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ORIGINAL RESEARCH |
From the 1Division of Epidemiology and Biostatistics and the 2Department of Obstetrics, Gynecology, and Reproductive Sciences, UMDNJ-Robert Wood Johnson Medical School, New Brunswick, New Jersey; the 3Department of Epidemiology, UMDNJ-School of Public Health; 4Department of Maternal and Child Health, University of Alabama at Birmingham, Birmingham, Alabama; and 5Council on African American Affairs, Washington, DC.
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ABSTRACT |
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METHODS: The Missouri maternally linked cohort data set containing births from 1978 through 1997 was used. We identified a cohort of women who delivered live births by cesarean delivery and a comparison cohort of women who delivered live births vaginally in their first pregnancies. We then compared the risks of stillbirth in the second pregnancy between the 2 groups.
RESULTS: We analyzed 396,441 women with information on first and second pregnancies, comprising 71,950 (18.1%) in the cesarean arm, and 324,491 (81.9%) in the vaginal birth arm. Rates of stillbirth among women with and those without history of cesarean delivery were 4.4 and 4.1 per 1,000 births, respectively (P = .2). The adjusted estimates also showed no difference in risk for stillbirth between the 2 groups (odds ratio [OR] 1.1, 95% confidence interval [CI] 1.0–1.3). Among whites, the stillbirth rates in women with and those without history of cesarean delivery were 3.7 and 3.6 per 1,000 births, respectively (OR 1.0, 95% CI 0.9–1.2). Among blacks, both the absolute and the adjusted relative risks for stillbirth were elevated in mothers with history of cesarean delivery (stillbirth rate 9.3 versus 6.8 per 1,000 births; OR 1.4, 95% CI 1.1–1.7).
CONCLUSION: Overall, our analysis did not detect an association between cesarean history and subsequent stillbirth. However, cesarean delivery may increase the risk for subsequent stillbirth among black mothers, a group with the highest cesarean delivery rate in the country.
Level of Evidence: III
Cesarean delivery impacts subsequent pregnancy outcomes of both the mother and her fetus. Uteroplacental bleeding disorders, including uterine rupture, placental abruption, and previa, occur at higher frequencies in women who have previously undergone a cesarean delivery.4,5 It has been found that, even with a stable uterine scar, the risk for stillbirth is higher in women with a history of a primary cesarean delivery after adjusting for other potential confounding factors.
However, whether an independent association exists between cesarean delivery and subsequent risk of stillbirth still remains poorly defined. In addition, in the United States, racial differences (notably between blacks and whites) in patient risk profiles and maternal and fetal outcomes, as well as likelihood of receipt of cesarean delivery, have been observed. The disparity in the number of stillbirth events between blacks and whites has been shown to be significantly influenced by biologic characteristics such as the number of fetuses in the uterus.10 We, therefore, conducted this analysis with the following working hypotheses: 1) a history of cesarean delivery is a risk factor for stillbirth, and 2) a history of cesarean delivery is a greater risk factor for subsequent stillbirth in blacks than in whites.
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MATERIALS AND METHODS |
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The Missouri maternally linked cohort data contains information on both live birth and fetal death for each sibling and provides a platform for a longitudinal study of birth outcomes for each pregnancy. Women who had 2 sequential singleton pregnancies beyond 20 weeks of gestation were selected. Figure 1 summarizes the sequential selection process that determined inclusion in the study. With regard to congenital anomalies, data for this item relate to 21 specific anomalies or anomaly groups including chromosomal aberrations. Women who delivered a liveborn infant in their first pregnancy were followed in their second pregnancy to determine pregnancy outcome. They were categorized into a study group (consisting of those who underwent a cesarean delivery in the first pregnancy) and a comparison group (those who had vaginal delivery in the first pregnancy). Subsequently, in their second pregnancy, we compared the 2 arms with respect to the occurrence of stillbirth (in utero fetal death at 
20 weeks). The interval between the first day of the last menstrual period (LMP) and the date of birth was used to compute gestational age in completed weeks.
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It is well known that certain maternal characteristics (eg, age of the mother) could influence birth outcomes in general. However, because the end point of interest in this study (namely, stillbirth in the subsequent pregnancy) was more likely to be influenced by the maternal characteristics in the second pregnancy than in the first, we compared the following sociodemographic characteristics between the 2 groups in the second pregnancy and also adjusted for them in subsequent multivariable analyses: maternal age (< 35 years and 35 years), educational level attained (< 12 years and 12 years), race/ethnicity (black versus white), marital status (married, single), reported use of tobacco during pregnancy (yes, no), adequacy of prenatal care (adequate and inadequate), and body mass index (BMI, expressed as kg/m2). We categorized BMI into 4 groups: underweight (< 19.8), normal (19.8–26.0), overweight (26.1–29.0), and obese (> 29.0), based on previous publication.15 Adequacy of prenatal care was assessed with the Revised Graduated Index of Prenatal Care Utilization (R-GINDEX) algorithm.16,17 The R-GINDEX assesses the adequacy of care based on 3 variables (trimester during which prenatal care began, number of visits, and the gestational age of the infant at birth).
We performed crude frequency comparisons for the presence of common obstetric complications, namely, anemia, cardiac disease, type 1 diabetes, other types of diabetes mellitus, chronic hypertension, preeclampsia, eclampsia, abruptio placenta, and placenta previa. We also constructed a composite variable indicating the presence of at least one of these conditions.
We conducted univariate analysis and evaluated differences in proportions by means of the 
2 test, and for continuous variables the Student t test was applied. The independent association between prior cesarean delivery and the occurrence of stillbirth in a subsequent pregnancy was assessed by means of an unconditional multivariable logistic regression modeling. The multivariate adjusted models included the following covariates: maternal age, parity, marital status, educational status, cigarette smoking during pregnancy, body mass index, interpregnancy interval, adequacy of prenatal care, and year of birth. The odds ratios generated were used to approximate relative risks. Missing values for a particular variable were dealt with by constructing a variable vector that contained the missing noncontributory information. This vector was not included in the adjusted models because it contributed no information.
All tests of hypothesis were 2-tailed, with a type 1 error rate fixed at 5%. This study was approved by the Institutional Review Board for human subjects at the University of Alabama at Birmingham.
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RESULTS |
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Pregnant women who had cesarean delivery in their first pregnancy were more likely to have medical complications such as anemia, cardiac disease, diabetes mellitus (insulin-dependent and other forms of diabetes), and chronic hypertension than their counterparts. Other pregnancy complications, such as preeclampsia, eclampsia, abruption placenta, and placenta previa, were also more prevalent in this group (Table 2).
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We compared the incidence of small for gestational age (SGA) and preterm delivery in the first pregnancy. Women who underwent a cesarean delivery had a similar incidence of SGA as did those who did not (10.7% versus 10.7%; P = .7). With respect to preterm delivery, significant differences were noted in the first pregnancy between the 2 maternal cohorts. Mothers who experienced a cesarean delivery had a higher rate of preterm infants (10.0% versus 8.9%; P < .001). There was no significant difference (P = .2) between women exposed (mean ± standard deviation 979 ± 781 days) and those unexposed (984 ± 847 days) to a cesarean delivery in terms of the interval between the first and the second pregnancy (interpregnancy interval).
In total, there were 1,612 cases of stillbirth in the second pregnancy; 19.4% of these cases occurred in mothers with a history of cesarean and 80.6% among those without such history. There were no differences in the absolute risk for stillbirth between the 2 maternal categories; 4.4/1,000 versus 4.1/1,000 for those with history of cesarean delivery and those without, respectively (P = .2). The absolute risk of stillbirth in subsequent pregnancy varied by race, with blacks showing a significantly higher stillbirth rate than whites (7.2/1,000 versus 3.6/1,000; P < .001). We also examined stillbirth rates for blacks and whites across gestational age couplets. The absolute risk for stillbirth declined with advancing gestational age regardless of race (P = .03). Black fetuses had a survival advantage early during pregnancy, up to around the 32nd week of gestational when the absolute risk reversed in favor of whites.
Upon stratification by prior mode of delivery, the absolute risk of stillbirth was comparable for white mothers, with (3.7/1,000) or without (3.6/1,000) a history of cesarean delivery (P = .5). By contrast, black mothers were more likely to experience a stillbirth in subsequent pregnancy when they had a cesarean delivery in their first pregnancy (9.3/1,000) than if they had delivered vaginally (6.8/1,000) (P = .001).
In Table 3, we present adjusted odds ratios for the association between exposure to a cesarean in the first pregnancy and subsequent risk of stillbirth. Overall, the results showed no significant association between prior cesarean and subsequent risk of fetal death (P = .2), a finding that was also observed among whites. However, when the analysis was restricted to black mothers, a 40% higher likelihood of stillbirth in the second pregnancy was detected in gravidas with a cesarean delivery in the first pregnancy (P = .02). We further examined the data by stratifying the adjusted estimates into 3 gestational age periods (based on the time of occurrence of the stillbirth in the second pregnancy) to determine whether the estimates varied with advancing fetal age (Table 4). The overall risk for stillbirth in the second pregnancy did not change across the gestational age categories, and the level of risk for stillbirth remained similar for both mothers with a cesarean delivery history in the first pregnancy and those without. A similar result was obtained among white gravidas. The adjusted risk for stillbirth in the second pregnancy among blacks was higher (between 40–50%) in those mothers who experienced a cesarean delivery in the first gestation although the only significant finding was for births at or beyond 35 gestational weeks in the second pregnancy. This could have been attributable to the relative paucity of counts of stillbirth in the earlier gestational ages (57 cases of stillbirth in 28–31 weeks, and 59 cases of stillbirth in the 32–35 weeks stratum) as compared with the later part of pregnancy (288 cases in the 35 gestational age stratum).
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We finally examined the data to estimate whether medical complications associated with pregnancy could be a pathway in our findings. The results are as displayed in Table 5. In both racial groups, there was no appreciable change in the adjusted odds ratios.
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DISCUSSION |
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Previous investigators have reported a raised level of risk for stillbirth resulting from cesarean delivery among Scottish gravidas.8 Although we did not observe a heightened risk in the general population, we did note that black women who had cesarean delivery exhibited a higher-than-expected likelihood for subsequent stillbirth. Stratified analysis by gestational age did not show any significant variation in risk in the entire population as well as in white women. The risk noted in black women was equivalent in magnitude across gestational age categories but reached statistical significance from 35 gestational weeks onward. The elevated risk for subsequent fetal death in black women who underwent a cesarean delivery in their first pregnancy is of concern because 1 of 3 black gravidas is currently delivered by cesarean delivery nationwide, and black women have the highest cesarean delivery rates of all racial groups.13
The consistency between the findings in the general population and the results in white women is easy to understand because white women represent the overwhelming majority in the state, and hence the overall result in the population reflects this subgroup dominance. On the other hand, it is difficult to explain the discordance in study findings in black women compared with those in white women when analysis was performed separately. It may be argued that black fetuses may have a higher susceptibility threshold to stillbirth than whites. A recent population-based analysis did demonstrate convincingly that, in both singleton and multiple births, black fetuses have lower in utero survival probabilities than their white counterparts.10 However, it is reasonable to expect the black-white disparity in stillbirth to be nondifferential (ie, both black women with prior cesarean history and those without should be expected to have higher rates of stillbirth than whites), and hence, this could not have explained our results. Higher rates of stillbirth among black women who underwent a cesarean delivery might be accounted for by increased frequency of maternal diseases and obstetric complications of pregnancy. However, the analysis that examined the role of common pregnancy-associated complications in this regard yielded results consistent with an overall independent association between prior cesarean and subsequent risk of stillbirth.
The association between prior cesarean in black women and risk of stillbirth in subsequent pregnancy may have some biologic explanation.8 Unintentional ligation of major uterine vessels during cesarean delivery in the first pregnancy could impact uterine blood flow in a subsequent pregnancy. This is, however, mere speculation because we are not aware of any study that has examined the pattern of uterine and fetal blood flow in pregnancies preceded by a prior cesarean birth. In addition, there is no reason to believe that unintentional uterine ligation should only occur in black women and not in white women undergoing cesarean delivery. Cesarean delivery per se is a precursor of abnormal placentation in subsequent pregnancies leading to abruption, placenta previa, and placenta accreta.4,5,18 Although our data provided information on placental abruption and previa, the presence or absence of abnormal placental adherence is not routinely documented. Consequently, the results generated from the multivariable model we constructed, which included variables of placental anomalies, might have been biased by the lack of complete information in this regard. It is, therefore, prudent to interpret our findings with this limitation in mind.
One limitation of this study is our inability to provide information on causes of stillbirths because the relevant data as indicated on birth certificates are not reliable. In a study carried out in 5 states, Kirby19 reported that approximately 30–45% of reports of causes of fetal death from vital records were not valid or useful. We also do not have data for the evaluation of the stillbirth (for example, infectious etiology, antiphospholipid syndrome evaluation, gross and pathology assessment of the fetus and placenta, and fetal autopsy and chromosomal analysis). Another limitation of the data to bear in mind in making interpretations is the long period of follow-up of these women, which spanned more than 20 years. Different infant cohorts were aggregated and analyzed together. Because these babies were probably exposed to varying obstetric practices across the period of study, the results we have presented might have been biased by this cohort effect. However, the divergent findings in blacks and whites cannot reasonably be explained by this potential source of bias. In addition, we also controlled for year of birth in the adjusted models.
The data source for this study is relatively accurate and complete in its ascertainment. Indeed, the Missouri data set has been adopted as the gold standard in gauging the accuracy of information documented and the verification procedures conducted on certain national vital record data files.13 Despite this merit, it should be understood that the results of this study should provide reasons for more refined studies to elucidate the potential relationship between cesarean delivery and subsequent stillbirth, rather than be construed as a basis for patient counseling in the clinical setting. On the other hand, the positive findings in black women constitute a strong reason to examine the current upsurge in cesarean delivery rates driven mostly by physician behavior, institutional factors, and increasing patient demand rather than by patient risk profiles.3
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Footnotes |
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This work was supported through a Young Clinical Scientist Award to Dr. Salihu by the Flight Attendant Medical Research Institute (FAMRI). The funding agency did not play any role in any aspect of the study. Dr. Ananth is partially supported through a grant (R01-HD038902) from the National Institutes of Health. The authors thank the staff of the Missouri Vital Statistics Department for access to the database.
Corresponding author: Hamisu Salihu, MD, PhD, Department of Obstetrics, Gynecology, and Reproductive Sciences, UMDNJ-Robert Wood Johnson Medical School, New Brunswick, NJ 08901-1977; e-mail: hamisu.salihu{at}gmail.com.
doi:10.1097/01.AOG.0000195103.46999.32
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REFERENCES |
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2. Hamilton BE, Martin JA, Sutton PD. Births: preliminary data for 2003. Natl Vital Stat Rep 2004;53:1–17.[Medline]
3. Bailit JL, Love TE, Mercer B. Rising cesarean rates: are patients sicker? Am J Obstet Gynecol 2004;191:800–3.[Medline]
4. Lydon-Rochelle M, Holt VL, Easterling TR, Martin DP. First-birth cesarean and placental abruption or previa at second birth. Obstet Gynecol 2001;97:765–9.
5. Hemminki E, Merilainen J. Long-term effects of cesarean sections: ectopic pregnancies and placental problems. Am J Obstet Gynecol 1996;174:1569–74.[Medline]
6. Lydon-Rochelle M, Holt VL, Easterling TR, Martin DP. Risk of uterine rupture during labor among women with a prior cesarean delivery. N Engl J Med 2001;345:3–8.
7. Smith GCS, Pell JP, Cameron AD, Dobbie R. Risk of perinatal death associated with labor after previous cesarean delivery in uncomplicated term pregnancies. JAMA 2002;287:2684–90.
8. Smith GC, Pell JP, Dobbie R. Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet 2003;362:1779–84.[Medline]
9. Salihu HM, Chatman LM, Alio AP, Aliyu MH, Kirby RS, Alexander GR. Single motherhood and neonatal survival of twins among blacks and whites. J Natl Med Assoc 2004;96:1618–25.[Medline]
10. Salihu HM, Kinniburgh BA, Aliyu MH, Kirby RS, Alexander GR. Racial disparity in stillbirth among singleton, twin, and triplet gestations in the United States. Obstet Gynecol 2004;104:734–40.
11. Salihu HM, Williams AT, McCainey TN, Kirby RS, Alexander GR. Early mortality among triplets in the United States: black-white disparity. Am J Obstet Gynecol 2004;190:477–84.[Medline]
12. Salihu HM, Alexander MR, Shumpert MN, Pierre-Louis BJ, Alexander GR. Infant mortality among twins born to teenagers in the United States. Black-white disparity. J Reprod Med 2003;48:257–67.[Medline]
13. Martin J, Curtin S, Saulnier M, Mousavi J. Development of the matched multiple birth file. In: 1995–1998 matched multiple birth dataset. Vital and Health Statistics CD-ROM Series 21, No. 13a. Hyattsville (MD): National Center for Health Statistics; 2003.
14. Herman AA, McCarthy BJ, Bakewell JM, Ward RH, Mueller BA, Maconochie NE, et al. Data linkage methods used in maternally-linked birth and infant death surveillance datasets from the United States (Georgia, Missouri, Utah and Washington State), Israel, Norway, Scotland and Western Australia. Paediatr Perinat Epidemiol 1997; 11 suppl: 5–22.[Medline]
15. Kuczmarski RJ, Flegal KM. Criteria for definition of overweight in transition: background and recommendations for the United States. Am J Clin Nutr 2000;72:1074–81.
16. Alexander GR, Kotelchuck M. Quantifying the adequacy of prenatal care: a comparison of indices. Public Health Rep 1996;111:408–18.[Medline]
17. Alexander GR, Cornely DA. Prenatal care utilization: its measurement and relationship to pregnancy outcome. Am J Prevent Med 1987;3:243–53.[Medline]
18. Rasmussen S, Irgens LS, Dalaker K. A history of placental dysfunction and risk of placental abruption. Paediatr Perinat Epidemiol 1999;13:9–21.[Medline]
19. Kirby RS. The coding of underlying cause of death from fetal death certificates: issues and policy considerations. Am J Public Health 1993;83:1088–91.
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  H. M. Salihu, A.-L. Dunlop, M. Hedayatzadeh, A. P. Alio, R. S. Kirby, and G. R. Alexander Extreme Obesity and Risk of Stillbirth Among Black and White Gravidas Obstet. Gynecol., September 1, 2007; 110(3): 552 - 557. [Abstract] [Full Text] [PDF]
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