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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
Obstet Gynecol. Author manuscript; available in PMC 2014 June 23.
Published in final edited form as:
PMCID: PMC4066022
NIHMSID: NIHMS579493

Timing of Delivery and Adverse Outcomes in Term Singleton Repeat Cesarean Deliveries

Giuseppe CHIOSSI, M.D., Yinglei LAI, Ph.D., Mark B. LANDON, M.D., Catherine Y. SPONG, M.D., Dwight J. ROUSE, M.D., Michael W. VARNER, M.D., Steve N. CARITIS, M.D., Yoram SOROKIN, M.D., Mary J. O’SULLIVAN, M.D., Baha M. SIBAI, M.D., John M. THORP, M.D., Susan M. RAMIN, M.D., and Brian M. MERCER, M.D., for the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Maternal-Fetal Medicine Units (MFMU) Network*

Abstract

Objective

To compare the maternal and neonatal risks of elective repeat cesarean delivery compared with pregnancy continuation at different gestational ages, starting from 37 weeks.

Methods

We analyzed the composite maternal and neonatal outcomes of repeat cesarean deliveries studied prospectively over 4 years at 19 U.S. centers. Maternal outcome was a composite of pulmonary edema, cesarean hysterectomy, pelvic abscess, thromboembolism, pneumonia, transfusion, or death. Composite neonatal outcome consisted of respiratory distress, transient tachypnea, necrotizing enterocolitis, sepsis, ventilation, seizure, hypoxic-ischemic encephalopathy, neonatal intensive care unit admission, 5 min Apgar of 3 or lower, or death. Outcomes after elective repeat cesarean delivery without labor at each specific gestational age were compared with outcomes for all who were delivered later due to labor onset, specific obstetric indications, or both.

Results

Twenty three thousand seven hundred ninety-four repeat cesareans were included. Elective delivery at 37 weeks had significantly higher risks of adverse maternal outcome (OR: 1.56, 95% CI 1.06–2.31); while elective delivery at 39 weeks was associated with better maternal outcome when compared with pregnancy continuation (OR: 0.51, 95% CI 0.36–0.72). Elective repeat cesareans at 37 and 38 weeks had significantly higher risks of adverse neonatal outcome (37 weeks OR: 2.02, 95% CI 1.73–2.36; 38 weeks OR: 1.39 95% CI 1.24–1.56); while delivery at 39 and 40 weeks presented better neonatal outcome as opposed to pregnancy continuation (39 weeks OR: 0.79, 95% CI 0.68–0.92; 40 weeks OR: 0.57 95% CI 0.43–0.75).

Conclusion

In women with prior cesarean delivery, 39 weeks of gestation is the optimal time for repeat cesarean delivery for both mother and baby.

INTRODUCTION

The risks and benefits of delivery at a specific gestational age need to be compared with the potential consequences of pregnancy continuation beyond that time point to determine the optimal timing for elective delivery. Elective delivery before 39 weeks is discouraged unless fetal lung maturity has been confirmed, as neonatal morbidity decreases with gestational age from 37 to 39 weeks (13). Some, however, argue that early deliveries may also have benefits such as avoidance of stillbirth or fetal compromise due to utero-placental insufficiency, removal of the fetus from a hostile uterine environment, and resolution of an underlying condition (eg, preeclampsia or gestational diabetes) before it worsens or secondary complications develop (46). In the event of a prior cesarean section, maternal risks of early delivery include complications related to a suboptimal development of the lower uterine segment and its relation with adhesions from prior surgery, accounting for increased intraoperative blood loss, and prolonged hospital stay (4). Early deliveries can also be beneficial as they can avert emergent unscheduled cesareans performed under suboptimal circumstances. Postponing repeat cesarean delivery until 39 weeks increases the chance that it will be performed unscheduled and after the onset of labor, as up to 25% of pregnant women experience uterine contractions associated with cervical changes between 38 and 39 weeks (5, 7). Moreover, repeat cesarean sections performed after the onset of labor carry higher risks of complications such as uterine rupture, infection and maternal mortality than elective procedures, performed in the absence of specific obstetric indications. This is particularly relevant when spontaneous labor occurs in women with placenta previa, accreta, prior classical cesarean delivery or myomectomy (811).

Prior studies have investigated the perinatal risks of elective delivery at 37–41 weeks and concluded that there is a higher risk of neonatal morbidity for deliveries before compared with delivery at 39 weeks (1, 3, 9). While these studies provide useful information, using women delivered at 39 weeks as the comparison group does not take into account the entire spectrum of adverse outcomes that could derive from delivery at later gestational ages. In order to be more relevant to clinical decision-making, the risk of delivery at a specific gestational age needs to be compared to the risk of delivering at a later time. Therefore, the objective of this study was to compare the risks of elective repeat cesarean delivery at each gestational age starting at 37 weeks, with the cumulative maternal and neonatal risks of pregnancy continuation beyond that time point.

MATERIALS AND METHODS

This is a secondary analysis of the Cesarean Section Registry of the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Maternal-Fetal Medicine Units (MFMU) Network. The study was approved by the human subjects committees at each participating center. The registry contains detailed, prospectively collected information on consecutive repeat cesareans performed at 19 United States academic centers from 1999 to 2002. Women with a singleton gestation at term and prior cesarean delivery were studied. The details of the study have been published elsewhere (12). For this analysis, data from four groups were included as previously reported by Spong et al (13): women delivering by elective (nonindicated) repeat cesarean delivery without labor, women delivering by elective (non indicated) repeat cesarean delivery performed after the onset of labor, women delivering by indicated repeat cesarean delivery without labor, and women delivering by indicated repeat cesarean delivery with labor (Figure 1).

Figure 1
Patients included in this secondary analysis of the Maternal-Fetal Medicine Units (MFMU) cesarean registry.

The primary outcomes analyzed were composites. Composite maternal outcome included any of the following: death, pulmonary edema, cesarean hysterectomy, pelvic or abdominal abscess, confirmed DVT or pulmonary embolism, pneumonia, or blood transfusion. Composite neonatal outcome consisted of any of the following: death, respiratory distress, transient tachypnea of the newborn, necrotizing enterocolitis, sepsis, mechanical ventilation, seizure, hypoxic-ischemic encephalopathy, NICU admission, or 5 min Apgar score of 3 or lower. The definitions of the specific components constituting the composite maternal and neonatal outcomes have been previously reported (3, 12, 14). In accordance with the Maternal-Fetal Medicine Units Network procedures, the data collected underwent routine edits and audits.

The timing of delivery was determined in completed weeks of gestation such that 37 weeks (for example) included deliveries at 37 0/7–37 6/7 weeks. Gestational age was based on the best obstetric estimate (last menstrual period compared to ultrasound) determined by providers and used for clinical decision-making (12).

The incidence of adverse maternal and neonatal outcomes was calculated for each completed week of gestation at the time of cesarean delivery. Odds ratios (ORs) were used to compare the composite maternal and neonatal outcomes after elective cesareans without labor at a specific gestational age with the outcomes of all who were delivered later due to labor onset, specific obstetric indications, or both. Logistic regression models were used to adjust for potential confounders including race/ethnicity, number of prior cesarean sections, marital status, payer, smoking, medical history, maternal age and BMI. Categorical variables were analyzed using the chi-square test or Fisher exact test. Continuous variables were analyzed using the Wilcoxon rank sum test. A two-sided p < 0.05 was considered statistically significant. Data were analyzed using SAS (SAS Institute Inc, Cary, NC).

RESULTS

Out of 378,063 women enrolled in the NICHD MFMU Network Cesarean Registry, 23,794 underwent repeat cesarean delivery at or after 37 0/7 weeks’ gestation. Among these, 14,993 were delivered by cesarean section before labor and in the absence of any medical or obstetric indications (Figure 1). Elective deliveries were defined according to Spong et al (13) (Figure 1). The detailed distribution of the stringent exclusion criteria applied to select prelabor elective cesarean delivery has been previously reported (3). Within the study population, 12.1% (n = 2866) were delivered at 37 completed weeks’ gestation, 30.6% (n = 7280) at 38 weeks, 41.7% (n = 9921) at 39 weeks, 11.0% (n = 2611) at 40 weeks, 3.8% (n = 901) at 41 weeks, and 0.9% (n = 215) at 42 weeks or later. The maternal characteristics of the study population are displayed in Table 1. Women delivered at specific gestational ages, when compared to those who were delivered at a later time, were more frequently affected by medical disorders, had undergone more than 1 previous cesarean delivery (37–40 weeks), were more likely Caucasian, married, and insured. The data on individual and composite adverse outcomes for both mothers and neonates are presented in Table 2. The incidence of blood transfusion was significantly higher among women delivered at 37 weeks as opposed to the ones expectantly managed (p = 0.016), the opposite trend was noticed with 39 week deliveries (p < 0.001). Similarly, pneumonia was more frequent with elective deliveries at 37 weeks (p = 0.042), while cesarean hysterectomy was more commonly encountered in those who were still pregnant after 39 weeks (p = 0.035). The rate of the composite maternal outcome was significantly higher among women electively delivered at 37 weeks when compared to women expectantly managed (p = 0.03), but it was significantly lower among 39 week deliveries as compared to later deliveries (p < 0.001). Respiratory distress syndrome (RDS), transient tachypnea of the newborn, sepsis, mechanical ventilation, and NICU admissions were significantly more prevalent within the groups electively delivered at 37 and 38 weeks, and among pregnancies expectantly managed after 40 weeks (except mechanical ventilation). Significantly more neonatal deaths were recorded when pregnancies were expectantly managed after 40 weeks as compared to the ones electively delivered at 39 weeks (p = 0.031).

Table 1
Demographics of the Patients Delivered at Successive Gestational Ages Compared With Those Who Were Delivered Later
Table 2
Composite and Individual Maternal and Neonatal Outcomes

Figure 2 and and33 respectively summarize the rate of composite maternal and neonatal outcomes in women electively delivered at successive gestational ages as compared to those expectantly managed. Both maternal and neonatal adverse outcomes are decreased in those electively delivered after 39 weeks, and increased in those expectantly managed after 39 weeks. Table 3 provides the crude and adjusted odds ratios for composite maternal and neonatal outcomes of elective cesarean delivery versus expectant management at various gestational ages. Elective delivery at 37 weeks’ gestation had a significantly higher risk of adverse maternal outcomes as compared to later deliveries (OR: 1.56, 95% CI 1.06 – 2.31); while, 39 week deliveries were associated with better maternal outcomes when compared to pregnancy continuation (OR: 0.51, 95% CI 0.36 – 0.72). Elective repeat cesarean deliveries at 37 and 38 weeks’ gestation had a significantly higher risk of adverse neonatal outcomes as compared to expectant management (37 weeks OR: 2.02, 95% CI 1.73 – 2.36; 38 weeks OR: 1.39, 95% CI 1.24 – 1.56); in contrast, 39 and 40 week deliveries were associated with better neonatal outcomes when compared to pregnancy continuation (39 weeks OR: 0.79, 95% CI 0.68 – 0.92; 40 weeks OR: 0.57, 95% CI 0.43 – 0.75). These associations remained after adjusting for confounders.

Figure 2
Composite maternal outcome for delivery compared with expectant management. Rate is expressed as percentage of women with adverse outcomes.
Figure 3
Composite neonatal outcome for delivery compared with expectant management. Rate is expressed as percentage of neonates with adverse outcomes.
Table 3
Crude and Adjusted Odds Ratios for Elective Cesarean Delivery Compared With Expectant Management at the Designated Week

This secondary analysis was not designed to evaluate the risks of stillbirths, as these were very rare events in the cohort (only 6 IUFDs were detected in pregnancies ≥ 37 weeks’ gestation, and these were excluded from the registry). Undoubtedly, some stillbirths could be prevented if repeat cesareans were performed at 37 or 38 weeks rather than waiting until 39 weeks. However, these are rare and earlier delivery would result in much higher risks of adverse maternal and neonatal outcomes imposed on many pregnancies to prevent a disproportionally low number of deaths in utero. Moreover, assuming an IUFD incidence of 0.5% at 37–40 wks and 0.1% at 41–42 wks (15, 16) more than 800,000 subjects would be needed to detect with adequate confidence and precision a decrease in stillbirth rate from 0.1% to 0.05% anticipating elective deliveries from 41 to 37 wks.

DISCUSSION

We found that in women with previous cesarean section, delivery during the 39th week of gestation is the optimal timing for elective delivery with the lowest risk of both maternal and neonatal complications, even after taking into consideration the risks associated with pregnancy continuation.

Concern that delivery at 39 weeks may be associated with adverse maternal outcomes, particularly among women with a prior cesarean delivery, has been suggested as one reason to recommend earlier delivery (17). However, we found that maternal outcomes tended to be better with continued pregnancy rather than elective cesarean at 37 or 38 weeks. Our findings are consistent with the work of Tita el al that showed a higher incidence of blood transfusion and maternal hospitalization > 5 days among elective repeat cesarean delivery at 37–38 gestational weeks as compared to 39 weeks (14). The authors speculated that the development of the lower uterine segment and its relation to adhesions due to prior surgery might not be optimal for avoiding blood loss before 39 weeks (14). Compared with spontaneous vaginal deliveries, cesarean deliveries are associated with increased maternal morbidity (18), but when carried out electively the risks of maternal complications are lower than the when performed in labor or emergently (10, 11). In fact, unscheduled cesareans performed during labor or due to maternal or fetal deterioration are associated with higher risks of uterine rupture, infection, DVT and maternal mortality than elective procedures; moreover, they also have higher anesthesia related complications such as failed intubation and pulmonary aspiration (811). In our analysis, we demonstrated decreased maternal complications with deliveries electively performed at 39 weeks; such findings can be related to the lower rates of cesarean sections performed in labor, as many women go into labor after 39 weeks (9).

Given that the majority of women with a previous cesarean delivery elect a repeat cesarean (19), that more than 25% of primary cesarean sections are scheduled (20), and that cesarean sections on maternal request are on the rise (21), the timing of cesarean delivery and its effect on infant outcomes have substantial public health importance. Our findings are consistent with the results of other cohort studies conducted in both the United States and Europe demonstrating increased neonatal morbidity and mortality with elective cesarean delivery before 39 gestational weeks (1, 3, 9, 22). Similarly, we confirmed that elective deliveries at 39 and 40 weeks are associated with fewer adverse neonatal outcomes than is pregnancy continuation (3).

The sudden death of a fetus in utero has tragic implications, especially when the alternative could have been a healthy neonate had delivery occurred earlier. The risk of unexplained stillbirth has been reported to increase after 37 weeks’ gestation (23, 24). Earlier delivery may also prevent pregnancy complications from uncontrolled gestational diabetes, gestational hypertension, preeclampsia and eclampsia that increase proportionally with gestational age (4, 25, 26). However, despite the large sample size, this secondary analysis was not designed to evaluate the risks of stillbirths.

The strengths of our analysis include the large sample size, the large number of sites and clinical practices represented, the prospective and rigorous collection of data, and our ability to adjust for multiple potential confounders. In addition, the use of a hazard approach to evaluate the risks involved in the decision to deliver versus not to deliver at various gestational ages is a more accurate representation of the actual implications of such decision. Previous studies have compared maternal and neonatal outcomes at different gestational ages, but did not account for the potential consequences of pregnancy continuation. Instead, the hazard approach allowed us to compare the outcomes after elective repeat cesareans at a specific gestational age with the outcomes of all who were delivered later. Our study also had some weaknesses. We did not have information about testing for lung maturity. Moreover, we were unable to determinate all the nuances surrounding elective cesarean sections, including delivery indications such as maternal fatigue or anxiety.

By accounting for the risk associated with continuing pregnancy beyond specific gestational ages, our analysis confirmed that 39 weeks is the optimal timing for elective delivery for both mother and baby. These findings further support enforcement of a policy that recommends repeat cesareans after 39 completed weeks in the absence of specific maternal or fetal indications for earlier delivery.

Supplementary Material

Supplemental Digital Content

Acknowledgments

The project described was supported by grants from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) of the National Institutes of Health (NIH) [HD21410, HD21414, HD27860, HD27861, HD27869, HD27905, HD27915, HD27917, HD34116, HD34122, HD34136, HD34208, HD34210, HD40500, HD40485, HD40544, HD40545, HD40560, HD40512, and HD36801] and its contents are solely the responsibility of the authors and do not necessarily represent the official view of NICHD or the NIH.

The authors thank Francee Johnson, R.N., B.S.N. for protocol development and coordination between clinical research centers; Elizabeth Thom, Ph.D, for protocol and data management and statistical analysis; and John C. Hauth, M.D. for protocol development and oversight.

Footnotes

Financial Disclosure

The authors did not report any potential conflicts of interest.

Dr. Spong, Associate Editor of Obstetrics & Gynecology, was not involved in the review or decision to publish this article.

Presented in part at the 31th Annual Meeting of the Society for Maternal-Fetal Medicine, Feb 6–11, 2012, Dallas, TX.

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