confidential enquiry of stillbirths in current obstetric practice. Int J Gynaecol Obstet. 1999 Mar;64(3):287-96. [PubMed]
- Chalumeau M, Bouvier-Colle MH, Breart G. Can clinical risk factors for late stillbirth in West Africa be detected during antenatal care or only during labour? Int J Epidemiol. 2002 Jun;31(3):661-8. [PubMed]
- Mazor M, Hershkovitz R, Bashiri A, Maymon E, Schreiber R, Dukler D, Katz M, Shoham-Vardi I. Meconium stained amniotic fluid in preterm delivery is an independent risk factor for perinatal complications. Eur J Obstet Gynecol Reprod Biol. 1998 Oct;81(1):9-13. [PubMed]
- Onderoglu L, Tuncer ZS. The clinical predictors of intrauterine fetal death. Turk J Pediatr. 1998 Oct-Dec;40(4):543-7. [PubMed]
- Agarwal DK, Agarwal A, Singh M, Satya K, Agarwal S, Agarwal KN. Pregnancy wastage in rural Varanasi: relationship with maternal nutrition and sociodemographic characteristics. Indian Pediatr. 1998 Nov;35(11):1071-9. [PubMed]
- Cnattingius S, Taube A. Stillbirths and rate of neonatal deaths in 76,761 postterm pregnancies in Sweden, 1982-1991; a register study. Acta Obstet Gynecol Scand. 1998 May;77(5):582-3. [PubMed]
- Winbo IG, Serenius FH, Dahlquist GG, Kallen BA. NICE, a new cause of death classification for stillbirths and neonatal deaths. Neonatal and Intrauterine Death Classification according to Etiology. Int J Epidemiol. 1998 Jun;27(3):499-504. [Free Full Text]
- Kunzel W. Intrauterine fetal death during pregnancy: limitations of fetal surveillance. J Obstet Gynaecol Res. 1998 Dec;24(6):453-60. [PubMed]
- Hilder L, Costeloe K, Thilaganathan B. Prolonged pregnancy: evaluating gestation-specific risks of fetal and infant mortality. Br J Obstet Gynaecol. 1998 Feb;105(2):169-73. [PubMed]