Obstetrics & Gynecology:
Timing of Delivery and Adverse Outcomes in Term Singleton Repeat Cesarean Deliveries
Chiossi, Giuseppe MD; Lai, Yinglei PhD; Landon, Mark B. MD; Spong, Catherine Y. MD; Rouse, Dwight J. MD; Varner, Michael W. MD; Caritis, Steve N. MD; Sorokin, Yoram MD; O'Sullivan, Mary J. MD; Sibai, Baha M. MD; Thorp, John M. MD; Ramin, Susan M. MD; Mercer, Brian M. MD; for the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Maternal-Fetal Medicine Units (MFMU) Network
Departments of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas, The Ohio State University, Columbus, Ohio, University of Alabama at Birmingham, Birmingham, Alabama, University of Utah, Salt Lake City, Utah, University of Pittsburgh, Pittsburgh, Pennsylvania, Wayne State University, Detroit, Michigan, University of Miami, Miami, Florida, University of Tennessee, Memphis, Tennessee, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, The University of Texas Health Science Center at Houston, Houston, Texas, and Case Western Reserve University–MetroHealth Medical Center, Cleveland, Ohio; The George Washington University Biostatistics Center, Washington, DC; and the Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland.
Corresponding author: Giuseppe Chiossi, MD, Department of Obstetrics and Gynecology, Division of Maternal and Fetal Medicine, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-0587; e-mail: Ossidi74seppie@yahoo.it.
* For a list of other members of the NICHD MFMU, see the Appendix online at http://links.lww.com/AOG/A346.
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 the NICHD or the NIH.
The authors thank Francee Johnson, RN, BSN, for protocol development and coordination between clinical research centers; Elizabeth Thom, PhD, for protocol and data management and statistical analysis; and John C. Hauth, MD, for protocol development and oversight.
Presented in part at the 31st Annual Meeting of the Society for Maternal-Fetal Medicine, February 6–11, 2012, Dallas, Texas.
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.
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-minute 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 as a result of labor onset, specific obstetric indications, or both.
RESULTS: Twenty-three thousand seven hundred ninety-four repeat cesarean deliveries were included. Elective delivery at 37 weeks of gestation had significantly higher risks of adverse maternal outcome (odds ratio [OR] 1.56, 95% confidence interval [CI] 1.06–2.31), whereas elective delivery at 39 weeks of gestation was associated with better maternal outcome when compared with pregnancy continuation (OR 0.51, 95% CI 0.36–0.72). Elective repeat cesarean deliveries at 37 and 38 weeks of gestation 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), whereas delivery at 39 and 40 weeks of gestation 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 neonate.
LEVEL OF EVIDENCE: II
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 of gestation is discouraged unless fetal lung maturity has been confirmed, because neonatal morbidity decreases with gestational age from 37 to 39 weeks.1–3 Some, however, argue that early deliveries may also have benefits such as avoidance of stillbirth or fetal compromise resulting from uteroplacental 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.4–6 In the event of a prior cesarean delivery, 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 because they can avert emergent unscheduled cesarean deliveries performed under suboptimal circumstances. Postponing repeat cesarean delivery until 39 weeks of gestation increases the chance that it will be performed unscheduled and after the onset of labor, because up to 25% of pregnant women experience uterine contractions associated with cervical changes between 38 and 39 weeks of gestation.5,7 Moreover, repeat cesarean deliveries 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.8–11
Prior studies have investigated the perinatal risks of elective delivery at 37–41 weeks of gestation and concluded that there is a higher risk of neonatal morbidity for deliveries before compared with delivery at 39 weeks of gestation.1,3,9 Although these studies provide useful information, using women delivered at 39 weeks of gestation as the comparison group does not take into account the entire spectrum of adverse outcomes that could derive from delivery at later gestational ages. To be more relevant to clinical decision-making, the risk of delivery at a specific gestational age needs to be compared with 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 Maternal-Fetal Medicine Units Network. The study was approved by the human subjects committees at each participating center. The registry contains detailed, prospectively collected information on consecutive repeat cesarean deliveries performed at 19 U.S. 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 al13: women delivering by elective (nonindicated) repeat cesarean delivery without labor, women delivering by elective (nonindicated) 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 (Fig. 1).
Patients included in...Image Tools
The primary outcomes analyzed were composites. Composite maternal outcome included any of the following: death, pulmonary edema, cesarean hysterectomy, pelvic or abdominal abscess, confirmed deep vein thrombosis 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, neonatal intensive care unit admission, or 5-minute 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 of gestation. Gestational age was based on the best obstetric estimate (last menstrual period compared with ultrasonography) determined by health care 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 cesarean deliveries without labor at a specific gestational age with the outcomes of all who were delivered later as a result of labor onset, specific obstetric indications, or both. Logistic regression models were used to adjust for potential confounders including race and ethnicity, number of prior cesarean deliveries, marital status, payer, smoking, medical history, maternal age, and body mass index (calculated as weight (kg)/[height (m)]2). Categorical variables were analyzed using the χ2 test or Fisher’s exact test. Continuous variables were analyzed using the Wilcoxon rank-sum test. A two-sided P<.05 was considered statistically significant. Data were analyzed using SAS.
Of 378,063 women enrolled in the Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network Cesarean Registry, 23,794 underwent repeat cesarean delivery at or after 37 0/7 weeks of gestation. Among these, 14,993 were delivered by cesarean before labor and in the absence of any medical or obstetric indications (Fig. 1). Elective deliveries were defined according to Spong et al13 (Fig. 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=2,866) were delivered at 37 completed weeks of gestation, 30.6% (n=7,280) at 38 weeks, 41.7% (n=9,921) at 39 weeks, 11.0% (n=2,611) 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 with those who were delivered at a later time, were more frequently affected by medical disorders, had undergone more than one previous cesarean delivery (37–40 weeks of gestation), and 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 of gestation as opposed to the ones expectantly managed (P=.016); the opposite trend was noticed with 39-week deliveries (P<.001). Similarly, pneumonia was more frequent with elective deliveries at 37 weeks of gestation (P=.042), whereas cesarean hysterectomy was more commonly encountered in those who were still pregnant after 39 weeks of gestation (P=.035). The rate of the composite maternal outcome was significantly higher among women electively delivered at 37 weeks of gestation when compared with women expectantly managed (P=.03), but it was significantly lower among 39-week deliveries as compared with later deliveries (P<.001). Respiratory distress syndrome, transient tachypnea of the newborn, sepsis, mechanical ventilation, and neonatal intensive care unit admissions were significantly more prevalent within the groups electively delivered at 37 and 38 weeks of gestation and among pregnancies expectantly managed after 40 weeks of gestation (except mechanical ventilation). Significantly more neonatal deaths were recorded when pregnancies were expectantly managed after 40 weeks of gestation as compared with the ones electively delivered at 39 weeks of gestation (P=.031).
Figures 2 and 3, respectively, summarize the rate of composite maternal and neonatal outcomes in women electively delivered at successive gestational ages as compared with those expectantly managed. Both maternal and neonatal adverse outcomes are decreased in those electively delivered after 39 weeks of gestation and increased in those expectantly managed after 39 weeks of gestation. Table 3 provides the crude and adjusted ORs for composite maternal and neonatal outcomes of elective cesarean delivery compared with expectant management at various gestational ages. Elective delivery at 37 weeks of gestation had a significantly higher risk of adverse maternal outcomes as compared with later deliveries (OR 1.56, 95% confidence interval [CI] 1.06–2.31), whereas 39-week deliveries were associated with better maternal outcomes when compared with pregnancy continuation (OR 0.51, 95% CI 0.36–0.72). Elective repeat cesarean deliveries at 37 and 38 weeks of gestation had a significantly higher risk of adverse neonatal outcomes as compared with 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 with 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.
This secondary analysis was not designed to evaluate the risks of stillbirths, because these were very rare events in the cohort (only six intrauterine fetal deaths were detected in pregnancies 37 weeks of gestation or greater and these were excluded from the registry). Undoubtedly, some stillbirths could be prevented if repeat cesarean deliveries were performed at 37 or 38 weeks of gestation rather than waiting until 39 weeks of gestation. 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 intrauterine fetal death incidence of 0.5% at 37–40 weeks of gestation and 0.1% at 41–42 weeks of gestation,15,16 more than 800,000 participants 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 weeks of gestation.
We found that in women with previous cesarean delivery, 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 of gestation 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 delivery at 37 or 38 weeks of gestation. Our findings are consistent with the work of Tita et al that showed a higher incidence of blood transfusion and maternal hospitalization greater than 5 days among elective repeat cesarean delivery at 37–38 weeks of gestation as compared with 39 weeks of gestation.14 The authors speculated that the development of the lower uterine segment and its relation to adhesions resulting from prior surgery might not be optimal for avoiding blood loss before 39 weeks of gestation.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 when performed in labor or emergently.10,11 In fact, unscheduled cesarean deliveries performed during labor or resulting from maternal or fetal deterioration are associated with higher risks of uterine rupture, infection, deep vein thrombosis, and maternal mortality than elective procedures; moreover, they also have higher anesthesia-related complications such as failed intubation and pulmonary aspiration.8–11 In our analysis, we demonstrated decreased maternal complications with deliveries electively performed at 39 weeks of gestation; such findings can be related to the lower rates of cesarean deliveries performed in labor, because many women go into labor after 39 weeks of gestation.9
Given that the majority of women with a previous cesarean delivery elect a repeat cesarean delivery,19 that more than 25% of primary cesarean deliveries are scheduled,20 and that cesarean deliveries on maternal request are on the rise,21 the timing of cesarean delivery and its effect on neonate outcomes has 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 weeks of gestation.1,3,9,22 Similarly, we confirmed that elective deliveries at 39 and 40 weeks of gestation 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 of 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.4,16,25 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 compared with 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 cesarean deliveries 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 deliveries, 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 of gestation is the optimal timing for elective delivery for both mother and neonate. These findings further support enforcement of a policy that recommends repeat cesarean deliveries after 39 completed weeks of gestation in the absence of specific maternal or fetal indications for earlier delivery.
1. Zanardo V, Simbi AK, Franzoi M, Soldà G, Salvadori A, Trevisanuto D. Neonatal respiratory morbidity risk and mode of delivery at term: influence of timing of elective caesarean delivery. Acta Paediatr 2004;93:643–7.
2. Cesarean delivery on maternal request. ACOG Committee Opinion No. 394. American College of Obstetricians and Gynecologists. Obstet Gynecol 2007;110:1501.
3. Tita AT, Landon MB, Spong CY, Lai Y, Leveno KJ, Varner MW, et al.. Timing of elective repeat cesarean delivery at term and neonatal outcomes. N Engl J Med 2009;360:111–20.
4. Spong CY, Mercer BM, D'alton M, Kilpatrick S, Blackwell S, Saade G. Timing of indicated late-preterm and early-term birth. Obstet Gynecol 2011;118:323–33.
5. Salim R, Shalev E. Health implications resulting from the timing of elective cesarean delivery. Reprod Biol Endocrinol 2010;8:68.
6. Helgadottir LB, Skjeldestad FE, Jacobsen AF, Sandset PM, Jacobsen EM. Incidence and risk factors of fetal death in Norway: a case-control study. Acta Obstet Gynecol Scand 2011;90:390–7.
7. Thomas J, Paranjothy S; Royal College of Obstetricians and Gynaecologists. Clinical effectiveness support unit. In: The National Sentinel Caesarean section audit report. London (UK): RCOG Press; 2001.
8. Department of Health, Scottish Executive Health Department, and Department of Health, Social Services and public Safety, Northern Ireland. Why mothers die. Fifth report on confidential enquiries into maternal deaths in the United Kingdom, 1997–1999. London (UK): RCOG Press; 2001.
9. Hansen AK, Wisborg K, Uldbjerg N, Henriksen TB. Risk of respiratory morbidity in term infants delivered by elective cesarean section: cohort study. BMJ 2008;336:85–7.
10. Rossi AC, D'Addario V. Maternal morbidity following a trial of labor after cesarean section vs elective repeat cesarean delivery: a systematic review with metaanalysis. Am J Obstet Gynecol 2008;199:224–31.
11. Allen VM, O'Connell CM, Baskett TF. Maternal morbidity associated with cesarean delivery without labor compared with induction of labor at term. Obstet Gynecol 2006;108:286–94.
12. Landon MB, Hauth JC, Leveno KJ, Spong CY, Leindecker S, Varner MW, et al.; National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Maternal and perinatal outcomes associated with a trial of labor after prior cesarean delivery. N Engl J Med 2004;351:2581–9.
13. Spong CY, Landom MB, Gilbert S, Rouse DJ, Leveno KJ, Varner MW, et al.. Risk of uterine rupture and adverse perinatal outcome at term after cesarean delivery. Obstet Gynecol 2007;110: 801–7.
14. Tita AT, Lai Y, Landon MB, Spong CY, Leveno KJ, Varner MW, et al.. Timing of elective repeat cesarean delivery at term and maternal perioperative outcomes. Obstet Gynecol 2011;117:280–6.
15. de la Vega A, Verdiales M. Failure of intensive fetal monitoring and ultrasound in reducing the stillbirth rate. P R Health Sci J 2002;21:123–5.
16. Caughey AB, Stotland NE, Escobar GJ. What is the best measure of maternal complications of term pregnancy: ongoing pregnancies or pregnancies delivered? Am J Obstet Gynecol 2003;189:1047–52.
17. Salim R, Zafran N, Shalev E, Tita AT, Landon MB, Spong CY. Timing of elective repeat cesarean delivery at term [Letter]. N Engl J Med 2009;360:1570.
18. Burrows LJ, Meyn LA, Weber AM. Maternal morbidity associated with vaginal versus cesarean delivery. Obstet Gynecol 2004;103:907–12.
19. Menacker F. Trends in cesarean rates for first births and repeat cesarean rates for low-risk women: United States, 1990–2003. Natl Vital Stat Rep 2005;54:1–8.
20. Meikle SF, Steiner CA, Zhang J, Lawrence WL. A national estimate of the elective primary cesarean delivery rate. Obstet Gynecol 2005;105:751–6.
21. National Institutes of Health state-of-the-science conference statement: cesarean delivery on maternal request March 27–29, 2006. Obstet Gynecol 2006;107:1386–97.
22. De Luca R, Boulvain M, Irion O, Berner M, Pfister RE. Incidence of early neonatal mortality and morbidity after late-preterm and term cesarean delivery. Pediatrics 2009;123:e1064–71.
23. Smith GC, Pell JP, Dobbie R. Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet 2003;362:1779–84.
24. Wood SL, Chen S, Ross S, Sauve R. The risk of unexplained antepartum stillbirth in second pregnancies following caesarean section in the first pregnancy. BJOG 2008;115:726–31.
25. Koopmans CM, Bijlenga D, Groen H, Vijgen SM, Aarnoudse JG, Bekedam DJ, et al.. Induction of labour versus expectant monitoring for gestational hypertension or mild pre-eclampsia after 36 weeks' gestation (HYPITAT): a multicentre, open-label randomised controlled trial. Lancet 2009;374:979–88.
Figure. No available...Image Tools
Supplemental Digital Content
© 2013 The American College of Obstetricians and Gynecologists
ACOG MEMBER SUBSCRIPTION ACCESS
If you are an ACOG Fellow and have not logged in or registered to Obstetrics & Gynecology, please follow these step-by-step instructions to access journal content with your member subscription.