Original Article
Previous Preterm and Small-for-Gestational-Age Births and the Subsequent Risk of Stillbirth
N Engl J Med 2004; 350:777-785February 19, 2004
- Abstract
Background
Some causes of stillbirth may also lead to fetuses that are small for gestational age (have a low birth weight with respect to their gestational age) or are delivered preterm (before 37 weeks of gestation). It is not known whether the birth of a previous small-for-gestational-age or preterm infant increases the subsequent risk of stillbirth.
Methods
We assessed the associations between previous adverse outcomes of pregnancy and the risk of stillbirth in a nationwide Swedish study of 410,021 women who delivered first and second consecutive singleton infants between 1983 and 1997. There were 1842 and 1062 stillbirths during the first and second pregnancies, respectively.
Results
As compared with women whose first infant was born at term (37 weeks of gestation or more) and was not small for gestational age, women whose first infant was born at term or preterm and was small for gestational age had an increased risk of stillbirth during their second pregnancy. The odds ratios for subsequent stillbirth, after adjustment for covariates known to be associated with an increased risk of stillbirth, were 2.1 (95 percent confidence interval, 1.6 to 2.8) among women with a first infant who was born at term and was small for gestational age, 3.4 (95 percent confidence interval, 2.1 to 5.6) among women with a first infant who was moderately (32 to 36 weeks of gestation) preterm and small for gestational age, and 5.0 (95 percent confidence interval, 2.5 to 9.8) among women with a first infant who was very (before 32 weeks of gestation) preterm and was small for gestational age. The odds ratio for subsequent stillbirth among women with a first stillborn infant was 2.5 (95 percent confidence interval, 1.4 to 4.7), as compared with women whose first infant was not stillborn. The rates of stillbirth in second pregnancies ranged from 2.4 per 1000 births among women whose first infant was born at term and was not small for gestational age to 19.0 per 1000 births among women whose first child was very preterm and was small for gestational age.
Conclusions
Delivery of a previous small-for-gestational-age infant is an important predictor of the subsequent risk of stillbirth, particularly if the infant was delivered preterm.
Media in This Article
Table 1
Outcomes of the First Pregnancy and Univariate Associations with the Risk of Stillbirth during the Second Pregnancy among Women Who Had Two Successive Singleton Births in Sweden between 1983 and 1997.Table 2
Distribution of Maternal Characteristics and Complications during the Second Pregnancy, According to the Outcome of the First Pregnancy.Article Activity
- Article
Stillbirth accounts for more than half of perinatal deaths in developed nations,1 and the rates of stillbirth range from 3 to 4 per 1000 births in Sweden and the United States.2,3 Although the cause of stillbirths is poorly understood, fetal growth restriction may be one of the major determinants. Fetuses that are small for gestational age, commonly defined as a birth weight for gestational age that is below the 10th percentile or more than 2 SD below the mean, have an increased risk of stillbirth,4 especially preterm stillbirth.5 Congenital malformations, placental abruption, and intrauterine infections are also associated with an increased risk of stillbirth,6-9 and they may also increase the risk of other adverse outcomes, including preterm birth and the delivery of an infant who is small for gestational age.10-13
The tendency for adverse pregnancy outcomes to be repeated in successive births is well known, and the risk of stillbirth is estimated to increase by a factor of 2 to 10 among women with a prior stillbirth.14,15 A history of stillbirth also increases the likelihood of having a subsequent infant who is small for gestational age16 or has a reduced birth weight.17 Moreover, among women whose first pregnancy ended in stillbirth, the risk of having a small-for-gestational-age infant in a subsequent pregnancy is higher among those in whom the stillbirth was assessed clinically to be related to growth restriction than among those with a previous stillbirth that was not related to growth restriction.18 Women whose first pregnancy was complicated by a stillbirth with an unknown cause have an increased risk of preterm delivery during their second pregnancy.17
However, little is known about the influence of previous delivery of a small-for-gestational-age infant or preterm birth on the risk of stillbirth in a subsequent pregnancy. Using the nationwide Swedish Medical Birth Register, we studied more than 400,000 women who had two successive singleton births between 1983 and 1997 in order to determine previous adverse pregnancy outcomes, including stillbirth and the delivery of a small-for-gestational-age or preterm infant, and their associations with the risk of stillbirth in subsequent pregnancies. Since the likelihood of fetal growth restriction may be higher in premature infants who are small for gestational age,19,20 we also studied the joint effect of gestational age and birth weight for gestational age in the first pregnancy on the subsequent risk of stillbirth.
Methods
Study Design
The Birth Register, which includes information on more than 99 percent of births in Sweden, recorded more than 1.5 million singleton births between January 1, 1983, and December 31, 1997. Our study population was restricted to 410,021 women who delivered first and second consecutive singleton infants. The Birth Register includes demographic data and prospectively collected information on reproductive history and complications that occur during pregnancy, delivery, and the neonatal period. By means of each individual's unique national registration number, the Birth Register can be linked with other Swedish data sources.
In Sweden, maternal characteristics are recorded in a standardized manner during a woman's first visit for antenatal care, which occurs before the 15th week of gestation in more than 95 percent of the pregnancies.21 We used information on maternal characteristics from each woman's second pregnancy. Women were categorized as nonsmokers, moderate smokers (1 to 9 cigarettes per day), or heavy smokers (at least 10 cigarettes per day). The family situation was defined according to whether or not the woman was living with the baby's father. Maternal age was categorized as less than 25 years, 25 to 29 years, 30 to 34 years, or 35 years or older. Height measurements during the second pregnancy were categorized as 159 cm or less, 160 to 164 cm, 165 to 169 cm, or 170 cm or more. From height and weight measurements we calculated the body-mass index (the weight in kilograms divided by the square of the height in meters). Women were categorized according to the body-mass index as lean (a body-mass index of less than 20.0), normal (a body-mass index of 20.0 through 24.9), overweight (a body-mass index of 25.0 through 29.9), or obese (a body-mass index of 30.0 or more). Height and weight measurements were available only from 1992 onward. The year of the second delivery was divided into three groups: 1983 through 1989, 1990 through 1993, and 1994 through 1997. The interpregnancy interval was calculated as the number of months between the birth of the first child and the estimated date of conception of the second child and categorized as 0 to 3 months, 4 to 7 months, 8 to 11 months, 12 to 35 months, 36 to 71 months, or 72 months or more. Through linkage with the Education Register, information on the number of years of formal education completed as of December 31, 1998, was obtained and categorized as 11 or fewer years or 12 or more years. Information on the mother's country of birth was obtained through linkage to the Immigration Register and classified as Nordic (Sweden, Denmark, Norway, Finland, and Iceland) or non-Nordic. Maternal disorders were classified according to the 8th, 9th, and 10th revisions of the International Classification of Diseases (ICD-8, ICD-9, and ICD-10, respectively), and were noted at the time of the woman's discharge from the hospital. Hypertensive disease was defined as chronic hypertension, gestational hypertension, preeclampsia, and eclampsia (ICD-8 codes 637.0, 637.1, and 637.9; ICD-9 code 642; and ICD-10 codes O10, O11, O13, O14, O15, and O16). Antepartum hemorrhage was defined as placental abruption, placenta previa, and other reasons for antepartum bleeding (ICD-8 codes 632 and 651, ICD-9 code 641, and ICD-10 codes O44, O45, and O46).
A woman's first delivery was categorized as a livebirth or a stillbirth. There were 1842 stillbirths during the first pregnancy. We defined very preterm birth as live birth before 32 completed weeks of gestation, moderately preterm birth as live birth at 32 to 36 completed weeks of gestation (from 32 weeks 0 days through 36 weeks 6 days), and term birth as live birth at 37 or more completed weeks of gestation. Small-for-gestational-age birth was defined as one with a birth weight that was more than 2 SD below the mean for gestational age on the Swedish reference curve of estimated fetal growth.22 Live births were subclassified into six categories: not-small-for-gestational-age term, moderately preterm, and very preterm births and small-for-gestational-age term, moderately preterm, and very preterm births. In the Swedish Birth Register, stillbirth is defined as fetal death at 28 weeks of gestation or later; there is no information about the underlying cause of death. To determine gestational age, we used the results of ultrasonography performed early in the second trimester, a procedure that has been offered to all pregnant women in Sweden since 1990, 95 percent of whom accept it.23 When this information was not available, gestational age was estimated from the date of a woman's last menstrual period.
The study was approved by the research ethics committee at Karolinska Institutet, Stockholm, Sweden. The research ethics committee did not require the women to provide informed consent.
Statistical Analysis
We used unconditional logistic-regression analysis to model the risk that the second birth would be a stillbirth as a function of the reproductive outcome of the first birth and maternal characteristics. Term liveborn infants who were not small for gestational age were used as the reference category. Odds ratios were calculated before and after adjustment for maternal characteristics and pregnancy complications.
In further analyses, we investigated the risks of preterm and term stillbirth during the second birth and of having a small-for-gestational-age stillborn infant or a stillborn infant who was not small for gestational age during the second birth. Adjusted odds ratios were estimated to model the risk of these specific subtypes of stillbirth in the second birth as a function of the reproductive outcome of the first birth.
Results
The overall rate of stillbirth during the second pregnancy was 2.6 per 1000 births (total, 1062), and the rates of stillbirth ranged from 2.4 per 1000 among women whose first child was born at term and was not small for gestational age to 19.0 per 1000 among women whose first child was very preterm and was small for gestational age at birth (Table 1Table 1
Outcomes of the First Pregnancy and Univariate Associations with the Risk of Stillbirth during the Second Pregnancy among Women Who Had Two Successive Singleton Births in Sweden between 1983 and 1997.). As compared with women whose first child was born at term and was not small for gestational age, women whose first child was very preterm and was not small for gestational age had a significantly increased risk of stillbirth during their second pregnancy. The birth of a first infant who was small for gestational age was also associated with an increased risk of stillbirth during the second pregnancy, and the risk increased with decreasing gestational age. As expected, there was also a tendency for repeated stillbirths in successive births (Table 1).The rates of antepartum hemorrhage and hypertension during the second pregnancy were 1.5 percent and 2.3 percent, respectively. As compared with women without antepartum hemorrhage during the second pregnancy, women with antepartum hemorrhage had a crude odds ratio for stillbirth of 9.0 (95 percent confidence interval, 7.4 to 10.8). As compared with women without hypertension during the second pregnancy, women with hypertension had a crude odds ratio for stillbirth of 1.5 (95 percent confidence interval, 1.1 to 2.1). As compared with lean women (a body-mass index of less than 20.0), women with higher body-mass indexes had increased crude odds ratios for stillbirth during the second pregnancy as follows: 1.4 (95 percent confidence interval, 1.0 to 1.9) among those with a normal body-mass index (20.0 to 24.9), 1.9 (95 percent confidence interval, 1.3 to 2.7) among those who were overweight (body-mass index, 25.0 to 29.9), and 2.3 (95 percent confidence interval, 1.5 to 3.6) among those who were obese (body-mass index, 30.0 or more). As previously reported, advanced maternal age (35 years or older), a non-Nordic country of birth, maternal smoking, and short (0 to 3 months) or long (72 months or more) interpregnancy intervals also increased the risk of stillbirth.2
Since reproductive history as well as maternal factors and pregnancy complications influenced the risk of stillbirth, we examined the associations between maternal risk factors in the second pregnancy and the outcome of the first birth. As compared with women whose first child was born at term and was not small for gestational age, women whose child was born preterm, was small for gestational age, or was stillborn generally had a higher prevalence of maternal risk factors and complications during the second pregnancy (Table 2Table 2
Distribution of Maternal Characteristics and Complications during the Second Pregnancy, According to the Outcome of the First Pregnancy.).As compared with women whose first infant was not small for gestational age and was delivered at term, women whose first infant was not small for gestational age but was delivered very preterm (before 32 weeks of gestation) had an adjusted risk of stillbirth in the subsequent birth of 2.2 (Model 1 in Table 3Table 3
Association between the Outcome of the First Pregnancy and the Adjusted Odds Ratios for Stillbirth during the Second Pregnancy.). The delivery of a first infant at term who was small for gestational age was also associated with an increased risk of stillbirth (odds ratio, 2.1), whereas the delivery of a first infant who was small for gestational age and moderately or very preterm increased the risk of stillbirth by factors of 3.8 and 6.3, respectively. When we also adjusted the analyses for maternal body-mass index and height during the second pregnancy (information that was available only from 1992 onward), delivery of a first very preterm infant who was not small for gestational age was no longer significantly associated with an increased risk of stillbirth, whereas the other results remained essentially unchanged (data not shown).Because pregnancy complications may lead to fetal growth restriction as well as stillbirth, we also included hypertensive diseases and antepartum hemorrhage during the second pregnancy as covariates. In this model, the risks of stillbirth related to previous preterm small-for-gestational-age births were attenuated but remained significantly increased (Table 3). Finally, when we also included information about hypertensive diseases and antepartum hemorrhage during the first pregnancy, the odds of stillbirth among women whose first child was very preterm and was small for gestational age were attenuated but were still significantly increased (adjusted odds ratio, 4.1; 95 percent confidence interval, 2.0 to 8.2); the other risk estimates were materially unchanged and remained significant (data not shown).
When the analyses were stratified according to preterm and term stillbirth, we found that previous adverse pregnancy outcomes were primarily associated with an increased risk of preterm stillbirth (Table 4Table 4
Association between the Outcome of the First Pregnancy and the Adjusted Odds Ratios for Preterm (before 37 Weeks of Gestation) and Term (37 Weeks of Gestation or More) Stillbirth during the Second Pregnancy.). As compared with women whose first infant was born at term and was not small for gestational age, women whose first child was very preterm and was small for gestational age had a risk of preterm stillbirth during their subsequent pregnancy of 5.9. A history of a previous stillbirth almost quadrupled the risk of preterm stillbirth in the subsequent delivery, but it was not associated with an increased risk of term stillbirth. Only previous very preterm and term small-for-gestational-age births increased the risk of term stillbirth during the subsequent pregnancy.Previous adverse pregnancy outcomes were associated with increased risks of delivery of a stillborn infant who was small for gestational age (i.e., a stillborn fetus classified as being small for gestational age at delivery), and the risk was particularly increased among women whose first infant was both small for gestational age and preterm (Table 5Table 5
Association between the Outcome of the First Pregnancy and the Adjusted Odds Ratios for Delivery of a Stillborn Second Infant Who Was or Was Not Small for Gestational Age.). As compared with women whose first child was born at term and was not small for gestational age, women whose first child was small for gestational age and was moderately or very preterm had a risk of delivering a small-for-gestational-age stillborn second child of 8.0 and 15.2, respectively.Discussion
We found that the delivery of a first infant who was small for gestational age increased the subsequent risk of stillbirth. When the first infant was small for gestational age as well as preterm, the association with subsequent stillbirth was further amplified, and the risk increased with decreasing gestational age at delivery.
The strong association between the birth of a first infant who was small for gestational age and the subsequent risk of stillbirth may be explained by the fact that similar factors may underlie the two conditions. Intrauterine malnourishment may lead to a liveborn small-for-gestational-age infant24 or a stillbirth,25 and many stillborn infants are classified as being small for gestational age at birth.4,5 Since women with a first small-for-gestational-age infant tend to have subsequent infants who are also small for gestational age,26,27 it was not surprising that a history of a small-for-gestational-age live birth increased the risk of a small-for-gestational-age stillbirth.
We found that the strength of the association between the live birth of a first small-for-gestational-age infant and the subsequent risk of stillbirth increased if the first infant was preterm (delivered before 37 completed weeks of gestation), especially if the first infant was delivered very preterm (before 32 weeks of gestation). Our definition of small size for gestational age was based on the Swedish fetal growth curve, which was developed to establish norms for intrauterine weight at different gestational ages.22 As compared with traditional birth-weight curves, fetal growth curves indicate that preterm infants are more likely than term infants to be small for gestational age and to have severe fetal growth restriction.19,20 The majority of preterm infants who are small for gestational age are delivered electively,19,20 primarily because of signs of fetal growth restriction or asphyxia.28 Since severe fetal growth restriction is closely associated with the preterm delivery of either a liveborn19,20,29 or stillborn1,5 infant who is small for gestational age, we speculate that some preterm infants who are small for gestational age would have been stillborn if they had been delivered at term.
The mechanisms accounting for the relations among the birth of a small-for-gestational-age infant, preterm birth, and the risk of a subsequent stillbirth are not clear. We controlled for maternal smoking status, one of the strongest risk factors for fetal growth restriction,13 as well as other maternal characteristics, such as body-mass index and level of education. When we also included information about maternal hypertensive diseases and antepartum bleeding as covariates, the risks were attenuated but remained significantly increased. Intergenerational research suggests that there may be genetic determinants of reproductive outcomes.30 Genetic or environmental factors that contribute to the development of fetal growth retardation and intrauterine asphyxia not only may lead to an increased risk of having subsequent infants who are small for gestational age or stillborn, but also may explain the association between the delivery of a previous small-for-gestational-age infant and the risk of stillbirth in subsequent pregnancies.
The rate of stillbirth during the second pregnancy was lower among women whose first infant had been stillborn (7.6 per 1000 births) than among women whose first infant had been very or moderately preterm and small for gestational age (19.0 per 1000 and 9.5 per 1000, respectively). Stillbirth has a heterogeneous cause, and the small number of repeated stillbirths did not allow us to subclassify them. Since the risk of recurrent stillbirth is well known,14,15 there is probably heightened supervision of women with a history of stillbirth. However, although the decline in stillbirth rates during the past three decades31 coincides with the introduction of diagnostic tools intended to increase fetal surveillance, it is not clear whether heightened supervision of women with previous stillbirths reduces the risk of recurrent stillbirth.
The strengths of our study include the small amount of missing data and the inclusion of virtually all births in Sweden during the study period. We adjusted for maternal factors and pregnancy complications related to stillbirth. Since some of the factors we adjusted for, such as smoking and placental abruption and hypertensive disease, are also known causes of small size for gestational age,10,24 these adjustments may have led to an underestimation of the relation between the delivery of a first infant who was small for gestational age and the subsequent risk of stillbirth. Our analysis also controlled for the maternal level of education; however, because maternal stress and socioeconomic status have been linked to preterm birth32 as well as stillbirth,33 there may be some residual confounding related to unmeasured social factors.
We were restricted to data included in the Swedish Birth Register and could not investigate previous pregnancy outcomes in relation to the underlying causes of stillbirth. Another limitation of this study is the use of small size for gestational age as a proxy for fetal growth restriction. Some infants classified as being small for gestational age will be small for reasons that are not related to fetal growth restriction, whereas other infants with a genetic disposition to be large may appear to be within the normal range, even though their growth has been restricted.5 For stillbirths, gestational age and birth weight were estimated at the time of delivery and not at the time of death, which may have led to falsely high rates of stillbirth classified as small for gestational age or term. However, most stillbirths in Sweden are delivered within 24 hours after the diagnosis,34 and a U.S. study of fetal histologic findings and stillbirth estimated that 80 percent of all stillbirths were delivered within one week after intrauterine death.35 Thus, the influence of this potential misclassification is probably minimal. The Swedish Birth Register includes information only on stillbirths that occur at or after 28 weeks of gestation, and our results should not be generalized to include fetal deaths that occur before 28 weeks of gestation. Although many of the odds ratios we report are large, it should be kept in mind that the rates and absolute risks of stillbirth during a second pregnancy are still quite low, and the overwhelming majority of women whose first infant was small for gestational age delivered liveborn second infants.
The strong association between the birth of a first infant who was small for gestational age and the subsequent risk of stillbirth further emphasizes the central role of fetal growth restriction in the etiologic process of stillbirth. Randomized, controlled trials have shown that the use of umbilical-artery Doppler velocimetry reduces the risk of perinatal mortality in high-risk pregnancies.36 Early recognition of fetal growth restriction may be a prerequisite to the prevention of some stillbirths, but we do not yet know the optimal clinical approach to the compromised, very-preterm fetus with growth restriction.29
Supported by the American–Scandinavian Foundation through a grant from the Thord–Gray Memorial Fund and a grant (2001-2247) from the Swedish Council for Working Life and Social Research.
Source Information
From the Departments of Medical Epidemiology and Biostatistics (P.J.S., O.S., P.W.D., S.C.) and Women's and Children's Health (O.S.), Karolinska Institutet, Stockholm, Sweden; and the Department of Maternal and Child Health, Harvard School of Public Health, Boston (P.J.S.).
- References
References
1
Cnattingius S ,Haglund B ,Kramer MS . Differences in late fetal death rates in association with determinants of small for gestational age fetuses: population based cohort study. BMJ 1998;316:1483-1487
CrossRef | Web of Science | Medline2
Stephansson O ,Dickman PW ,Cnattingius S . The influence of interpregnancy interval on the subsequent risk of stillbirth and early neonatal death. Obstet Gynecol 2003;102:101-108
CrossRef | Web of Science | Medline3
Barfield WD ,Tomashek KM ,Flowers LM ,Iyasu S . Contribution of late fetal deaths to US perinatal mortality rates, 1995-1998. Semin Perinatol 2002;26:17-24
CrossRef | Web of Science | Medline4
Clausson B ,Gardosi J ,Francis A ,Cnattingius S . Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. Br J Obstet Gynaecol 2001;108:830-834
CrossRef5
Gardosi J ,Mul T ,Mongelli M ,Fagan D . Analysis of birthweight and gestational age in antepartum stillbirths. Br J Obstet Gynaecol 1998;105:524-530
CrossRef | Medline6
Fretts RC ,Boyd ME ,Usher RH ,Usher HA . The changing pattern of fetal death, 1961-1988. Obstet Gynecol 1992;79:35-39
Web of Science | Medline7
Schneider J . Repeated pregnancy loss. Clin Obstet Gynecol 1973;16:120-133
CrossRef | Medline8
Benirschke K ,Robb JA . Infectious causes of fetal death. Clin Obstet Gynecol 1987;30:284-294
CrossRef | Web of Science | Medline9
Tolockiene E ,Morsing E ,Holst E , et al. Intrauterine infection may be a major cause of stillbirth in Sweden. Acta Obstet Gynecol Scand 2001;80:511-518
CrossRef | Web of Science | Medline10
Ananth CV ,Berkowitz GS ,Savitz DA ,Lapinski RH . Placental abruption and adverse perinatal outcomes. JAMA 1999;282:1646-1651
CrossRef | Web of Science | Medline11
Garbaciak JA Jr . Prematurity prevention: who is at risk? Clin Perinatol 1992;19:275-289
Web of Science | Medline12
Khoury MJ ,Erickson JD ,Cordero JF ,McCarthy BJ . Congenital malformations and intrauterine growth retardation: a population study. Pediatrics 1988;82:83-90
Web of Science | Medline13
Kramer MS . Intrauterine growth and gestational duration determinants. Pediatrics 1987;80:502-511
Web of Science | Medline14
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
CrossRef | Web of Science | Medline15
Samueloff A ,Xenakis EM ,Berkus MD ,Huff RW ,Langer O . Recurrent stillbirth: significance and characteristics. J Reprod Med 1993;38:883-886
Web of Science | Medline16
Miller HC ,Jekel JF . Associations between unfavorable outcomes in successive pregnancies. Am J Obstet Gynecol 1985;153:20-24
Web of Science | Medline17
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
CrossRef | Web of Science | Medline18
Freeman RK ,Dorchester W ,Anderson G ,Garite TJ . The significance of a previous stillbirth. Am J Obstet Gynecol 1985;151:7-13
Web of Science | Medline19
Papiernik E . Fetal growth retardation: a limit for the further reduction of preterm births. Matern Child Health J 1999;3:63-69
CrossRef | Medline20
Lackman F ,Capewell V ,Richardson B ,daSilva O ,Gagnon R . The risks of spontaneous preterm delivery and perinatal mortality in relation to size at birth according to fetal versus neonatal growth standards. Am J Obstet Gynecol 2001;184:946-953
CrossRef | Web of Science | Medline21
Lindmark G ,Cnattingius S . The scientific basis of antenatal care: report from a state-of-the-art conference. Acta Obstet Gynecol Scand 1991;70:105-109
CrossRef | Medline22
Marsal K ,Persson PH ,Larsen T ,Lilja H ,Selbing A ,Sultan B . Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr 1996;85:843-848
CrossRef | Web of Science | Medline23
Hogberg U ,Larsson N . Early dating by ultrasound and perinatal outcome: a cohort study. Acta Obstet Gynecol Scand 1997;76:907-912
CrossRef | Web of Science | Medline24
Stein ZA ,Susser M . Intrauterine growth retardation: epidemiological issues and public health significance. Semin Perinatol 1984;8:5-14
Web of Science | Medline25
Cnattingius S ,Stephansson O . The epidemiology of stillbirth. Semin Perinatol 2002;26:25-30
CrossRef | Web of Science | Medline26
Patterson RM ,Gibbs CE ,Wood RC . Birth weight percentile and perinatal outcome: recurrence of intrauterine growth retardation. Obstet Gynecol 1986;68:464-468
Web of Science | Medline27
Bakketeig LS ,Hoffman HJ ,Harley EE . The tendency to repeat gestational age and birth weight in successive births. Am J Obstet Gynecol 1979;135:1086-1103
Web of Science | Medline28
Hershkovitz R ,Erez O ,Sheiner E , et al. Comparison study between induced and spontaneous term and preterm births of small-for-gestational-age neonates. Eur J Obstet Gynecol Reprod Biol 2001;97:141-146
CrossRef | Web of Science | Medline29
Marsal K . Intrauterine growth restriction. Curr Opin Obstet Gynecol 2002;14:127-135
CrossRef | Web of Science | Medline30
Emanuel I . Invited commentary: an assessment of maternal intergenerational factors in pregnancy outcome. Am J Epidemiol 1997;146:820-825
Web of Science | Medline31
Martin JA ,Hoyert DL . The national fetal death file. Semin Perinatol 2002;26:3-11
CrossRef | Web of Science | Medline32
Hoffman HJ ,Bakketeig LS . Risk factors associated with the occurrence of preterm birth. Clin Obstet Gynecol 1984;27:539-552
CrossRef | Web of Science | Medline33
Stephansson O ,Dickman PW ,Johansson AL ,Cnattingius S . The influence of socioeconomic status on stillbirth risk in Sweden. Int J Epidemiol 2001;30:1296-1301
CrossRef | Web of Science | Medline34
Radestad I ,Steineck G ,Nordin C ,Sjogren B . Psychological complications after stillbirth -- influence of memories and immediate management: population based study. BMJ 1996;312:1505-1508
CrossRef | Web of Science | Medline35
Genest DR ,Williams MA ,Greene MF . Estimating the time of death in stillborn fetuses. I. Histologic evaluation of fetal organs: an autopsy study of 150 stillborns. Obstet Gynecol 1992;80:575-584
Web of Science | Medline36
Westergaard HB ,Langhoff-Roos J ,Lingman G ,Marsal K ,Kreiner S . A critical appraisal of the use of umbilical artery Doppler ultrasound in high-risk pregnancies: use of meta-analyses in evidence-based obstetrics. Ultrasound Obstet Gynecol 2001;17:466-476
CrossRef | Web of Science | Medline
- Citing Articles (59)
Citing Articles
1
Chantal A. A. Heppolette, Donald Palmer, Susan E. Ozanne. 2011. 3 Experimental models of low birth weight – insight into the developmental programming of metabolic health, aging and immune function. , 11-26.
CrossRef2
Anna-Karin Wikström, Tobias Svensson, Helle Kieler, Sven Cnattingius. (2011) Recurrence of placental dysfunction disorders across generations. American Journal of Obstetrics and Gynecology 205:5, 454.e1-454.e8
CrossRef3
Shane Reeves, Henry L. Galan. 2011. Fetal growth restriction. , 329-344.
CrossRef4
Uma M. Reddy. 2011. Fetal death. , 390-396.
CrossRef5
Robert M. Silver. (2011) Previous Stillbirth, Late Preterm, and Early-Term Birth. Seminars in Perinatology 35:5, 302-308
CrossRef6
Michael Tchirikov, Miriam Tchirikov, Ralph Buchert, Florian Wilke, Winfried Brenner. (2011) Glucose uptake in the placenta, fetal brain, heart and liver related to blood flow redistribution during acute hypoxia. Journal of Obstetrics and Gynaecology Research 37:8, 979-985
CrossRef7
George Saade. 2011. Management of the Subsequent Pregnancy. , 242-250.
CrossRef8
Ruth Fretts. 2011. High Income Countries. , 1-18.
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CrossRef10
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CrossRef11
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CrossRef12
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CrossRef13
Ranjit Akolekar, Sarah Bower, Nicola Flack, Caterina M. Bilardo, Kypros H. Nicolaides. (2011) Prediction of miscarriage and stillbirth at 11-13 weeks and the contribution of chorionic villus sampling. Prenatal Diagnosis 31:1, 38-45
CrossRef14
Uma M. Reddy, S. Katherine Laughon, Liping Sun, James Troendle, Marian Willinger, Jun Zhang. (2010) Prepregnancy Risk Factors for Antepartum Stillbirth in the United States. Obstetrics & Gynecology 116:5, 1119-1126
CrossRef15
M. Nørgaard, H. Larsson, L. Pedersen, F. Granath, J. Askling, H. Kieler, A. Ekbom, H. T. Sørensen, O. Stephansson. (2010) Rheumatoid arthritis and birth outcomes: a Danish and Swedish nationwide prevalence study. Journal of Internal Medicine 268:4, 329-337
CrossRef16
GORDON C. S. SMITH. (2010) Predicting Antepartum Stillbirth. Clinical Obstetrics and Gynecology 53:3, 597-606
CrossRef17
UMA M. REDDY. (2010) Management of Pregnancy After Stillbirth. Clinical Obstetrics and Gynecology 53:3, 700-709
CrossRef18
AH Herring, UM Reddy. (2010) Recurrence risk of stillbirth in the second pregnancy. BJOG: An International Journal of Obstetrics & Gynaecology 117:10, 1173-1174
CrossRef19
RUTH FRETTS. (2010) Stillbirth Epidemiology, Risk Factors, and Opportunities for Stillbirth Prevention. Clinical Obstetrics and Gynecology 53:3, 588-596
CrossRef20
Michael Tchirikov, Miriam Strohner, Alexander Scholz. (2010) Cardiac output and blood flow volume redistribution during acute maternal hypoxia in fetal sheep. Journal of Perinatal Medicine 38:4, 387-392
CrossRef21
Olof Stephansson, Heidi Larsson, Lars Pedersen, Helle Kieler, Fredrik Granath, Jonas F. Ludvigsson, Henrik Falconer, Anders Ekbom, Henrik Toft Sørensen, Mette Nørgaard. (2010) Crohn's Disease Is a Risk Factor for Preterm Birth. Clinical Gastroenterology and Hepatology 8:6, 509-515
CrossRef22
G Singh, K Sidhu. (2010) Bad obstetric history: A prospective study. Medical Journal Armed Forces India 66:2, 117-120
CrossRef23
RuthC Fretts, FrederikJ Frøen, Vicki Flenady. 2010. Stillbirths and prevention strategies in developing and developed countries. , 65-70.
CrossRef24
UmaM Reddy. 2010. Prediction and prevention of recurrent stillbirth. , 55-64.
CrossRef25
Jack K. Leiss, Denise Giles, Kristin M. Sullivan, Rahel Mathews, Glenda Sentelle, Kay M. Tomashek. (2010) U.S. Maternally Linked Birth Records May Be Biased for Hispanics and Other Population Groups. Annals of Epidemiology 20:1, 23-31
CrossRef26
A. Elvira, A. Oyarzabal, A. Murgiondo, J. Paredes, G. Juaristi. (2010) Muerte fetal anteparto y síndrome de Sjögren oculto. Clínica e Investigación en Ginecología y Obstetricia 37:1, 41-44
CrossRef27
Lesley McCowan, Richard P. Horgan. (2009) Risk factors for small for gestational age infants. Best Practice & Research Clinical Obstetrics & Gynaecology 23:6, 779-793
CrossRef28
Svein Rasmussen, Lorentz M. Irgens, Rolv Skjærven, Kari Klungsøyr Melve. (2009) Prior Adverse Pregnancy Outcome and the Risk of Stillbirth. Obstetrics & Gynecology 114:6, 1259-1270
CrossRef29
Emmanuel Ngui, Alicia Cortright, Kathleen Blair. (2009) An Investigation of Paternity Status and Other Factors Associated with Racial and Ethnic Disparities in Birth Outcomes in Milwaukee, Wisconsin. Maternal and Child Health Journal 13:4, 467-478
CrossRef30
E. REY, P. GARNEAU, M. DAVID, R. GAUTHIER, L. LEDUC, N. MICHON, F. MORIN, C. DEMERS, S. R. KAHN, L. A. MAGEE, M. RODGER. (2009) Dalteparin for the prevention of recurrence of placental-mediated complications of pregnancy in women without thrombophilia: a pilot randomized controlled trial. Journal of Thrombosis and Haemostasis 7:1, 58-64
CrossRef31
Maximilian B. Franz, Nicholas Lack, Barbara Schiessl, Ioannis Mylonas, Klaus Friese, Franz Kainer. (2009) Stillbirth following previous cesarean section in Bavaria/Germany 1987–2005. Archives of Gynecology and Obstetrics 279:1, 29-36
CrossRef32
Phillip G. Stubblefield, Dean V. Coonrod, Uma M. Reddy, Raja Sayegh, Wanda Nicholson, Daniel F. Rychlik, Brian W. Jack. (2008) The clinical content of preconception care: reproductive history. American Journal of Obstetrics and Gynecology 199:6, S373-S383
CrossRef33
M Mohsin, B Jalaludin. (2008) Influence of previous pregnancy outcomes and continued smoking on subsequent pregnancy outcomes: an exploratory study in Australia. BJOG: An International Journal of Obstetrics & Gynaecology 115:11, 1428-1435
CrossRef34
John R. Barton, Baha M. Sibai. (2008) Prediction and Prevention of Recurrent Preeclampsia. Obstetrics & Gynecology 112:2, Part 1, 359-372
CrossRef35
Anne Lang Dunlop, Cynthia Dubin, B. Denise Raynor, George W. Bugg, Brian Schmotzer, Alfred W. Brann. (2008) Interpregnancy Primary Care and Social Support for African-American Women at Risk for Recurrent Very-low-birthweight Delivery: A Pilot Evaluation. Maternal and Child Health Journal 12:4, 461-468
CrossRef36
A. Elvira, A. Oyarzabal, M. Lure, A. Becerro. (2008) Factores de riesgo de la muerte fetal anteparto. Clínica e Investigación en Ginecología y Obstetricia 35:2, 56-60
CrossRef37
E. K. Williams, M. B. Hossain, R. K. Sharma, V. Kumar, C. M. Pandey, A. H. Baqui. (2008) Birth Interval and Risk of Stillbirth or Neonatal Death: Findings from Rural North India. Journal of Tropical Pediatrics 54:5, 321-327
CrossRef38
M Black, A Shetty, S Bhattacharya. (2008) Obstetric outcomes subsequent to intrauterine death in the first pregnancy. BJOG: An International Journal of Obstetrics & Gynaecology 115:2, 269-274
CrossRef39
Lesley M. E. McCOWAN, Maha GEORGE-HADDAD, Tomasina STACEY, John M. D. THOMPSON. (2007) Fetal growth restriction and other risk factors for stillbirth in a New Zealand setting. The Australian and New Zealand Journal of Obstetrics and Gynaecology 47:6, 450-456
CrossRef40
Janet M. Catov, Lisa M. Bodnar, Kevin E. Kip, Carl Hubel, Roberta B. Ness, Gail Harger, James M. Roberts. (2007) Early pregnancy lipid concentrations and spontaneous preterm birth. American Journal of Obstetrics and Gynecology 197:6, 610.e1-610.e7
CrossRef41
Uma M. Reddy. (2007) Prediction and Prevention of Recurrent Stillbirth. Obstetrics & Gynecology 110:5, 1151-1164
CrossRef42
Gordon CS Smith, Ruth C Fretts. (2007) Stillbirth. The Lancet 370:9600, 1715-1725
CrossRef43
Puza P. Sharma, Hamisu M. Salihu, Russel S. Kirby. (2007) Stillbirth recurrence in a population of relatively low-risk mothers. Paediatric and Perinatal Epidemiology 21:s1, 24-30
CrossRef44
L Högberg, S Cnattingius. (2007) The influence of maternal smoking habits on the risk of subsequent stillbirth: is there a causal relation?. BJOG: An International Journal of Obstetrics & Gynaecology 114:6, 699-704
CrossRef45
GCS Smith, I Shah, IR White, JP Pell, JA Crossley, R Dobbie. (2007) Maternal and biochemical predictors of antepartum stillbirth among nulliparous women in relation to gestational age of fetal death. BJOG: An International Journal of Obstetrics & Gynaecology 114:6, 705-714
CrossRef46
R Gray, MA Quigley, C Hockley, JJ Kurinczuk, M Goldacre, P Brocklehurst. (2007) Caesarean delivery and risk of stillbirth in subsequent pregnancy: a retrospective cohort study in an English population. BJOG: An International Journal of Obstetrics & Gynaecology 114:3, 264-270
CrossRef47
ROBERT M. SILVER, JENNIFER E. WARREN. (2006) Preconception Counseling for Women With Thrombophilia. Clinical Obstetrics and Gynecology 49:4, 906-919
CrossRef48
Hamisu M Salihu, Puza P Sharma, Shillena Peters. (2006) Twinning and Risk of Stillbirth Subtypes in Pediatric Mothers. Twin Research and Human Genetics 9:5, 673-676
CrossRef49
&NA;. (2006) Is Race a Determinant of Stillbirth Recurrence?. Obstetric Anesthesia Digest 26:3, 112-113
CrossRef50
Stephen ROBSON, Jane THOMPSON, David ELLWOOD. (2006) Obstetric management of the next pregnancy after an unexplained stillbirth: An anonymous postal survey of Australian obstetricians. The Australian and New Zealand Journal of Obstetrics and Gynaecology 46:4, 278-281
CrossRef51
Hamisu M. Salihu, Puza P. Sharma, Muktar H. Aliyu, Sibylle Kristensen, Jaqui Grimes-Dennis, Russell S. Kirby, John Smulian. (2006) Is Small for Gestational Age a Marker of Future Fetal Survival In Utero?. Obstetrics & Gynecology 107:4, 851-856
CrossRef52
Puza P. Sharma, Hamisu M. Salihu, Yinka Oyelese, Cande V. Ananth, Russell S. Kirby. (2006) Is Race a Determinant of Stillbirth Recurrence?. Obstetrics & Gynecology 107:2, Part 1, 391-397
CrossRef53
Ruth C. Fretts. (2005) Etiology and prevention of stillbirth. American Journal of Obstetrics and Gynecology 193:6, 1923-1935
CrossRef54
Muktar H. Aliyu, Hamisu M. Salihu, Louis G. Keith, John E. Ehiri, M Aminul Islam, Pauline E. Jolly. (2005) Extreme Parity and the Risk of Stillbirth. Obstetrics & Gynecology 106:3, 446-453
CrossRef55
Michael J. Paidas, De-Hui W. Ku, Jens Langhoff-Roos, Yale S. Arkel. (2005) Inherited Thrombophilias and Adverse Pregnancy Outcome: Screening and Management. Seminars in Perinatology 29:3, 150-163
CrossRef56
Karim Jarjoura, Patricia C. Devine, Annette Perez-Delboy, Miriam Herrera-Abreu, Mary D'Alton, Panos N. Papapanou. (2005) Markers of periodontal infection and preterm birth. American Journal of Obstetrics and Gynecology 192:2, 513-519
CrossRef57
V CRUZANGUIANO, J TALAVERA, L VAZQUEZ, A ANTONIO, A CASTELLANOS, M LEZANA, N WACHER. (2004) The importance of quality of care in perinatal mortality: a case-control study in Chiapas, Mexico. Archives of Medical Research 35:6, 554-562
CrossRef58
S. London. (2004) Poor Outcome in First Pregnancy May Predict Stillbirth in Second One. Perspectives on Sexual and Reproductive Health 36:3, 133-134
CrossRef59
Zhang, Jun, Klebanoff, Mark A., . (2004) Small-for-Gestational-Age Infants and Risk of Fetal Death in Subsequent Pregnancies. New England Journal of Medicine 350:8, 754-756
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