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Original Research

Extreme Obesity and Postcesarean


Maternal Complications
David M. Stamilio,

MD, MSCE,

and Christina M. Scifres,

MD

OBJECTIVE: To estimate the association of obesity and


extreme obesity with maternal complications after cesarean delivery.

adjusted OR 2.7, CI 1.26.1), wound infection (18.8%,


adjusted OR 3.4, CI 1.48.0), and emergency department
visit (23.1%, adjusted OR 2.2, CI 1.034.9).

METHODS: This was a secondary cohort analysis of


a randomized controlled trial. The parent study was
designed to estimate the effect of supplemental oxygen
on postcesarean infectious morbidity. Because the study
intervention had no effect, study groups were combined as
a cohort. For this secondary analysis, the exposure was
obesity, stratified as normal or overweight (body mass
index [BMI] less than 30), obese (BMI 3045), or extremely
obese (BMI higher than 45). The primary outcome was
a composite of wound infection and endometritis. Secondary outcomes included wound infection, endometritis,
wound opening, hematoma or seroma, and emergency
department visit. We performed unadjusted and multivariable logistic regression analyses. Adjusted odds ratios
(ORs) and 95% confidence intervals (CIs) are reported.

CONCLUSION: Maternal extreme obesity is associated


with a considerable increase in postcesarean wound complications.

RESULTS: We included 585 women in the analysis. Eightyfive patients (14.5%) had BMIs higher than 45. Rates of
black race, chronic hypertension, diabetes, and gestational
diabetes increased and operative duration increased with
increasing obesity severity. Obese patients were more
likely to have a cesarean delivery after labor and have
a vertical skin incision or classical uterine incision. After
controlling for confounders, extremely obese patients had
a twofold to fourfold increase in postoperative complications, including the primary infectious outcome (18.8%,
From the Department of Obstetrics and Gynecology, University of North
Carolina School of Medicine, Chapel Hill, North Carolina; and the Department
of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh
School of Medicine, Pittsburgh, Pennsylvania.
Supported by a grant from the Barnes Jewish Foundation.
Presented at the Society for Maternal Fetal Medicine 33rd Annual Meeting,
February 11-16, 2013, San Francisco, California.
Corresponding author: David M. Stamilio, MD, MSCE, 101 Manning Drive,
CB#7516, Chapel Hill, NC 27599; e-mail: stamilio@med.unc.edu.
Financial Disclosure
The authors did not report any potential conflicts of interest.
2014 by The American College of Obstetricians and Gynecologists. Published
by Lippincott Williams & Wilkins.
ISSN: 0029-7844/14

VOL. 124, NO. 2, PART 1, AUGUST 2014

CLINICAL TRIAL REGISTRATION: ClinicalTrials.gov,


www.clinicaltrials.gov, NCT00602603.
(Obstet Gynecol 2014;124:22732)
DOI: 10.1097/AOG.0000000000000384

LEVEL OF EVIDENCE: II

besity is pandemic, resulting in a substantial disease burden worldwide. In the United States, more
than 50% of nonpregnant reproductive-aged patients and
35% of preconception or interconception women are
overweight or obese; 8% of reproductive-aged women
are extremely obese.1,2 Cesarean delivery is one of the
most prevalent surgical procedures in the United States.3
Unfortunately, obese patients are at increased risk not
only for requiring cesarean delivery, but also for postoperative complications.47 Although obesity is known
to increase pregnancy complications, the effect of varying degrees of obesity on maternal postoperative risks is
not well characterized.411 The paucity of information on
perioperative risks associated with increasing severity of
obesity limits the clinician in counseling and clinical
decision-making. Thus, we designed a cohort study to
estimate the effect of obesity and extreme obesity on
postcesarean maternal complications.

MATERIALS AND METHODS


This is a retrospective cohort study of 585 patients
enrolled between 2008 and 2010 performed in
a prospective randomized controlled trial designed
to evaluate the efficacy of supplemental oxygen for
the prevention of postcesarean infectious morbidity.
Details of the trial were published previously but are
summarized briefly.12 In the initial trial, patients
were randomized in a one-to-one ratio to receive
either 2 L of oxygen using a nasal cannula during

OBSTETRICS & GYNECOLOGY

227

cesarean delivery (standard care) or 10 L of oxygen


using a nonrebreather mask (intervention group)
during and 2 hours after cesarean delivery. Women
received standardized preoperative iodine-based skin
antiseptic preparation and perioperative prophylactic antibiotics. During the study period, cefazolin was
used as primary preoperative prophylaxis, and clindamycin was used for patients with penicillin allergy.
Women undergoing scheduled or intrapartum cesarean delivery with regional anesthesia were eligible
for participation and were followed for 1 month postoperatively. We recruited women for study participation from the antepartum service and labor and
delivery. Exclusion criteria included emergency surgery, human immunodeficiency virus infection,
chronic corticosteroid therapy or other immunosuppressive therapy, general anesthesia, and a diagnosis
of extrauterine infection. We obtained institutional
review board approval at Washington University
School of Medicine before patient enrollment, and
written informed consent was obtained from all participants. Washington University institutional review
board approval was also granted for the current secondary study before initiation. The primary outcome
for the parent study, a composite outcome consisting
of endometritis and wound infection, and secondary
adverse postoperative complications were defined
using strict and distinct diagnostic criteria.12 All outcomes were assessed by the primary care team, and
the diagnoses were abstracted from the chart by trained
study personnel. The medical record was reviewed at the
time of the 2- to 4-week postoperative visit, and all
women who did not present for a postoperative visit
within 4 weeks postoperatively or who had planned
follow-up at an outside clinic were contacted by the
research nurse for a standardized telephone interview
(23%) to inquire about postoperative complications. All
data collection was performed using detailed standardized data collection forms. Data were entered into a database by two trained research team members including
a dedicated research nurse and one investigator (C.M.S.).
Data were validated prospectively with recurrent
research team meetings (usually monthly) to validate
collected data, especially with regard to wound outcomes, and to achieve consensus on questionable outcomes. Data were also validated retrospectively with
internal validation methods by the two primary investigators (C.M.S. and D.M.S.).
The study intervention, supplemental oxygen, had
no effect on maternal morbidity; thus, we combined
the two intervention groups into one cohort for this
analysis. The primary composite outcome for this
secondary analysis is maternal infectious morbidity,

228

Stamilio and Scifres

including endometritis and wound infection. A patient


was diagnosed with endometritis if she had an oral
temperature higher than 38C after the first 24 hours
postoperatively and either 1) fundal or lower abdominal
tenderness greater than expected; or 2) foul-smelling
or purulent lochia. Endometritis was diagnosed only if
other causes for the patients signs and symptoms
were not identified. Patients had to have been treated
with intravenous antibiotics for a diagnosis of endometritis to meet our study definition. The diagnosis of
wound infection required a wound opening larger than
1 cm or other surgical intervention such as laparotomy
or dbridement of tissue plus at least one of the following: 1) purulent drainage from the wound; 2) erythema
or induration of the surrounding tissues; 3) maternal
oral temperature higher than 38C; or 4) radiographic
evidence of infection. Secondary outcomes include
each composite outcome component (endometritis,
wound infection) as well as wound opening (larger than
1 cm), wound hematoma or seroma, hospital readmission within 4 weeks, and emergency department visits.
The exposure under study is obesity, stratified as normal or overweight (body mass index [BMI, calculated
as weight (kg)/[height (m)]2] less than 30), obese (BMI
3045), or extremely obese (BMI higher than 45). Body
mass index was calculated based on weight at the
time of study enrollment. All patients were enrolled
in the third trimester and within 12 days before
delivery. Therefore, BMI assessment is most relevant
to the time of surgery. Before study initiation, we
defined obesity using the BMI (30) cutoff recommended by the World health Organization and extreme
obesity using a BMI cutoff derived from a review of
the obstetric literature.7,11,13,14
The primary aim for this cohort study is to
compare the maternal composite postcesarean infectious morbidity outcome across the three maternal
weight exposure strata: nonobese, obese, and extremely
obese. We also compared the secondary outcomes
across the same BMI-defined patient groups. We first
compared the BMI exposure groups for key demographic variables, comorbidities, and outcomes in an
unadjusted analysis using analysis of variance and x2 or
Fishers exact tests as appropriate for variable type and
frequency. We used logistic regression analysis to perform multivariable analysis to estimate the independent
effect of obesity on postcesarean complication rate controlling for important confounders of the association
between obesity and adverse outcomes. Obesity was
included in the multivariable model as an indicator (also
known as a dummy) variable because it is a trichotomous categorical variable. We selected covariates for
inclusion in the initial regression models based on the

Extreme Obesity and Cesarean Complications

OBSTETRICS & GYNECOLOGY

unadjusted analysis results, biologic plausibility, and


prior published research. Candidate variables were
selected from the unadjusted analysis if they were associated with the outcome (P,.10). To achieve the final
best-fit multivariable models, we used a nonautomated
process of backward variable elimination, testing
sequentially for significant differences between hierarchical models with the likelihood ratio test or Wald test.
We assessed the final explanatory regression model for
goodness of fit with the HosmerLemeshow summary
statistic. We report adjusted odds ratios (to estimate
relative risk) and 95% confidence intervals (CIs) as estimates of the effect of obesity level on postcesarean
complication risk. Because all data were collected prospectively, there were very few missing data points. All
data collected before hospital discharge were complete
with one exception: cord blood gas results were available only for 89.7% of patients. There were 2% of patients (n511) lost to follow-up for the 4-week infectious
morbidity outcomes assessment. These patients were
assumed to not have an infectious morbidity in the
analysis because patients in this population rarely seek
postoperative care outside of our facility.
With a goal to identify attributable factors in the
association between obesity and postoperative morbidity, we performed stratified analyses on operative
characteristics, including uterine incision type, skin
incision type, operative time, and closure technique.
These variables were not included in the multivariable
analyses because they are likely in the causal pathway
and if adjusted for could introduce bias into the effect
estimates in the association between obesity and outcome. Preoperative antibiotic administration was not
assessed as a potential attributable factor because nearly
all patients undergoing cesarean delivery receive this
standardized preventive therapy at our institution.
We did not perform a formal sample size calculation because the sample size was fixed at the
completion of the parent clinical trial. However,
before initiating this study, we estimated that we
would have 80% power to detect a 2.2-fold increased
risk in the composite morbidity outcome associated
with obesity class using the available sample size,
a 10% baseline risk of the outcome, an extreme
obesity prevalence of 15% within the cohort, and
assuming statistical significance at a P value ,.05.

RESULTS
In this prospective cohort of 585 patients, postcesarean infectious morbidity, defined as the composite of
endometritis and wound infection, occurred in 10.4%
of all patients in the cohort. Rates of normal or
overweight (BMI less than 30) and obesity class I

VOL. 124, NO. 2, PART 1, AUGUST 2014

(BMI 3034.99), class II (BMI 3539.99), and class III


(BMI 40 or higher) were 25.1%, 30.1%, 14.9%, and
29.9%, respectively. Eighty-five patients (14.5%) had
extreme obesity, with BMIs higher than 45.
We display demographics, clinical factors, and
surgical characteristics compared across obesity classifications in Table 1. Rates of maternal black race,
chronic hypertension, diabetes, and gestational diabetes increased with increasing obesity severity. Operative duration increased with increasing obesity
severity, and the mean operative time in extremely
obese patients was 15 minutes longer than in nonobese patients. Rates of vertical skin incision and nontransverse uterine incision increased with increasing
obesity. As anticipated, rates of preoperative antibiotic use were high and similar across obesity categories. Exposure groups were also similar with regard to
the rates of cesarean delivery after labor and cesarean
delivery after rupture of membranes.
After controlling for relevant confounders,
extremely obese patients had a nearly threefold
increase in the rate of the composite postoperative
infectious morbidity outcome compared with nonobese
patients (Table 2). We also observed a two- to fourfold
increase in other postoperative complications in
extremely obese patients, although the associations
with endometritis, wound opening, seroma and hematoma development, and hospital readmission within 4
weeks were not statistically significant (Table 2).
Extremely obese patients had statistically significant increases in the rates of wound infection and emergency
department evaluation. Obese and extremely obese patients combined appeared to be readmitted to the hospital within 4 weeks after delivery two times more
frequently than nonobese patients; however, the difference in these point estimates was not statistically significant (relative risk 2.5, 95% CI 0.88.2, P5.1). Point
estimates for rates of most adverse outcomes in patients
with obesity not characterized as extreme appeared
higher, but the relative risks were not statistically significant (Table 2).
We performed stratified analyses on skin and
uterine incision types among only obese patients.
Neither skin nor uterine incision type was associated
with morbidity in all obese (data not shown) or
extremely obese patients. However, this subanalysis is
limited by the restricted sample size and the consequentially low power. Among the 85 extremely obese
patients, we observed an excess of the primary composite infection outcome in those who had transverse
(21.9%) compared with vertical (0%) uterine incisions,
but this was not statistically significant (P5.07). Among
extremely obese patients, the observed rate of seroma

Stamilio and Scifres

Extreme Obesity and Cesarean Complications

229

Table 1. Baseline and Operative Characteristics of the Exposure Groups


Demographic
Maternal age (y)
Gravidity
Nulliparity
Maternal race
White
Black
Other
Chronic hypertension
Gestational diabetes
Diabetes mellitus
Smoking
Prior cesarean delivery
Operative characteristics
Operative time (min)
Preoperative antibiotics
Skin incision type
Pfannenstiel
Vertical
Uterine incision type
Low transverse
Classical or T
Cesarean delivery after labor
Preoperative rupture of fetal
membranes
Subcutaneous sutures
Intraabdominal drain

Not Obese: BMI (kg/m2)


Less Than 30 (n5147)*

Obesity: BMI 3045


(n5353)*

Extreme Obesity: BMI


Higher Than 45 (n585)*

27.666.5
2.961.6
40 (27.2)

27.766.2
3.161.8
92 (26.1)

27.965.1
3.161.6
18 (21.2)

56
72
19
4
4
4
21
84

111 (31.4)
226 (64.0)
16 (4.5)
38 (10.8)
27 (7.7)
17 (4.8)
57 (16.2)
199 (65.0)

18 (21.2)
64 (75.3)
3 (3.5)
13 (15.3)
8 (9.4)
9 (10.6)
9 (10.6)
55 (71.4)

54.6622.5
144 (98.0)

58.4622.5
344 (97.5)

69.5626.6
84 (98.8)

145 (98.6)
2 (1.4)

342 (96.9)
11 (3.1)

75 (88.2)
10 (11.8)

140 (95.2)
7 (4.8)
23 (15.7)
35 (23.8)

334 (94.6)
19 (5.4)
82 (23.2)
89 (25.2)

73
12
20
19

52 (35.4)
1 (0.7)

76 (21.5)
5 (1.4)

12 (14.1)
1 (1.2)

(38.1)
(49.0)
(12.9)
(2.7)
(2.7)
(2.7)
(14.3)
(66.7)

P
.04
.15
.57
,.001

.003
.07
.03
.42
.59
,.001
.73
,.001
.007

(85.9)
(14.1)
(23.5)
(22.4)

.14
.84
,.001
.79

BMI, body mass index.


* Data are mean6standard deviation or n (%).

Primary surgeon training level was assessed (Postgraduate Year resident level, Fellow, or attending) but was not different across exposure
groups (data available on request).

or hematoma was higher with vertical (20%) compared


with transverse (5.3%) skin incisions, but this was not
statistically significant (P5.09). We also performed stratified analyses on other key operative characteristics. We
explored the effect of long operative times on maternal
postoperative morbidity. Although obese patients had
longer operative times on average, a long operative
timedefined as higher than the 90th percentile for nonobese patients (83 minutes)was not associated with an
increase in the composite infectious morbidity outcome
in obese, extremely obese, or nonobese patients (data
not shown). Lastly, we explored the effect of placing
sutures in the subcutaneous tissue on postoperative
morbidity. Subcutaneous suture placement did not
affect the postcesarean infectious morbidity rate in
obese, extremely obese, or nonobese patients; relative
risks (95% CI) for the primary infectious morbidity outcome with subcutaneous suture use were 0.8 (0.31.8),
1.4 (0.54.2), and 1.0 (0.33.4) for the respective weight
categories. The lack of observed associations between
various operative characteristics and infectious morbidity

230

Stamilio and Scifres

could alternately be attributed to low statistical power


rather than a proven equivalence.
We assessed the effect of obesity severity on coarse
measures of neonatal outcome. Birth weight increased
with increasing severity of maternal obesity; mean birth
weight (standard deviation) was 2,878 g (827), 3,126 g
(805), and 3,310 g (702) for nonobese, obese, and
extremely obese patients, respectively (x2 for trend
P,.001). Mean umbilical cord blood pH was lower
for extremely obese patients compared with nonobese
and obese patients (7.23 compared with 7.27, P5.003).
However, cord blood base deficit and 5-minute Apgar
score were similar across maternal weight classifications
(data not shown). Unexpectedly, the rate of admission
to the neonatal intensive care unit or special care nursery was significantly lower (P,.001) in extremely obese
patients (18.8%) compared with obese (30.9%) or nonobese patients (36.7%). In logistic regression analysis,
longer operative time did not confound or modify the
association between extreme obesity and neonatal
intensive care unit admission.

Extreme Obesity and Cesarean Complications

OBSTETRICS & GYNECOLOGY

Table 2. Multivariable Analysis of Primary and Secondary Outcomes in Obese and Nonobese Patients

Primary composite
outcome
Secondary outcomes
Wound infection
Endometritis
Wound opening
Seroma or
hematoma
Emergency
department visit
Hospital
readmission

Normal or
Overweight (n5147)

Obesity
(n5353)

Extreme Obesity
(n585)

Adjusted OR*
(95% CI)

Adjusted OR
(95% CI)

11 (7.5)

34 (9.6)

16 (18.8)

1.2 (0.62.5)

2.7 (1.26.1)

10
1
8
6

33
5
16
9

16
3
9
6

1.4
1.7
0.8
0.6

3.4
4.4
2.1
1.8

(6.8)
(0.7)
(5.4)
(4.1)

(9.4)
(1.4)
(4.5)
(2.6)

(18.8)
(3.5)
(10.6)
(7.1)

(0.72.9)
(0.214.9)
(0.31.9)
(0.21.8)

(1.48.0)
(0.444.1)
(0.85.7)
(0.65.7)

14 (10.4)

44 (13.7)

18 (23.1)

1.3 (0.72.4)

2.2 (1.034.9)

3 (2.2)

18 (5.6)

4 (5.2)

2.6 (0.89.0)

2.4 (0.511.1)

OR, odds ratio; CI, confidence interval.


Data are n (%) unless otherwise specified.
Multivariable models adjusted for labor before cesarean, prior cesarean, maternal race, hypertension, and diabetes. Not all covariates were
retained in all models if nonsignificant.
* Adjusted OR for obesity compared with normal or overweight.

Adjusted OR for extreme obesity compared with normal or overweight.

Composite outcome includes endometritis and wound infection.

DISCUSSION
Using a well-characterized cohort of general obstetric
patients who required cesarean delivery, we observed
that obese patients, particularly those with extreme
obesity, have a considerable increase in risk for
postoperative complications compared with nonobese
patients. Patients with lesser degrees of obesity
appeared to have estimates for adverse outcome rates
that were higher than nonobese patients but risks were
not statistically increased compared with nonobese
patients. In our cohort, postcesarean complication
risks associated with obesity were not significantly
worsened by other comorbidities such as diabetes
mellitus or hypertension. Thus, risks were mostly
attributable to obesity rather than chronic disease.
Although previous studies have shown a decrease in
risk for postoperative wound complications with the
use of subcutaneous adipose sutures,15 we did not
observe a risk reduction with the use of this wound
closure approach. This may have been the result of
limited power to detect a difference or the fact that the
subcutaneous suture approach was not used consistently because the technique was not randomized or
prescribed by the study protocol. Surprisingly, subcutaneous closure was used in only 14% of extremely
obese patients and the frequency that surgeons used
the subcutaneous closure technique decreased as obesity increased. This counterintuitive practice pattern
may be an indication that the technique could be used
more universally at our institution to reduce postoperative risk among obese patients.

VOL. 124, NO. 2, PART 1, AUGUST 2014

Unfortunately, there is limited clinical research


on the effects of increasing severity of obesity on
perioperative cesarean complications and risks.14,16
Most recently, Connor and colleagues17 performed
a retrospective cohort study that revealed a positive
doseresponse relationship between obesity severity
and cesarean wound complication rate. Our findings
corroborate those of Connor and colleagues.
The advantages of our study design enabled us to
better characterize perioperative complications as well
as validate findings of previous observational studies.
Potential for misclassification bias is minimal because
the cohort data were collected prospectively for a clinical
trial designed to study postcesarean wound complications. Thus, wound complications were strictly defined
and both exposure and outcome data are accurate and
complete. Data on surgical technique are also robust
because they were a focus of the primary study.
Although our study has advantages, it is important
to acknowledge its limitations. Because the parent study
was designed primarily to assess maternal risks, data on
neonatal outcomes are limited to gross measurements of
neonatal outcome. This study population is derived from
a metropolitan referral center; therefore, findings may
not be generalizable to other populations. The sample
size is restricted for the purpose of subanalyses of surgical
technique and stratified analyses such as skin and uterine
incision types. Furthermore, because surgical technique
was not randomly allocated, there is a distinct possibility
for selection bias or confounding by indication with
regard to the association between various surgical

Stamilio and Scifres

Extreme Obesity and Cesarean Complications

231

techniques and complications. Specifically, we observed


no relationship between skin incision type or uterine
incision type and wound complications within obese or
extremely obese patients, but the study has limited
power to detect an association. Data are conflicting, but
most observational studies of obese patients do not
reveal a difference in postcesarean wound complication
rates between vertical and transverse skin incisions.1821
In conclusion, extremely obese pregnant patients
are at increased risk for postcesarean infectious
morbidity and other postoperative complications.
These data can be used to counsel extremely obese
patients on operative risks. Our findings suggest that
clinicians should consider obesity in delivery mode
decisions and may need to alter the threshold for
using cesarean delivery in extremely obese patients
compared with nonobese patients. Additionally, clinicians should consider earlier or more frequent postoperative follow-up in extremely obese patients to
monitor for wound complications. Our results confirm an urgent need for clinical trials to research novel
strategies to reduce the chance of cesarean delivery
and to develop perioperative methods to reduce the
risks of cesarean delivery in extremely obese patients.

10. Pallasmaa N, Ekblad U, Aitokallio-Tallberg A, Uotila J,


Raudaskoski T, Ulander VM, et al. Cesarean delivery in Finland: maternal complications and obstetric risk factors. Acta
Obstet Gynecol Scand 2010;89:896902.

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