Skip Navigation


American Journal of Epidemiology Advance Access originally published online on October 25, 2006
American Journal of Epidemiology 2007 165(2):194-202; doi:10.1093/aje/kwj354
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
165/2/194    most recent
kwj354v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Smith, G. C. S.
Right arrow Articles by Dobbie, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Smith, G. C. S.
Right arrow Articles by Dobbie, R.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

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

Gordon C. S. Smith1, Imran Shah1, Ian R. White2, Jill P. Pell3 and Richard Dobbie4

1 Department of Obstetrics and Gynaecology, Cambridge University, The Rosie Hospital, Cambridge, United Kingdom
2 Medical Research Council Biostatistics Unit, Institute of Public Health, Cambridge, United Kingdom
3 Department of Public Health, Greater Glasgow National Health Service Board, Glasgow, United Kingdom
4 Information and Statistics Division, Common Services Agency, Edinburgh, United Kingdom

Correspondence to Dr. Gordon C. S. Smith, Department of Obstetrics and Gynaecology, Cambridge University, Box 223, The Rosie Hospital, Robinson Way, Cambridge CB2 2SW, United Kingdom (e-mail: gcss2{at}cam.ac.uk).

Received for publication April 13, 2006. Accepted for publication May 30, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Women with a previous stillbirth are known to be at increased risk of stillbirth in subsequent pregnancies. However, few studies have addressed the association between other complications of pregnancy and the future risk of stillbirth. Using linkage of national pregnancy and perinatal death registries, the authors performed a retrospective cohort study of 133,163 women having a second birth in Scotland between 1992 and 2001 whose first infant was liveborn. The risk of unexplained stillbirth was increased among women with a previous preterm birth (adjusted hazard ratio (HR) = 2.04, 95% confidence interval (CI): 1.34, 3.11), previous delivery of a small for gestational age (SGA) infant (HR = 2.14, 95% CI: 1.59, 2.87), and previous preeclampsia (HR = 1.68, 95% CI: 1.07, 2.62). The associations were similar after adjustment for maternal age, height, marital and smoking status, and interpregnancy interval. There was a statistically significant positive interaction between previous delivery of a SGA infant and previous preeclampsia (p = 0.01): Women with this combination in their first pregnancy had an approximately fivefold risk of unexplained stillbirth in the second pregnancy (HR = 4.95, 95% CI: 2.63, 9.32). Associations were stronger with SGA unexplained stillbirths. The authors conclude that complicated first births of liveborn infants are associated with an increased risk of unexplained stillbirth in the next pregnancy.

pregnancy complications; risk; stillbirth

Abbreviations: CI, confidence interval; HR, hazard ratio; ICD, International Classification of Diseases; OR, odds ratio; SGA, small for gestational age


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Antepartum stillbirth is death of the fetus before the onset of labor. It accounts for two thirds of all perinatal deaths and affects approximately one in 200 pregnancies (1). Approximately two thirds of antepartum stillbirths have no direct cause and are referred to as "unexplained." The risk of both unexplained stillbirth and other pregnancy complications is associated with indicators of placental function, such as low levels of pregnancy-associated plasma protein A (2, 3), high levels of maternal serum alpha-fetoprotein (4), and a high resistance pattern of uterine artery Doppler flow velocimetry (5). Consequently, it is plausible that unexplained stillbirth and other complications of pregnancy are different clinical manifestations of a common problem in placentation.

It is well recognized that specific pregnancy complications, such as spontaneous preterm delivery and abruption, are likely to recur (6, 7). It is likely that this reflects, at least in part, a persistent predisposition to impaired placentation. Given that unexplained stillbirth and other pregnancy complications appear to have common placental determinants, we hypothesized that women who had pregnancies complicated by preeclampsia, preterm birth, or intrauterine growth restriction may be at increased risk of unexplained stillbirth in their subsequent pregnancies. Here we report the relation between complications in a first livebirth and the risk of unexplained stillbirth in 133,163 second pregnancies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Data sources
The Scottish Morbidity Record 2 collects information on clinical and demographic characteristics and outcomes for all patients discharged from Scottish maternity hospitals. The register is subjected to regular quality assurance checks and has been greater than 99 percent complete since the late 1970s (8). A quality assurance exercise was performed in 1996–1997, where 5 percent of case records were compared with the Scottish Morbidity Record 2 database over a 6-month period (n = 1,414). This exercise demonstrated that all fields used in the present study had less than 2 percent errors with the exception of the following (percent errors in parentheses): maternal height (4.4 percent) and estimated gestation (5.6 percent). International Classification of Diseases (ICD) diagnostic codes were found to be 80–90 percent accurate for the first four diagnoses and 70–80 percent accurate for the remainder (9).

Records of singleton births from the Scottish Morbidity Record 2 between 1985 and 2001 were identified and linked to records from the Scottish Stillbirth and Infant Death Enquiry (a national register that routinely classifies all perinatal deaths in Scotland) by use of a probability-based matching approach, which has been shown to match correctly approximately 98 percent of records (10). Coding of the cause of death is performed by a single medically qualified individual (the Scottish coordinator) in the Information and Statistics Division of the National Health Service on the basis of clinical information obtained from local coordinators and pathologists. Cases are identified through registration of stillbirths and neonatal deaths with the General Registrar's Office, which is a legal requirement following a perinatal death. The register is 100 percent complete when compared with the death certificate database and has been described in detail elsewhere (11, 12). Approval for the record linkage was provided by the Privacy Advisory Committee of the Information and Statistics Division of the National Health Service Scotland.

Study cohort
The population studied consisted of all second births in Scotland between 1992 and 2001, where there was a record for the first birth in the linked database. The analysis focused on second births after 1991, since smoking status was included only in the Scottish Morbidity Record 2 database from 1992 onward. Women were excluded whose first record had missing data for gestation or for infant's sex or birth weight; where the gestational age at delivery was outside the range of 24–43 weeks; and where the infant was stillborn. Women were excluded whose second record had missing data for gestation, infant's sex, birth weight, or any of the other maternal characteristics. Records were also excluded where the second infant died during the perinatal period as the result of congenital abnormality or rhesus isoimmunization or where delivery was outside the range of 24–43 weeks. Women were also excluded where the pair of records yielded an interpregnancy interval that was negative or implausibly short and where there was a discrepancy between the documented mode of delivery in the first record and the previous cesarean delivery field in the second record.

Definitions of maternal and obstetric characteristics
In the comparison of risk of unexplained antepartum stillbirth, the following demographic factors were considered as possible confounders: socioeconomic deprivation, smoking, maternal age, maternal height, and marital status. The postcode of residence was used to derive Carstairs socioeconomic deprivation scores (13). These are based on 1991 census data on car ownership, unemployment, overcrowding, and social class within postcode sectors of residence that contain, on average, around 1,600 residents. The deprivation scores were then used to assign women to categories of socioeconomic deprivation within the study cohort. Higher numbers indicate a greater degree of deprivation. "Smoking" was defined as the smoking status of the woman at the time of first attendance for antenatal care. "Maternal age" was defined as the age of the mother at the time of birth. Maternal height was measured in centimeters, and the value used was that documented in each woman's clinical record. "Gestational age at birth" was defined as the completed weeks of gestation on the basis of the estimated date of delivery in each woman's clinical record. Gestational age has been confirmed by ultrasound in the first half of pregnancy in more than 95 percent of women in the United Kingdom since the early 1990s (14). "Preterm birth" was defined as birth before 37 weeks of gestation. Birth weight was classified into sex- and gestational age-specific percentiles on the basis of 1,002,834 singleton livebirths between 1985 and 2001 entered into the Scottish Morbidity Record 2. "Small for gestational age (SGA) birth weight" was defined as a birth weight in the smallest 10 percent for sex and gestation. "Interpregnancy interval" was defined as the number of days from the first birth until the estimated date of the last menstrual period of the second. The estimated date of the last menstrual period was calculated by subtracting the estimated gestational age from the date of delivery. "Preeclampsia" was defined as the presence of an appropriate diagnostic code (ICD, Ninth Revision, code 642.4 or 642.5 or ICD, Tenth Revision, code O140, O141, or O149) in the delivery record.

Definition of stillbirths
Stillbirths were classified as antepartum (deaths before the onset of labor) and intrapartum (deaths during labor). "Deaths caused by congenital anomaly" were defined as any structural or genetic defect incompatible with life or potentially treatable but causing death. The cause of antepartum stillbirth was classified in the Scottish Stillbirth and Infant Death Enquiry according to a modified version of the Wigglesworth hierarchical system (15), which is described in detail elsewhere (12). Stillbirths were classified according to direct obstetric causes (in order): toxemia (i.e., preeclampsia or eclampsia), hemorrhage (antepartum), mechanical, maternal, miscellaneous, and unexplained. Unexplained stillbirths included those that were SGA. The hierarchy dictates that a perinatal death where there was severe preeclampsia complicated by abruption would be classified as being due to toxemia, since toxemia is above hemorrhage in the hierarchy.

Statistical analyses
Continuous variables were summarized by the median and interquartile range, and comparisons between groups were made by the Mann-Whitney U test. Univariate comparisons of dichotomous data were made by use of the chi-square test and the test for trend, as appropriate. The p values for all hypothesis tests were two sided, and statistical significance was set at p < 0.05. The risk of stillbirth was compared between groups by time-to-event analyses (Kaplan-Meier and Cox proportional hazard model) in which the week of gestation was used as the time scale, antepartum stillbirth due to the specified cause was defined as the event, and all other births were treated as censored. This method uses ongoing pregnancies as the denominator, as previously suggested (16), but accounts for censoring due to birth, allows multivariate analysis (17), and can be used in situations where not all individuals would ultimately experience the event (18). This analytical approach allows assessment of the relative risk accounting for variation in the duration of pregnancy. Survival data were plotted as the cumulative percentage with event as recommended for rare outcomes (19), and univariate statistical comparisons were made with the log-rank test. Crude and adjusted hazard ratios were estimated by use of the proportional hazards model (20). The statistical significance of interactions between first pregnancy outcomes was assessed with the likelihood ratio test. The proportional hazards assumption was tested with the test of Grambsch and Therneau (21) as previously described for the analysis of stillbirth risk (9, 22). Logistic regression analysis was used to estimate adjusted odds ratios within given gestational windows. In these analyses, the number of antepartum stillbirths within the given range was the numerator, and the number of all births at the given or later gestations was the denominator. All statistical analyses were performed with STATA, version 8.2, software (StataCorp LP, College Station, Texas).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The Scottish Morbidity Record 2 contained 196,842 records of second singleton births between 1992 and 2001. Of these, 166,552 (84.6 percent) could be linked to a record for the first birth; 33,389 of these records (20.0 percent) were excluded (figure 1), leaving a study group of 133,163. There were 357 (0.3 percent) antepartum stillbirths not due to fetal abnormality or rhesus isoimmunization: 105 (29.4 percent) were explained (toxemia, hemorrhage, mechanical, maternal, and miscellaneous), and 252 (70.6 percent) were unexplained. Women whose second pregnancy ended in antepartum stillbirth were more likely in their first pregnancy to have delivered a SGA infant, delivered preterm, had a diagnosis of preeclampsia, and delivered by cesarean section (table 1). The interpregnancy interval varied in relation to whether the second pregnancy was an antepartum stillbirth, with a greater proportion of these women experiencing very prolonged intervals. Women experiencing a stillbirth were shorter and, at the time of the second pregnancy, were more likely to live in an area of high socioeconomic deprivation, to smoke, and to be unmarried.


Figure 1
View larger version (23K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		FIGURE 1 Selection of study cohort from all second singleton births in Scotland recorded in the Scottish Morbidity Record 2, 1992–2001.

 

View this table:
[in this window]
[in a new window]

  		TABLE 1 Maternal characteristics and outcome by occurrence of antepartum stillbirth in the second pregnancy, Scotland, 1992–2001

 
Preterm birth, delivery of a SGA infant, and preeclampsia in the first pregnancy were each associated with an approximately two- to threefold risk of stillbirth in the second pregnancy (table 2). The risk of explained stillbirth was approximately sixfold among women with a previous preterm delivery and approximately threefold among women with previous delivery of a SGA infant or with preeclampsia. When analyzed by cause of stillbirth, previous preterm birth was associated with a sixfold risk of stillbirth due to preeclampsia, a fourfold risk of stillbirth due to abruption, and a 16-fold risk of stillbirth due to maternal disease. Previous delivery of a SGA infant was associated with sixfold risk of stillbirth due to preeclampsia and a fourfold risk of stillbirth due to abruption. Previous preeclampsia was associated with an 11-fold risk of stillbirth due to preeclampsia and a sixfold risk of stillbirth due to maternal disease. Preterm birth, delivery of a SGA infant, and preeclampsia in the first pregnancy were each associated with an approximately twofold risk of unexplained stillbirth. The strength of association was very similar when the analysis was confined to previous spontaneous preterm birth (hazard ratio (HR) = 1.92, 95 percent confidence interval (CI): 1.14, 3.23).


View this table:
[in this window]
[in a new window]

  		TABLE 2 First pregnancy outcome and the risk of explained and unexplained stillbirth in the second pregnancy, Scotland, 1992–2001

 
In relation to the risk of unexplained stillbirth, there were no statistically significant interactions between previous preterm delivery and previous delivery of a SGA infant (HRinteraction = 1.10, 95 percent CI: 0.41, 2.95; p = 0.85) or between previous preterm birth and previous preeclampsia (HRinteraction = 0.48, 95 percent CI: 0.15, 1.59; p = 0.21). However, there was a statistically significant interaction between previous preeclampsia and previous delivery of a SGA infant (HRinteraction = 3.37, 95 percent CI: 1.34, 8.45; p = 0.01). All subsequent analysis of the risk of unexplained stillbirth examined combinations of previous delivery of a SGA infant and previous preeclampsia. The risk of unexplained stillbirth was approximately 60 percent higher among women with a previous preterm birth (figure 2A; table 3). The risk of unexplained stillbirth was approximately 70 percent higher among women with a previous delivery of a SGA infant in the absence of a diagnosis of preeclampsia. A previous diagnosis of preeclampsia was not associated with the subsequent risk of unexplained stillbirth if the infant was appropriate for gestational age. However, the risk of unexplained stillbirth was fivefold among women with the combination of previous preeclampsia and delivery of a SGA infant (figure 2B; table 3). The association between previous preterm birth and previous cesarean section significantly varied across the range of 24–43 weeks (table 3). The association with previous preterm birth was strong at 24–32 weeks (odds ratio (OR) = 2.71, 95 percent CI: 1.56, 4.71) and not statistically significant at 33–36 weeks (OR = 1.34, 95 percent CI: 0.52, 3.47) or 37–43 weeks (OR = 0.39, 95 percent CI: 0.12, 1.24).


Figure 2
View larger version (11K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		FIGURE 2 Kaplan-Meier plot of cumulative probability of unexplained stillbirth (expressed per 1,000 pregnancies) in the second birth in relation to the outcome of the first birth, Scotland, 1992–2001. A, comparison of women whose first birth was at term (dashed line) with those who had previously delivered preterm (solid line); B, comparison of women who delivered an appropriate for gestational age infant and had no diagnosis of preeclampsia in their first pregnancy (dashed line) with women who delivered a small for gestational age (SGA) infant and had a documented diagnosis of preeclampsia in their first pregnancy (solid line).

 

View this table:
[in this window]
[in a new window]

  		TABLE 3 Unadjusted and adjusted hazard ratios for unexplained stillbirth in the second pregnancy, Scotland, 1992–2001

 
We found an association between cesarean delivery in the first pregnancy and the risk of unexplained stillbirth in the second (table 4), which is consistent with our previous study (9). However, there would have been considerable overlap between the patients in our previous study (eligible second births in Scotland in 1992–1998) and those in the present study. We repeated the analysis of previous cesarean delivery confined to the 32,628 births from 1999 to 2001, that is, in women who were not included in our previous analysis. The hazard ratio for unexplained stillbirth associated with previous cesarean delivery in births from 1999 to 2001 was 2.27 (95 percent CI: 1.38, 3.73; p = 0.001).


View this table:
[in this window]
[in a new window]

  		TABLE 4 Relation between first pregnancy outcome and small for gestational age and appropriate for gestational age unexplained stillbirth, Scotland, 1992–2001*

 
We analyzed the relation between the outcome of the first pregnancy and the risk of unexplained stillbirth, dividing the outcome into those that were SGA and those that were appropriate for gestational age. Associations tended to be stronger for unexplained stillbirth where the birth weight was SGA (table 4).

The main analysis was then performed in the approximately 31,000 women excluded because of missing data in relation to the second pregnancy. This addressed whether the cohort studied may have been unrepresentative of the whole population; for example, it may have systematically excluded women who delivered without booking for prenatal care, leading to biases. Among these women, the unadjusted hazard ratio for unexplained stillbirth was 2.57 (95 percent CI: 1.27, 5.18) for women with a prior history of preterm birth, 2.08 (95 percent CI: 1.18, 3.67) for women with previous delivery of a SGA infant, and 1.91 (95 percent CI: 0.91, 4.00) for women with previous preeclampsia. The strength of the associations did not significantly differ from those observed among women with complete data (p = 0.7, 0.9, and 0.8, respectively).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
It is well recognized that women who have a stillbirth in one pregnancy are at increased risk of stillbirth in future pregnancies (23). These women are typically offered additional fetal surveillance and early elective delivery at term. The key finding of the present study is that women who experienced preterm birth, delivery of a SGA infant, or preeclampsia in a first birth of a liveborn infant were also at increased risk of unexplained stillbirth in the second. Moreover, there was a synergistic association between previous delivery of a SGA infant and previous preeclampsia: This combination carried a fivefold risk of unexplained stillbirth in the second pregnancy.

Previous preterm birth, previous delivery of a SGA infant, and previous preeclampsia were also associated with an increased risk of explained stillbirth. These observations are likely to reflect, at least in part, the recurrence of specific complications, such as abruption and preeclampsia. The association between prior complications and the risk of explained stillbirth in the second pregnancy may also reflect common associations among preexisting maternal disease, obstetric complications, and stillbirth. For example, women with insulin-dependent diabetes mellitus are at increased risk of preterm birth and preeclampsia (24). The increased risk of explained stillbirth among women with previous complicated births is, therefore, plausible but probably merely reflects the known recurrence risk of obstetric complications and common associations among maternal disease, obstetric complications, and stillbirth.

There has been only one large-scale study, to our knowledge, that has previously addressed the association between previous obstetric complications and the future risk of stillbirth (25). The major weakness of that study was that they lacked data on the cause of stillbirth. Therefore, antepartum and intrapartum stillbirths were pooled, as were explained and unexplained stillbirths. That study demonstrated an approximately twofold risk of stillbirth associated with both previous preterm birth and previous delivery of a SGA infant. No data were reported on previous preeclampsia. It was unclear from that study whether these associations were explained by simply recurrence of complications (abruption and preeclampsia) or by common associations with maternal disease, as discussed above. In the present study, we show that prior pregnancy complications are associated with the risk of both explained and unexplained antepartum stillbirth.

The current findings are biologically plausible. Previous studies have shown that the same biochemical or biophysical measurements of placental function in early pregnancy are associated with both unexplained stillbirth and other adverse obstetric outcomes (2–5). Although the determinants of poor placentation remain obscure, it is known that placentally related complications tend to recur (6). Furthermore, women with elevated levels of maternal serum alpha-fetoprotein (an indicator of placental permeability) in one pregnancy are more likely to have elevated levels of this protein in the next pregnancy (26). The current findings suggest that women who have a tendency to impaired placentation may manifest this with different complications in different pregnancies. The factors that determine which complications arise in a given pregnancy remain unclear. Consistent with this interpretation, the association that we found between previous pregnancy complications and the risk of unexplained stillbirth tended to be stronger for unexplained stillbirths where the infant was SGA. Previous studies have shown associations between placental function and SGA unexplained stillbirths but not those with birth weight appropriate for gestational age (3).

We had previously demonstrated an association between cesarean delivery in the first pregnancy and the risk of unexplained stillbirth in the second (9). We observed a very similar association in the current analysis. However, the current data expand on our previous analysis in two ways. First, we now show that the association is similar after adjustment for a diagnosis of preeclampsia in the first pregnancy. Second, we repeated the analysis confined to births between 1999 and 2001 (our previous study had examined second births in Scotland between 1992 and 1998, and many of these would also have been included in the present study). We found a very similar strength of association between previous cesarean delivery in the first pregnancy and the risk of unexplained stillbirth in the second in births between 1999 and 2001. Thus, it is unlikely that this association is a chance finding.

In conclusion, women with previous placentally related complications in a livebirth are at increased risk of unexplained stillbirth. The association is particularly strong among those with the combination of previous preeclampsia and previous delivery of a SGA infant, which suggests that the underlying defect in placentation leading to that combination may be similar to the defect predisposing to stillbirth.


   ACKNOWLEDGMENTS
 
Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Information and Statistics Division, NHS Scotland. (2001) Scottish perinatal and infant mortality and morbidity report 2000(ISD Publications, Edinburgh, United Kingdom) (Scottish Programme for Clinical Effectiveness in Reproductive Health (SPCERH) publication no. 14).
  2. Smith GCS, Stenhouse EJ, Crossley JA, et al. (2002) Early pregnancy levels of pregnancy-associated plasma protein A and the risk of intra-uterine growth restriction, premature birth, pre-eclampsia and stillbirth. J Clin Endocrinol Metab 87:1762–7.[Abstract/Free Full Text]
  3. Smith GCS, Crossley JA, Aitken DA, et al. (2004) First-trimester placentation and the risk of antepartum stillbirth. JAMA 292:2249–54.[Abstract/Free Full Text]
  4. Waller DK, Lustig LS, Smith AH, et al. (1993) Alpha-fetoprotein: a biomarker for pregnancy outcome. Epidemiology 4:471–6.[Web of Science][Medline]
  5. Lees C, Parra M, Missfelder-Lobos H, et al. (2001) Individualized risk assessment for adverse pregnancy outcome by uterine artery Doppler at 23 weeks. Obstet Gynecol 98:369–73.[CrossRef][Web of Science][Medline]
  6. Rasmussen S, Irgens LM, Dalaker K. (2000) Outcome of pregnancies subsequent to placental abruption: a risk assessment. Acta Obstet Gynecol Scand 79:496–501.[CrossRef][Web of Science][Medline]
  7. Iams JD. (2003) The epidemiology of preterm birth. Clin Perinatol 30:651–64.[CrossRef][Web of Science][Medline]
  8. Cole SK. (1980) Scottish maternity and neonatal records. In Chalmers I and McIlwaine GM (Eds.). Perinatal audit and surveillance(Royal College of Obstetricians and Gynaecologists, London, United Kingdom) pp. 39–51.
  9. Smith GCS, Pell JP, Dobbie R. (2003) Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet 362:1779–84.[CrossRef][Web of Science][Medline]
  10. Kendrick S and Clarke J. (1993) The Scottish Record Linkage System. Health Bull (Edinb) 51:72–9.
  11. McIlwaine GM, Dunn FH, Howat RC, et al. (1985) A routine system for monitoring perinatal deaths in Scotland. Br J Obstet Gynaecol 92:9–13.[Web of Science][Medline]
  12. Information and Statistics Division, NHS Scotland. (2000) Scottish perinatal and infant mortality and morbidity report 1999(Common Services Agency, Edinburgh, United Kingdom).
  13. McLoone P and Boddy FA. (1994) Deprivation and mortality in Scotland, 1981 and 1991. BMJ 309:1465–70.[Abstract/Free Full Text]
  14. Campbell S and Soothill PW. (1993) Detection and management of intrauterine growth retardation: a British approach. In Chervenak FA, Isaacson GC, Campbell S (Eds.). Ultrasound in obstetrics and gynaecology(Little Brown, Boston, MA) Vol 2: pp. 1432–5.
  15. Cole SK, Hey EN, Thomson AM. (1986) Classifying perinatal death: an obstetric approach. Br J Obstet Gynaecol 93:1204–12.[Web of Science][Medline]
  16. Yudkin PL, Wood L, Redman CW. (1987) Risk of unexplained stillbirth at different gestational ages. Lancet 1:1192–4.[Web of Science][Medline]
  17. Smith GCS. (2001) Life-table analysis of the risk of perinatal death at term and post term in singleton pregnancies. Am J Obstet Gynecol 184:489–96.[CrossRef][Web of Science][Medline]
  18. Maller RA and Zhou X. (1996) Survival analysis with long-term survivors(John Wiley & Sons, New York, NY).
  19. Pocock SJ, Clayton TC, Altman DG. (2002) Survival plots of time-to-event outcomes in clinical trials: good practice and pitfalls. Lancet 359:1686–9.[CrossRef][Web of Science][Medline]
  20. Hosmer DW and Lemeshow S. (1999) Applied survival analysis: regression modeling of time to event data(John Wiley & Sons, New York, NY).
  21. Grambsch PM and Therneau TM. (1994) Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 81:515–26.[Abstract/Free Full Text]
  22. Platt RW, Joseph KS, Ananth CV, et al. (2004) A proportional hazards model with time-dependent covariates and time-varying effects for analysis of fetal and infant death. Am J Epidemiol 160:199–206.[Abstract/Free Full Text]
  23. Samueloff A, Xenakis EM, Berkus MD, et al. (1993) Recurrent stillbirth. Significance and characteristics. J Reprod Med 38:883–6.[Web of Science][Medline]
  24. Moore TR. (1999) Diabetes in pregnancy. In Creasy RK and Resnik R (Eds.). Maternal-fetal medicine(W B Saunders, Philadelphia, PA) pp. 964–95.
  25. Surkan PJ, Stephansson O, Dickman PW, et al. (2004) Previous preterm and small-for-gestational-age births and the subsequent risk of stillbirth. N Engl J Med 350:777–85.[Abstract/Free Full Text]
  26. Wax JR, Lopes AM, Benn PA, et al. (2000) Unexplained elevated midtrimester maternal serum levels of alpha fetoprotein, human chorionic gonadotropin, or low unconjugated estriol: recurrence risk and association with adverse perinatal outcome. J Matern Fetal Med 9:161–4.[CrossRef][Medline]

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?



This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
165/2/194    most recent
kwj354v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Smith, G. C. S.
Right arrow Articles by Dobbie, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Smith, G. C. S.
Right arrow Articles by Dobbie, R.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?