Published online August 1, 2008
PEDIATRICS Vol. 122 No. 2 August 2008, pp. 285-292 (doi:10.1542/peds.2007-2620)
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ARTICLE

Impact of Cesarean Section on Neonatal Mortality Rates Among Very Preterm Infants in the United States, 2000–2003

Michael H. Malloy, MD, MS

Department of Pediatrics, University of Texas Medical Branch, Galveston, Texas


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. The objective of this analysis was to compare the neonatal mortality rates for infants delivered through primary cesarean section versus vaginal delivery, taking into consideration a number of potentially risk-modifying conditions.

METHODS. US linked birth and infant death certificate files for 2000–2003 were used. Demographic, medical, and labor and delivery complications were abstracted from the files with infant information. The primary outcome examined was neonatal death (death at 0–27 days of age). Because of concern regarding misclassification of gestational age, a procedure was used to trim away births for which the birth weight for a specific gestational age was incongruous. Adjusted odds ratios were calculated for the risk of neonatal death relative to the mode of delivery (primary cesarean section versus vaginal delivery), using logistic regression analysis.

RESULTS. There were data for 13 733 neonatal deaths and 106 809 survivors available from the trimmed data set for analysis for the 4-year period. More than 80% of pregnancies with delivery between 22 and 31 weeks of gestation experienced ≥1 risk factor. Adjusted odds ratios demonstrated significantly reduced risk of neonatal death for infants delivered through cesarean section at 22 to 25 weeks of gestation (adjusted odds ratios of 0.58, 0.52, 0.72, and 0.81 for 22, 23, 24, and 25 weeks, respectively).

CONCLUSION. Cesarean section does seem to provide survival advantages for the most immature infants delivered at 22 to 25 weeks of gestation, independent of maternal risk factors for cesarean section.

Key Words: cesarean section • very preterm births • neonatal death

Abbreviations: OR—odds ratio • CI—confidence interval • AGA—appropriate for gestational age • LGA—large for gestational age • SGA—small for gestational age

The cesarean section rate in the United States increased to an all-time high of 30% in 2005.1 Increasing cesarean section rates have been reported since 1996, and the rate increase is occurring across all gestational age categories.2 In 2003, the cesarean section rate among infants at <32 weeks of gestation was reported to be almost 50%. In addition, the gestational age at which active intervention is considered (rightly or wrongly) is being pushed below 24 weeks of gestation.2–4 Despite the increasing cesarean section rate, the infant mortality rate for very low birth weight infants (<1500 g) has remained relatively stable since 2000; rates were reported as 244.3 deaths per 1000 live births in 2000 and 244.5 deaths per 1000 live births in 2004.5

Whether delivery through cesarean section offers any survival advantage for very preterm (<32 weeks of gestation) or very low birth weight infants, independent of risk factors reportedly averted through cesarean delivery, has been debated in the literature for some time and continues to be a topic lacking consensus.6–17 Obstetricians' willingness to perform cesarean sections at extremely preterm gestational ages has been demonstrated to improve survival rates, albeit with serious morbidity.18 Recently, Lee and Gould16 reported a survival advantage among very low birth weight infants delivered through cesarean section, independent of a number of maternal medical and labor complications and demographic risk factors. Over the range of birth weights from 500 to 1499 g, the adjusted odds ratio (OR) for neonatal death (death at <28 days) was 0.53 (95% confidence interval [CI]: 0.49–0.57). A problem associated with examining neonatal mortality rates according to birth weight is the effect of intrauterine growth on survival rates. Infants who are smaller than expected for any particular gestational age may be more likely to survive, thus decreasing the mortality rate for any particular range of birth weights. In a subsequent publication, the same authors reported that the survival advantage of cesarean section seemed to be limited to infants who were small for gestational age (SGA) for gestational ages of 26 to 36 weeks, which suggested that prematurity alone is not a valid indication for cesarean section.17 Independent of known risk factors, is there any reason to consider a cesarean section for the delivery of a very preterm infant? Given the reduction in the gestational age at which intervention is considered by some health care providers, the purpose of this analysis was to determine whether there is any survival advantage to cesarean delivery among infants delivered at 22 to 31 weeks of gestation.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
US linked birth and infant death certificate files were obtained from the National Center for Health Statistics for the years 2000–2003.19 These files contained maternal demographic characteristics, medical complications of pregnancies, labor and delivery complications, method of delivery, and infant characteristics. Demographic variables in the analysis included maternal race (Hispanic, non-Hispanic black, non-Hispanic white, or other), maternal age, and maternal education. Files were created by using SAS software (SAS Institute, Cary, NC) that extracted all survivors and deaths with a best estimated gestational age between 22 and 31 weeks.

The best estimated gestational age uses the recorded date of the last normal menses or a clinical estimate of gestational age if the latter appears inconsistent with birth weight.20 The algorithm for determining whether a birth weight should be considered inconsistent for a particular gestational age, however, has exceptionally large ranges for gestations of <32 weeks.21 For example, birth weights of up to 2000 g are considered consistent with gestational ages of 22 and 23 weeks, birth weights of up to 3000 g are considered consistent with gestational ages of 24 to 27 weeks, and birth weights of up to 4000 g are considered consistent with gestational ages of 28 to 31 weeks. Because of these exceptionally broad ranges, a trimming procedure was used to select records that were much more likely to be representative of infants born at these very preterm gestational ages. The mode and interquartile range of the birth weight distribution for each gestational week were determined, and records for each gestational week that were within one half of the interquartile range on either side of the mode of the distribution were selected for analysis in a trimmed data set. This procedure resulted in reduction of the number of records from 230 271 to 120 542 (52% of the original number).

Specific risk factors for cesarean section examined in this analysis included whether the pregnancy was a multiple birth, whether the presentation was breech, whether a fetal anomaly was present, and whether a medical diagnosis or complication of labor and delivery was present. Eighteen medical diagnoses and 16 complications of labor and delivery are listed on standard birth certificates (see Appendix 1 for specific diagnoses and complications). The presence of ≥1 of the diagnoses or complications was recorded in an indicator variable for complications. SGA infants were considered to be at potential risk for cesarean section. Infant size, that is, SGA (<10th percentile), appropriate for gestational age (AGA) (10th to 90th percentile), or large for gestational age (LGA) (>90th percentile), was determined by examining the birth weight distribution for each week of gestation according to gender, using the trimmed data set. An Apgar score of <4 at 5 minutes was considered a proxy for a risk factor for which a cesarean section might have been performed because of an intrauterine asphyxiating event.


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  		APPENDIX 1 Medical Diagnoses and Labor and Delivery Complications Derived From Birth Certificates

 
The {chi}2 test for general association was used for nominal variables, and Student's t test was used to compare means of continuous variables. Logistic regression models were used to determine ORs and 95% CIs for the primary outcome variable, neonatal death (death between birth and 27 days), and the method of delivery (primary cesarean section versus vaginal delivery), with adjustment for potentially confounding factors. All analyses were conducted by using SAS software. An arbitrary P value of .05 was designated to indicate statistical significance.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In the trimmed data set, there were 4783 neonatal deaths among 63 588 primary cesarean deliveries (neonatal mortality rate: 75.2 deaths per 1000 live births) and 8950 neonatal deaths among 56 954 vaginal deliveries (neonatal mortality rate: 157.1 deaths per 1000 live births), producing a significantly reduced cesarean section/vaginal delivery neonatal mortality rate ratio of 0.48 (Table 1). In fact, all characteristics listed in Table 1 demonstrated significantly reduced neonatal mortality rate ratios for cesarean deliveries.


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  		TABLE 1 Neonatal Mortality Rates and Population Characteristics According to Method of Delivery for Live Births at 22 to 31 Weeks of Gestation

 
The mean and range of birth weights in the trimmed data set were well within the 10th and 90th percentiles used by other trimming methods through 26 weeks of gestation (Table 2). 22–24 At 27 weeks, the minimum birth weight values dipped below the 5th percentile values used in the other methods, although the mean birth weight values for infants calculated to be SGA approximated the 10th percentile values used in the other methods. The ranges for AGA, SGA, and LGA weights were much narrower than reported for other trimming methods.


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  		TABLE 2 Birth Weights According to Infant Size and Gestational Age

 
The mean birth weights for infants delivered vaginally were significantly lower than those for infants delivered through cesarean section for weeks 22 to 24, whereas infants delivered vaginally were significantly heavier for weeks 25 to 31 (Table 3). The cesarean section/vaginal delivery neonatal mortality rate ratio was significantly reduced for weeks 22 to 25 and was not significant for the remainder of the weeks (Table 3). Of note are the relatively small proportions of total pregnancies with delivery through cesarean section at 22 and 23 weeks (7.3% and 21.3%, respectively).


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  		TABLE 3 Birth Weights and Neonatal Mortality Rates According to Gestational Age

 
The distribution of the age of death was skewed, such that the primary advantage for infants delivered through cesarean section at <26 weeks was on the day of birth (Fig 1). For days 1 to 6, 7 to 27, and 28 to 364, the percentage mortality rates for cesarean sections exceeded those for vaginal deliveries. Nevertheless, the overall survival rate for infants delivered through cesarean section exceeded that for vaginally delivered infants at gestational ages of 22 to 25 weeks (61.5% vs 37.8%). The top 10 underlying causes of death among the cesarean section-delivered infants reflected this later age of death, with the inclusion of intraventricular hemorrhage, bronchopulmonary dysplasia, and necrotizing enterocolitis, which did not appear among the top 10 causes for vaginally delivered infants.


Figure 1
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  		FIGURE 1 Percentage distribution of total births at 22 to 25 weeks of gestation for survivors and deaths, according to day of death and mode of delivery.

 
After adjustment for all of the characteristics listed in Table 1, the adjusted ORs for neonatal death remained significantly reduced for weeks 22 to 25 (Table 4). At no gestational age was the risk of neonatal death significantly greater among infants delivered through cesarean section, compared with those delivered vaginally. An analysis was performed to examine the population of pregnancies that had ≥1 risk factor present. A logistic analysis of this group with adjustment for maternal age, education, race, and birth weight in the model demonstrated a significant reduction in the OR for neonatal death for infants delivered through cesarean section for every week of gestation except weeks 27, 28, and 29 (Table 4). The upper 95% confidence limits for the 3 weeks of gestation that did not attain significance came very close to significance, with upper limits of 1.03, 1.02, and 1.07; the point estimates for those 3 weeks were 0.84, 0.84, and 0.87, respectively. Therefore, the point estimates for the risk of neonatal death for all of the weeks examined suggested a reduced risk of death for infants delivered to mothers with any risk associated with the pregnancy. A separate logistic model was used for SGA infants. There was no consistent protective effect of primary cesarean section across gestational ages for those infants (Table 4).


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  		TABLE 4 Adjusted ORs for Neonatal Death for Primary Cesarean Section Versus Vaginal Delivery

 
To take into consideration the possibility of an intention-to-treat bias for infants delivered at the earliest gestational ages, an analysis was performed to examine the neonatal mortality rates for infants who received mechanical ventilation after birth, with the thought being that any infant who received mechanical ventilation would have been provided resuscitation and a commitment to treat the infant established. Although the numbers were relatively small at 22 weeks, 75 infants delivered through cesarean section underwent ventilation and 260 delivered vaginally underwent ventilation. The cesarean section/vaginal delivery neonatal mortality rate ratio was significantly reduced at 22 and 23 weeks (Table 5). The adjusted OR for neonatal death at 22 weeks was 0.51 (95% CI: 0.25–1.05), and that at 23 weeks was 0.62 (95% CI: 0.44–0.89). The adjusted ORs for the rest of the gestational ages failed to attain significance.


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  		TABLE 5 Neonatal Mortality Rates for Mechanically Ventilated Infants and Adjusted ORs for Primary Cesarean Section Versus Vaginal Delivery

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This analysis suggests that cesarean section was associated with a reduced neonatal mortality rate for infants at ≤25 weeks of gestation, independent of other risk factors that might lead to a cesarean section. In addition, for pregnancies with ≥1 risk factor, the risk for neonatal death was significantly reduced for deliveries through cesarean section at all gestational ages from 22 to 31 weeks except for 27, 28, and 29 weeks, which bordered on significant reductions. The intention-to-treat bias for infants delivered through cesarean section among the most-preterm infants, at 22 and 23 weeks, was addressed by examining a group of infants who underwent mechanical ventilation regardless of mode of delivery. Examination of this group also suggested survival advantages for infants delivered through cesarean section.

Examination of the impact of cesarean section on neonatal mortality rates and other outcomes provided mixed results when the basis of analysis was birth weight categories. An analysis of mortality rates among very low birth weight infants (500–1500 g) in Missouri demonstrated reduced first-day mortality rates in the 500- to 749-g stratum for cesarean section-delivered infants, but this was nullified by an excess number of deaths during the first week of life among cesarean section-delivered infants.9 ORs for neonatal death in fully adjusted models of risk factors associated with the need for cesarean section demonstrated no differences between cesarean section and vaginal deliveries (OR: 0.85; 95% CI: 0.51–1.40). An analysis of the National Institute of Child Health and Human Development Neonatal Research Network data reported similar findings.10 That is, there was no difference in the ORs for neonatal death between cesarean section and vaginal delivery for infants of 500 to 1500 g, after adjustment for a number of risk factors and gestational age. Even with stratification according to 250-g birth weight increments, no statistically significant differences were observed in the ORs derived for each stratum. Stratification according to birth weight was an important component of that analysis, because of the significant interaction observed between birth weight and mode of delivery. Although gestational age was included in those models as a continuous variable, no account of the significant interaction between gestational age and mode of delivery was taken. Averaging ORs across all gestational ages examined within a particular birth weight stratum may produce an invalid estimate of the OR. Averaging ORs across all gestational age strata examined continues to be a problem in more-recent analyses finding no significant effect of cesarean section on mortality rates.13

Interestingly, Lee and Gould16 reported a significant protective effect independent of maternal risk factors for cesarean section among infants of 500 to 1499 g, using US vital statistics data for the years 1999 and 2000 (OR: 0.53; 95% CI: 0.49–0.57). The model used for that analysis included a birth weight variable stratified according to 200-g increments. Therefore, the OR for the risk of neonatal death was averaged over 5 strata of birth weights. The unadjusted OR for each stratum demonstrated significant reductions in mortality rates for cesarean sections, except for the largest stratum of 1300 to 1499 g (OR: 0.84; 95% CI: 0.68–1.05). No account of gestational age, however, was taken in the final overall model, which included all birth weight strata. A subsequent analysis of the same data by those authors, taking into account gestational age and size for gestational age, demonstrated a significant protective effect of cesarean section for SGA infants but no protective effect for AGA infants.17 The gestational ages examined for that analysis ranged from 26 to 36 weeks. With stratification according to gestational age, the protective effect for SGA infants extended only for weeks 26 to 30. In the analysis presented here, no consistent protective effect of cesarean section for SGA infants was observed. This may be attributable to the fact that the mean birth weight among the SGA infants in this trimmed data set was consistently higher than that in the analysis by Lee and Gould.17 The lower range of birth weights in the study by Lee and Gould17 might include infants who had been misclassified to a higher gestational age. Therefore, the protective effect of cesarean section reported among the infants of <10th weight percentile could relate more to their degree of immaturity than to their size at birth.

An argument for examining neonatal mortality rates according to gestational age rather than birth weight can be made on the basis of the idea that gestational age reflects more clearly the organ maturational state of the fetus and is more likely to affect clinical decision-making.3,25,26 A major drawback of using gestational age is the uncertainty with which it is ascertained in some instances, particularly in vital statistics data.20,21 Trimming techniques to exclude birth weights beyond what may be considered an acceptable range have been used to include records with gestational age assessments that are assumed to be more valid.22–24 The method of trimming used for the analysis presented in this article is very restrictive. The rationale for this was to focus on the records that would be most representative of the outcomes for infants at these very preterm gestational ages.

On the basis of this analysis, it seems that infants from 22 to 25 weeks of gestation, independent of any risk factors, may benefit from delivery through cesarean section, in terms of reduced neonatal mortality rates, primarily on the day of birth. It is important to remember that ≥80% of infants delivered during the gestational period from 22 to 31 weeks come from pregnancies with ≥1 risk factor. In an analysis of the group of infants coming from pregnancies with ≥1 risk factor, the ORs for neonatal death were significantly reduced for all gestational ages except for 27, 28, and 29 weeks, for which the ORs approached but did not attain significant reductions. In addition, in contrast to the study by Lee and Gould,17 this analysis did not note a significant increase in the risk of neonatal death for gestational ages of 29 to 31 weeks with delivery through cesarean section, after adjustment for infant size. An increased risk of neonatal death for low-risk term infants delivered through cesarean section has been reported and continues to stir debate on the safety of cesarean section in the absence of indications for this procedure.27 In contrast, the analysis presented here suggests that there is no increased risk of neonatal death among these very preterm infants after indications for cesarean section have been considered. This does not take into consideration the morbidity that the mother may incur as a result of the cesarean section.28–30 The literature concerning maternal morbidity for extremely preterm cesarean deliveries is exceptionally sparse.12,31

It may be argued that the apparent protective effect of cesarean section delivery among exceptionally preterm infants (22–23 weeks) is a result of bias on the part of health care providers to make a greater effort to resuscitate infants delivered through cesarean section at these early gestational ages. The observation that the protective effect persisted for the subpopulation of infants who received mechanical ventilation after birth, regardless of mode of delivery, does support the positive impact of cesarean section. The fact that the protective effect was not apparent in the subpopulation receiving mechanical ventilation at gestational ages of >23 weeks may be related more to issues associated with the need for mechanical ventilation among infants at 24 to 31 weeks of gestation. As with late preterm and term infants delivered through cesarean section, the prevalence of mechanical ventilation (as a proxy for the need for respiratory support) was greater among cesarean deliveries than among vaginal deliveries.32 This may well be related to the impact of the mode of delivery on lung fluid physiologic features.33

The mechanism through which cesarean section confers a decrease in the neonatal mortality rate for preterm infants of <26 weeks of gestation, independent of risk factors indicating the need for cesarean section, is uncertain. Whether it involves diminished stress and trauma that may be associated with labor and vaginal delivery remains highly speculative. A relative reduction in such stress could modify the newborn infant's inflammatory response to noxious exogenous exposures shortly after birth, such as barotrauma, cardiovascular equilibration, or infectious agent exposures.34–36 As pointed out by Lee and Gould,17 SGA infants or infants with intrauterine growth restriction at 26 to 30 weeks of gestation seem to benefit particularly from cesarean section, which suggests that the stress of vaginal delivery may contribute to the vulnerability of these infants, who may have limited physiologic reserves.37,38

In conjunction with the vulnerability of these infants because of their immaturity, the vulnerability of male infants continues to be apparent independent of mode of delivery.39 Within the adjusted models for neonatal death (Table 4), boys were at marginally greater risk than girls from 22 to 25 weeks of gestation (adjusted ORs: 1.16–1.26), at significantly greater risk at 26 to 28 weeks (adjusted ORs: 1.17–1.37), and at only marginally greater risk at 29 to 31 weeks (adjusted ORs: 1.08–1.14). There did not seem to be any particular survival advantage for boys or girls according to mode of delivery.

The observation of reduced neonatal mortality rates for infants delivered through cesarean section at the threshold of viability has serious implications for counseling parents on the options for delivery. As discussed by the American Academy of Pediatrics, Committee on Fetus and Newborn,3 not only the likelihood of survival but also the likelihood of neurodevelopmental disability should be discussed. Although Wilson-Costello et al4 suggested some improvement in neurodevelopmental outcomes over time in extremely low birth weight infants, others reports did not show improvement.40,41 The likelihood of only 23% to 24% of infants born at 23 and 24 weeks, respectively, being unimpaired may cause pause regarding aggressive therapy among some families.40 The fact that motor and executive function at 6 years of age in extremely preterm infants without cerebral palsy and in mainstream education programs may be diminished adds to the concern regarding the ultimate outcomes of this high-risk population.42 The issue of the virtue of survival at all costs thus remains a highly personal decision.

The use of vital statistics data to assess outcomes among very preterm infants has limitations. As addressed above, the validity of the recorded gestational age may be in question because of dependence on last menstrual period dates, on which the vast majority of gestational ages were based (95.4% in 2003). However, this analysis attempted to circumvent this problem by focusing on a very restricted group of records that were well within birth weight ranges published by others using trimmed data sets.23,24 Information on maternal characteristics recorded in vital statistics data seems valid; however, medical, pregnancy, and labor and delivery complications may well be underreported.20 Therefore, the observation of a reduction in the neonatal mortality rate for the preterm infants at 22 to 25 weeks of gestation may reflect the protective effect of cesarean section for a complication not reported. In addition, the validity of the information regarding the occurrence of mechanical ventilation at delivery is not known. Many of these infants may receive nasal continuous positive airway pressure treatment at birth, which may or may not be considered mechanical ventilation by the birth certificate recorders. There does not seem to be any reason, however, why greater underascertainment of the use of nasal continuous positive airway pressure treatment would occur for one mode of delivery than for the other.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
This analysis of very preterm infants at 22 to 31 weeks of gestation demonstrated a significantly reduced OR for neonatal death among infants delivered through primary cesarean section between 22 and 25 weeks of gestation, independent of a number of risk factors that might indicate the need for cesarean section. For pregnancies in which ≥1 risk factor was present, infants delivered through cesarean section had odds for neonatal death that were either significantly reduced or approached significance for every gestational age examined. Although the choice of cesarean section for the most immature of these infants may offer survival advantages, consideration of the neurodevelopmental risks associated with survival at this early age and consideration of the maternal costs of cesarean section also must be taken into account.


   FOOTNOTES
 
Accepted Nov 9, 2007.

Address correspondence to Michael H. Malloy, MD, MS, Department of Pediatrics, University of Texas Medical Branch, 301 University Blvd, Galveston, TX 77555-0526. E-mail: mmalloy{at}utmb.edu

These data were presented in part at the annual meeting of the Pediatrics Academic Societies; May 8, 2007; Toronto, Ontario, Canada.

The author has indicated he has no financial relationships relevant to this article to disclose.


What's Known on This Subject

There is lack of consensus regarding whether cesarean section offers survival advantages in the delivery of extremely preterm infants.

 

What This Study Adds

This study observed increased survival rates among infants delivered through cesarean section at 22 to 25 weeks of gestation.

 


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Hamilton BE, Martin JA, Ventura SJ. Births: preliminary data for 2005. Natl Vital Stat Rep. 2006;55 (11):1 –18[Medline]
  2. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2003. Natl Vital Stat Rep. 2005;54 (2):1 –116[Medline]
  3. MacDonald H, American Academy of Pediatrics, Committee on Fetus and Newborn. Perinatal care at the threshold of viability. Pediatrics. 2002;110 (5):1024 –1027[Abstract/Free Full Text]
  4. Wilson-Costello D, Friedman H, Minich N, et al. Improved neurodevelopmental outcomes for extremely low birth weight infants in 2000–2002. Pediatrics. 2007;119 (1):37 –45[Abstract/Free Full Text]
  5. Mathews TJ, MacDorman MF. Infant mortality statistics from the 2004 period linked birth/infant death data set. Natl Vital Stat Rep. 2007;55 (14):1 –32[Medline]
  6. Stewart AL, Turcan DM, Rawlings G, Reynolds EOR. Prognosis for infants weighing 1000 g or less at birth. Arch Dis Child. 1977;52 (2):97 –104[Abstract/Free Full Text]
  7. Williams RL, Chen PM. Identifying the sources of the recent decline in perinatal mortality rates in California. N Engl J Med. 1982;306 (4):207 –214[Abstract]
  8. Sachs BP, McCarthy BJ, Rubin G, Burton A, Terry J, Tyler CW. Cesarean section: risk and benefits for mother and fetus. JAMA. 1983;250 (16):2157 –2159[Abstract/Free Full Text]
  9. Malloy MH, Rhoads GG, Schramm W, Land G. Increasing cesarean section rates in very low-birth weight infants. JAMA. 1989;262 (11):1475 –1478[Abstract/Free Full Text]
  10. Malloy MH, Onstad L, Wright E, National Institute of Child Health and Human Development Neonatal Research Network. The effect of cesarean delivery on birth outcome in very low birth weight infants. Obstet Gynecol. 1991;77 (4):498 –503[Web of Science][Medline]
  11. Holmgren PA, Högberg U. The very preterm infant: a population-based study. Acta Obstet Gynecol Scand. 2001;80 (6):525 –531[CrossRef][Web of Science][Medline]
  12. Lumley J. Method of delivery for the preterm infant. BJOG. 2003;110 (suppl 20):88 –92[Web of Science][Medline]
  13. Riskin A, Riskin-Mashiah S, Lusky A, Reichman B. The relationship between delivery mode and mortality in very low birthweight singleton vertex-presenting infants. BJOG. 2004;111 (12):1365 –1371[Web of Science][Medline]
  14. Håkansson S, Farooqi A, Holmgren PA, Högberg U. Proactive management promotes outcome in extremely preterm infants: a population-based comparison of two perinatal management strategies. Pediatrics. 2004;114 (1):58 –64[Abstract/Free Full Text]
  15. Högberg U, Håkansson S, Serenius F, Holmgren PA. Extremely preterm cesarean delivery: a clinical study. Acta Obstet Gynecol Scand. 2006;85 (12):1442 –1447[Web of Science][Medline]
  16. Lee HC, Gould JB. Survival advantage associated with cesarean delivery in very low birth weight vertex neonates. Obstet Gynecol. 2006;107 (1):97 –105[Web of Science][Medline]
  17. 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 (6). Available at: www.pediatrics.org/cgi/content/full/118/6/e1836
  18. Bottoms SF, Paul RH, Iams JD, et al. Obstetric determinants of neonatal survival: influence of willingness to perform cesarean delivery on survival of extremely low-birth-weight infants. Am J Obstet Gynecol. 1997;176 (5):960 –966[CrossRef][Web of Science][Medline]
  19. National Center for Health Statistics. United States Linked Birth/Infant Death Period Public Use Files, Years 2000, 2001, 2002, and 2003. Hyattsville, MD: National Center for Health Statistics; 2003
  20. National Center for Health Statistics. Vital Statistics of the United States, 2003: Technical Appendix, Natality. Hyattsville, MD: National Center for Health Statistics; 2005:26 –27
  21. National Center for Health Statistics. Instruction Manual Part 12: Computer Edits for Natality Data, Effective 1993: Vital Statistics, Data Preparation. Hyattsville, MD: National Center for Health Statistics; 1995:33 –35. Available at: www.cdc.gov/nchs/data/dvs/instr12.pdf. Accessed June 10, 2008
  22. Williams RL. Appendix: final report for contract 75–5395 (MCH). In: Cunningham GC, Hawes WE, Madore C, et al, eds. Intrauterine Growth and Neonatal Risk in California. Santa Barbara, CA: University of California Community and Organization Research Institute; 1976:16
  23. Malloy MH, Hoffman HJ. Prematurity, sudden infant death syndrome, and age of death. Pediatrics. 1995;96 (3):464 –471[Abstract/Free Full Text]
  24. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol. 1996;87 (2):163 –168[CrossRef][Web of Science][Medline]
  25. Arnold CC, Kramer MS, Hobbs CA, McLean FH, Usher RH. Very low birth weight: a problematic cohort for epidemiological studies of very small or immature neonates. Am J Epidemiol. 1991;134 (6):604 –613[Abstract/Free Full Text]
  26. Hellmann J, Baylis F. Ethics in perinatal and neonatal medicine. In: Martin RJ, Fanaroff AA, Walsh MC, eds. Neonatal-Perinatal Medicine. 8th ed. Philadelphia, PA: Mosby-Elsevier; 2006:39 –40
  27. MacDorman MF, Declercq E, Menacker F, Malloy MH. Infant and neonatal mortality for primary cesarean and vaginal births to women with "no indicated risk," United States, 1998–2001 birth cohorts. Birth. 2006;33 (3):175 –182[CrossRef][Web of Science][Medline]
  28. Vadnais M, Sachs B. Maternal mortality with cesarean delivery: a literature review. Semin Perinatol. 2006;30 (5):242 –246[CrossRef][Web of Science][Medline]
  29. Wax JR. Maternal request cesarean versus planned spontaneous vaginal delivery: maternal morbidity and short term outcomes. Semin Perinatol. 2006;30 (5):247 –252[CrossRef][Web of Science][Medline]
  30. Liu S, Liston RM, Joseph KS, Heaman M, Sauve R, Kramer MS. Maternal mortality and severe morbidity associated with low-risk planned cesarean delivery versus planned vaginal delivery at term. CMAJ. 2007;176 (4):455 –460[Abstract/Free Full Text]
  31. Hillemanns P, Hasbargen U, Strauss A, Schulze A, Boroviczeny O, Hepp H. Maternal and neonatal morbidity of emergency caesarean sections with a decision-to-delivery interval under 30 minutes: evidence from 10 years. Arch Gynecol Obstet. 2003;268 (3):136 –141[CrossRef][Medline]
  32. Jain L, Eaton DC. Physiology of fetal lung fluid clearance and the effect of labor. Semin Perinatol. 2006;30 (1):34 –43[CrossRef][Web of Science][Medline]
  33. Jain L, Dudell GG. Respiratory transition in infants delivered by cesarean section. Semin Perinatol. 2006;30 (5):296 –304[CrossRef][Web of Science][Medline]
  34. Saugstad OD. Bronchopulmonary dysplasia: oxidative stress and antioxidants. Semin Neonatol. 2003;8 (1):39 –49[CrossRef][Medline]
  35. Back SA, Rivkees SC. Emerging concepts in periventricular white matter injury. Semin Perinatol. 2004;28 (6):405 –414[CrossRef][Web of Science][Medline]
  36. Gupta M, Mestan KK, Martin CR, et al. Impact of clinical and histologic correlates of maternal and fetal inflammatory response on gestational age in preterm births. J Matern Fetal Neonatal Med. 2007;20 (1):39 –46[CrossRef][Web of Science][Medline]
  37. Thornburg KL. Fetal response to intrauterine stress. Ciba Found Symp. 1991;156 :17 –29[Medline]
  38. Kanaka-Gantenbein C, Mastorakos G, Chrousos GP. Endocrine-related causes and consequences of intrauterine growth retardation. Ann N Y Acad Sci. 2003;997 :150 –157[CrossRef][Web of Science][Medline]
  39. Stevenson DK, Verter J, Fanaroff AA, et al. Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage. Arch Dis Child Fetal Neonatal Ed. 2000;83 (3):F182 –F185[Abstract/Free Full Text]
  40. Hintz SR, Kendrick DE, Vohr BR, Poole WK, Higgins RD. Changes in neurodevelopmental outcomes at 18 to 22 months' corrected age among infants of less than 25 weeks' gestational age born in 1993–1999. Pediatrics. 2005;115 (6):1645 –1651[Abstract/Free Full Text]
  41. Tommiska V, Heinonen K, Lehtonen L, et al. No improvement in outcome of nationwide extremely low birth weight infant populations between 1996–1997 and 1999–2000. Pediatrics. 2007;119 (1):29 –36[Abstract/Free Full Text]
  42. Marlow N, Hennessy EM, Bracewell MA, Wolke D. Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics. 2007;120 (4):793 –803[Abstract/Free Full Text]
PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics

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One-Year Survival of Extremely Preterm Infants After Active Perinatal Care in Sweden
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