Obesity: Original Research
Trial of Labor Compared With Cesarean Delivery in Superobese Women Jennifer L. Grasch, MD, Jennifer L. Thompson, and Sarah S. Osmundson, MD, MS
MD,
OBJECTIVE: To examine whether labor compared with planned cesarean delivery is associated with increased maternal and neonatal morbidity. METHODS: We conducted a retrospective cohort study of all women with body mass indexes (BMIs) at delivery of 50 or greater delivering a live fetus at 34 weeks of gestation of greater between January 1, 2008, and December 31, 2015. Pregnancies with multiple gestations and major fetal anomalies were excluded. The primary outcome was a composite of maternal and neonatal morbidity and was estimated to be 50% in superobese women based on institutional data. A sample size of 338 women determined the study period and was selected to show a 30% difference in the incidence of the primary outcome between the two groups. Multivariate logistic regression adjusted for potential confounders. RESULTS: There were 344 women with BMIs of 50 or greater who met eligibility criteria, of whom 201 (58%) labored and 143 (42%) underwent planned cesarean delivery. Women who labored were younger, more likely to be nulliparous, and less likely to have pre-existing diabetes. Among women who labored, 45% underwent a cesarean delivery, most commonly for labor arrest (61%) or nonreassuring fetal status (28%). Composite maternal and neonatal morbidity was reduced among women who labored even after adjusting for age, parity, pre-existing diabetes, and prior cesarean delivery (adjusted odds ratio 0.42, 95% CI 0.24–0.75). In the sub-
From the Vanderbilt University Medical Center, Nashville, Tennessee. Presented at the Society for Maternal-Fetal Medicine Annual Meeting, January 22–28, 2017, Las Vegas, Nevada. Each author has indicated that he or she has met the journal’s requirements for authorship. Corresponding author: Jennifer L. Grasch, MD, 1161 21st Avenue South, B1118 MCN, Nashville, TN 37232; email: [email protected]. Financial Disclosure The authors did not report any potential conflicts of interest. © 2017 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0029-7844/17
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J. Michael Newton,
MD, PhD,
Amy W. Zhai,
MD,
group of women (n5234) who underwent a cesarean delivery, whether planned (n5143) or after labor (n591), there were no differences in maternal and neonatal morbidity except that severe maternal morbidity was increased in women (n512) who labored (8.8% compared with 2.1%, relative risk 4.2, 95% CI 1.14–15.4). CONCLUSION: Despite high rates of cesarean delivery in women with superobesity, labor is associated with lower composite maternal and neonatal morbidity. Severe maternal morbidity may be higher in women who require a cesarean delivery after labor. (Obstet Gynecol 2017;0:1–7) DOI: 10.1097/AOG.0000000000002257
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n the United States, the prevalence of obesity has increased dramatically over the past three decades, reaching epidemic proportions. Almost 40% of adult women are obese, and approximately 8% are extremely obese (body mass index [BMI, calculated as weight (kg)/[height (m)]2] 40 or greater).1,2 Superobesity is defined by the National Institutes of Health Consensus Development Panel as a BMI 50 or greater2,3 Although once rare, the prevalence of superobesity has increased fivefold in the past 20 years and is estimated to be 1–2% of the obstetric population.4,5 Multiple studies support an association between maternal obesity and perinatal morbidity, often in a dose-dependent manner.6–10 Less clear is how to approach delivery in this population. In general, vaginal delivery is associated with reduced maternal and neonatal morbidity.11–13 However, with overall cesarean delivery rates as high as 50% in superobese women,5,14,15 the risk that trial of labor will result in cesarean delivery is substantial. Compared with planned cesarean delivery, a failed trial of labor can be associated with worse maternal and neonatal outcomes, as seen in women undergoing trial of labor after cesarean delivery.16,17 Additionally, the ability to perform an emergent cesarean delivery in laboring
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superobese women, and resulting increased risk of neonatal morbidity, is of concern.16,18 In addition, labor in obese women is associated with greater duration, oxytocin requirements, risk for failed induction, and postpartum hemorrhage compared with women with normal BMI.5,7,14,19 Conversely, primary cesarean delivery in superobese women can be technically challenging and is associated with significant risk for surgical and postoperative complications without clear neonatal benefit.8,14,20,21 Given the present lack of data to inform delivery planning in superobese women, we undertook this study to examine whether trial of labor or planned cesarean delivery is associated with differential maternal and neonatal morbidity in this high-risk and growing population.
MATERIALS AND METHODS This is a retrospective cohort study of all women with BMIs of 50 or greater at delivery admitted for delivery of a viable fetus between January 1, 2008, and December 31, 2015, at Vanderbilt University Medical Center. Women with multiple gestations, carrying fetuses with major anomalies, or delivering at 34 weeks of gestation or less were excluded. These women were excluded because these factors were likely to be significantly associated with neonatal morbidity, independent of the route of the delivery. Major anomalies were defined as any anomaly detected prenatally or postnatally that was directly associated with the need for immediate neonatal interventions, prolonged hospital stay, or neonatal death. After obtaining approval from Vanderbilt University institutional review board, women were identified by extracting height and weight data associated with a delivery from the electronic medical record. For women with multiple pregnancies during the study period, only the first pregnancy was included. Counseling regarding recommended mode of delivery for each patient was left to the discretion of the managing obstetric care provider. The primary exposure was planned cesarean delivery compared with trial of labor, defined as an attempt at vaginal delivery whether induced or spontaneous. Women presenting in spontaneous early labor or with ruptured membranes, but who had planned for and underwent a cesarean delivery, were included in the cesarean delivery group. The primary outcome was a composite of maternal and neonatal morbidity. Maternal morbidity included infectious and wound complications, severe
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maternal morbidity as defined by the Centers for Disease Control and Prevention22 (Box 1) and Kuklina et al23 as well as maternal death, readmission within 6 weeks postpartum, reoperation, prolonged length of stay (greater than 2 days for a vaginal delivery, greater than 4 days for a cesarean delivery), uterine rupture, intensive care unit admission, and third- or fourth-degree perineal lacerations. Infectious complications included endometritis (defined as temperature greater than 38°C with fundal tenderness and antibiotic administration), radiographically diagnosed pneumonia, deep tissue abscess, and urinary tract infection (greater than 100,000 colony-forming units/mL of a single uropathogen on urine culture). Wound complications included cellulitis treated with antibiotics, wound separation requiring packing or vacuum, or need for wound exploration. Neonatal morbidity included neonatal or intrapartum death, hypoxic–ischemic encephalopathy (defined as an umbilical cord pH less than 7.0 and seizures or evidence of end-organ damage), neonatal intensive care unit stay greater than 72 hours, sepsis, intraventricular hemorrhage class III or IV, respiratory distress syndrome, umbilical artery pH less than 7.10, and 5-minute Apgar score less than 7. Secondary outcomes were the individual components of the primary outcome. The senior author (SO) reviewed the chart of any patient identified as having experienced a severe maternal morbidity.
Box 1. Severe Maternal Morbidity Indicators as Defined by the Centers for Disease Control and Prevention22
Acute myocardial infarction Acute renal failure Adult respiratory distress syndrome Amniotic fluid embolism Cardiac arrest or ventricular fibrillation Disseminated intravascular coagulation Eclampsia Heart failure or arrest during surgery or procedure Puerperal cerebrovascular disorders Pulmonary edema or acute heart failure Ruptured aneurysm Severe anesthesia complications Sepsis Shock Sickle cell disease with crisis Air and thrombotic embolism Blood transfusion greater than two units Conversion of cardiac rhythm Hysterectomy Temporal tracheostomy Ventilation
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Patient demographic characteristics, comorbidities, and delivery outcomes were extracted from the medical record. A new hypertensive disorder of pregnancy was defined as new blood pressure elevation of greater than 140/90 mm Hg occurring at greater than 20 weeks of gestation. Weight gain in pregnancy was calculated as the difference between the weight recorded closest to delivery and the weight recorded at the first prenatal visit. As a result of changes in the delivery record at our institution, the time from uterine incision to delivery could only be calculated for women delivering after September 15, 2012. All statistical analyses were performed using SAS 9.4. x2 or Fisher exact tests were used to analyze categorical variables where appropriate and Student t test or Mann-Whitney U test was used to analyze continuous variables depending on their distributions. A priori, we planned to examine results in the subgroup of women who underwent a cesarean delivery regardless of whether labor or planned cesarean delivery preceded it. Multivariable logistic regression was performed to examine the relationship between trial of labor and composite maternal and neonatal morbidity by accounting for potential confounding variables. We identified risk factors for maternal and neonatal morbidity using a manual backward elimination model selection that retained only those covariates that were significant at the .05 significance level. Logistic regression examining the relationship between trial of labor and severe maternal morbidity could not be performed as a result of the small number of patients with this outcome. Relative risks and odds ratios were calculated when appropriate. Based on preliminary data, we estimated the incidence of the primary outcome to be 50% in this population. We calculated that a sample size of 338 women would be required to show a 30% difference in the primary outcome with a two-sided a of 0.05 and a power of 80%.
RESULTS During the study period, 434 women with BMI 50 or greater were admitted for delivery with a viable fetus. After excluding 48 women who delivered at less than 34 weeks of gestation, 9 with multiple gestations, and 33 carrying fetuses with major fetal anomalies, the final sample size included 344 women. The median BMI at delivery was 53 with a range of 50–94. Fortyone percent of the total population entered pregnancy with medical comorbidities including 34% with chronic hypertension and 10% with type 2 diabetes. In this population, 58% of women (n5201) experienced labor and 42% (n5143) underwent a cesarean
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delivery without trial of labor. Of women who labored, 45% underwent a cesarean delivery, most commonly for labor arrest (61%) and nonreassuring fetal status (28%). The most common indications for planned cesarean delivery were prior cesarean delivery (69%), suspected macrosomia (8%), and malpresentation (7%). The frequency of cesarean delivery among nulliparous women who labored was 61% (n575/122). Even among women with a prior vaginal delivery, the frequency of cesarean delivery after labor was 21% (n516/77). Nine women underwent trial of labor after cesarean delivery and 44% (4/9) had a successful vaginal birth. Women who labored were younger, more likely to be nulliparous and African American, and less likely to have pregestational diabetes (Table 1). Composite morbidity, which encompassed both maternal and neonatal outcomes, was the primary outcome and was reduced among women who labored [odds ratio (OR) 0.46, 95% CI 0.30–0.72]. After adjusting for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery, this relationship remained significant (adjusted OR 0.42, 95% CI 0.24–0.75) (Table 2). Women who labored also experienced lower risks of the secondary outcomes of infectious, wound, and neonatal morbidity (Table 3). Risk of severe maternal morbidity was not statistically different in women who labored compared with those who underwent planned cesarean delivery. Of the 12 cases of severe maternal morbidity, one occurred in a woman who underwent a vaginal delivery. This patient was admitted 3 weeks postpartum with fever, hypotension, and had blood and urine cultures positive for Escherichia coli, consistent with urosepsis. Three cases occurred in women with planned cesarean delivery. The majority of cases (8/ 12) occurred in women who underwent a cesarean delivery after labor. These complications included postpartum hysterectomy, hemorrhagic shock, cardiac arrest, fascial dehiscence, and reoperation for intraabdominal abscess. Finally, we examined the subgroup of 234 women who underwent a cesarean delivery, whether planned (n5143) or after labor (n591). In this group, there were no statistically significant differences in composite, infectious, wound, or neonatal morbidity; however, severe maternal morbidity was significantly increased in women who had labored (8.8% compared with 2.1%, relative risk 4.2, 95% CI 1.14– 15.4). After adjusting for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery, labor was not associated with
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Table 1. Demographic and Clinical Characteristics Variable
Labor (n5201)
Planned Cesarean Delivery (n5143)
P
Maternal age (y) Nulliparity African American race Smoking during pregnancy Public insurance BMI (kg/m2) Pregestational diabetes Chronic hypertension High school education or less Prior cesarean delivery New hypertensive disorder of pregnancy Weight gain in pregnancy (kg) Gestational diabetes Induction of labor Cesarean delivery Vertical skin incision Classic hysterotomy Emergent delivery Time from skin incision to delivery (min)
27.765.5 122 (60.7) 93 (46.2) 29 (14.4) 127 (63.5) 53.3 (51.5–57.4) 13 (6.5) 64 (31.8) 124 (65.3) 9 (4.5) 59 (29.3) 10.8 (5.7–16.8) 29 (14.4) 141 (66.2) 91 (45.3) 16 (17.8) 18 (17.7) 11 (12.1) 17.769.8
30.964.8 20 (14.0) 53 (37.1) 36 (25.2) 104 (73.2) 53.7 (51.5–58.3) 23 (16.1) 53 (37.1) 99 (73.3) 114 (79.7) 32 (22.4) 9.5 (4.1–14.3) 28 (19.6) 0 (0.00) 143 (100.0) 39 (27.5) 37 (28.0) 4 (2.8) 21.6611.5
,.001 ,.001 .09 .06 .06 .47 .004 .31 .12 ,.001 .15 .09 .21 N/A ,.001 .09 .09 .006 .01
BMI, body mass index; N/A, not applicable. Data are mean6SD, n (%), or median (interquartile range) unless otherwise specified.
composite, infectious, or neonatal morbidity. However, labor was associated with increased odds for wound morbidity (OR 2.32, 95% CI 1.01–5.37). Severe maternal morbidity could not be examined in logistic regression as a result of the small number of women with the outcome (n512).
DISCUSSION This study examined delivery strategy—trial of labor compared with planned cesarean delivery—in superobese women (BMI 50 or greater) delivering after 34 weeks of gestation. Our study finds decreased composite maternal and neonatal morbidity in women undergoing trial of labor compared with planned cesarean delivery. Women who undergo cesarean
delivery after trial of labor may have a higher risk of wound complications and severe maternal morbidity compared with women who underwent planned cesarean delivery, but these rare outcomes warrant further study. For most pregnant women, trial of labor is the preferred delivery strategy because the desired outcome—a vaginal delivery—will occur for the majority of women, and vaginal delivery is associated with reduced maternal and neonatal morbidity compared with cesarean delivery.11–13,24 In superobese women, the preferred strategy is less clear. Although the risk of a failed trial of labor is significantly higher in this population, cesarean delivery is technically challenging and associated with high complication
Table 2. Association Between Labor and Maternal and Neonatal Morbidity Unadjusted OR (95% CI)
Morbidity Composite morbidity (n5143) Composite maternal morbidity (n5109) Severe maternal morbidity (n512) Infectious maternal morbidity (n574) Wound morbidity (n581) Composite neonatal morbidity (n569)
0.46 0.59 2.21 0.52 0.48 0.40
(0.30–0.72) (0.31–0.93) (0.59–8.31) (0.31–0.88) (0.29–0.79) (0.24–0.69)
Adjusted OR* (95% CI) 0.42 (0.24–0.75) 0.49 (0.27–0.90) N/A† 0.52 (0.27–1.0) 0.48 (0.25–0.92) 0.87 (0.56–1.34)
Unadjusted RR (95% CI) in the Subgroup of Women Who Underwent Cesarean Delivery (n5235) 1.11 1.27 4.12 1.16 1.23 0.49
(0.88–1.40) (0.94–1.69) (1.12–15.11) (0.78–1.72) (0.87–1.75) (0.25–0.98)
OR, odds ratio; RR, relative risk; N/A, not applicable. For all comparisons, planned cesarean delivery serves as the reference group. * Adjusted for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery. † Unable to perform logistic regression as a result of small number with outcome of severe maternal morbidity.
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Table 3. Maternal and Neonatal Morbidity in Women With Labor Compared With Planned Cesarean Delivery Morbidity
Labor (n5201)
Composite morbidity (primary outcome) Maternal morbidity (composite) Severe maternal morbidity (composite) Cardiac arrest Respiratory failure Sepsis Shock Pulmonary embolism Blood transfusion greater than 2 units Hysterectomy Infectious morbidity Endometritis Pneumonia Deep tissue abscess Wound infections Urinary tract infections Wound complications Cellulitis Wound separation with packing Wound vacuum Wound exploration Other morbidity Maternal death Prolonged length of stay Postpartum readmission Uterine rupture or dehiscence ICU admission 3rd- or 4th-degree laceration Neonatal morbidity (composite) Neonatal death Intrapartum death NICU stay greater than 72 h Neonatal sepsis Intraventricular hemorrhage Respiratory distress syndrome Umbilical artery gas less than 7.10 5-min Apgar score less than 7
68 54 9 1 1 3 2 2 1 2 34 7 0 1 33 5 36 33 19 8 3 0 0 13 19 0 5 1 28 0 1 12 9 1 43 15 5
(33.7) (26.7) (4.5) (0.5) (0.5) (1.5) (1.0) (0.9) (0.5) (1.0) (16.8) (3.5) (0.0) (0.5) (16.3) (2.5) (17.8) (16.3) (9.4) (3.8) (1.5) (0.0) (0.0) (6.4) (9.5) (0.0) (2.5) (0.5) (13.9) (0.0) (0.5) (5.9) (4.5) (0.5) (1.5) (7.4) (2.5)
Planned Cesarean Delivery (n5143) 76 55 3 0 0 1 0 0 2 1 40 2 0 0 38 1 45 40 15 6 3 2 0 6 7 1 3 0 41 2 0 24 10 0 13 13 11
(55.3) (38.7) (2.1) (0.0) (0.0) (0.7) (0.0) (0.0) (1.4) (0.7) (28.2) (1.4) (0.0) (0.0) (26.8) (0.7) (31.7) (28.2) (10.6) (4.6) (2.1) (2.0) (0.0) (4.2) (5.0) (0.7) (2.1) (0.0) (28.9) (1.4) (0.0) (16.9) (7.0) (0.0) (9.2) (9.2) (7.8)
RR (95% CI)
P
0.64 (0.50–0.82) 0.69 (0.50–0.94) 2.13 (0.59–7.73) N/A N/A 2.11 (0.22–20.08) N/A N/A 0.35 (0.03–3.84) 1.4 (0.13–15.36) 0.60 (0.40–0.89) 2.46 (0.52–11.67) N/A N/A 0.61 (0.40–0.92) 3.50 (0.42–29.76) 0.56 (0.38–0.82) 0.58 (0.39–0.87) 0.89 (0.47–1.09) 0.83 (0.29–2.32) 0.70 (0.14–3.43) 0.14 N/A 1.52 (0.59–3.91) 1.90 (0.82–4.41) N/A 1.17 (0.29–4.81) N/A 0.48 (0.31–0.74) N/A N/A 0.35 (0.18–0.68) 0.63 (0.26–1.52) N/A 0.16 (0.05–0.56) 0.81 (0.40–1.65) 0.32 (0.11–0.90)
,.001 .03 .37 1.0 1.0 .65 .51 .51 .57 1.0 .02 .32 N/A 1.0 .02 .41 .004 .01 .82 .72 .69 N/A .38 .12 .41 1.00 1.0 ,.001 0.17 1.0 .002 .30 1.0 .001 .56 .02
RR, relative risk; N/A, not applicable; ICU, intensive care unit; NICU, neonatal intensive care unit. Data are n (%) unless otherwise specified.
rates.5,7–9,15,25–27 Adequate fetal monitoring may be difficult to achieve, especially with a closed cervix and before internal monitors can be placed. Furthermore, incision to delivery times are increased in obese women, which raises issues about the capacity to perform an emergent cesarean delivery in circumstances of nonreassuring fetal status.6,20 These concerns have led some authors to question the value of trial of labor in superobese women. On the other hand, maternal risks associated with cesarean delivery in obese women are well documented. Alanis et al21 found that nearly one in three superobese women have significant complications
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after cesarean delivery. The most common complications are wound and infectious complications, which is consistent with our findings in this study.20 Obese women have higher rates of failed regional anesthesia, are more likely to require general anesthesia, and difficult intubation rates are higher compared with nonobese populations.28–30 The incidence of severe maternal morbidity is greater among women undergoing cesarean delivery, but the relationship to maternal obesity is less clear.22,31,32 Very few studies have examined outcomes of trial of labor in morbidly obese women compared with planned cesarean delivery. Subramaniam et al14
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compared induction of labor with planned cesarean delivery in women with BMIs of 40 or greater. Women in spontaneous labor were excluded. Similar to our study, planned cesarean delivery was not associated with improved overall morbidity. In contrast, our study found a reduction, rather than no difference, in maternal morbidity and no increase in neonatal morbidity among women who underwent trial of labor. Their study raised similar concerns about outcomes of women with a failed trial of labor, although they found higher risks of operative complications and infectious and wound morbidity in this group, which were not found in our study. The consistent findings in both studies of no significant difference in neonatal outcomes suggest that route of delivery should be driven by relative risk of maternal morbidity. A major strength of our study is the data source. Most prior studies in this population use vital records data, which may not provide uniform ascertainment of certain exposures such as trial of labor that are subject to different interpretation by various health care providers. In contrast, our study utilizes detailed review of individual patient charts with predetermined definitions for important exposures, improving proper classification of these exposures. Additionally, our primary focus on the exposure (trial of labor compared with planned cesarean delivery) rather than the outcome (cesarean delivery compared with vaginal delivery) more closely approximates the clinical decision that health care providers encounter when arriving at a delivery strategy for superobese women. Inclusion of women in spontaneous labor makes our study generalizable to the entire population of superobese women. Limitations of our study include its retrospective nature and the inherent biases associated with this study design. In our study, women undergoing trial of labor were different at baseline from women undergoing planned cesarean delivery. Although we attempted to control for these differences, we acknowledge that residual confounding may exist, creating a scenario in which women who are advised to attempt trial of labor are inherently lower risk individuals than women undergoing planned cesarean delivery. Finally, although we decided a priori to examine the subgroup of women who underwent cesarean delivery after laboring, we acknowledge that our sample size may not be large enough to draw conclusions about this population. Among the subgroup of women who underwent cesarean delivery, the finding of no difference between women who experienced trial of labor compared with planned
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cesarean delivery may represent lack of statistical power. The finding of increased severe maternal morbidity in this group also deserves serious consideration. Although the finding is concerning, the small number of women with these outcomes limits our ability to adequately examine this outcome by controlling for differences in baseline characteristics. Similarly, small numbers (n59) limit our ability to examine outcomes of superobese women undergoing trial of labor after cesarean delivery; however, the one intrapartum fetal death in our study occurred in this group. In summary, despite high rates of cesarean delivery among superobese women, trial of labor is associated with decreased risk for maternal morbidity with no difference in neonatal morbidity. These data are useful to inform delivery planning and counseling in this high-risk population and suggest that maternal superobesity alone should not be an indication for cesarean delivery. REFERENCES 1. Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011–2014. NCHS Data Brief 2015:1–8. 2. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 2012;307:491–7. 3. Mason EE, Doherty C, Maher JW, Scott DH, Rodriguez EM, Blommers TJ. Super obesity and gastric reduction procedures. Gastroenterol Clin North Am 1987;16:495–502. 4. Sturn R. Increases in clinically severe obesity in the United States, 1986–2000. Arch Intern Med 2003;163:2146–8. 5. Marshall NE, Guild C, Cheng YW, Caughey AB, Halloran DR. Maternal superobesity and perinatal outcomes. Am J Obstet Gynecol 2012;206:417.e1–6. 6. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, et al. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 2001;25:1175–82. 7. Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 2001;91:436–40. 8. Blomberg M. Maternal obesity, mode of delivery, and neonatal outcome. Obstet Gynecol 2013;122:50–5. 9. Marchi J, Berg M, Dencker A, Olander EK, Begley C. Risks associated with obesity in pregnancy, for the mother and baby: a systematic review of reviews. Obstet Rev 2015;16:621–38. 10. Schummers L, Hutcheon JA, Bodnar LM, Lieberman E, Himes KP. Risk of adverse pregnancy outcomes by prepregnancy body mass index: a population-based study to inform prepregnancy weight loss counseling. Obstet Gynecol 2015; 125:133–43. 11. Burrows LJ, Meyn LA, Weber AM. Maternal morbidity associated with vaginal versus cesarean delivery. Obstet Gynecol 2004;103:907–12. 12. Curtin SC, Gregory KD, Korst LM, Uddin SFG. Maternal morbidity for vaginal and cesarean deliveries, according to pre-
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Trial of Labor Compared With Cesarean Delivery in Superobese Women Jennifer L. Grasch, MD, Jennifer L. Thompson, and Sarah S. Osmundson, MD, MS
MD,
OBJECTIVE: To examine whether labor compared with planned cesarean delivery is associated with increased maternal and neonatal morbidity. METHODS: We conducted a retrospective cohort study of all women with body mass indexes (BMIs) at delivery of 50 or greater delivering a live fetus at 34 weeks of gestation of greater between January 1, 2008, and December 31, 2015. Pregnancies with multiple gestations and major fetal anomalies were excluded. The primary outcome was a composite of maternal and neonatal morbidity and was estimated to be 50% in superobese women based on institutional data. A sample size of 338 women determined the study period and was selected to show a 30% difference in the incidence of the primary outcome between the two groups. Multivariate logistic regression adjusted for potential confounders. RESULTS: There were 344 women with BMIs of 50 or greater who met eligibility criteria, of whom 201 (58%) labored and 143 (42%) underwent planned cesarean delivery. Women who labored were younger, more likely to be nulliparous, and less likely to have pre-existing diabetes. Among women who labored, 45% underwent a cesarean delivery, most commonly for labor arrest (61%) or nonreassuring fetal status (28%). Composite maternal and neonatal morbidity was reduced among women who labored even after adjusting for age, parity, pre-existing diabetes, and prior cesarean delivery (adjusted odds ratio 0.42, 95% CI 0.24–0.75). In the sub-
From the Vanderbilt University Medical Center, Nashville, Tennessee. Presented at the Society for Maternal-Fetal Medicine Annual Meeting, January 22–28, 2017, Las Vegas, Nevada. Each author has indicated that he or she has met the journal’s requirements for authorship. Corresponding author: Jennifer L. Grasch, MD, 1161 21st Avenue South, B1118 MCN, Nashville, TN 37232; email: [email protected]. Financial Disclosure The authors did not report any potential conflicts of interest. © 2017 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0029-7844/17
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J. Michael Newton,
MD, PhD,
Amy W. Zhai,
MD,
group of women (n5234) who underwent a cesarean delivery, whether planned (n5143) or after labor (n591), there were no differences in maternal and neonatal morbidity except that severe maternal morbidity was increased in women (n512) who labored (8.8% compared with 2.1%, relative risk 4.2, 95% CI 1.14–15.4). CONCLUSION: Despite high rates of cesarean delivery in women with superobesity, labor is associated with lower composite maternal and neonatal morbidity. Severe maternal morbidity may be higher in women who require a cesarean delivery after labor. (Obstet Gynecol 2017;0:1–7) DOI: 10.1097/AOG.0000000000002257
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n the United States, the prevalence of obesity has increased dramatically over the past three decades, reaching epidemic proportions. Almost 40% of adult women are obese, and approximately 8% are extremely obese (body mass index [BMI, calculated as weight (kg)/[height (m)]2] 40 or greater).1,2 Superobesity is defined by the National Institutes of Health Consensus Development Panel as a BMI 50 or greater2,3 Although once rare, the prevalence of superobesity has increased fivefold in the past 20 years and is estimated to be 1–2% of the obstetric population.4,5 Multiple studies support an association between maternal obesity and perinatal morbidity, often in a dose-dependent manner.6–10 Less clear is how to approach delivery in this population. In general, vaginal delivery is associated with reduced maternal and neonatal morbidity.11–13 However, with overall cesarean delivery rates as high as 50% in superobese women,5,14,15 the risk that trial of labor will result in cesarean delivery is substantial. Compared with planned cesarean delivery, a failed trial of labor can be associated with worse maternal and neonatal outcomes, as seen in women undergoing trial of labor after cesarean delivery.16,17 Additionally, the ability to perform an emergent cesarean delivery in laboring
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superobese women, and resulting increased risk of neonatal morbidity, is of concern.16,18 In addition, labor in obese women is associated with greater duration, oxytocin requirements, risk for failed induction, and postpartum hemorrhage compared with women with normal BMI.5,7,14,19 Conversely, primary cesarean delivery in superobese women can be technically challenging and is associated with significant risk for surgical and postoperative complications without clear neonatal benefit.8,14,20,21 Given the present lack of data to inform delivery planning in superobese women, we undertook this study to examine whether trial of labor or planned cesarean delivery is associated with differential maternal and neonatal morbidity in this high-risk and growing population.
MATERIALS AND METHODS This is a retrospective cohort study of all women with BMIs of 50 or greater at delivery admitted for delivery of a viable fetus between January 1, 2008, and December 31, 2015, at Vanderbilt University Medical Center. Women with multiple gestations, carrying fetuses with major anomalies, or delivering at 34 weeks of gestation or less were excluded. These women were excluded because these factors were likely to be significantly associated with neonatal morbidity, independent of the route of the delivery. Major anomalies were defined as any anomaly detected prenatally or postnatally that was directly associated with the need for immediate neonatal interventions, prolonged hospital stay, or neonatal death. After obtaining approval from Vanderbilt University institutional review board, women were identified by extracting height and weight data associated with a delivery from the electronic medical record. For women with multiple pregnancies during the study period, only the first pregnancy was included. Counseling regarding recommended mode of delivery for each patient was left to the discretion of the managing obstetric care provider. The primary exposure was planned cesarean delivery compared with trial of labor, defined as an attempt at vaginal delivery whether induced or spontaneous. Women presenting in spontaneous early labor or with ruptured membranes, but who had planned for and underwent a cesarean delivery, were included in the cesarean delivery group. The primary outcome was a composite of maternal and neonatal morbidity. Maternal morbidity included infectious and wound complications, severe
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maternal morbidity as defined by the Centers for Disease Control and Prevention22 (Box 1) and Kuklina et al23 as well as maternal death, readmission within 6 weeks postpartum, reoperation, prolonged length of stay (greater than 2 days for a vaginal delivery, greater than 4 days for a cesarean delivery), uterine rupture, intensive care unit admission, and third- or fourth-degree perineal lacerations. Infectious complications included endometritis (defined as temperature greater than 38°C with fundal tenderness and antibiotic administration), radiographically diagnosed pneumonia, deep tissue abscess, and urinary tract infection (greater than 100,000 colony-forming units/mL of a single uropathogen on urine culture). Wound complications included cellulitis treated with antibiotics, wound separation requiring packing or vacuum, or need for wound exploration. Neonatal morbidity included neonatal or intrapartum death, hypoxic–ischemic encephalopathy (defined as an umbilical cord pH less than 7.0 and seizures or evidence of end-organ damage), neonatal intensive care unit stay greater than 72 hours, sepsis, intraventricular hemorrhage class III or IV, respiratory distress syndrome, umbilical artery pH less than 7.10, and 5-minute Apgar score less than 7. Secondary outcomes were the individual components of the primary outcome. The senior author (SO) reviewed the chart of any patient identified as having experienced a severe maternal morbidity.
Box 1. Severe Maternal Morbidity Indicators as Defined by the Centers for Disease Control and Prevention22
Acute myocardial infarction Acute renal failure Adult respiratory distress syndrome Amniotic fluid embolism Cardiac arrest or ventricular fibrillation Disseminated intravascular coagulation Eclampsia Heart failure or arrest during surgery or procedure Puerperal cerebrovascular disorders Pulmonary edema or acute heart failure Ruptured aneurysm Severe anesthesia complications Sepsis Shock Sickle cell disease with crisis Air and thrombotic embolism Blood transfusion greater than two units Conversion of cardiac rhythm Hysterectomy Temporal tracheostomy Ventilation
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Patient demographic characteristics, comorbidities, and delivery outcomes were extracted from the medical record. A new hypertensive disorder of pregnancy was defined as new blood pressure elevation of greater than 140/90 mm Hg occurring at greater than 20 weeks of gestation. Weight gain in pregnancy was calculated as the difference between the weight recorded closest to delivery and the weight recorded at the first prenatal visit. As a result of changes in the delivery record at our institution, the time from uterine incision to delivery could only be calculated for women delivering after September 15, 2012. All statistical analyses were performed using SAS 9.4. x2 or Fisher exact tests were used to analyze categorical variables where appropriate and Student t test or Mann-Whitney U test was used to analyze continuous variables depending on their distributions. A priori, we planned to examine results in the subgroup of women who underwent a cesarean delivery regardless of whether labor or planned cesarean delivery preceded it. Multivariable logistic regression was performed to examine the relationship between trial of labor and composite maternal and neonatal morbidity by accounting for potential confounding variables. We identified risk factors for maternal and neonatal morbidity using a manual backward elimination model selection that retained only those covariates that were significant at the .05 significance level. Logistic regression examining the relationship between trial of labor and severe maternal morbidity could not be performed as a result of the small number of patients with this outcome. Relative risks and odds ratios were calculated when appropriate. Based on preliminary data, we estimated the incidence of the primary outcome to be 50% in this population. We calculated that a sample size of 338 women would be required to show a 30% difference in the primary outcome with a two-sided a of 0.05 and a power of 80%.
RESULTS During the study period, 434 women with BMI 50 or greater were admitted for delivery with a viable fetus. After excluding 48 women who delivered at less than 34 weeks of gestation, 9 with multiple gestations, and 33 carrying fetuses with major fetal anomalies, the final sample size included 344 women. The median BMI at delivery was 53 with a range of 50–94. Fortyone percent of the total population entered pregnancy with medical comorbidities including 34% with chronic hypertension and 10% with type 2 diabetes. In this population, 58% of women (n5201) experienced labor and 42% (n5143) underwent a cesarean
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delivery without trial of labor. Of women who labored, 45% underwent a cesarean delivery, most commonly for labor arrest (61%) and nonreassuring fetal status (28%). The most common indications for planned cesarean delivery were prior cesarean delivery (69%), suspected macrosomia (8%), and malpresentation (7%). The frequency of cesarean delivery among nulliparous women who labored was 61% (n575/122). Even among women with a prior vaginal delivery, the frequency of cesarean delivery after labor was 21% (n516/77). Nine women underwent trial of labor after cesarean delivery and 44% (4/9) had a successful vaginal birth. Women who labored were younger, more likely to be nulliparous and African American, and less likely to have pregestational diabetes (Table 1). Composite morbidity, which encompassed both maternal and neonatal outcomes, was the primary outcome and was reduced among women who labored [odds ratio (OR) 0.46, 95% CI 0.30–0.72]. After adjusting for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery, this relationship remained significant (adjusted OR 0.42, 95% CI 0.24–0.75) (Table 2). Women who labored also experienced lower risks of the secondary outcomes of infectious, wound, and neonatal morbidity (Table 3). Risk of severe maternal morbidity was not statistically different in women who labored compared with those who underwent planned cesarean delivery. Of the 12 cases of severe maternal morbidity, one occurred in a woman who underwent a vaginal delivery. This patient was admitted 3 weeks postpartum with fever, hypotension, and had blood and urine cultures positive for Escherichia coli, consistent with urosepsis. Three cases occurred in women with planned cesarean delivery. The majority of cases (8/ 12) occurred in women who underwent a cesarean delivery after labor. These complications included postpartum hysterectomy, hemorrhagic shock, cardiac arrest, fascial dehiscence, and reoperation for intraabdominal abscess. Finally, we examined the subgroup of 234 women who underwent a cesarean delivery, whether planned (n5143) or after labor (n591). In this group, there were no statistically significant differences in composite, infectious, wound, or neonatal morbidity; however, severe maternal morbidity was significantly increased in women who had labored (8.8% compared with 2.1%, relative risk 4.2, 95% CI 1.14– 15.4). After adjusting for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery, labor was not associated with
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Table 1. Demographic and Clinical Characteristics Variable
Labor (n5201)
Planned Cesarean Delivery (n5143)
P
Maternal age (y) Nulliparity African American race Smoking during pregnancy Public insurance BMI (kg/m2) Pregestational diabetes Chronic hypertension High school education or less Prior cesarean delivery New hypertensive disorder of pregnancy Weight gain in pregnancy (kg) Gestational diabetes Induction of labor Cesarean delivery Vertical skin incision Classic hysterotomy Emergent delivery Time from skin incision to delivery (min)
27.765.5 122 (60.7) 93 (46.2) 29 (14.4) 127 (63.5) 53.3 (51.5–57.4) 13 (6.5) 64 (31.8) 124 (65.3) 9 (4.5) 59 (29.3) 10.8 (5.7–16.8) 29 (14.4) 141 (66.2) 91 (45.3) 16 (17.8) 18 (17.7) 11 (12.1) 17.769.8
30.964.8 20 (14.0) 53 (37.1) 36 (25.2) 104 (73.2) 53.7 (51.5–58.3) 23 (16.1) 53 (37.1) 99 (73.3) 114 (79.7) 32 (22.4) 9.5 (4.1–14.3) 28 (19.6) 0 (0.00) 143 (100.0) 39 (27.5) 37 (28.0) 4 (2.8) 21.6611.5
,.001 ,.001 .09 .06 .06 .47 .004 .31 .12 ,.001 .15 .09 .21 N/A ,.001 .09 .09 .006 .01
BMI, body mass index; N/A, not applicable. Data are mean6SD, n (%), or median (interquartile range) unless otherwise specified.
composite, infectious, or neonatal morbidity. However, labor was associated with increased odds for wound morbidity (OR 2.32, 95% CI 1.01–5.37). Severe maternal morbidity could not be examined in logistic regression as a result of the small number of women with the outcome (n512).
DISCUSSION This study examined delivery strategy—trial of labor compared with planned cesarean delivery—in superobese women (BMI 50 or greater) delivering after 34 weeks of gestation. Our study finds decreased composite maternal and neonatal morbidity in women undergoing trial of labor compared with planned cesarean delivery. Women who undergo cesarean
delivery after trial of labor may have a higher risk of wound complications and severe maternal morbidity compared with women who underwent planned cesarean delivery, but these rare outcomes warrant further study. For most pregnant women, trial of labor is the preferred delivery strategy because the desired outcome—a vaginal delivery—will occur for the majority of women, and vaginal delivery is associated with reduced maternal and neonatal morbidity compared with cesarean delivery.11–13,24 In superobese women, the preferred strategy is less clear. Although the risk of a failed trial of labor is significantly higher in this population, cesarean delivery is technically challenging and associated with high complication
Table 2. Association Between Labor and Maternal and Neonatal Morbidity Unadjusted OR (95% CI)
Morbidity Composite morbidity (n5143) Composite maternal morbidity (n5109) Severe maternal morbidity (n512) Infectious maternal morbidity (n574) Wound morbidity (n581) Composite neonatal morbidity (n569)
0.46 0.59 2.21 0.52 0.48 0.40
(0.30–0.72) (0.31–0.93) (0.59–8.31) (0.31–0.88) (0.29–0.79) (0.24–0.69)
Adjusted OR* (95% CI) 0.42 (0.24–0.75) 0.49 (0.27–0.90) N/A† 0.52 (0.27–1.0) 0.48 (0.25–0.92) 0.87 (0.56–1.34)
Unadjusted RR (95% CI) in the Subgroup of Women Who Underwent Cesarean Delivery (n5235) 1.11 1.27 4.12 1.16 1.23 0.49
(0.88–1.40) (0.94–1.69) (1.12–15.11) (0.78–1.72) (0.87–1.75) (0.25–0.98)
OR, odds ratio; RR, relative risk; N/A, not applicable. For all comparisons, planned cesarean delivery serves as the reference group. * Adjusted for maternal age, nulliparity, pre-existing diabetes, gestational age at delivery, and prior cesarean delivery. † Unable to perform logistic regression as a result of small number with outcome of severe maternal morbidity.
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Table 3. Maternal and Neonatal Morbidity in Women With Labor Compared With Planned Cesarean Delivery Morbidity
Labor (n5201)
Composite morbidity (primary outcome) Maternal morbidity (composite) Severe maternal morbidity (composite) Cardiac arrest Respiratory failure Sepsis Shock Pulmonary embolism Blood transfusion greater than 2 units Hysterectomy Infectious morbidity Endometritis Pneumonia Deep tissue abscess Wound infections Urinary tract infections Wound complications Cellulitis Wound separation with packing Wound vacuum Wound exploration Other morbidity Maternal death Prolonged length of stay Postpartum readmission Uterine rupture or dehiscence ICU admission 3rd- or 4th-degree laceration Neonatal morbidity (composite) Neonatal death Intrapartum death NICU stay greater than 72 h Neonatal sepsis Intraventricular hemorrhage Respiratory distress syndrome Umbilical artery gas less than 7.10 5-min Apgar score less than 7
68 54 9 1 1 3 2 2 1 2 34 7 0 1 33 5 36 33 19 8 3 0 0 13 19 0 5 1 28 0 1 12 9 1 43 15 5
(33.7) (26.7) (4.5) (0.5) (0.5) (1.5) (1.0) (0.9) (0.5) (1.0) (16.8) (3.5) (0.0) (0.5) (16.3) (2.5) (17.8) (16.3) (9.4) (3.8) (1.5) (0.0) (0.0) (6.4) (9.5) (0.0) (2.5) (0.5) (13.9) (0.0) (0.5) (5.9) (4.5) (0.5) (1.5) (7.4) (2.5)
Planned Cesarean Delivery (n5143) 76 55 3 0 0 1 0 0 2 1 40 2 0 0 38 1 45 40 15 6 3 2 0 6 7 1 3 0 41 2 0 24 10 0 13 13 11
(55.3) (38.7) (2.1) (0.0) (0.0) (0.7) (0.0) (0.0) (1.4) (0.7) (28.2) (1.4) (0.0) (0.0) (26.8) (0.7) (31.7) (28.2) (10.6) (4.6) (2.1) (2.0) (0.0) (4.2) (5.0) (0.7) (2.1) (0.0) (28.9) (1.4) (0.0) (16.9) (7.0) (0.0) (9.2) (9.2) (7.8)
RR (95% CI)
P
0.64 (0.50–0.82) 0.69 (0.50–0.94) 2.13 (0.59–7.73) N/A N/A 2.11 (0.22–20.08) N/A N/A 0.35 (0.03–3.84) 1.4 (0.13–15.36) 0.60 (0.40–0.89) 2.46 (0.52–11.67) N/A N/A 0.61 (0.40–0.92) 3.50 (0.42–29.76) 0.56 (0.38–0.82) 0.58 (0.39–0.87) 0.89 (0.47–1.09) 0.83 (0.29–2.32) 0.70 (0.14–3.43) 0.14 N/A 1.52 (0.59–3.91) 1.90 (0.82–4.41) N/A 1.17 (0.29–4.81) N/A 0.48 (0.31–0.74) N/A N/A 0.35 (0.18–0.68) 0.63 (0.26–1.52) N/A 0.16 (0.05–0.56) 0.81 (0.40–1.65) 0.32 (0.11–0.90)
,.001 .03 .37 1.0 1.0 .65 .51 .51 .57 1.0 .02 .32 N/A 1.0 .02 .41 .004 .01 .82 .72 .69 N/A .38 .12 .41 1.00 1.0 ,.001 0.17 1.0 .002 .30 1.0 .001 .56 .02
RR, relative risk; N/A, not applicable; ICU, intensive care unit; NICU, neonatal intensive care unit. Data are n (%) unless otherwise specified.
rates.5,7–9,15,25–27 Adequate fetal monitoring may be difficult to achieve, especially with a closed cervix and before internal monitors can be placed. Furthermore, incision to delivery times are increased in obese women, which raises issues about the capacity to perform an emergent cesarean delivery in circumstances of nonreassuring fetal status.6,20 These concerns have led some authors to question the value of trial of labor in superobese women. On the other hand, maternal risks associated with cesarean delivery in obese women are well documented. Alanis et al21 found that nearly one in three superobese women have significant complications
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after cesarean delivery. The most common complications are wound and infectious complications, which is consistent with our findings in this study.20 Obese women have higher rates of failed regional anesthesia, are more likely to require general anesthesia, and difficult intubation rates are higher compared with nonobese populations.28–30 The incidence of severe maternal morbidity is greater among women undergoing cesarean delivery, but the relationship to maternal obesity is less clear.22,31,32 Very few studies have examined outcomes of trial of labor in morbidly obese women compared with planned cesarean delivery. Subramaniam et al14
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compared induction of labor with planned cesarean delivery in women with BMIs of 40 or greater. Women in spontaneous labor were excluded. Similar to our study, planned cesarean delivery was not associated with improved overall morbidity. In contrast, our study found a reduction, rather than no difference, in maternal morbidity and no increase in neonatal morbidity among women who underwent trial of labor. Their study raised similar concerns about outcomes of women with a failed trial of labor, although they found higher risks of operative complications and infectious and wound morbidity in this group, which were not found in our study. The consistent findings in both studies of no significant difference in neonatal outcomes suggest that route of delivery should be driven by relative risk of maternal morbidity. A major strength of our study is the data source. Most prior studies in this population use vital records data, which may not provide uniform ascertainment of certain exposures such as trial of labor that are subject to different interpretation by various health care providers. In contrast, our study utilizes detailed review of individual patient charts with predetermined definitions for important exposures, improving proper classification of these exposures. Additionally, our primary focus on the exposure (trial of labor compared with planned cesarean delivery) rather than the outcome (cesarean delivery compared with vaginal delivery) more closely approximates the clinical decision that health care providers encounter when arriving at a delivery strategy for superobese women. Inclusion of women in spontaneous labor makes our study generalizable to the entire population of superobese women. Limitations of our study include its retrospective nature and the inherent biases associated with this study design. In our study, women undergoing trial of labor were different at baseline from women undergoing planned cesarean delivery. Although we attempted to control for these differences, we acknowledge that residual confounding may exist, creating a scenario in which women who are advised to attempt trial of labor are inherently lower risk individuals than women undergoing planned cesarean delivery. Finally, although we decided a priori to examine the subgroup of women who underwent cesarean delivery after laboring, we acknowledge that our sample size may not be large enough to draw conclusions about this population. Among the subgroup of women who underwent cesarean delivery, the finding of no difference between women who experienced trial of labor compared with planned
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cesarean delivery may represent lack of statistical power. The finding of increased severe maternal morbidity in this group also deserves serious consideration. Although the finding is concerning, the small number of women with these outcomes limits our ability to adequately examine this outcome by controlling for differences in baseline characteristics. Similarly, small numbers (n59) limit our ability to examine outcomes of superobese women undergoing trial of labor after cesarean delivery; however, the one intrapartum fetal death in our study occurred in this group. In summary, despite high rates of cesarean delivery among superobese women, trial of labor is associated with decreased risk for maternal morbidity with no difference in neonatal morbidity. These data are useful to inform delivery planning and counseling in this high-risk population and suggest that maternal superobesity alone should not be an indication for cesarean delivery. REFERENCES 1. Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011–2014. NCHS Data Brief 2015:1–8. 2. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 2012;307:491–7. 3. Mason EE, Doherty C, Maher JW, Scott DH, Rodriguez EM, Blommers TJ. Super obesity and gastric reduction procedures. Gastroenterol Clin North Am 1987;16:495–502. 4. Sturn R. Increases in clinically severe obesity in the United States, 1986–2000. Arch Intern Med 2003;163:2146–8. 5. Marshall NE, Guild C, Cheng YW, Caughey AB, Halloran DR. Maternal superobesity and perinatal outcomes. Am J Obstet Gynecol 2012;206:417.e1–6. 6. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, et al. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 2001;25:1175–82. 7. Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 2001;91:436–40. 8. Blomberg M. Maternal obesity, mode of delivery, and neonatal outcome. Obstet Gynecol 2013;122:50–5. 9. Marchi J, Berg M, Dencker A, Olander EK, Begley C. Risks associated with obesity in pregnancy, for the mother and baby: a systematic review of reviews. Obstet Rev 2015;16:621–38. 10. Schummers L, Hutcheon JA, Bodnar LM, Lieberman E, Himes KP. Risk of adverse pregnancy outcomes by prepregnancy body mass index: a population-based study to inform prepregnancy weight loss counseling. Obstet Gynecol 2015; 125:133–43. 11. Burrows LJ, Meyn LA, Weber AM. Maternal morbidity associated with vaginal versus cesarean delivery. Obstet Gynecol 2004;103:907–12. 12. Curtin SC, Gregory KD, Korst LM, Uddin SFG. Maternal morbidity for vaginal and cesarean deliveries, according to pre-
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Grasch et al
Delivery in Superobese Women
Copyright Ó by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
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