PEDIATRICS Vol. 118 No. 6 December 2006, pp. e1836-e1844 (doi:10.1542/10.1542/peds.2006-1327)
ARTICLE |
Survival Rates and Mode of Delivery for Vertex Preterm Neonates According to Small- or Appropriate-for-Gestational-Age Status
Division of Neonatal and Developmental Medicine, Stanford University, Palo Alto, California
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. The goal was to characterize the relationship between cesarean section delivery and death for preterm vertex neonates according to intrauterine growth.
METHODS. Maternal and infant data from the National Center for Health Statistics for 1999 and 2000 were analyzed. Neonates with gestational ages of 26 to 36 weeks were characterized as small for gestational age (<10th percentile) or appropriate for gestational age (10th to 90th percentile). Mortality rates at 28 days and relative risks were calculated for each gestational age group according to mode of delivery.
RESULTS. Cesarean section rates were higher for small-for-gestational-age neonates compared with appropriate-for-gestational-age neonates, most prominently from 26 weeks to 32 weeks of gestation, at which small-for-gestational-age neonates had cesarean section rates of 50% to 67%, whereas appropriate-for-gestational-age neonates had rates of 22% to 38%. Small-for-gestational-age neonates at gestational ages of <31 weeks had increased survival rates associated with cesarean section, whereas small-for-gestational-age neonates at >33 weeks and appropriate-for-gestational-age neonates overall had decreased survival rates associated with cesarean section. After adjustment for sociodemographic and medical factors, the survival advantage for small-for-gestational-age neonates at gestational ages of 26 to 30 weeks persisted.
CONCLUSIONS. Cesarean section delivery was associated with survival for preterm small-for-gestational-age neonates but not preterm appropriate-for-gestational-age neonates. We speculate that vaginal delivery may be particularly stressful for small-for-gestational-age neonates. We found no evidence that prematurity alone is a valid indication for cesarean section for preterm appropriate-for-gestational-age neonates.
Key Words: birth weight • survival • gestational age • cesarean section
Abbreviations: NCHS—National Center for Health Statistics • CI—confidence interval • OR—odds ratio • RR—relative risk • SGA—small for gestational age • AGA—appropriate for gestational age • VLBW—very low birth weight
The optimal route of delivery for preterm vertex neonates continues to be debated. Some studies demonstrated benefits from cesarean section delivery, with lower mortality rates, higher 1-minute Apgar scores, and less intraventricular hemorrhage.1–3 Other studies showed no improvement in mortality rates and other outcomes for vertex neonates born through cesarean section.4–9 Despite the uncertainty regarding benefits for preterm vertex neonates, cesarean section delivery rates have increased for this group.10
Previous studies that evaluated modes of delivery and outcomes for preterm vertex neonates had several limitations, including being single-center or multicenter trials with relatively small sample sizes1,2,5,7,8 or increasing sample sizes by evaluating outcomes over time periods of 10 to 15 years, during which practice patterns might have been evolving.2,9 In addition, some studies were performed before the widespread use of prenatal steroid treatment and surfactant therapy, which might influence the impact of delivery mode on outcomes.3,5,6,8
Recently, we examined the births recorded in the 1999 and 2000 National Center for Health Statistics (NCHS) linked birth/death data sets and found that cesarean section delivery was associated with a survival advantage for very low birth weight (VLBW) vertex neonates who weighed <1300 g.11 Although the advantage of cesarean section was most prominent in the smallest birth weight groups, ranging from a relative risk (RR) of death of 2.24 at 500 to 699 g to 1.26 at 1100 to 1299 g, the potential mechanisms that might contribute to this survival advantage were not explored.
In reviewing our findings, we hypothesized that small-for-gestational-age (SGA) neonates might have a different response to cesarean section delivery than appropriate-for-gestational-age (AGA) neonates. Cortisol and dehydroepiandrosterone sulfate levels have been found to differ in preterm neonates according to the mode of delivery, with neonates delivered through cesarean section having decreased levels regardless of the presence or absence of labor.12,13 Because SGA status can be a marker for intrauterine growth restriction, these neonates might have been in an environment of placental insufficiency and relative hypoxia, making them particularly vulnerable to any added stress. To evaluate this hypothesis, we performed additional analysis of the 1999/2000 NCHS study cohort according to gestational age, examining the relationship between mode of delivery, intrauterine growth (as estimated with birth weight percentile), and neonatal mortality rates for preterm neonates.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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We used the US birth cohort linked birth/infant death certificate data sets for 1999 and 2000, published by the NCHS.14 In that 2-year cohort population, 7779300 singleton live births were recorded. Our study evaluated 6643622 singleton neonates born in the vertex position to US residents without a previous cesarean section delivery. Of those, 67475 (1%) could not be studied because they had no recorded gestational age. We excluded 4289 neonates whose deaths were associated with congenital anomalies.
Our previous research indicated that a cesarean section birth advantage was seen only for neonates of <1300 g.11 We limited this analysis to the 621332 neonates whose gestational age was 
36 weeks and 
26 weeks. We chose not to include neonates of <26 weeks to decrease the likelihood of treatment decisions based on nonmedical factors, such as the perceived viability of infants at <26 weeks of gestation. The gestational ages reported in the NCHS data sets were derived from calculations based on the last menstrual period. When this calculation resulted in an age inconsistent with the birth weight, NCHS used the recorded "clinical estimate of gestation" (6.1% of the final analytic cohort). On some records, the month and year, but not the day, of the last menstrual period were recorded. According to NCHS procedures, the gestational age was imputed in such circumstances (8.0% of the analytic cohort).15,16
We divided the cohort into SGA or AGA according to birth weight percentiles, using the work performed by Oken et al,17 which characterized the US birth cohort during the same time period. Neonates with birth weights of <10th percentile were considered SGA, whereas neonates with birth weights of 10th to 90th percentile were considered AGA. Our analysis did not consider large-for-gestational age neonates (>90th percentile; 78728 neonates). In our primary analysis, we also excluded neonates whose birth weights were <1st percentile (5325 neonates), because there was no other lower limit of birth weight in the analysis by Oken et al17 to use as a lower bound for birth weight. The delivery method was unknown for 0.3% of the SGA neonates (180 neonates) and 0.3% of the AGA neonates (1584 neonates). This resulted in an analytic cohort of 535515 preterm neonates (53975 SGA and 481540 AGA).
We calculated gestational age–specific cesarean section rates according to SGA or AGA status and compared cesarean section rates within and between the SGA and AGA populations according to each sociodemographic category (maternal age, education, race, and prenatal care) by using the 
2 statistic. For each week of gestational age, we compared mean birth weights between SGA and AGA neonates delivered through vaginal delivery and cesarean section by using Student's t test. To evaluate the relationships between intrauterine growth, mode of delivery, and mortality rates, we calculated gestational age–specific 28-day mortality rates (deaths per 1000 live births) for vaginally delivered and cesarean section-delivered infants and observed RRs and risk-adjusted odds ratios (ORs) of death according to mode of delivery, with estimates of their 95% confidence intervals (CIs), for the AGA and SGA cohorts. As advised by the NCHS, we calculated mortality rates by assigning a weight to each neonate to account for death records that could not be linked to their corresponding birth certificates. The rationale and details of this approach were detailed previously.11
To estimate the risk-adjusted impact of mode of delivery on mortality rates, we used separate multivariate logistic models for the SGA and the AGA infants, which took into account sociodemographic and medical risk factors and estimated adjusted ORs with 95% Wald CIs. Models were created for each 1-week SGA and AGA gestational age group. In each of these single-gestational age group models, birth weight was included as a predictor variable. Using the age groups for which a risk-adjusted survival advantage for cesarean section was observed (26–30 weeks), we constructed a general model, taking into account all of the aforementioned factors as well as gestational age, and applied it to the SGA and AGA cohorts.
Sociodemographic factors included maternal race (white, black, or other), ethnicity (Hispanic or non-Hispanic), maternal age (reference: 20–29 years), education (reference: high school), and adequacy of prenatal care. Adequacy of care was measured with a modification of the Kessner index.18 Medical complications that demonstrated a univariate association with death (P < .05) were also included; these were maternal anemia, hydramnios/oligohydramnios, incompetent cervix, uterine bleeding, maternal fever, premature rupture of membranes, placental abruption, other excessive bleeding, cephalopelvic disproportion, cord prolapse, nonreassuring fetal status, and hypertensive disorder (pregnancy-associated hypertension, eclampsia, or chronic hypertension).
All states had uniform reporting requirements for demographic and medical factors. Various states did not have specific items on their certificates. Of the variables relevant to our analysis, the only category that was not reported by a state was congenital anomalies (in New Mexico). States also had varying levels of completeness of data. For example, in 1999, the mode of delivery was reported for 99% of certificates in 46 states. However, 28.9% of certificates from Oklahoma lacked this information. Such records could not be included in our analysis. Birth weight was noted in 98.8% to 100% of records. More-detailed information regarding the completeness of data according to state has been published.15,16
We analyzed the SGA cohort more thoroughly by separating the cohort into finer birth weight percentile groups (ie, 1st to <3rd percentile and 3rd to <10th percentile).19 For this analysis, we also examined neonates who had birth weights recorded below the 1st percentile. RRs of death according to mode of delivery and adjusted ORs were estimated for these 3 subsets according to the previously described procedures.
All analyses were performed by using SAS 9.1 (SAS Institute, Cary, NC). This study was approved by the Stanford University institutional review board.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Sociodemographic characteristics of the study population are outlined in Table 1. Compared with AGA neonates, SGA neonates were more likely to be non-Hispanic and black and were less likely to have had adequate prenatal care. For both the SGA and AGA cohorts, cesarean section rates were higher for non-Hispanic women, white women, more highly educated women, and older women. However, across all sociodemographic categories, cesarean section rates were always significantly higher for SGA neonates. The cesarean section rates for SGA neonates were also higher than the rates for AGA neonates for all gestational age groups (Fig 1). For gestational ages of 26 to 32 weeks, cesarean section rates ranged from 50% to 67% for SGA neonates and from 22% to 38% for AGA neonates.
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Table 2 shows a comparison of birth weight ranges, average birth weights, and observed gestational age–specific neonatal mortality rates according to mode of delivery for SGA and AGA neonates. We found that the mortality rates for the SGA neonates were 1.4 to 12.9 times higher than those for the AGA neonates. For SGA neonates, vaginal delivery was associated with higher mortality rates at gestational ages of 26 to 30 weeks, with vaginal delivery conferring
2 times the risk of death, compared with cesarean section (Fig 2). This finding, expressed as the OR for death with vaginal delivery versus cesarean section, persisted after controlling for possible differences in the incidence of sociodemographic and medical risk factors (Table 2). At 31 to 33 weeks, there was no longer a statistically significant difference in the mortality rates for vaginally delivered and cesarean section-delivered SGA neonates, although the trend favored an association between cesarean section and survival. At gestational ages of 34 weeks, mortality rates were significantly lower for SGA neonates born vaginally. However, even with control for sociodemographic and medical risk factors, AGA neonates born vaginally had significantly lower risks of death than did those born through cesarean section at most gestational ages (Table 2 and Fig 3).
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To assess the relative importance of mode of delivery in comparison with other risk factors, we constructed multivariate models examining death and mode of delivery that included only the gestational ages for which the SGA population was observed to have a risk-adjusted survival advantage associated with cesarean section, namely,
30 weeks. The sociodemographic and medical factors included in this model were the same as those used to obtain the results in Table 2. SGA and AGA neonates were analyzed separately (Table 3). In the model for SGA neonates, inadequate prenatal care, maternal age of >40 years, and incompetent cervix were associated with higher mortality rates. For AGA neonates, inadequate prenatal care, nonreassuring fetal status, and hydramnios/oligohydramnios were associated with higher mortality rates. Hypertensive disorder was associated with greater survival rates for both SGA and AGA preterm neonates. After adjustment for risk factors, vaginal delivery was associated with a 180% increase in the odds of neonatal death for SGA neonates from 26 weeks to 30 weeks (OR: 2.8; 95% CI: 2.2–3.5) and was the strongest predictor of death in this model. For AGA neonates, however, vaginal delivery was associated with a 20% decrease in the odds of death (OR: 0.8; 95% CI: 0.7–0.9).
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We analyzed more thoroughly the data for SGA neonates at gestational ages of 26 to 31 weeks by partitioning subjects into categories of 1st to <3rd percentile and 3rd to <10th percentile. We also analyzed data for neonates whose birth weights were <1st percentile for gestational age (Table 4). Vaginal delivery was associated with increased mortality rates across weight percentile groups for these SGA neonates, with similar effects for the <1st percentile group (OR: 3.2; 95% CI: 2.0–5.1), the 1st to <3rd percentile group (OR: 2.2; 95% CI: 1.5–3.3), and the 3rd to <10th percentile group (OR: 2.8; 95% CI: 2.2–3.6).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In our analysis of a national cohort of preterm neonates born in 1999 or 2000, we found that preterm SGA but not AGA neonates had higher mortality rates associated with vaginal delivery. This finding was present for neonates defined as SGA with birth weights of <10th percentile at gestational ages of 26 to 30 weeks and persisted after adjustment for medical and sociodemographic factors. In contrast to SGA neonates, AGA neonates had higher mortality rates associated with cesarean section, compared with vaginal delivery.
In our previous analysis of VLBW neonates, we saw an association between increased survival rates and cesarean section that increased with decreasing birth weight. We postulated several potential reasons for this observation. The first was that there might have been a selection bias, that is, physicians and patients who were choosing to be less aggressive in management of the delivery and resuscitation of the newborn at younger gestational ages might have elected to forego cesarean section delivery. To account in part for this potential bias, we limited our analysis to gestational ages of 26 weeks. Although many practitioners would consider a neonate at 24 weeks to be viable, practice patterns may depend on regional attitudes toward extreme prematurity. We eliminated this potential gray zone of gestational ages of 23 to 25 weeks, for which cesarean section rates might be lower because of the decision not to pursue aggressive measures. In the current analysis, the cesarean section rates for gestational ages of 26 to 29 weeks were similar at 40%, which supports the premise that, at >26 weeks of gestation, practice patterns were fairly consistent.
We also speculated that avoidance of the physiologic stresses of vaginal delivery could play a role in the outcomes of preterm neonates and that this would be particularly prominent for SGA neonates, who might already have been in an environment of stress and relative hypoxia. The survival advantage for SGA neonates born through cesarean section might be attributable to avoidance of the added stress of vaginal birth. However, it is important to note that, in addition to placental insufficiency, small size at birth might be attributable to nonplacental factors such as heredity, congenital infections, and genetic syndromes. Therefore, the advantage of cesarean section delivery might be attributable to other factors that cannot be determined from this study.
Our finding that the cesarean section survival advantage for SGA neonates was limited primarily to 26 to 30 weeks supports the findings of Gezer et al,20 who reported that, for SGA neonates with gestational ages of >33 weeks, there was no advantage to cesarean section. In contrast to the SGA neonates, we found that, for AGA neonates at most gestational ages and for all neonates at >34 weeks, mortality rates were higher after cesarean section delivery. This apparent disadvantage to cesarean section delivery may be attributable not to the procedure itself but rather to medical factors in the pregnancy and delivery that led to the cesarean section delivery. Although we attempted to account for this in our multivariate analysis by including other medical factors, there might have been some risk factors that were not included in this database. Elective cesarean section in term neonates has been associated with severe respiratory disease.21–23 Similar factors may explain why late preterm SGA neonates demonstrated increased mortality rates in association with cesarean section delivery. The association of cesarean section with higher mortality rates for most AGA groups contrasts sharply with the association of cesarean section with survival for preterm SGA neonates and suggests that, in the absence of specific indications, it is unlikely that cesarean section would be associated with improved survival rates for preterm AGA neonates.
In evaluating this cohort and taking into account both gestational age and birth weight, we might have shed some light on the seemingly contradictory evidence that has been published regarding the benefit of cesarean section for premature neonates. Our previous study evaluating the association between mortality rates and cesarean section for US preterm neonates showed a significant advantage of cesarean section up to a birth weight of 1300 g, whereas a similar study based on gestational age and covering the same era in Israel showed no advantage.4,11 That analysis, limited to birth weights of <1500 g, accounted for prenatal steroid use and had more-detailed data on pregnancy dating. However, a key difference was that, whereas our study used birth weight as a predictor variable, the Israeli study used gestational age. Although those authors accounted for SGA status in their multivariate analysis, they did not analyze SGA neonates separately.
When we combined the AGA and SGA neonates and performed an analysis of our entire cohort on the basis of gestational age, we could not demonstrate an advantage to cesarean section delivery for extremely preterm neonates by using risk-adjusted models for 1-week intervals or for 26 to 30 weeks combined. We speculate that, in an analysis based on gestational age, the cesarean section survival advantage seen for the 10% of neonates who are SGA is obscured by the higher mortality rates seen for the AGA majority. However, when the cohort is subdivided into neonates who are SGA and those who are AGA, a survival advantage for SGA infants can be demonstrated clearly. This holds true even when this comparison is made within a narrowly defined range of birth weights. For example, in the birth weight group of 800 to 1000 g, we found that the advantage of cesarean section was seen only for SGA neonates (RR: 2.2; 95% CI: 1.4–3.4) and not for AGA neonates (RR: 1.0; 95% CI: 0.8–1.2). Details of these analyses are available on request. These findings demonstrate that, although gestational age and birth weight are highly correlated, they may not always be interchangeable as predictor variables, particularly in studies that investigate birth weight–specific outcomes for extremely low birth weight neonates, a group that might be weighted heavily with SGA neonates.
Studies investigating preterm neonatal outcomes often limit analysis to VLBW defined as birth weights of <1500 g, as did our previous analysis on this subject, in which we concluded that cesarean section was associated with increased survival rates for VLBW neonates.11 In the current analysis, we refined the analysis by analyzing a larger group of preterm neonates according to SGA and AGA status. We found that, even among VLBW neonates, the advantage associated with cesarean section was limited to SGA neonates only. Although, by definition, SGA should account for 10% of the population, SGA neonates accounted for 33% of VLBW neonates in this cohort. Studies of VLBW neonates would thus have over-representation of SGA neonates, a group that might have different responses to treatments, compared with AGA neonates. This might have implications for the design of clinical trials and epidemiologic studies involving perinatal outcomes.
Mothers who underwent cesarean section might have had different prenatal care than did those who did not undergo cesarean section. We attempted to control for this possibility by including adequacy of prenatal care, as well as sociodemographic factors such as maternal race and education, in the risk-adjusted model.
Our study, being based on national birth certificates, has limitations with respect to both the depth and accuracy of the clinical information available for analysis. Because of the uncertainty of pregnancy dating in some situations, the NCHS uses clinical estimates and imputation for some records. To assess this potential source of error, we performed a separate analysis of the SGA cohort that excluded neonates whose gestational ages were based on clinical estimation (10.8%) or were imputed (8.5%). The adjusted risk of death associated with SGA vaginal delivery at 26 to 30 weeks remained essentially the same (OR: 2.81; 95%: CI: 2.19–3.63; primary analysis: OR: 2.8; 95% CI: 2.2–3.5). Nevertheless, the potential error in the dating of pregnancy is a limitation of this study. For example, dating of pregnancy in this data set relied primarily on the last menstrual period. Errors in gestational age estimations can occur with this method. However, because errors in dating could be in either direction, we do not think that this would cause systematic bias, leading to the results we found.
We were also limited by the scope of the medical information reported on the birth certificates and by the fact that it was not collected in a prospective manner. This information might not have been sufficient to adjust adequately for the risk associated with cesarean section in some situations. In particular, the risk of death associated with cesarean section for preterm AGA neonates might be explained in part by limitations in recording medical risk factors, rather than cesarean section delivery. In our previous study, we found that 30% of VLBW neonates delivered through cesarean section had no recorded medical risk factors.11
This data set lacked data on prenatal steroid treatment and the level of perinatal care provided at the birth hospital. In a review of a network of US hospitals caring for VLBW neonates, prenatal steroid administration increased dramatically for neonates with gestational ages of 25 to 30 weeks, from <20% before the 1994 National Institutes of Health Consensus Conference to 70% to 80% in 1996 to 1998, after which levels seemed to plateau.24 If preterm SGA neonates delivered through cesarean section were more likely to have received steroids or to be born at hospitals with a higher level of perinatal care than SGA neonates delivered vaginally, then these factors could contribute to decreased mortality rates. However, if this were the case, then we would expect to see a similar pattern of decreased mortality rates associated with cesarean section delivery for AGA neonates, which we did not find. If women with incompetent cervix were less likely to receive a full course of prenatal steroid therapy, then this could explain in part why incompetent cervix was associated with higher mortality rates (Table 3).
We examined 28-day neonatal mortality rates, which we think best reflect the effect of perinatal care on neonatal outcomes. It might also be informative to investigate infant mortality rates, because delivery method could influence long-term morbidities, which could lead to later death. Although we speak of a survival advantage, because of the epidemiologic design of this study, a causal relationship between cesarean section delivery and decreased mortality rates for SGA neonates cannot be proved. Before our investigation, it was considered unlikely that a sufficiently large, randomized, controlled study would be developed to address the issue of cesarean section delivery for all preterm neonates.11 However, considering the 2.8-fold increase in odds of survival for SGA neonates seen in our analysis, focusing a randomized, clinical trial on pregnancies with growth-restricted fetuses would be feasible and important. Such a trial could also address limitations of our study related to outcomes by including maternal and neonatal morbidities, as well as long-term infant outcomes.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Our study provides no evidence that prematurity alone is a valid indication for cesarean section for AGA preterm neonates. However, given the strong relationship between cesarean section delivery and decreased mortality rates for SGA preterm neonates, we think that cesarean section delivery may be the optimal mode of delivery for intrauterine growth-restricted, preterm neonates with placental insufficiency.
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ACKNOWLEDGMENTS |
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Dr Lee is the recipient of the Elizabeth and Russell Siegelman Pediatric Fellowship.
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FOOTNOTES |
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Accepted Jul 14, 2006.
Address correspondence to Henry Chong Lee, MD, Division of Neonatal and Developmental Medicine, Stanford University, 750 Welch Rd, Suite 315, Palo Alto, CA 94304. E-mail: hclee{at}stanford.edu
The authors have indicated they have no financial relationships relevant to this article to disclose.
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