SMFM Papers
ajog.org
Incidence and recurrence rate of placental abruption: a longitudinal linked national cohort study in the Netherlands Laura Ruiter, MD; Anita C. J. Ravelli, PhD; Irene M. de Graaf, MD, PhD; Ben Willem J. Mol, MD, PhD; Eva Pajkrt, MD, PhD OBJECTIVE: Women who have experienced a placental abruption have
a risk of recurrence, but exact information to quantify this risk is currently not available. We studied the incidence and recurrence rate of placental abruption in a subsequent pregnancy and the influence of hypertensive disorders. STUDY DESIGN: We conducted a retrospective national cohort study of
all singleton pregnancies that ended from 1999-2007 in the Netherlands. A longitudinal linked national cohort of these women with information on a subsequent singleton delivery was used. We calculated and compared incidence and recurrence rates of placental abruption for women in total, stratified by gestational age of first placental abruption and by the presence of a hypertensive disorder in their first pregnancy. RESULTS: We studied 1,570,635 women of which 3496 (0.22%)
experienced a placental abruption. Information was available on a subsequent singleton delivery for 264,424 deliveries. Of these, 521 women (0.20%) had a placental abruption in the first pregnancy vs 214 women (0.08%) in the second pregnancy. The risk of placental abruption in a subsequent pregnancy was significantly higher in women with a previous placental abruption compared with women without (5.8% vs 0.06%; adjusted odds ratio [aOR], 93; 95%
confidence interval [CI], 62e139). Women with a placental abruption that occurred at term in their first pregnancy were more at risk for recurrence (aOR, 188; 95% CI, 116e306) than women with a preterm (aOR, 52; 95% CI, 25e111) or early preterm (<32 weeks of gestation) placental abruption in their first pregnancy (aOR, 39; 95% CI, 13e116). Placental abruption was more frequent among women with a hypertensive disorder compared with normotensive women (0.44% vs 0.16%; odds ratio, 2.7; 95% CI, 2.3e3.3). Women with a hypertensive disorder were less at risk for recurrence than were normotensive women (aOR, 0.68; 95% CI, 0.27e1.6). No interaction between a hypertensive disorder in the first pregnancy and the recurrence risk was found. CONCLUSION: Women with a placental abruption in their first pregnancy have a greatly increased risk of placental abruption in a subsequent pregnancy. Hypertensive disorders increase the risk of placental abruption but do not increase the recurrence rate in a subsequent pregnancy. We suggest elective induction from 37 weeks of gestation for women with a history of placental abruption at term in a previous pregnancy.
Key words: hypertension, incidence, placental abruption, recurrence
Cite this article as: Ruiter L, Ravelli ACJ, de Graaf IM, et al. Incidence and recurrence rate of placental abruption: a longitudinal linked national cohort study in the Netherlands. Am J Obstet Gynecol 2015;213:573.e1-8.
P
lacental abruption, the premature dehiscence of a normally inserted placenta from the uterine wall, is associated with significant perinatal morbidity and accounts for 12% of all perinatal deaths in the United States.1 Early diagnosis of placental abruption potentially can improve the outcome of
the children who are involved in these pregnancies by closely monitoring women who are at risk.2 Advanced maternal age, multiparity,3 chronic hypertension,3 smoking,4,5 cocaine use,6 previous cesarean delivery,5,7 uterine surgery,5 and short interpregnancy interval7 are reported risk factors for
From the Departments of Obstetrics and Gynecology (Drs Ruiter, de Graaf, and Pajkrt), and Medical Informatics (Dr Ravelli), Academic Medical Center, Amsterdam, the Netherlands, and the Robinson Institute, School of Pediatrics and Reproductive Health, University of Adelaide, SA, Australia (Dr Mol). Received March 6, 2015; revised April 30, 2015; accepted June 3, 2015. The authors report no conflict of interest. Presented as a poster at the 35th annual meeting of the Society for Maternal-Fetal Medicine, San Diego, CA, Feb. 2-7, 2015. Corresponding author: Laura Ruiter, MD.
[email protected] 0002-9378/$36.00 ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2015.06.019
placental abruption. In patients who experienced a placental abruption in a previous pregnancy, there seems to be a tendency for recurrence, although most studies on the incidence and recurrence rate of placental abruption are dated or include relatively small samples of patients.8,9 Knowledge of these subjects potentially can help in providing specialized prenatal care for women who are at risk for placental abruption for the reason of beneficial outcome.10 Our objective was to investigate the incidence and recurrence rate of placental abruption in a retrospective study of 2 subsequent deliveries in the Netherlands between 1999 and 2007. Moreover, we assessed the influence of hypertensive disorders on the incidence and recurrence rate.
OCTOBER 2015 American Journal of Obstetrics & Gynecology
573.e1
SMFM Papers M ATERIALS
AND
M ETHODS
This study was performed in a retrospective nationwide cohort with the use of the Netherlands Perinatal Registry (PRN). The PRN consists of prospectively collected population-based data that contain information on pregnancies, deliveries, and (re)admissions until 28 days after birth. The database is obtained by a validated linkage of 3 different registries: the midwifery registry, the obstetrics registry, and the neonatology registry of hospital admissions of newborn infants.11,12 The coverage of the PRN registry is approximately 96% of all deliveries in the Netherlands, and it contains all pregnancies that ended in live births and stillbirths at >22 weeks of gestation and a birthweight of at least 500 g. Furthermore, all admissions to the neonatology care unit are registered until 28 days after birth. It is used primarily for annual assessment of the quality indicators of obstetric care. The records included in the PRN registry are entered at child’s level. There is no unique maternal identifier available in the registry to follow up on outcomes of subsequent pregnancies of the same mother. Previously, a longitudinal probabilistic-linkage procedure in which records of children of the same mother are linked was performed to create a mother identifier. This resulted in a cohort of 272,551 women with complete data on first and second deliveries of the same mother. Details on this linkage procedure are described elsewhere.13 The data in the PRN database are anonymous; the Dutch Perinatal Registry gave their approval for the use of the data for this study (approval no. 12.71).
Inclusion and exclusion criteria We selected all women who delivered in the Netherlands between Jan. 1, 1999, and Dec. 31, 2007. We excluded women with a multiple gestation (n ¼ 7,472) and women with a gestational age at delivery of >42 þ 6 weeks (n ¼ 655). Outcome measures Our primary outcome was placental abruption. We identified all women with
ajog.org a placental abruption that had been registered in the PRN registry with a code for placental abruption. Codes are assigned by midwives, residents, and obstetricians based on information in the patients’ medical record. A clinical diagnosis of placental abruption is made based on a combination of the following clinical symptoms: vaginal bleeding, abdominal pain, or fetal distress and further supported by ultrasonographic findings as retro placental bleeding. After delivery, the diagnosis may be confirmed by a couvelaire uterus, gory amniotic fluid, or examination of the placenta that reveals a clot.14 Placental abruption primarily is documented by 2 of the care providers after delivery; there is no stratification in severity in the PRN database. In addition, all women with a positive history of placental abruption at the start of the second pregnancy were labelled as cases of placental abruption in the first pregnancy. The gestational age at delivery of the fetus was used as the gestational age of placental abruption.
Characteristics We extracted demographic and obstetric baseline characteristics from the PRN registry as ethnicity, maternal age, socioeconomic status, pregnancy interval, hypertension, and neonatal sex. All characteristics were primarily documented by the care providers. Ethnicity was categorized into white (native Dutch and other white women) and non-white (different ethnic groups as African/Surinamese, South Asian, Moroccan and Turkish) for this study. The continuous socioeconomic status score (based on mean income level, the percentage of households with a low income, inhabitants without a paid job, and households with, on average, a low education in a postal code area) was categorized into a high, middle, and low group based on percentile ranges ( 25th percentile, middle, >75th percentile). Gestational age was based on last menstrual period or ultrasound measurements at <20 weeks of gestation. If the estimation by ultrasound measurement differed >6 days from the last menstrual period, then the ultrasound measurement was considered the dominant measurement.
573.e2 American Journal of Obstetrics & Gynecology OCTOBER 2015
Hypertensive disorders (HTD) included chronic hypertension, pregnancy-induced hypertension, and preeclampsia. The clinical diagnosis of hypertension was made with a systolic blood pressure of 140 mm Hg and/or a diastolic blood pressure of 90 mm Hg. Preeclampsia was diagnosed with hypertension and proteinuria.15 Cases of placental abruption were analyzed in total and stratified into 3 groups based on the gestational age at the time of placental abruption in the first pregnancy; early preterm (22þ0 e 31þ6 weeks of gestation), late preterm (32þ0e 36þ6 weeks of gestation), and term (37þ0e 42þ6 weeks of gestation). In addition, we stratified the analysis by HTD in the first pregnancy: women with an HTD in their first pregnancy and women without an HTD in their first pregnancy.
Analysis We calculated the incidence of placental abruption in our cohort of 1,570,635 singleton deliveries by dividing the number of placental abruptions by the total number of deliveries. We calculated the incidence per gestational week by dividing the number of placental abruptions in a particular week by the total number of deliveries in that given week. We selected all women with a subsequent singleton delivery and compared incidence of placental abruption in a subsequent pregnancy in women with and without a placental abruption in their first pregnancy. In addition, we compared their demographic and obstetric baseline characteristics. Comparison of the baseline characteristics was by univariate analysis that was performed with the unpaired t-test for normally distributed continuous variables and with the c2 test for categoric variables. All tests were 2-sided with a probability value of .05 as the threshold for statistical significance. To estimate the effect of a history of placental abruption on the occurrence of placental abruption in a subsequent pregnancy, logistic regression modeling was used and was expressed as odds ratio with a 95% confidence interval (CI). In addition, the effect of gestational
SMFM Papers
ajog.org age at placental abruption in the first pregnancy was estimated and expressed as odds ratio with 95% CI. To account for the effect of potential confounders, we used a multivariate logistic regression analysis to adjust for variables that were distributed unequally in the baseline characteristics. When a low incidence of placental abruption was found, Firths’ penalized likelihood approach was performed to minimize small sample size bias. Kaplan-Meier curves by gestational age of first placental abruption were constructed for the recurrent placental abruptions. We tested for an association between placental abruption and HTD in the first pregnancy. When statistically significant, analyses were also performed separately for HTD and non-HTD cases per 3 strata of gestational age of first placental abruption. In addition, we tested for interaction between HTD in the first pregnancy and the recurrence of placental abruption in a subsequent pregnancy by adding an interaction term to our logistic regression model.
The data were analyzed with the SAS statistical software package (version 9.3; SAS Institute Inc, Cary, NC).
R ESULTS Between Jan. 1, 1999, and Dec. 31, 2007, a total of 1,570,635 singleton pregnancies were identified; 3496 pregnancies (0.22%) were complicated by a placental abruption. The overall incidence was highest between 28 and 31 weeks of gestation, with 40.8 per 1000 deliveries (4.1%). Between 32 and 34 weeks of gestation, the incidence was 20.5 per 1000 deliveries (2.1%); between 39 and 42 weeks of gestation, the incidence was 0.8 per 1000 (0.08%; Figure 1). A total of 264,424 women (528,848 deliveries) were available for the analysis of the recurrence rate and incidence of placental abruption in a subsequent pregnancy. Baseline characteristics of our linked cohort are listed in Table 1. In the first pregnancy, 521 women (0.20%) had a placental abruption, among these women an age of <25 years, non-white
ethnicity, low socioeconomic status, and HTDs were more prevalent. Of the 521 women with a placental abruption in the first pregnancy, 30 women (5.8%) had a recurrent placental abruption in the subsequent pregnancy. Placental abruption in a subsequent pregnancy occurred in 184 parous women (0.07%) without a history of placental abruption. Figure 2 shows all women with a placental abruption in the first pregnancy and their time to a recurrent placental abruption, stratified by gestational age of the first placental abruption. After adjustment for maternal age, ethnicity, socioeconomic status, and hypertension, a placental abruption in the first pregnancy was associated with a significantly increased risk of placental abruption in a subsequent pregnancy (adjusted odds ratio, 93; 95% CI, 62e139). Table 2 shows the distribution of placental abruption in a subsequent pregnancy in women with and without a history of placental abruption and the crude and adjusted odds ratios of
FIGURE 1
Incidence of placental abruption
Graph shows the incidence of placental abruption per 1000 deliveries per gestational week of pregnancy. Ruiter. Incidence and recurrence rate of placental abruption in singletons. Am J Obstet Gynecol 2015.
OCTOBER 2015 American Journal of Obstetrics & Gynecology
573.e3
SMFM Papers
ajog.org
TABLE 1
Baseline characteristics of the linked cohort Characteristics of the first pregnancy
Placental abruption in first pregnancy (n [ 521)
No placental abruption in first pregnancy (n [ 263,903)
P value
Maternal characteristics 28.0 4.6
Maternal age, ya Maternal age <25 y, n (%) Mean gestational age, wk
a
Non-white maternal ethnicity, n (%)
42,784 (16.2)
34.6 4.3
39.2 2.2
.0001 .0003 < .0001
74 (14.2)
28,826 (10.9)
.0165
Low socioeconomic status, n (%)
149 (28.6)
57,732 (21.9)
.0002
Hypertensive disorder, n (%)
147 (28.2)
33,186 (12.6)
< .0001
283 (54.3)
135,887 (51.5)
.1970
Fetal characteristic: male, n (%) a
115 (22.1)
28.6 4.2
Data are presented as mean SD.
Ruiter. Incidence and recurrence rate of placental abruption in singletons. Am J Obstet Gynecol 2015.
placental abruption in the first pregnancy on the recurrence rate of placental abruption in a subsequent pregnancy, stratified by gestational age of first placental abruption. The odds ratio of a history of placental abruption on the recurrence in a subsequent pregnancy was higher for women with a placental abruption in the term period of the first pregnancy than for women with a previous late or early preterm placental abruption. Of the 264,424 first singleton pregnancies, a total of 33,333 women (12.6%) had an HTD. In the second pregnancy, 17,378 women (6.6%) had an HTD. In the first pregnancy, placental abruption was more prevalent in the HTD group compared with the nonHTD group (0.44% vs 0.16%; odds ratio, 2.73; 95% CI, 2.26e3.31). In the second pregnancy, placental abruption was also more prevalent in the HTD group compared with the non-HTD group (0.52% vs 0.17%). Table 3 shows that, in both women with and without HTD in their first pregnancy, the recurrence risk of placental abruption is increased for women with a history of placental abruption compared with women without a history of placental abruption. Table 3 also shows that the odds ratio of a history of placental abruption on the recurrence risk is lower for women with an HTD in their first pregnancy compared with women who
were normotensive in their first pregnancy. Although the initial risk of placental abruption is increased by the presence of an HTD, the interaction between an HTD in the first pregnancy and the recurrence risk of placental abruption in a subsequent pregnancy was not statistically significant (P ¼ .1).
C OMMENT In this study, we investigated the overall incidence and recurrence rate of placental abruption among singleton pregnancies. Moreover, we investigated the influence of HTD on placental abruption. The incidence of placental abruption among singleton pregnancies was 0.22%. The incidence was higher in women with an HTD compared with normotensive women. The risk of placental abruption in a subsequent pregnancy was significantly higher in women with a previous placental abruption, compared with women without a previous placental abruption. Women with a first placental abruption at term were most at risk for recurrence. Our study has both strengths and limitations. Because placental abruption is a rare, but important, event, large amounts of data are needed to detect differences in populations. Our study was performed with data from a large population-based national registry in which data are collected prospectively. This provides validity of the results
573.e4 American Journal of Obstetrics & Gynecology OCTOBER 2015
because it represents a national outcome, which avoids recall and reporting bias by prospective collection and avoids selection bias that is created potentially by hospital-based studies. However, this study was a retrospective study, which comes with limitations. We needed to rely on the available information in the PRN; thus, we cannot rule out misclassification bias. It is likely that some cases have been missed, especially the mild or concealed ones. Another limitation is the unavailability of gestational age of abruption. From 32 weeks of gestation, placental abruption will be followed mostly by immediate delivery. Placental abruption can also be managed expectantly when it occurs at <32 weeks of gestation. The gestational age of abruption is then different than the date of delivery. The PRN registry does not provide this information; therefore, the difference in preterm and term incidence of placental abruption may be higher than found in this study. Data on possible confounders as body mass index and tobacco use also are not available in the PRN, and the usage of a linked database comes with restrictions as no linkage because of missing values of the linkage variables. The incidence of placental abruption that has been described in previous studies is 0.3-1%, which is higher than in our study.3-5 There are several potential explanations for this difference (for
SMFM Papers
ajog.org
FIGURE 2
Recurrent placental abruption by gestational age of first placental abruption
Graph shows the time to placental abruption in a subsequent pregnancy after the first early preterm, late preterm, or term placental abruption. PA, placental abruption. Ruiter. Incidence and recurrence rate of placental abruption in singletons. Am J Obstet Gynecol 2015.
example, missing cases because of the retrospective character of this study as mentioned before or inconsistencies in diagnostic criteria of placental abruption); there are neither laboratory tests nor diagnostic methods to detect placental abruption accurately. A previous study revealed that inconsistencies in the composition of placental abruption cases lead to differences in incidence.3 Most studies on incidence include singleton and multiple pregnancies. The latter are associated with a higher incidence of placental abruption, thus exclusion of multiple pregnancies from our analysis may have led to a lower incidence.16 With the exclusion of subsequent multiple pregnancies, we potentially excluded some women with a history of placental abruption as well. Furthermore, the incidence of placental abruption per 1000 deliveries decreases by gestational age. Some studies included pregnancies with a minimum gestational age of 16 weeks, whereas the PRN registry comprises only pregnancies from a gestational age of 22 weeks. 17-19 In general, the incidence of placental abruption seems to be lower in Nordic
countries than in the United States, where the population consists of more women from African American ethnicity. These women are more at risk for placental abruption than white women because HTD, smoking, alcohol, and cocaine use are more prevalent in this population.20-23 Our study population is relatively more homogenous, consisting of 90% maternal white ethnicity, thus potentially leading to a lower incidence. Furthermore, the percentage of cesarean delivery and thus the number of women with a history of cesarean delivery is significantly lower in our country compared with the United States.24 Studies in the United States found an increasing incidence of placental abruption over time, in contrast to Tikkanen et al,25 who performed a large population-based cohort study in Finland and found a decrease in the incidence of placental abruption from 1980e2005. Because we calculated the incidence on a recent cohort in the Netherlands that included mainly deliveries in the 21st century, this partially might explain our slightly lower incidence than studies
performed from 1980-2000. Also, improvements in prenatal care over the last decades may have contributed. Women with HTD, preeclampsia, or small-forgestational-age fetuses are diagnosed earlier and delivered before their due date, which potentially could decrease the risk of a placental abruption. Unfortunately, studies, for example, on medical decisionmaking in pregnancy-induced hypertension or preeclampsia frequently are underpowered to find significant effects on placental abruption.25,26 On the other hand, several risk factors for placental abruption, such as advanced maternal age and a previous cesarean section, are on the rise; therefore, the exact development of incidence of placental abruption remains difficult to determine. The decrease in incidence of placental abruption with advancing gestation in our study has been found in previous studies.17-19,25,27 Our distribution of incidence by gestational age is similar to Tikkanen et al. 25 The overall recurrence rate of placental abruption in this study was 5.8% (range, 2.3e11%). An increased risk for placental abruption after a previous placental abruption is found in
OCTOBER 2015 American Journal of Obstetrics & Gynecology
573.e5
SMFM Papers
ajog.org
TABLE 2
Placental abruption in a subsequent pregnancy in total and by gestational age of placental abruption in the first pregnancy Placental abruption in second pregnancy, wk
Odds ratio (95% confidence interval)
22 D 0 to 31 D 6, n
32 D 0 to 36 D 6, n
37 D 0 to 42 D 6, n
Total abruption second pregnancy, n (%)
Crude
Adjusteda
26
62
70
158 (0.1)
Reference
Reference
2
13
15
30 (5.8)
95 (64e142)
93 (62e139)
22 þ 0 to 31 þ 6 wk (n ¼ 128)
1
1
1
3 (2.3)
43 (16e126)
39 (13e116)
32 þ 0 to 36 þ 6 wk (n ¼ 210)
0
4
3
7 (3.3)
57 (27e120)
52 (25e111)
37 þ 0 to 42 þ 6 wk (n ¼ 183)
1
8
11
20 (11)
193 (119e313)
188 (116e306)
Variable Complete cohort of women with first-term delivery, no placental abruption in first pregnancy (n ¼ 243,799) Complete cohort placental abruption first pregnancy (n ¼ 521) Gestational age of placental abruption in the first pregnancy
a
Adjusted for hypertension, maternal age, ethnicity, and low socioeconomic status.
Ruiter. Incidence and recurrence rate of placental abruption in singletons. Am J Obstet Gynecol 2015.
previous studies, although in less welldefined populations, and data of these studies are dated.3,5,9,28-34 The true recurrence rate may even be higher than found in our study because women who have had placental abruption are less likely than women without a history placental abruption to have another pregnancy.8 In addition, elective delivery at term before labor in women with a history of placental abruption may also distort the true recurrence rate because, in these women, it is not known whether placental abruption would have occurred. On the contrary, obstetricians potentially are more likely to diagnose
and correctly code a placental abruption in women with a history of placental abruption compared with women without this history, which can amplify the recurrence rate. To the best of our knowledge, only one previous study investigated the influence of gestational age at first placental abruption on the recurrence rate.2 Rasmussen et al2 suggested that women with a history of placental abruption should receive special surveillance 6 weeks before the gestational age of the first placental abruption to reduce the recurrence risk to the initial risk. This is in line with our results that showed that
almost 60% of the second placental abruptions occurred in the same gestational period and that 40% of all women with placental abruption in the term period of the first pregnancy experienced recurrence in the late preterm period. We may add to these results that primarily women with first-term placental abruption are at risk for recurrence (11%). Thus, even though the incidence of placental abruption in the preterm period is higher than the incidence of placental abruption at term, the consequences for a subsequent pregnancy seem to be lower. However, we must interpret these results with caution
TABLE 3
Placental abruption in a subsequent pregnancy by presence of hypertensive disorder in the first pregnancy Complete cohort placental abruption first pregnancy (n [ 521)
Placental abruption in second pregnancy, wk 22 D 0 to 31 D 6, n
32 D 0 to 36 D 6, n
37 D 0 to 42 D 6, n
Total abruption second pregnancy, n (%)
Hypertensive disorder in first pregnancy (n ¼ 147)
0
2
4
6 (4.1)
No hypertensive disorder in first pregnancy (n ¼ 347)
2
11
11
24 (6.9)
a
Adjusted for maternal age, ethnicity, and low socioeconomic status.
Ruiter. Incidence and recurrence rate of placental abruption in singletons. Am J Obstet Gynecol 2015.
573.e6 American Journal of Obstetrics & Gynecology OCTOBER 2015
Odds ratio (95% confidence interval) Crude
Adjusteda
0.66 (0.27e1.60)
0.68 (0.28e1.63)
Reference
Reference
SMFM Papers
ajog.org because it is likely that term placental abruptions are diagnosed more accurately and reported than are early preterm abruptions. The association between HTD and placental abruption has been found in previous studies.3,35 The absent interaction between HTD and the recurrence of placental abruption in a subsequent pregnancy that was found in our study has not been described before. From our results, it seems that placental abruptions in normotensive women are more likely to recur than placental abruptions in women with an HTD. This possibly may be explained partially by the fact that the prevalence of HTD is less in second than in first pregnancies, attenuating this as a risk factor.36,37 It might also be due to more intensive monitoring of women in subsequent pregnancies after a previous pregnancyinduced hypertension or preeclampsia and lead to earlier diagnosis of complications and delivery. It would be valuable to stratify recurrence risk of placental abruption by type of HTD, because chronic hypertension and severe preeclampsia are stronger predictors for placental abruption than pregnancyinduced hypertension and mild preeclampsia; however, the design of the PRN registry did not allow us to perform such analysis.3,38 Furthermore, we would suggest elective induction at 37 weeks of gestation in women with a previous placental abruption in the term period of pregnancy. Although the design of this study cannot provide a clear answer to the question on the best strategy in these women and because multiple factors influence delivery timing beyond just the recurrence probability of placental abruption, >50% of the recurrent abruptions occurred after 37 weeks of gestation. In conclusion, the findings of this study show that women with placental abruption are at increased risk for recurrence, especially when the first placental abruption occurred in the term period. HTDs increase the initial risk of placental abruption. Potentially, normotensive women with a placental abruption in their first pregnancy are more at risk for recurrence than are women with an
HTD in their first pregnancy. It is desirable to monitor pregnant women with a history of placental abruption in tertiary centers and to monitor them closely in the gestational period of first placental abruption. ACKNOWLEDGMENTS We thank all Dutch midwives, obstetricians, neonatologists, and other perinatal health care providers for the registration of perinatal information and the Foundation of The Netherlands Perinatal Registry (www.perinatreg.nl) for permission to use the registry data.
REFERENCES 1. Ananth CV, Wilcox AJ. Placental abruption and perinatal mortality in the United States. Am J Epidemiol 2001;153:332-7. 2. Rasmussen S, Irgens LM, Albrechtsen S, Dalaker K. Women with a history of placental abruption: when in a subsequent pregnancy should special surveillance for a recurrent placental abruption be initiated? Acta Obstet Gynecol Scand 2001;80:708-12. 3. Ananth CV, Savitz DA, Williams MA. Placental abruption and its association with hypertension and prolonged rupture of membranes: a methodologic review and meta-analysis. Obstet Gynecol 1996;88:309-18. 4. Ananth CV, Savitz DA, Luther ER. Maternal cigarette smoking as a risk factor for placental abruption, placenta previa, and uterine bleeding in pregnancy. Am J Epidemiol 1996;144:881-9. 5. Tikkanen M, Nuutila M, Hiilesmaa V, Paavonen J, Ylikorkala O. Prepregnancy risk factors for placental abruption. Acta Obstet Gynecol Scand 2006;85:40-4. 6. Hulse GK, Milne E, English DR, Holman CD. Assessing the relationship between maternal cocaine use and abruptio placentae. Addiction 1997;92:1547-51. 7. Getahun D, Oyelese Y, Salihu HM, Ananth CV. Previous cesarean delivery and risks of placenta previa and placental abruption. Obstet Gynecol 2006;107:771-8. 8. Rasmussen S, Irgens LM, Dalaker K. The effect on the likelihood of further pregnancy of placental abruption and the rate of its recurrence. BJOG 1997;104:1292-5. 9. Karegard M, Gennser G. Incidence and recurrence rate of abruptio placentae in Sweden. Obstet Gynecol 1986;67:523-8. 10. Oyelese Y, Ananth CV. Placental abruption. Obstet Gynecol 2006;108:1005-16. 11. Meray N, Reitsma JB, Ravelli AC, Bonsel GJ. Probabilistic record linkage is a valid and transparent tool to combine databases without a patient identification number. J Clin Epidemiol 2007;60:883-91. 12. Tromp M, Ravelli AC, Meray N, Reitsma JB, Bonsel GJ. An efficient validation method of probabilistic record linkage including readmissions and twins. Methods Inf Med 2008;47:356-63.
13. Schaaf JM, Hof MH, Mol BW, Abu-Hanna A, Ravelli AC. Recurrence risk of preterm birth in subsequent singleton pregnancy after preterm twin delivery. Am J Obstet Gynecol 2012;207: 279.e1-7. 14. Guideline blood loss in the second and third trimester of pregnancy. Utrecht: The Dutch Society of Obstetrics and Gynecology; 2008. 15. Guideline hypertensive disorders in pregnancy. Utrecht: The Dutch Society of Obstetrics and Gynecology; 2011. 16. Ananth CV, Smulian JC, Demissie K, Vintzileos AM, Knuppel RA. Placental abruption among singleton and twin births in the United States: risk factor profiles. Am J Epidemiol 2001;153:771-8. 17. Sheiner E, Shoham-Vardi I, Hadar A, Hallak M, Hackmon R, Mazor M. Incidence, obstetric risk factors and pregnancy outcome of preterm placental abruption: a retrospective analysis. J Matern Fetal Neonatal Med 2002;11: 34-9. 18. Sheiner E, Shoham-Vardi I, Hallak M, et al. Placental abruption in term pregnancies: clinical significance and obstetric risk factors. J Matern Fetal Neonatal Med 2003;13:45-9. 19. Rasmussen S, Irgens LM, Bergsjo P, Dalaker K. The occurrence of placental abruption in Norway 1967-1991. Acta Obstet Gynecol Scand 1996;75:222-8. 20. Ananth CV, Berkowitz GS, Savitz DA, Lapinski RH. Placental abruption and adverse perinatal outcomes. JAMA 1999;282:1646-51. 21. Ananth CV, Oyelese Y, Yeo L, Pradhan A, Vintzileos AM. Placental abruption in the United States, 1979 through 2001: temporal trends and potential determinants. Am J Obstet Gynecol 2005;192:191-8. 22. Pritchard JA, Cunningham FG, Pritchard SA, Mason RA. On reducing the frequency of severe abruptio placentae. Am J Obstet Gynecol 1991;165:1345-51. 23. Nilsen RM, Vollset SE, Rasmussen SA, Ueland PM, Daltveit AK. Folic acid and multivitamin supplement use and risk of placental abruption: a population-based registry study. Am J Epidemiol 2008;167:867-74. 24. American College of Obstetricians Gynecologists, Society for Maternal-Fetal M, et al. Safe prevention of the primary cesarean delivery. Am J Obstet Gynecol 2014;210:179-93. 25. Tikkanen M, Riihimaki O, Gissler M, et al. Decreasing incidence of placental abruption in Finland during 1980-2005. Acta Obstet Gynecol Scand 2012;91:1046-52. 26. Koopmans CM, Bijlenga D, Groen H, et al. Induction of labour versus expectant monitoring for gestational hypertension or mild preeclampsia after 36 weeks’ gestation (HYPITAT): a multicentre, open-label randomised controlled trial. Lancet 2009;374:979-88. 27. Tikkanen M, Nuutila M, Hiilesmaa V, Paavonen J, Ylikorkala O. Clinical presentation and risk factors of placental abruption. Acta Obstet Gynecol Scand 2006;85:700-5. 28. Toivonen S, Heinonen S, Anttila M, Kosma VM, Saarikoski S. Obstetric prognosis
OCTOBER 2015 American Journal of Obstetrics & Gynecology
573.e7
SMFM Papers after placental abruption. Fetal Diagn Ther 2004;19:336-41. 29. Yla-Outinen A, Palander M, Heinonen PK. Abruptio placentae: risk factors and outcome of the newborn. Eur J Obstet Gynecol Reprod Biol 1987;25:23-8. 30. Pritchard JA, Brekken AL. Clinical and laboratory studies on severe abruptio placentae. Am J Obstet Gynecol 1967;97: 681-700. 31. Hibbard BM, Hibbard ED. Aetiological factors in abruptio placentae. BMJ 1963;2: 1430-6.
ajog.org 32. Hibbard BM, Jeffcoate TN. Abruptio placentae. Obstet Gynecol 1966;27:155-67. 33. Paterson ME. The aetiology and outcome of abruptio placentae. Acta Obstet Gynecol Scand 1979;58:31-5. 34. Rasmussen S, Irgens LM. Occurrence of placental abruption in relatives. BJOG 2009;116:693-9. 35. Ananth CV, Savitz DA, Bowes WA Jr, Luther ER. Influence of hypertensive disorders and cigarette smoking on placental abruption and uterine bleeding during pregnancy. BJOG 1997;104:572-8.
573.e8 American Journal of Obstetrics & Gynecology OCTOBER 2015
36. Surapaneni T, Bada VP, Nirmalan CP. Risk for recurrence of pre-eclampsia in the subsequent pregnancy. J Clin Diagn Res 2013;7: 2889-91. 37. Hargood JL, Brown MA. Pregnancyinduced hypertension: recurrence rate in second pregnancies. Med J Aust 1991;154:376-7. 38. Ananth CV, Smulian JC, Vintzileos AM. Incidence of placental abruption in relation to cigarette smoking and hypertensive disorders during pregnancy: a meta-analysis of observational studies. Obstet Gynecol 1999;93: 622-8.