Obstetrics & Gynecology:
Stillbirth Risk in a Second Pregnancy
Gordon, Adrienne MBChB, MPH; Raynes-Greenow, Camille MPH, PhD; McGeechan, Kevin MBiostat, PhD; Morris, Jonathan MBChB, PhD; Jeffery, Heather MBBS, MRCP
From the Department of Neonatal Medicine, Royal Prince Alfred Hospital, Sydney School of Public Health and Sydney Medical School, the University of Sydney, and Perinatal Research, Kolling Institute of Medical Research, Sydney University, Royal North Shore Hospital, St Leonards, New South Wales, Australia.
See related editorial on page 495.
Camille Raynes-Greenow was supported by a National Health and Medical Research Council postdoctoral fellowship.
The authors thank Lee Taylor and the Centre for Epidemiology and Research at the New South Wales Department of Health for providing the MDC and perinatal death data. They also thank the Centre for Health Record Linkage for performing probabilistic record linkage of the data sets.
Corresponding author: Adrienne Gordon, MBChB, MRCP, FRACP, MPH (Hons), Department of Neonatal Medicine, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Sydney, NSW 2050, Australia; e-mail: email@example.com.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To estimate the risk of stillbirth in a second pregnancy when previous stillbirth, preterm, and small-for-gestational age (SGA) births occurred in the previous pregnancy.
METHODS: This was a population-based cohort study in New South Wales Australia from 2002 to 2006. Singleton births in a first pregnancy were linked to a second pregnancy using data from the New South Wales Midwives Data Collection and the New South Wales Perinatal Death Database. Deaths were classified according to the Perinatal Mortality Classifications of the Perinatal Society of Australia and New Zealand. Crude and adjusted hazard ratios were estimated using a proportional hazards model.
RESULTS: Delivery of an SGA newborn in the first pregnancy was associated with increased risks of stillbirth in a second pregnancy (hazard ratio 1.73, 95% confidence interval [CI] 1.15–2.60) and risk was further increased with prematurity (hazard ratio 5.65, 95% CI 1.76–18.12). Stillbirth in a first pregnancy had a nonsignificant association with stillbirth in the second pregnancy (hazard ratio 2.03, 95% CI 0.60–6.90). For women aged 30–34 years, the absolute risk of stillbirth up to 40 completed weeks of gestation was 4.84 per 1,000 among women whose first pregnancy was a stillbirth and 7.19 per 1,000 among women whose first pregnancy was preterm and SGA.
CONCLUSION: Delivering an SGA and preterm neonate in a first pregnancy is associated with greater risks for stillbirth in a second pregnancy than delivering a previous stillbirth. All factors merit improved surveillance in a subsequent pregnancy, and research should address underlying factors common to all three outcomes.
LEVEL OF EVIDENCE: II
Stillbirth is estimated to occur in 2.65 million births globally each year.1 It is a tragedy both for the family and their maternity health care provider. One of the greatest challenges is how to counsel regarding recurrence risk of stillbirth and management of a subsequent pregnancy. Reported recurrence risks vary widely with estimates ranging from a two to a 10-fold increase.2 However, these data arise from studies performed in the 1990s in selected or case–control populations that did not perform adjusted analyses and therefore their clinical usefulness is limited.3,4 It is apparent that recurrence risks are dependent on whether an initial cause of death was established2,5 with some conditions such as those with genetic causes associated with well-defined recurrence.6 However, with much of recent data on stillbirth coming from large established population-based data collections, it is unusual to be able to interpret recurrence risks based on previous cause because such data are often not available. The three largest population-based studies to date do not contain any information on cause of death.7–9
From being relatively understudied, stillbirth research is increasing globally.10 There remains a relative paucity of data on recurrence. A recent meta-analysis of population-based studies in high-income countries pooled data from five studies (three cohorts and two case–control studies) and demonstrated increased risk of stillbirth after previous stillbirth with an adjusted odds ratio (OR) of 2.61 (95% confidence interval [CI] 1.50–4.55)11 There was variation in results resulting in important statistical heterogeneity. One large population-based study from the United States demonstrated a large effect (adjusted OR 5.8, 95% CI 3.70–9.00)12 and two other studies showed no difference.13,14
One major issue in interpreting available data on recurrence risk is how factors known to be associated with stillbirth are adjusted for. Recently exposures in a previous pregnancy and how they relate to subsequent stillbirth have also been examined. Exposures studied include: infant mortality, preterm birth, growth restriction, and cesarean delivery. A summary of the relevant literature, confounders adjusted for, and whether these are from the first or second pregnancy is presented in Appendix 1 (available online at http://links.lww.com/AOG/A280).3,4,7–9,12,13,15–27 For studies in which underlying causal mechanisms are the focus, it seems appropriate to adjust for factors known to be associated a priori with stillbirth and present in a subsequent pregnancy. This, however, includes factors known to be present only at or after the time of delivery such as placental abruption or the neonate being small for gestational age. For a family who attends antenatal counseling in a pregnancy after a previous stillbirth, this information is not yet known when assessing their risk of a subsequent stillbirth.
The purpose of this study was to estimate clinically useful appropriate risks for counseling families regarding subsequent stillbirth using information available from the previous pregnancy and delivery and known current pregnancy risk factors.
MATERIALS AND METHODS
This was a statewide population-based cohort study using deidentified linked data from two New South Wales data sets: the New South Wales Midwives Data Collection and the Perinatal Death Data from the New South Wales Maternal and Perinatal Committee. Ethical approval was obtained from the New South Wales Department of Health Ethics Committee Reference No. DoHEC 2005-06-11. New South Wales is the most populous state in Australia and its 90,000 births per annum account for approximately 30% of the nation's births.
The New South Wales Midwives Data Collection is a mandated population-based surveillance system covering all births in New South Wales public and private hospitals as well as home births.28 It encompasses all live births and stillbirths of at least 20 weeks of gestation or at least 400 g birth weight and performs well in validation studies.29 The Midwives Data Collection requires the attending midwife or doctor to complete a notification form when a birth occurs and collects demographic, maternal health, pregnancy, labor, delivery, and perinatal outcomes data28 (Appendix 2, available online at http://links.lww.com/AOG/A281). The majority of these data is submitted electronically to the Department of Health. The New South Wales Maternal and Perinatal Committee is a quality assurance committee established under the New South Wales Health Administration Act 1982 and is privileged under this Act to carry out confidential reviews of both maternal and perinatal deaths.28 Members are appointed by the Minister for Health.28 A subcommittee called the Perinatal Outcomes Working Party reviews and classifies perinatal deaths using the Perinatal Society of Australia and New Zealand–Perinatal Mortality Classification System, which has been documented to have a high interobserver reliability with a κ value of 0.83–0.95.30 Information available to the working party includes a confidential report on perinatal death (Appendix 3, available online at http://links.lww.com/AOG/A282), postmortem, and placental pathology reports. These reports are forwarded by local hospital perinatal death review committees plus other information that may be relevant, eg, microbiologic results. The classification system has been used throughout all New South Wales since 2002 and formed part of a policy directive, which mandated hospital procedures for review and reporting of perinatal deaths.31 The directive included recommended investigations for stillbirth, a requirement for autopsy to be discussed and offered to every family, and for the placenta to be examined pathologically. The classifications assigned by the Committee after review of the hospital information comprise the final cause of death reported in the population data.
Records for neonates born between 2002 and 2006 from the Midwives Data Collection and Perinatal Deaths data compiled by the New South Wales Maternal and Perinatal Committee subgroup Perinatal Outcomes Working Party were linked using probabilistic record linkage methods in Centre for Health Record Linkage. Neonates were included if they were at least 22 weeks of gestation. Cause of death classification was extracted from the Perinatal Death Database on all stillborn fetuses that had been reviewed by the Perinatal Outcomes Working Party. Perinatal deaths classified as being the result of congenital abnormality by the Perinatal Society of Australia and New Zealand Perinatal Death Classification System (see Appendix 3, http://links.lww.com/AOG/A282) were excluded. This category includes deaths in which a congenital abnormality (structural, functional, or chromosomal) is considered to have made a major contribution to the death and includes terminations of pregnancy for congenital abnormality. Demographic data were collected from both data sets.
Gestational age was determined by certain dates confirmed by ultrasonography before 20 weeks of gestation or, if dates uncertain, by ultrasonography alone before 20 weeks of gestation or, rarely, if both are unavailable, by examination of the newborn. Stillbirth was defined as a neonate born of at least 20 weeks of gestation or 400 g birth weight who did not, at any time after delivery, breathe or show any evidence of life such as a heartbeat. Cause of death was defined using the Perinatal Society of Australia and New Zealand Perinatal Death Classification (Appendix 3, http://links.lww.com/AOG/A282).32 Unexplained stillbirth was defined as the “death of a normally formed fetus before the onset of labor where no predisposing factors are considered likely to have caused the death“ (Perinatal Society of Australia and New Zealand Perinatal Death Classification of 10 or 11). Explained stillbirth was defined as a Perinatal Society of Australia and New Zealand Perinatal Death Classification of 2–9. Small for gestational age (SGA) was defined as a birth weight less than the 10th percentile using Australian population-based percentile charts.33 Premature birth was defined as delivery before 37 weeks of gestation. Further analysis of prematurity and SGA in the first pregnancy was performed after subclassifying births into four categories: appropriate-for-gestational-age term; appropriate-for-gestational-age preterm; SGA term; and SGA preterm.
Crude rates for stillbirth were computed as number of events divided by total number of births and multiplied by 1,000. Univariable comparisons of dichotomous data for frequency distributions of second pregnancy characteristics were made by use of the χ2 test, the χ2 test for trend, or Fisher's exact as appropriate.34 The P values for all hypotheses tests were two-sided, and statistical significance was set at P<.05. The risk of stillbirth was compared between groups by time-to-event analyses using gestation as the time scale and stillbirth as the event. All other births were censored. Crude and adjusted hazard ratios were estimated using a Cox proportional hazards model. The proportional hazards assumption was tested using Schoenfeld residuals, which were plotted against each covariate and the graphs inspected for any trend in the residuals.35,36 Interactions between the log of gestational age and each covariate was created and added to the model individually to test for any departure from the proportional hazards assumption.37 Records with missing data for the variables analyzed were excluded. Statistical analysis was performed using SAS 9.2.
Of 176,260 women who had a first pregnancy in New South Wales between 2002 and 2006, 53,607 had a second pregnancy. After exclusion of missing data, the study group for adjusted analysis of stillbirth risk consisted of 52,110 second pregnancies (Fig. 1). Stillbirth rates for first, second, and third consecutive pregnancies are shown in Figure 2. The first pregnancy stillbirth rate was 4.8 per 1,000. For women whose first pregnancy resulted in a stillbirth, the rate of stillbirth in their subsequent pregnancy was approximately doubled to 8.6 per 1,000. Conversely, for women in whom the first neonate was liveborn, the stillbirth rate in their second pregnancy was 2.8 per 1,000. There were very few stillbirths related to third pregnancies in this cohort; however, increased risks were seen in the third pregnancy relative to a first pregnancy stillbirth (30 per 1,000) even when the second neonate was liveborn.
Table 1 compares the frequency distribution of second pregnancy characteristics between women who had a stillbirth or not in their first pregnancy using univariable analyses. There were significant differences in maternal age with more women younger than 20 years and 40 years or older in the second pregnancy who had experienced a stillbirth in the first pregnancy. There were also higher incidences of both pre-existing and gestational diabetes, preeclampsia, and smoking as well as a higher rate of stillbirth in the subsequent pregnancy. Table 2 shows the adjusted hazard ratios (HRs) for stillbirth in the second pregnancy based on first pregnancy outcome and characteristics of the second pregnancy. Stillbirth in the first pregnancy did not significantly increase the risk for the subsequent pregnancy when the other confounders were adjusted for HR 2.03 (95% CI 0.60–6.90). Significant association remained for subsequent stillbirth if the previous birth was SGA (HR 1.73, 95% CI 1.15–2.60) and a similar increase in risk, although not reaching statistical significance for previous prematurity (HR 1.75, 95% CI 0.97–3.15). There was some evidence (P=.03) that the proportional hazards assumption was not met for preterm birth in the first pregnancy with the risk not constant through gestation and higher before 32 weeks of gestation. Allowing for this nonproportional hazards with the inclusion of an interaction term did not affect the estimates of the other HRs. We did not find an increase in subsequent stillbirth with previous cesarean delivery.
The outcome of the first pregnancy was grouped into five categories based on premature birth and fetal growth restriction to further explore their association with stillbirth (Table 3). Although numbers of stillbirths in the second pregnancy were small, significant risks were observed for previous SGA term births (HR 1.66, 95% CI 1.01–2.74) and the risk increased if the SGA neonate was also premature (HR 5.65, 95% CI 1.76–18.12). The risk of subsequent stillbirth for women who previously delivered a liveborn SGA neonate at less than 37 weeks of gestation was greater than the risk conferred by previous stillbirth. For women aged 30–34 years (median age group) without any of the risk factors listed in Table 2, the estimated absolute risk of stillbirth at 40 weeks of gestation or before for the second pregnancy was 2.39 per 1,000. Absolute risks of stillbirth in the second pregnancy related to first pregnancy outcomes were: 4.84 per 1,000 among women whose first pregnancy was a stillbirth; 4.17 per 1,000 among women whose first pregnancy was preterm but not SGA; and 4.12 per 1,000 among women whose first pregnancy was SGA but not preterm. The highest risk was 7.19 per 1,000 among women whose first pregnancy was both preterm and SGA.
Perinatal Society of Australia and New Zealand Classification of cause of death was available for 85% of the first pregnancy stillbirths and 81% of the second pregnancy stillbirths (Table 4); the remaining 15% and 19% could not be classified based on incomplete or not forwarded confidential reports. Placental histopathology was performed in 90% of the classified initial stillbirths (560/624) and postmortem examination in 51% (317/624). There remained substantial numbers of stillbirths classified as unexplained despite these two investigations: 49% of the placental examinations (273 of 560) and 52% of the postmortems (166 of 317). The risk of stillbirth in the second pregnancy did not differ based on whether the first stillbirth was explained or not; however it must be noted that there were only three second pregnancy stillbirths to women whose first fetus was stillborn. The adjusted risk for previous explained stillbirth was HR 1.82 (95% CI 0.24–13.75) compared with previous unexplained stillbirth (HR 3.11, 95% CI 0.72–13.50).
This is a large population-based study from Australia examining stillbirth recurrence in consecutive pregnancies. Although absolute risks of stillbirth are approximately doubled in a subsequent pregnancy, the finding is not statistically significant after adjusting for current pregnancy characteristics and previous pregnancy outcome. It confirms the findings of prior research that previous pregnancy outcomes of SGA and preterm birth are particularly important when counseling regarding subsequent risks of stillbirth and, in this cohort, conferred greater risk than a previous stillbirth alone.
The strengths of this study include the large record-linked population-based data set and the ability to assess consecutive pregnancies. New South Wales is representative of national data comprising one third of the country's births and is generalizable to other high-income countries. There were few missing data (1.8%) and the data collection has previously been validated.29 The only other published population-based Australian study to assess recurrence risk for stillbirth was published in 2001 and was likely underpowered.24 The standardized Perinatal Society of Australia and New Zealand Perinatal Death Classification System has been used routinely in New South Wales since 2002 and access to these classifications has enabled this analysis to have some significant advantages. The first is the ability to exclude deaths as a result of congenital abnormality from a recurrence risk analysis. This exclusion is important because 1) many of the diagnosed abnormalities may result in a termination of pregnancy beyond 20 weeks of gestation; 2) genetic abnormalities may have high recurrence risks; and 3) many abnormalities are associated with both prematurity and growth restriction. All of these issues could lead to an overestimate of recurrence risk of stillbirth when these deaths remain in the data set. The second advantage is the ability to assess future risk of stillbirth based on the initial cause of death. We did not find any difference in subsequent risk based on whether the initial stillbirth was explained or not; however, there were only three second pregnancy stillbirths for women in whom the first fetus was stillborn, so a definitive answer to this question remains unanswered. There was also a high proportion of unexplained deaths in the first pregnancy. The contribution of unexplained deaths in studies of stillbirth is variable ranging from 10% to 70%38–40 and depends on the classification system used.41 Recent classification systems that are focused toward particular underlying causes or risks for stillbirth such as placental pathologies or growth restriction yield low proportions of unexplained deaths.39,42 Earlier classification systems (eg, the extended Wigglesworth or modified Aberdeen classifications) were usually applied after minimal investigation of perinatal deaths and resulted in high proportions of deaths classed as unexplained.43–45 The Perinatal Society of Australia & New Zealand Perinatal Death Classification definition of unexplained antepartum deaths is “deaths of normally formed fetuses before the onset of labor where no predisposing factors are considered likely to have caused the death.”32 Unlike unexplained sudden infant death syndrome, this definition does not require autopsy findings or a mandated set of investigations. The proportion of stillbirths classified as unexplained is lower in studies with an extensive set of investigations and higher autopsy rates.38,46 New South Wales has a low autopsy rate for stillbirths with the most recent report stating that an autopsy was performed in only 30.8% of unexplained antepartum deaths.28 Although the majority of the stillbirths in this cohort had placental pathology performed (90%), only half (51%) had a postmortem. We are unable to assess the extent of other recommended investigations for stillbirth because those data are not routinely collected on a population basis. It is likely, however, that many of the unexplained deaths in this cohort were underinvestigated. The Perinatal Society of Australia & New Zealand Perinatal Death Classification forms are part of a clinical practice guideline on Perinatal Mortality published in 2005.32 Although there has been national consensus to use the classification system, the guideline also recommends a set of core investigations for stillbirth; however, uptake of the full guideline is variable.47 When the recommended investigations are performed in a tertiary hospital setting, the proportion of deaths classified as unexplained using Perinatal Society of Australia & New Zealand Perinatal Death Classification has been shown to decrease from 34% to 13%.48 Because our cohort only extends until 2006, it is likely that uptake of all aspects of the guideline at the time of the data collection was inadequate.
There are inherent limitations in using population-based data. Analysis is limited to what routine variables are collected and we have not been able to assess the effect of maternal obesity because prepregnancy weight or body mass index are not routinely collected in these population-based data sets. It is of note, however, that the most recently published population-based study that assessed subsequent stillbirth and previous infant mortality showed no increase in stillbirth risk with maternal prepregnancy obesity (HR 1.05, 95% CI 0.9–1.20).16 We also were unable to assess the effect of interpregnancy interval because the deidentification of the data set did not include date of birth. We used a definition of SGA as a birth weight less than the 10th percentile using Australian population-based birth weight percentiles rather than customized percentiles because data on maternal weight and height are unavailable. This definition will not identify all neonates who have failed to reach their growth potential and will include both pathologically and constitutionally small neonates; however, it would be consistent with definitions used in other population-based data. We were only able to use time of delivery, not estimated time of death, which could also affect classification of neonates as SGA. A further limitation is that this cohort only comprises 5 years of data and therefore there are relatively small numbers of stillbirths seen for second pregnancies. A priori, we aimed to perform this analysis with the ability to analyze stillbirths classified using the Perinatal Society of Australia & New Zealand classification system and therefore could only start the analysis from 2002 onward when it was in routine use throughout the state. The precision of the recurrence risk estimates of stillbirth in second pregnancies are likely to be affected by the small numbers as indicated by the wide CIs. A database of over a million births would be required to provide a more definitive answer. There are potential benefits of analyzing recent data, which is more representative of current obstetric practice. It is possible that smaller recurrence risks than previously reported are being seen because these women are already being managed differently in a subsequent pregnancy. Findings within our data suggest that this might be the case because although the proportions of women diagnosed with gestational diabetes and preeclampsia are greater in the subsequent pregnancy, these factors are then not associated with the subsequent second pregnancy stillbirth risk. It is also known that many women with a previous stillbirth will be electively induced or delivered in a subsequent pregnancy potentially reducing second pregnancy risks.49
The finding of greater risk of subsequent stillbirth with a previous SGA neonate adds to the increasing literature that supports common underlying mechanisms for stillbirth related to placental dysfunction.20,23,50 Mandating placental examination for every stillbirth and improving adequate investigations of stillbirth will enable population-based data to play a greater role in assisting with further research into potential underlying mechanisms but many of these research questions will need to be answered in a basic science setting. The finding that previous preterm birth increases the association with subsequent stillbirth in the SGA neonates and conveys stronger risks at less than 32 weeks of gestation supports other literature that suggests recurrence of stillbirth occurs within the same “gestational age window.”9,20 Our data suggest that in the absence of growth restriction and preterm, birth women are at low risk of a subsequent stillbirth.
In summary, we found that the delivery of an SGA neonate in a first pregnancy increases the risk of stillbirth in a second pregnancy, especially if the SGA neonate was also premature. These previous pregnancy outcomes conferred greater risk than previous stillbirth. Although absolute risks remain small, all these factors merit improved surveillance and counseling in a subsequent pregnancy. Future population-based studies on stillbirth should include standardized cause of death classifications to assess future risks based on previous cause and also need to address how women are managed in subsequent pregnancies and whether different strategies affect outcome.
1. Lawn JE, Blencowe H, Pattinson R, Cousens S, Kumar R, Ibiebele I, et al.. Stillbirths: Where? When? Why? How to make the data count? Lancet 2011;377:1448–63.
2. Reddy UM. Prediction and prevention of recurrent stillbirth. Obstet Gynecol 2007;110:1151–64.
3. Samueloff A, Xenakis EM, Berkus MD, Huff RW, Langer O. Recurrent stillbirth. Significance and characteristics. J Reprod Med 1993;38:883–6.
4. Greenwood R, Samms-Vaughan M, Golding J, Ashley D. Past obstetric history and risk of perinatal death in Jamaica. Paediatr Perinat Epidemiol 1994;8(suppl 1):40–53.
5. Management of stillbirth. ACOG Practice Bulletin No. 102. American College of Obstetricians and Gynecologists. Obstet Gynecol 2009;113:748–61.
6. Wapner RJ, Lewis D. Genetics and metabolic causes of stillbirth. Semin Perinatol 2002;26:70–4.
7. Bhattacharya S, Prescott GJ, Black M, Shetty A. Recurrence risk of stillbirth in a second pregnancy. BJOG 2010;117:1243–7.
8. Lykke JA, Paidas MJ, Langhoff-Roos J. Recurring complications in second pregnancy. Obstet Gynecol 2009;113:1217–24.
9. Melve KK, Skjaerven R, Rasmussen S, Irgens LM. Recurrence of stillbirth in sibships: population-based cohort study. Am J Epidemiol 2010;172:1123–30.
11. Flenady V, Koopmans L, Middleton P, Froen JF, Smith GC, Gibbons K, et al.. Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis. Lancet 2011;377:1331–40.
12. Sharma PP, Salihu HM, Kirby RS. Stillbirth recurrence in a population of relatively low-risk mothers. Paediatr Perinat Epidemiol 2007;21(suppl 1):24–30.
13. Black M, Shetty A, Bhattacharya S. Obstetric outcomes subsequent to intrauterine death in the first pregnancy. BJOG 2008;115:269–74.
14. Flenady V. Causes and risk factors of stillbirth in Australia. Perinatal Society of Australia and New Zealand Congress. Gold Coast: Journal of Paediatrics and Child Health; 2008. p. A2–10.
15. Salihu HM, Duan J, Nabukera SK, Mbah AK, Alio AP. Younger maternal age (at initiation of childbearing) and recurrent perinatal mortality. Eur J Obstet Gynecol Reprod Biol 2011;154:31–6.
16. August EM, Salihu HM, Weldeselasse H, Biroscak B, Mbah A, Alio AP. Infant mortality and subsequent risk of stillbirth: a retrospective cohort study. BJOG 2011;118:1636–45.
17. Measey MA, Tursan d'Espaignet E, Charles A, Douglass C. Unexplained fetal death: are women with a history of fetal loss at higher risk? Aust N Z J Obstet Gynaecol 2009;49:151–7.
18. Goy J, Dodds L, Rosenberg MW, King WD. Health-risk behaviours: examining social disparities in the occurrence of stillbirth. Paediatr Perinat Epidemiol 2008;22:314–20.
19. Lurie S, Eldar I, Glezerman M, Sadan O. Pregnancy outcome after stillbirth. J Reprod Med 2007;52:289–92.
20. Smith GS, Shah I, White IR, Pell JP, Dobbie R. Previous preeclampsia, preterm delivery, and delivery of a small for gestational age infant and the risk of unexplained stillbirth in the second pregnancy: a retrospective cohort study, Scotland, 1992–2001. Am J Epidemiol 2007;165:194–202.
21. Sharma PP, Salihu HM, Oyelese Y, Ananth CV, Kirby RS. Is race a determinant of stillbirth recurrence? Obstet Gynecol 2006;107:391–7.
22. Onwude JL, Eisman V, Selo-Ojeme DO. Recurrent stillbirths: a matched case–control study of unexplained stillbirths at term. J Obstet Gynaecol 2006;26:205–7.
23. Surkan PJ, Stephansson O, Dickman PW, Cnattingius S. Previous preterm and small-for-gestational-age births and the subsequent risk of stillbirth. N Engl J Med 2004;350:777–85.
24. Robson S, Chan A, Keane RJ, Luke CG. Subsequent birth outcomes after an unexplained stillbirth: preliminary population-based retrospective cohort study. Aust N Z J Obstet Gynaecol 2001;41:29–35.
25. Heinonen S, Kirkinen P. Pregnancy outcome after previous stillbirth resulting from causes other than maternal conditions and fetal abnormalities. Birth 2000;27:33–7.
26. Weeks JW, Asrat T, Morgan MA, Nageotte M, Thomas SJ, Freeman RK. Antepartum surveillance for a history of stillbirth: when to begin? Am J Obstet Gynecol 1995;172:486–92.
27. Freeman RK, Dorchester W, Anderson G, Garite TJ. The significance of a previous stillbirth. Am J Obstet Gynecol 1985;151:7–13.
28. Centre for Epidemiology and Research. New South Wales mothers and babies 2008. New South Wales (Australia): NSW Department of Health; 2010.
29. NSW Health Department. Validation study: NSW midwives data collection 1998. NSW Public Health Bull 2000;9:97–9.
30. Chan A, King JF, Flenady V, Haslam RH, Tudehope DI. Classification of perinatal deaths: development of the Australian and New Zealand classifications. J Paediatr Child Health 2004;40:340–7.
32. Flenady V, King J, Charles A, Gardener G, Ellwood D, Day K, et al.. PSANZ clinical practice guideline for perinatal mortality. Version 2.2. Available at: www.psanzpnmsig.org
, 2009. Retrieved , 2011.
33. Roberts CL, Lancaster PA. Australian national birthweight percentiles by gestational age. Med J Aust 1999;170:114–8.
34. Armitage P, Berry G, Matthews JNS. Trends in proportions. In: Malden M. editor. Statistical methods in medical research. 4th ed. Oxford (UK): Blackwell Science; 2002.
35. Grambsch PM, Therneau TM. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 1994;81:515–26.
36. Platt RW, Joseph KS, Ananth CV, Grondines J, Abrahamowicz M, Kramer MS. A proportional hazards model with time-dependent covariates and time-varying effects for analysis of fetal and infant death. Am J Epidemiol 2004;160:199–206.
37. Hosmer DS, Lemeshow SM. Applied survival analysis: regression modeling of time-to-event data. 2nd ed. Chichester (UK): Wiley; 2008.
38. Petersson K, Bremme K, Bottinga R, Hofsjö A, Hulthén-Varli I, Kublickas M, et al.. Diagnostic evaluation of intrauterine fetal deaths in Stockholm 1998–99. Acta Obstet Gynecol Scand 2002;81:284–92.
39. Korteweg FJ, Gordijn SJ, Timmer A, Erwich JJ, Bergman KA, Bouman K, et al.. The Tulip classification of perinatal mortality: introduction and multidisciplinary inter-rater agreement. BJOG 2006;113:393–401.
40. Maternal and Child Health Research Consortium. Confidential enquiry into stillbirths and deaths in infancy (CESDI). 8th annual report. London (UK): Maternal and Child Health Research Consortium; 2001.
41. Gordon A, Jeffery HE. Classification and description of stillbirths in New South Wales, 2002–2004. Med J Aust 2008;188:645–8.
42. Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. BMJ 2005;331:1113–7.
43. Wigglesworth J. Monitoring perinatal mortality. A pathophysiological approach. Lancet 1980;2:684–6.
44. Cole SK, Hey EN, Thomson AM. Classifying perinatal death: an obstetric approach. Br J Obstet Gynaecol 1986;93:1204–12.
45. Hey EN, Lloyd DJ, Wigglesworth JS. Classifying perinatal death: fetal and neonatal factors. Br J Obstet Gynaecol 1986;93:1213–23.
46. Pauli RM, Reiser CA. Wisconsin Stillbirth Service Program: II. Analysis of diagnoses and diagnostic categories in the first 1,000 referrals. Am J Med Genet 1994;50:135–53.
47. Uptake of the PSANZ perinatal mortality audit guidelines: a survey of midwives and obstetricians in Australia and New Zealand. Melbourne (Australia): Perinatal Society of Australia and New Zealand Congress; 2007.
48. Headley E, Gordon A, Jeffery H. Reclassification of unexplained stillbirths using clinical practice guidelines. Aust N Z J Obstet Gynaecol 2009;49:285–9.
49. Robson SJ, Leader LR. Management of subsequent pregnancy after an unexplained stillbirth. J Perinatol 2010;30:305–10.
50. Wikström A-K, Svensson T, Kieler H, Cnattingius S. Recurrence of placental dysfunction disorders across generations. Am J Obstetr Gynecol 2011;205:454.e1–8.
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