ORIGINAL ARTICLE: ENDOMETRIOSIS

Association between surgically

diagnosed endometriosis and
adverse pregnancy outcomes
Innie Chen, M.D., M.P.H.,a,b Shifana Lalani, M.Sc., M.D.,a,b Ri-hua Xie, Ph.D., R.N.,b,c Minxue Shen, M.D., Ph.D.,b
Sukhbir S. Singh, M.D.,a,b and Shi-Wu Wen, M.B., Ph.D.a,b
a
Department of Obstetrics and Gynaecology, University of Ottawa, Ottawa, Ontario, Canada; b Ottawa Hospital Research
Institute, Ottawa, Ontario, Canada; and c Nanhai Hospital, Southern Medical University, Guangdong, People's Republic of
China

Objective: To examine the association between surgically diagnosed endometriosis and pregnancy outcomes in subsequent pregnancies.
Design: Retrospective cohort study of women who delivered a singleton live birth from 2003 to 2013 in Ottawa, Ontario, Canada.
Setting: Tertiary level academic center.
Patient(s): Pregnant women with surgically diagnosed endometriosis were identified using International Classification of Diseases-10
codes from previous hospital admissions and were compared with pregnant women with no prior admission for endometriosis for the
occurrences of adverse pregnancy outcomes.
Intervention(s): Observational study.
Main Outcome Measure(s): Gestational hypertension, preeclampsia, placenta previa, placental abruption, postpartum hemorrhage,
preterm birth, low birth weight, small for gestational age, and neonatal intensive care unit admission.
Results: Among the 52,202 eligible mother-infant pairs, we identified 469 mothers with surgically diagnosed endometriosis from a
previous hospital encounter. Compared with women without endometriosis, women with endometriosis were on average older and
were more likely to be primiparous, have lower gravidity, have a history spontaneous abortion, conceive with assisted reproductive
technology, and reside in areas with higher neighborhood income and lower proportion of immigrants. Women with endometriosis
were found to have an elevated risk of placenta previa (relative risk [RR], 3.30; 95% confidence interval [CI], 1.65–5.40) and
cesarean delivery (RR, 1.24; 95% CI, 1.10–1.40). After adjustment for potential confounding factors, women with endometriosis
were found to have a significantly elevated risk of placenta previa compared with women without endometriosis (adjusted RR, 2.54;
95% CI, 1.39–4.64).
Conclusion(s): This study identifies baseline demographic differences between women with and without endometriosis and suggests
that women affected by endometriosis have an independently elevated risk of placenta previa in pregnancy. (Fertil SterilÒ 2018;109:
142–7. Ó2017 by American Society for Reproductive Medicine.)
Key Words: Endometriosis, pregnancy outcomes, placenta previa, caesarean delivery
Discuss: You can discuss this article with its authors and with other readers at https://www.fertstertdialog.com/users/16110-
fertility-and-sterility/posts/20566-24631

E
ndometriosis, a condition charac- problem, affecting approximately 10%– difficulty conceiving (4–6). Despite the
terized by the presence of endome- 15% of women of reproductive age (3). negative impact of endometriosis on
trial glands and stroma outside of Endometriosis is linked to infertility, fertility, more women with
the uterine cavity and diagnosed by and current estimates suggest 30%–50% endometriosis are conceiving with the
surgery (1, 2), is a common health of women with endometriosis have assistance of reproductive technologies
(7). However, it is possible that
Received July 5, 2017; revised September 1, 2017; accepted September 22, 2017; published online mechanisms that interfere with fertility
November 29, 2017. in women with endometriosis may also
I.C. has nothing to disclose. S.L. has nothing to disclose. R-h.X. has nothing to disclose. M.S. has nothing
to disclose. S.S.S. has nothing to disclose. S-W.W. has nothing to disclose.
have adverse maternal and infant
I.C. is supported by a University of Ottawa Clinical Research Chair in Reproductive Population Health outcomes.
and Health Services. Shifana Lalani is the recipient of a Physicians' Services Incorporated (PSI) There are several reasons why
Foundation Resident Research Grant. The study team is supported by PSI Foundation and the Ca-
nadian Institutes for Health Research to conduct this research. endometriosis may contribute to
Reprint requests: Dr. Innie Chen, M.D., M.P.H., Ottawa Hospital, Department of Obstetrics and Gyne- adverse pregnancy outcomes. Aside
cology, Room 7236-3, 1967 Riverside Drive, Ottawa, Ontario K1H 7W9, Canada (E-mail: ichen@
toh.on.ca). from alterations in the uterine envi-
ronment due to the regional anatomic
Fertility and Sterility® Vol. 109, No. 1, January 2018 0015-0282/$36.00 changes, endometriosis may also be
Copyright ©2017 American Society for Reproductive Medicine, Published by Elsevier Inc.
https://doi.org/10.1016/j.fertnstert.2017.09.028 associated with altered ovulation

142 VOL. 109 NO. 1 / JANUARY 2018


and oocyte production, increased inflammatory cells in the
peritoneal fluid, endometrial P resistance, and inadequate
uterine contractility, all of which may compromise normal
embryonic development and pregnancy implantation (5–9).
Research on the pathogenesis of poor pregnancy outcomes
suggests that such disturbances in the peri-implantation
period may perpetuate throughout the later stages in preg-
nancy (8, 9).
At a population level, the detection of adverse maternal
and infant outcomes in observational studies generally
requires large sample sizes. Several smaller studies—with
sample sizes <1,000—have reported conflicting findings
with respect to the presence of endometriosis and various
perinatal outcomes, suggesting the possibility of reduced
statistical power in some cases (10–15).
Studies with larger sample sizes have reported association
with various differing adverse pregnancy outcomes. In one
study (n ¼ 1,140), women with ovarian endometrioma were
found to be at increased risk of preterm birth and small for
gestational age (SGA). However, in the analyses, women
with endometriosis and assisted reproduction were compared
with women with natural conception, so the independent
effect of endometriosis from that of assisted reproductive
technology was difficult to ascertain (16). In another study
(n ¼ 30,284), endometriosis was associated with pregnancy
loss and stillbirth, after adjustment for age, gestational age,
birth weight, and body mass index. However, this study did
not control for the effect of assisted reproduction as a poten-
tial confounder (17). One study of nulliparous women
(n ¼ 205,640) did not find association between endometriosis
and preeclampsia after adjustment for various confounders.
However, preeclampsia was the only outcome studied (18).
One large national Swedish study (n ¼ 1,442,675) reported as-
sociations with preterm birth, preeclampsia, antepartum
bleeding, and cesarean section, after adjustment for age,
smoking, body mass index, parity, years of formal education,
and year of birth. In further analyses, the outcome of preterm
birth was stratified by whether the woman underwent assisted
reproduction, but this stratification was not performed for
other reported outcomes (6).
Thus, despite a number of reports on the association be-
tween endometriosis and various adverse pregnancy out-
comes, the published literature in this area is difficult to
interpret, with conflicting findings (10–12, 16–22). Some of
these studies may have been limited by smaller sample size,
inappropriate comparison groups, or lack of consideration
for some potentially important confounders. Furthermore,
most of the studies did not document whether included
patients had diagnostic laparoscopy to confirm the presence
of endometriosis, which may impact the strength of the
association between endometriosis and pregnancy
outcomes. Given the prevalence of endometriosis and the
clinical significance of adverse pregnancy outcomes, we
conducted a large Canadian cohort study to investigate the
association between endometriosis and several important
maternal and fetal outcomes with the consideration of
clinically relevant confounders.
VOL. 109 NO. 1 / JANUARY 2018
Fertility and Sterility®
MATERIAL AND METHODS
Study Population and Record Linkage
We obtained approval from the Ottawa Hospital Research Ethics
Board before the commencement of this study. Women who had
a singleton live birth at the Ottawa Hospital between January 1,
2003, and December 31, 2013, were identified from the Cana-
dian Institute for Health Information Discharge Abstract Data-
base (CIHI-DAD). In cases where more than one birth record was
available for a patient, only information from the first record
was included in the analysis. The birth records for these women
were linked by healthcare numbers to surgical hospital records
to ascertain their surgical history. Women with a history of fi-
broids (International Classification of Diseases [ICD]-10 code:
D25) were excluded. The included women were then divided
into those with surgically diagnosed endometriosis as captured
by the ICD (ICD-10 code: N80) and those without surgically
diagnosed endometriosis. Maternal records were linked to in-
fant records using the maternal-infant chart number in the
CIHI-DAD, so that the associations between maternal character-
istics and infant outcomes could be analyzed.
Baseline Characteristics
Baseline characteristics in this study included maternal age,
neighborhood income, immigrant population, gravidity, par-
ity, previous spontaneous and therapeutic abortions, use of
assisted reproductive technology, chronic hypertension
(ICD-10 code: I10, I11, I12, I13, I15), preexisting diabetes
(ICD-10 code: E10, E12, E13, E14), and infant sex.
The relationship between endometriosis and socioeco-
nomic status (6, 23), and the relationship between adverse
perinatal outcomes and socioeconomic status (6, 24), have
previously been reported in the literature. As such, markers
of socioeconomic status were included as potential
confounders. The two socioeconomic status measures—
neighborhood income and immigration population—were
based on the mother's resident dissemination area
determined by patient postal code. A dissemination area is a
small, relatively stable geographic unit composed of one or
more adjacent dissemination blocks, defined by Statistics
Canada (25). It is the smallest standard geographic area for
which all census data are disseminated. Neighborhood
income was defined as per person equivalent, a household
size-adjusted measure of household income, based on 2006
census summary data, in quintiles. Neighborhood immigra-
tion population was defined as proportion of immigrant pop-
ulation, again based on 2006 census summary data, in tertiles.
Main Outcome Measures
Maternal outcomes of interest included gestational hyperten-
sion and preeclampsia (ICD-10 code: O11, O13, O14, O15),
placenta previa (ICD-10 code: O44), placental abruption
(ICD-10 code: O45), and postpartum hemorrhage (ICD-10
code: O72). Infant outcomes of interest included preterm birth
(before 37 completed weeks of gestation), low birth weight
(<2,500 g), SGA, defined by either third or fifth percentiles
143
ORIGINAL ARTICLE: ENDOMETRIOSIS

according to national standards (23), and need for neonatal
intensive care unit (NICU) admission.
Statistical Analysis
Baseline characteristics and occurrences of adverse maternal
and infant outcomes of women with endometriosis and those
without endometriosis were compared, using c2-tests or t-
tests. Multivariable log binomial regression analysis was per-
formed to estimate the independent effect of endometriosis on
various adverse maternal and infant outcomes after adjusting
for potential confounders. Potential confounders included in
the multivariable log binomial regression model were
maternal age at childbirth, neighborhood income quintile,
neighborhood proportion of immigration population tertile,
parity, history of spontaneous or therapeutic abortion, use as-
sisted reproductive technology, chronic hypertension, preex-
isting diabetes, and infant sex. All analyses were performed
using SAS-PC statistical software version 9.4 (SAS Inc.).
RESULTS
A total of 52,202 eligible mother-infant pairs were identified
from the Ottawa Hospital birth records. Of them, 469 mothers
(1%) had surgically diagnosed endometriosis from a previous
hospital encounter.

TABLE 1

Baseline characteristics of women with and without endometriosis, Ottawa Hospital, Canada, 2003–2013.
Total (N [ 52,202), Endometriosis (N [ 469), Control (N [ 51,733),
Characteristics n (%) n (%) n (%) P value
Age at delivery (y) < .0001
Mean SD 30.50  5.60 32.25  4.89 30.45  5.56
<20 1,685 (3.23) 2 (0.43) 1,683 (3.25)
20–24 6,033 (11.56) 31 (6.61) 6,002 (11.60)
25–29 13,978 (26.78) 91 (19.40) 13,887 (26.84)
30–34 18,048 (34.57) 199 (42.43) 17,849 (34.50)
35–39 9,981 (19.12) 119 (25.37) 9,862 (19.06)
R40 2,477 (4.75) 27 (5.76) 2, 450 (4.74)
Neighborhood income per person < .0001
equivalent (quintile)
Lowest 11,638 (22.29) 63 (0.64) 11,575 (22.37)
Medium-low 9,301 (17.82) 83 (13.43) 9,218 (17.82)
Middle 10,332 (19.79) 104 (17.7) 10,228 (19.77)
Medium-high 10,703 (20.50) 117 (24.95) 10,586 (20.46)
Highest 9,712 (18.60) 99 (21.11) 9,613 (18.58)
Immigrant population (tertile) .04
Lowest 33,589 (64.34) 317 (67.59) 33,272 (64.31)
Middle 16,234 (31.10) 143 (30.49) 16,091 (31.10)
Highest 1,598 (3.06) 5 (1.07) 1,593 (3.08)
Gravidity .002
1 23,292 (44.62) 253 (53.94) 23,039 (44.53)
%2 14,172 (27.15) 110 (23.45) 14,062 (27.18)
>2 14,738 (28.23) 106 (22.60) 14,632 (28.28)
Parity < .0001
Mean SD 0.60  1.20 0.23  0.52 0.59  1.22
0 32,830 (62.91) 377 (80.56) 32,453 (62.75)
1 12,353 (23.67) 77 (16.45) 12,276 (23.74)
R2 7,004 (13.42) 14 (2.99) 6,990 (13.52)
Spontaneous abortion .0076
Yes 12,952 (24.82) 141 (30.13) 12,811 (24.77)
No 39,235 (75.18) 327 (69.87) 38,908 (75.23)
Therapeutic abortion .6379
Yes 5,887 (11.28) 56 (11.97) 5,831 (11.27)
No 46,300 (88.72) 412 (88.03) 45,888 (88.73)
Use of assisted reproduction
Yes 435 (0.83) 36 (7.68) 399 (0.77) < .0001
No 51,767 (99.17) 433 (92.32) 51,334 (99.23)
Chronic hypertension .54
Yes 202 (0.39) 1 (0.21) 201 (0.39)
No 52,000 (99.61) 468 (99.79) 51,532 (99.61)
Preexisting diabetes .60
Yes 187 (0.36) 1 (0.21) 186 (0.36)
No 52,015 (99.64) 468 (99.79) 51,547 (99.64)
Infant sex .85
Male 26,718 (51.19) 238 (50.75) 26,480 (51.19)
Female 25,475 (48.81) 231 (49.25) 25,244 (48.81)
Gestational age (wk), mean  SD 38.7 (2.4) 38.6 (2.5) 38.7 (2.4)
Birth weight (g), mean  SD 3,330.9 (659.4) 3,308.1 (676.5) 3,331.1 (659.3)
Note: Data presented as mean  standard deviation (SD) or n (%), unless stated otherwise.
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 Fertility and Sterility®

The baseline characteristics of study participants are pre-
sented in Table 1. The average age of women was 30.5 (stan-
dard deviation [SD], 5.6) years. The majority of women were
primiparous (62.9%) and lived in middle- or high-income
neighborhoods with low immigration populations. The prev-
alences of chronic hypertension and preexisting diabetes were
0.39% and 0.36%, respectively. Fifty-one percent of the in-
fants were male. The mean (SD) gestational age was 38.7
(2.4) weeks, and mean (SD) birth weight was 3,330.9 (659.4) g.
Women with endometriosis, compared with women
without endometriosis, were on average older (mean age 
SD, 32.25  4.89 vs. 30.50  5.60) and were more likely to
be primiparous (80.56% vs. 62.91%), have lower gravidity,
have a history of spontaneous abortion (30.13% vs.
24.77%), conceive with assisted reproductive technology
(7.68% vs. 0.83%), and reside in areas with higher neighbor-
hood income and lower proportion of immigrants (all P< .05).
Table 2 compares the maternal and infant outcomes be-
tween the two study groups. In bivariate analyses, women
with endometriosis had increased risks of placenta previa
(relative risk [RR], 3.30; 95% confidence interval [CI], 1.65–
5.40), and cesarean section (RR, 1.24; 95% CI, 1.10–1.40).
Risks for most other adverse maternal and infant outcomes,
with the exception of SGA—also tended to be higher in
women with endometriosis than in women without, although
the differences were not statistically significant. After adjust-
ment for potential confounding factors, women with endo-
metriosis were found to have a significantly elevated risk of
placenta previa compared with women without endometriosis
(adjusted RR, 2.54; 95% CI, 1.39–4.64).
DISCUSSION
Our retrospective cohort study found that differences exist be-
tween women with and without endometriosis with respect to
age, gravidity, parity, history of spontaneous abortion, use of
assisted reproduction, and markers of socioeconomic status.
Further, compared with mothers who were not affected by
endometriosis, mothers affected by surgically confirmed
endometriosis had an increased risk of placenta previa after
adjustment for potential confounders.
The detection of baseline demographic differences between
women with and without endometriosis is an important
finding, as these differences have the potential to confound
the associations between endometriosis and adverse perinatal
outcomes observed in the literature. Our study suggests the
need to consider not only differences in clinical and obstetrical
history but also in markers of socioeconomic status. We found
that women with endometriosis were more likely to reside in a
neighborhood with higher incomes and fewer immigrants. This
association between endometriosis and socioeconomic status
has previously been reported in the literature (23) and adjusted
for in a previous analysis (6). Proposed explanations for this
relationship have included genetic predisposition to endome-
triosis, as well as differential access to healthcare (23). Further
studies are required to elucidate the factors influencing these
associations.
Our study also detected a more than two-fold increase in
the risk of placenta previa among women with surgically
diagnosed endometriosis. Some smaller studies have not
found an association between endometriosis and placenta
previa (10, 11), and it is possible that our findings may be
due to chance alone. However, we found several other
studies in the literature to corroborate these findings,
reporting 5- (14) to 16-fold (15) increased odds. We also found
that women with endometriosis were more likely to have a
history of spontaneous abortion, raising the possibility of me-
chanical endometrial trauma from uterine evacuation as a po-
tential explanation. However, the association between
endometriosis and placenta previa persisted even after adjust-
ment for patient history of spontaneous or therapeutic abor-
tion, suggesting the presence of additional mechanisms for

TABLE 2

Association between endometriosis and maternal and infant outcomes, Ottawa Hospital, Canada, 2003–2013.
Endometriosis Control Crude RR Adjusted RRa
Variable (N [ 469) (N [ 51,733) (95% CI) (95% CI)
Maternal outcome
Gestational hypertension and 37 (7.89) 4,064 (7.86) 1.00 (0.74, 1.37) 0.85 (0.62, 1.15)
preeclampsiab
Placenta previa 11 (2.40) 406 (0.80) 3.30 (1.65, 5.40) 2.54 (1.39, 4.64)
Placental abruption 10 (2.13) 893 (1.73) 1.24 (0.67, 2.29) 1.23 (0.66, 2.29)
Preterm premature rupture of 90 (19.19) 8,979 (17.36) 1.11 (0.92, 1.33) 0.96 (0.80, 1.16)
membranes
Cesarean delivery 175 (37.31) 15,527 (30.01) 1.24 (1.10, 1.40) 1.08 (0.97, 1.20)
Postpartum hemorrhage 35 (7.46) 3,548 (6.86) 1.09 (0.79, 1.50) 1.02 (0.74, 1.41)
Infant outcomes
Preterm birth 58 (12.37) 5,683 (11.05) 1.12 (0.88, 1.43) 1.07 (0.84, 1.37)
Low birth weight 40 (8.57) 4,377 (8.48) 1.01 (0.75, 1.36) 0.98 (0.73, 1.31)
SGA (<third percentile) 13 (2.80) 1,488 (2.90) 0.96 (0.56, 1.64) 0.92 (0.53, 1.57)
SGA (<fifth percentile) 15 (3.20) 1,997 (3.88) 0.82 (0.50, 1.36) 0.78 (0.47, 1.29)
NICU admission 87 (18.55) 8,893 (17.19) 1.08 (0.89, 1.31) 1.02 (0.85, 1.24)
Note: Data presented as n (%), unless stated otherwise. CI ¼ confidence interval; NICU ¼ neonatal intensive care unit; RR ¼ relative risk; SGA ¼ small for gestational age.
a
Adjusted for maternal age at delivery (continuous), parity (continuous), assisted reproductive technology (dichotomous), previous abortions (dichotomous), infant sex (dichotomous), chronic hy-
pertension (dichotomous), preexisting diabetes (dichotomous), neighborhood income per person equivalent (quintile), and immigrant population (tertile).
b
Chronic hypertension removed from independent variable list.
Chen. Endometriosis and pregnancy outcomes. Fertil Steril 2017.

VOL. 109 NO. 1 / JANUARY 2018 145

ORIGINAL ARTICLE: ENDOMETRIOSIS
the observed relationship. Other postulated reasons for
abnormal placentation have included endometrial P resis-
tance, endometrial inflammation and impaired free radical
metabolism, inadequate uterine contractility, and alteration
in uterine junctional zone (8).
Though nonsignificant trends were observed for several
infant outcomes, we did not observe significantly elevated
risks for other maternal and infant outcomes after controlling
for potential confounders. In the literature, the association
between endometriosis and adverse fetal outcomes has been
reported in two large population-based studies (6, 26) but
was not observed in smaller studies (10, 11, 14). When
associations were found, the effect sizes tended to be small,
with less than two-fold differences in risk. As many studies
in the literature did not control for many of the potential
confounders identified in our study, it is unclear the extent
to which the associations observed in the literature are due
to residual confounding.
There are several strengths in this study. First, it is based
on a fairly large sample of singleton births. Second, the
CIHI-DAD is a national database system that contains
detailed clinical, demographic, and administrative data for
hospital admissions and day surgeries across the country.
It has been validated extensively for research purposes
(27–29) and provides the basis for this large database
study. Third, all women affected by endometriosis were
surgically confirmed, thereby substantially reducing the
risk of misclassification. Fourth, since both surgical care
and maternity care were provided by the same center, bias
introduced by variable care issues, such as differences in
treatment protocol, practice style, and quality of care, was
less likely to occur. Finally, we employed various means to
control for potential confounding, such as the restriction
of study subjects to singleton births, exclusion of patients
with a history of fibroids, and use of multiple regression
models.
One limitation in our study is that our data set only in-
cludes records from the Ottawa Hospital. Even though our
institution serves the majority of patients seeking healthcare
within the region, women who had surgical diagnosis of
endometriosis at another hospital would not have been
included in the endometriosis group. While this may lead to
potential misclassification for a small fraction of cases, the
potential effect would be bias toward the null hypothesis.
Also, detailed clinical information, such as the severity and
type of endometriosis, patient body mass index, and ethnic
background, was not available for analysis. Finally, this study
is observational in nature, and although we have employed
various approaches to control for confounding, residual con-
founding may still exist.
Conclusions
Our large, Canadian, retrospective cohort study suggests that
pregnant women affected by endometriosis differ from
women without endometriosis by clinical and sociodemo-
graphic characteristics and have an independently elevated
risk of placenta previa. This finding adds to the growing
body of literature surrounding endometriosis and adverse
146
pregnancy outcomes. Further large, population-based studies
with appropriate control of potential confounders are needed
to corroborate these findings. Basic scientific studies are also
needed to explore the molecular basis for these associations.
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