The cesarean delivery rate is significantly higher in preterm deliveries than in term deliveries.1 Undoubtedly many preterm cesarean deliveries are performed for necessary indications such as abruption or nonreassuring fetal status. However, it is uncertain how the route of delivery affects the outcome of the preterm neonate. Given the increased maternal morbidity and cost associated with preterm cesarean deliveries, it is vital that cesarean deliveries be reserved for instances in which they have clear benefit for the neonate or mother.
Previous studies have demonstrated mixed results. Deulofeut et al2 evaluated the smallest neonates born before 34 weeks of gestation and suggested a reduction in mortality and intraventricular hemorrhage with vaginal delivery. Additionally, Lee at al3 showed a decrease in mortality with vaginal delivery in appropriately grown preterm neonates. Other studies have found no significant difference between cesarean and vaginal deliveries with regard to neonatal outcomes in appropriately grown premature neonates.4–6 Even in small-for-gestational-age neonates, a prior study by the authors of this article found no difference in neonatal outcomes between cesarean and vaginal deliveries except with regard to neonatal respiratory distress, which was moderately decreased with vaginal delivery.7 This decrease has been hypothesized to result from active labor expelling excess fluid from the fetal lungs.
We sought to examine the association between route of delivery and neonatal outcomes in a large, diverse cohort of preterm, appropriate-for-gestational-age neonates. We were particularly interested in examining the outcomes based on indication for delivery (maternal medical condition or obstetric complication) and gestational age (at or before 34 weeks of gestation and at or before 31 weeks of gestation).
MATERIALS AND METHODS
Data on live births between 1995 and 2003 from the New York City Department of Health and Mental Hygiene were linked to the hospital discharge data from the Statewide Planning and Research Cooperative System. Our study population was limited to deliveries in which birth certificates could be successfully linked to hospital discharge records using a matching algorithm used in multiple other studies (n=1,025,903).7–9 Our study population included women delivering cephalic-presenting, singleton neonates between 24 and 34 completed weeks of gestation (n=25,615). Neonates with congenital anomalies, those with growth restriction or a neonatal weight less 500 g, those who were large for gestational age, and those with missing information on neonatal weight were excluded. Growth restriction was defined as a birth weight less than the 10th percentile based on gestational age, gender-specific U.S. standard birth weights, and large for gestational age was defined as a birth weight greater than the 90th percentile based on the same norms.10–12 Neonates delivered by vacuum or forceps were also excluded from this analysis given the possibility that operative deliveries may independently increase morbidity or mortality for the preterm neonate. Mode of delivery was determined both by birth certificate information and procedural codes in the Statewide Planning and Research Cooperative System database. Based on these inclusion and exclusion criteria, the study population in this analysis was 20,231 (see Fig. 1).
Several additional subanalyses were performed within this cohort. To investigate the effect that delivery indication could have on mode of delivery and outcome, we subdivided the cohort based on 1) deliveries for maternal medical indications (n=5,828); 2) deliveries for obstetric complications (n=9,318); and 3) deliveries with no medical or obstetric complications (n=7,511). The complete list of conditions composing each category is contained in Box 1 and is similar to the indications used in other studies.13 The maternal medical conditions and obstetric complications were not mutually exclusive; therefore, a given birth could be represented in both of these categories (n=2,426). Additionally, to investigate the effect that early gestational age could have on mode of delivery and outcome, we performed a subgroup analysis in which we limited the study population to those with a gestational age less than or equal to 31 weeks of gestation (n=5,997).
Box 1 Indication Categories Cited Here...
Category A: Maternal Medical Conditions (n=5,828)*
* Cardiac disease
* Acute or chronic lung disease
* Chronic hypertension
* Pregnancy-associated hypertension
* Seizures during labor
* Renal disease
Category B: Obstetric Complications (n=9,318)*
* Anhydramnios or oligohydramnios
* Incompetent cervix
* Rh sensitization
* Uterine bleeding
* Premature rupture of membranes (more than 12 h)
* Abruptio placenta
* Placenta previa
* Other excessive bleeding
* Cord prolapse
* Nonreassuring fetal status
Category C: Other (n=7,511)
* Preterm labor
* Premature rupture of membranes (12 h or less)
* Categories A and B are not mutually exclusive. Some deliveries had both obstetric and maternal complications.
The outcomes of interest in this study included neonatal death before discharge, neonatal respiratory distress, sepsis, intraventricular hemorrhage, seizure, subdural hemorrhage, or 5-minute Apgar score less than 7. Neonatal death was determined by discharge data included in the Statewide Planning and Research Cooperative System data set. Neonatal morbidities including respiratory distress, sepsis, intraventricular hemorrhage, seizure, and subdural hemorrhage were ascertained using International Classification of Diseases, 9th Revision, Clinical Modification codes from the neonate’s hospitalization record. Unfortunately, more detailed information on these diagnoses such as the grade of intraventricular hemorrhage or how respiratory distress was diagnosed (clinically or radiographically) was not available. Neonatal seizure was defined by the presence of this complication in either the Statewide Planning and Research Cooperative System or the birth certificate data because seizure is also identified on the birth certificate. Five-minute Apgar scores were obtained from birth certificate data.
Maternal characteristics were examined as covariates and potential confounders based on previous literature. Maternal information derived from birth certificates included age, parity, race or ethnicity, level of education, insurance status, prepregnancy weight, and tobacco use. Prepregnancy weight was used as a surrogate for body mass index because the mother's height was not available.9,14 We used categorical variables for maternal age based on the fields defined in New York State birth certificates (aged younger than 20 years, aged 20–34 years, and aged 35 years or older). These categories were used because advanced maternal age (aged 35 years and older) and teenage pregnancy (aged less than 20 years) are associated with increased risk for some complications.
Pregnancy and medical complications used as covariates include diabetes, hypertension, and gestational age of delivery based on the clinical estimate reported on the birth certificate. We adjusted for gestational age using the clinical estimate in weeks reported on the birth certificate. This represents the delivering physician's best estimate of gestation. Pregnancies complicated by diabetes and gestational diabetes were determined by a previously described algorithm that used information from both the hospital discharge and birth data.15 We combined diabetes and gestational diabetes because both are associated with fetal weight abnormalities and neonatal morbidity.16 Presence of maternal hypertension included preeclampsia, hypertension with onset during pregnancy, and pre-existing hypertension because all can be associated with impaired fetal growth.17–19
We estimated univariable associations between delivery mode and neonatal outcomes using the χ2 statistic. Logistic regression was used to determine the odds of each neonatal morbidity and neonatal mortality for cesarean delivery compared with vaginal delivery adjusting for potential confounders as described previously. Covariates were considered for inclusion in the multivariable model if the univariable χ2 P values were <.01.
All potential confounders were found to be significant based on this criterion and thus included. Analyses were conducted using the SAS System 9.2. This study was approved by the Yale University human investigations committee.
Of the 20,321 neonates meeting the study criteria, 14,023 (69.3%) were delivered vaginally and 6,208 (30.7%) were delivered by cesarean. Baseline characteristics for those delivered vaginally and by cesarean are presented in Table 1. Given the large study population, all maternal and pregnancy characteristics differed significantly between comparison groups (P<.01). Women who underwent cesarean delivery were older, heavier, more educated, and more likely to have private insurance. They also were more likely to have diabetes and much more likely to have hypertensive disorders. Interestingly, women who had cesarean deliveries were also more likely to be parous compared with those who had vaginal deliveries.
Table 2 presents the proportions and unadjusted and adjusted odds of neonatal complications including in-hospital neonatal mortality with cesarean delivery compared with vaginal delivery. Neonates born by cesarean delivery had a higher risk of respiratory distress syndrome, 5-minute Apgar score less than 7, sepsis, seizure, and death compared with those delivered vaginally. After adjusting for maternal age, race, parity, education, insurance status, prepregnancy weight, diabetes, hypertension, smoking, and gestational age at delivery, cesarean delivery continued to be associated with increased odds of respiratory distress syndrome, 5-minute Apgar score less than 7, and death compared with vaginal delivery. To prevent one case of neonatal respiratory distress, 7.35 vaginal deliveries compared with cesarean deliveries were needed.
When the study population was examined based on indication, cesarean delivery was more common than vaginal delivery if a maternal medical condition was identified (2,995 [51.4%] by cesarean delivery and 2,833 [48.6%] by vaginal delivery). Vaginal delivery was more frequent when the indication for delivery was obstetric complication (5,343 [57.3%] by vaginal delivery and 3,975 [42.7%] by cesarean delivery). Vaginal delivery was also far more common if the delivery did not involve a maternal or obstetric complication (6,816 [90.8%] by vaginal delivery and 695 [9.2%] by cesarean delivery). Regardless of indication for delivery, cesarean delivery was associated with increased odds of respiratory distress compared with vaginal delivery (see Table 3).
When the cohort was limited to the population delivered at or before 30 weeks of gestation, the association between cesarean delivery and increased risk of respiratory distress (adjusted odds ratio [OR] 1.41, 95% confidence interval [CI] 1.24–1.59) and Apgar score less than 7 at 5 minutes (adjusted OR 1.43, 95% CI 1.22–1.68) persisted.
Cesarean deliveries have been increasing steadily for the past two decades. Very preterm neonates (less than 34 weeks of gestation) have the highest rate of cesarean delivery, approaching 50% according to the National Vital Statistics.1 A few studies have found an association between cesarean delivery and increased odds of respiratory distress,7,20,21 but others have found no increased neonatal risk with cesarean delivery.4 Our study, like Lee et al, challenges the notion that cesarean deliveries are equivalent to vaginal deliveries for preterm neonates.3 For appropriately grown neonates, especially between 31 weeks and 34 weeks of gestation, vaginal delivery is associated with decreased odds of neonatal death, respiratory distress, and low Apgar scores. This suggests that when medically safe, vaginal delivery may be advantageous for the neonate or, at minimum, that it does no harm and avoids the potentially negative effect of cesarean delivery.
Interestingly, the indication for delivery, maternal or obstetric, did not significantly alter the ORs for respiratory distress. Even in the low-risk population with no known maternal or obstetric complications, respiratory distress remained associated with cesarean delivery compared with vaginal delivery. This suggests that the birthing process itself may provide early neonatal benefits above cesarean delivery.
This study has several strengths. Birth before 34 weeks of gestation is relatively uncommon and, given improved neonatal care, morbidity and mortality, especially after 31 weeks of gestation, is less common, requiring a large cohort. New York City provides an ideal study population for such a study because it is large and socially, racially, and economically diverse. Additionally, the database used combines birth certificate data and hospital discharge information. This pairing of analyzed variables has been shown to significantly improve the quality of the data.22
Although the population size and scope of this study would be difficult to obtain in a prospective fashion, using a retrospective, nonrandomized cohort has significant limitations. Misclassification of gestational age and mode of delivery as well as underreporting of neonatal poor outcomes may have occurred in some cases.23 Additionally, some desired data were unavailable. We were not able to differentiate those patients who were induced from those patients who labored spontaneously. We also were unable to identify patients who underwent cesarean deliveries without labor from those who labored and then had a cesarean delivery. Finally, we could not adequately access the urgency of the delivery. For example, although nonreassuring fetal status was recorded as an indication, there was no distinction between a prolonged bradycardia and recurrent variables. The urgency of the delivery is particularly important because pregnancies complicated by emergent cesarean deliveries may not have benefited from steroids. Unfortunately, steroid administration data were not available for this cohort. Thus, despite extensive efforts to control for baseline differences in risks when comparing vaginal deliveries with cesarean deliveries, confounding by indication remains a possible explanation for our results.
Despite the limitations of this study, it underscores the lack of benefit to preterm neonates from the increasing cesarean delivery rate. There may be significant benefit to labor and vaginal delivery, ie, untapped when preterm neonates undergo a cesarean delivery. This benefit seems most pronounced in those deliveries that are preterm but not extremely premature. Prospective studies are needed to explore this association more completely. However, while awaiting future studies, the findings of this study suggest that it is most prudent to attempt a vaginal delivery in all preterm neonates needing to be delivered if it is medically safe to do so.
1. Menacker F, Hamilton BE. Recent trends in cesarean delivery in the United States. NCHS Data Brief 2010:1–8.
2. Deulofeut R, Sola A, Lee B, Buchter S, Rahman M, Rogido M. The impact of vaginal delivery in premature infants weighing less than 1,251 grams. Obstet Gynecol 2005;105:525–31.
3. Lee HC, Gould JB. Survival rates and mode of delivery for vertex preterm neonates according to small- or appropriate-for-gestational-age status. Pediatrics 2006;118:e1836–44.
4. Wylie BJ, Davidson LL, Batra M, Reed SD. Method of delivery and neonatal outcome in very low-birthweight vertex-presenting fetuses. Am J Obstet Gynecol 2008;198:640.e1–7.
5. Riskin A, Riskin-Mashiah S, Lusky A, Reichman B; Israel Neonatal Network. The relationship between delivery mode and mortality in very low birthweight singleton vertex-presenting infants. BJOG 2004;111:1365–71.
6. Jonas HA, Lumley JM. The effect of mode of delivery on neonatal mortality in very low birthweight infants born in Victoria, Australia: caesarean section is associated with increased survival in breech-presenting, but not vertex-presenting, infants. Paediatr Perinat Epidemiol 1997;11:181–99.
7. Werner EF, Savitz DA, Janevic TM, Ehsanipoor RM, Thung SF, Funai EF, et al.. Mode of delivery and neonatal outcomes in preterm, small-for-gestational-age newborns. Obstet Gynecol 2012;120:560–4.
8. Werner EF, Janevic TM, Illuzzi J, Funai EF, Savitz DA, Lipkind HS. Mode of delivery in nulliparous women and neonatal intracranial injury. Obstet Gynecol 2011;118:1239–46.
9. Rosenberg TJ, Garbers S, Lipkind H, Chiasson MA. Maternal obesity and diabetes as risk factors for adverse pregnancy outcomes: differences among 4 racial/ethnic groups. Am J Public Health 2005;95:1545–51.
10. Oken E, Kleinman KP, Belfort MB, Hammitt JK, Gillman MW. Associations of gestational weight gain with short- and longer-term maternal and child health outcomes. Am J Epidemiol 2009;170:173–80.
11. Oken E, Kleinman KP, Rich-Edwards J, Gillman MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr 2003;3:6.
12. Peleg D, Kennedy CM, Hunter SK. Intrauterine growth restriction: identification and management. Am Fam Physician 1998;58:453–60, 466–7.
13. Reddy UM, Zhang J, Sun L, Chen Z, Raju TN, Laughon SK. Neonatal mortality by attempted route of delivery in early preterm birth. Am J Obstet Gynecol 2012;207:117.e1–8.
14. Rosenberg TJ, Garbers S, Chavkin W, Chiasson MA. Prepregnancy weight and adverse perinatal outcomes in an ethnically diverse population. Obstet Gynecol 2003;102:1022–7.
15. Savitz DA, Janevic TM, Engel SM, Kaufman JS, Herring AH. Ethnicity and gestational diabetes in New York City, 1995–2003. BJOG 2008;115:969–78.
16. Aljohani N, Rempel BM, Ludwig S, Morris M, Cheang M, Murray R, et al.. Impact of diabetes on maternal-fetal outcomes in Manitoba: relationship with ethnic and environmental factors. Clin Invest Med 2008;31:E338–45.
17. Sibai BM, Koch MA, Freire S, Pinto e Silva JL, Rudge MV, Martins-Costa S, et al.. The impact of prior preeclampsia on the risk of superimposed preeclampsia and other adverse pregnancy outcomes in patients with chronic hypertension. Am J Obstet Gynecol 2011;204:345.e1–6.
18. Gilbert WM, Young AL, Danielsen B. Pregnancy outcomes in women with chronic hypertension: a population-based study. J Reprod Med 2007;52:1046–51.
19. Tuuli MG, Rampersad R, Stamilio D, Macones G, Odibo AO. Perinatal outcomes in women with preeclampsia and superimposed preeclampsia: do they differ? Am J Obstet Gynecol 2011;204:508.e1–7.
20. Malloy MH. Impact of cesarean section on intermediate and late preterm births: United States, 2000–2003. Birth 2009;36:26–33.
21. Hansen AK, Wisborg K, Uldbjerg N, Henriksen TB. Risk of respiratory morbidity in term infants delivered by elective caesarean section: cohort study. BMJ 2008;336:85–7.
22. Lydon-Rochelle M, Holt VL, Cárdenas V, Nelson JC, Easterling TR, Gardella C, et al.. The reporting of pre-existing maternal medical conditions and complications of pregnancy on birth certificates and in hospital discharge data. Am J Obstet Gynecol 2005;193:125–34.
23. Vinikoor LC, Messer LC, Laraia BA, Kaufman JS. Reliability of variables on the north carolina birth certificate: a comparison with directly queried values from a cohort study. Paediatr Perinat Epidemiol 2010;24:102–12.