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Postgraduate Training Course in Reproductive Health/Chronic Disease

Systematic review on the incidence/prevalence of stillbirths

Review prepared for the 12th Postgraduate Course in Reproductive Medicine and Biology, Geneva, Switzerland

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:

  1. general information
  2. characteristics of the study
  3. 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

  1. 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]
  2. 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]
  3. 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]
  4. 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]
  5. 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]
  6. 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]
  7. 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]
  8. Rahlenbeck S, Hakizimana C. Deliveries at a district hospital in Rwanda, 1997-2000. Int J Gynaecol Obstet. 2002 Mar;76(3):325-8. [PubMed]
  9. 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]
  10. 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]
  11. Erdem G. Perinatal mortality in Turkey. Paediatr Perinat Epidemiol. 2003 Jan;17(1):17-21. [PubMed]
  12. 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]
  13. 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]
  14. Bracero LA, Byrne DW. Optimal maternal weight gain during singleton pregnancy. Gynecol Obstet Invest. 1998;46(1):9-16. [PubMed]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. 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]
  20. 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]
  21. 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]
  22. Onderoglu L, Tuncer ZS. The clinical predictors of intrauterine fetal death. Turk J Pediatr. 1998 Oct-Dec;40(4):543-7. [PubMed]
  23. 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]
  24. 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]
  25. 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]
  26. Kunzel W. Intrauterine fetal death during pregnancy: limitations of fetal surveillance. J Obstet Gynaecol Res. 1998 Dec;24(6):453-60. [PubMed]
  27. 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]